Afr J Ecol 201856759ndash776 wileyonlinelibrarycomjournalaje emsp|emsp759copy 2018 John Wiley amp Sons Ltd
Received14May2018emsp |emsp Revised10October2018emsp |emsp Accepted10October2018DOI101111aje12574
S P E C I A L S E C T I O N C A M E R A T R A P P I N G I N A F R I C A
Using camera trap data to characterise terrestrial larger‐bodied mammal communities in different management sectors of the Dja Faunal Reserve Cameroon
Tom Bruce1 emsp|emspRajan Amin2emsp|emspTim Wacher2emsp|emspOliver Fankem1emsp|emspConstant Ndjassi1emsp|emsp Madeleine Ngo Bata1emsp|emspAndrew Fowler1emsp|emspHilaire Ndinga3emsp|emspDavid Olson1
1ZoologicalSocietyofLondonndashCameroonYaoundeacuteCameroon2GlobalConservationProgrammesZoologicalSocietyofLondonLondonUK3MinistryofForestsandWildlifeMINFOFDjaFaunalReserveYaoundeacuteCameroon
CorrespondenceTomBruceZoologicalSocietyofLondonndashCameroonYaoundeacuteCameroonEmailtombrucemyjcueduau
Funding informationUSFishandWildlifeService(USFWS)AfricanElephantConservationandIUCNSOSFondationSegreacutePangolinConservationInitiative
AbstractCameratrapsurveyscanbeusefulincharacterisingterrestriallarger‐bodiedmammalcommunities inCentralAfrica forestsTwo40‐trapminimumof100days surveygrids conducted in theDja FaunalReserveof southernCameroon showeddiffer‐encesinthemammalcommunitiesoftwosites32kmapartMammalrichnessdiver‐sityguildstructurebody‐sizepatternsandrelativeabundanceoftaxaweremeasuredbytrappingratesandoccupancyofthetwomammalcommunitiesOneofthesurveysiteswas(a)lessrichinterrestrialmammalspecies(b)missingdisturbance‐sensitivefelids and white‐bellied duiker (Cephalophus leucogaster subsp leucogaster Gray1873)(c)greaterinabundanceofsomedisturbance‐tolerantspeciesand(d)lowerinabundanceoflarger‐bodiedspeciesSeveralindicatorssuggestahigherhuntingpres‐sureatthissiteandthismaybeacontributingfactortothesedifferences
ReacutesumeacuteLeseacutetudesavecpiegravegesphotographiquespeuventecirctreutilespourcaracteacuteriserdescommunauteacutesdegrandsmammifegraveresterrestresdans les forecirctsdrsquoAfriquecentraleDeuxgrillesderecherchesde40piegravegessurunminimumde100joursreacutealiseacuteesdanslaReacuteservedeFauneduDjadanslesudduCamerounontmontreacutedesdiffeacuterencesdansdescommunauteacutesdedeuxsitesseacutepareacuteslrsquoundelrsquoautrede32kmLarichesseenmammifegraveresladiversiteacutelastructuredesguildeslescheacutemadestaillescorporellesetlrsquoabondance relative des taxons ont eacuteteacute mesureacute drsquoapregraves le taux de pieacutegeage etlrsquooccupationdesdeuxcommunauteacutesanimalesUnedessiteseacutetudieacuteseacutetait(a)moinsricheenespegravecesdemammifegraveresterrestres(b)deacutepourvudetoutfeacutelinsensibleauxperturbationsetdeceacutephalopheagraveventreblancCephalophus leucogastersubsp leu-cogasterGray1873(c)pluspeupleacutedecertainesespegravecesplustoleacuterantesvis‐agrave‐visdesperturbationset(d)moinspeupleacutedrsquoespegravecesdeplusgrandetaillePlusieursindica‐teurssuggegraverentuneplusfortepressiondelachassesurcesiteetcelapourraitecirctreunfacteurcontribuantagravecettediffeacuterence
K E Y W O R D S
cameratrapCameroonDjaFaunalReservemammaloccupancy
760emsp |emsp emspensp Bruce et al
1emsp |emspINTRODUC TION
WildlifeinCentralAfricanforestsisunderincreasingpressurefromhabitatlosshabitatfragmentationandintensivehuntingforbush‐meatandwildlifeparts(HansenStehmanampPotapov2010Mallonet al 2015Mambeya et al 2018 Potapov et al 2012 Poulsenet al 2017) Hunting is a daily occurrence in Central African vil‐lages(AbernethyCoadTaylorLeeampMaisels2013Ziegleretal2016) and is an important factor contributing to the distributionof mammal species within protected areas (Muchaal amp Ngandjui1999) and around settlements (Abrahams Peres amp Costa 2017)BushmeatmarketsurveyswithinCentralAfricahavedemonstratedthatmammalsrepresentgt90ofthecarcassessold(Faetal2006)Themotivesbehindhuntingrangefromtraditionalsubsistenceandcommercialhunting forbushmeat to targetingspecies for the ille‐galwildlifetradesuchasgreatapesforbodypartsforestelephant(Loxodonta cyclotisMatschie1900)forivoryandpangolinsfortheirscales(Craigieetal2010Stiles2011)
Reduction and extirpation of mammal populations in CentralAfrican forests have cascading ecological impacts on forest eco‐systemsInparticularthelossoftoppredators(MalhiAdu‐BreduAsareLewisampMayaux2013)keyseeddispersersincludinggreatapes and forest elephants (Blake Deem Mossimbo Maisels ampWalsh2009)andlandscapearchitectssuchaselephantsthatkeepclearingsopeninCentralAfricanforests(Maiselsetal2013)canhavelong‐termandfar‐reachingimpactsonforestcommunitiesandprocesses(Abernethyetal2013Lauranceetal2012)
Understanding the interplay of patterns of hunting (for exam‐ple distribution intensity target species frequency and huntingmethods)amajordriverofmammaliandefaunationand resultantimpactsonthecompositionstructureanddistributionofmedium‐to larger‐bodied terrestrialmammals in Central Africa forests caninform management actions (Abernethy et al 2013 Bennett etal 2007 Laurance et al 2006Nielsen 2006 SeddonGriffithsSooraeampArmstrong2014)
Forexample can regular effectivepatrollingby rangersmain‐tain robust wildlife communities within ldquodefendedrdquo zones whensurroundingareasareexperiencinghigherlevelsofhuntingThean‐swerwilldependinpartonthelong‐termreachofhuntingimpactsonmammalcommunitiesacrossforestlandscapesAslarger‐bodiedmammalsareusuallymorewide‐rangingoccuratlowdensitiesandhavelonggestationperiodsthismakesthemparticularlyvulnerabletoextinction(PurvisGittlemanCowlishawampMace2000TuckerOrdampRogers2014)whereasspecieswithsmallerhomerangesandhigherdensitiesonaveragemaybemoreresilientastheminimumareaneededtomaintainviablepopulationsissmallerThusarefinedunderstandingoftheprocessofdefaunationacrossforestedCentralAfrican landscapeswill help identifymanagement actions and thescales atwhich they aremost effective for slowing and reversingit (Bruce et al 2017 Campbell Kuehl Diarrassouba NrsquoGoran ampBoesch2011Redford1992)
Camera trap surveys arewell‐suitedas amethodology todoc‐umenttherichnessoffaunasandunderstanddielactivitypatterns
andhabitatpreferencesofmediumtolargeterrestrialmammalspe‐cies in dense forests (Ahumada et al 2011 Hedwig et al 2018Silveira Jacomo amp Diniz‐Filho 2003 Tobler Carrillo‐PercasteguiLeitePitmanMaresampPowell2008)Theyprovideacost‐effectiveefficient non‐invasive and replicable surveymethod (Ahumada etal2011RoveroampMarshall2009Tobleretal2008)Importantlythey removemuchof thehumanerror anduncertaintyassociatedwithothersurveytypessuchasdistancesamplingthroughlinetran‐sectsandinterviewswiththelocalpopulations(AhumadaHurtadoampLizcano2013Hedwigetal2018)thatareoftenbiasedtowardslarger‐bodied diurnal species and fail to detect rare and elusivenocturnalspecies(Srbek‐AraujoampChiarello2005)Theuseofstan‐dardisedcameratrappingmethodsandclassifyingspeciesintofunc‐tionalgroupssuchasbytrophiccategorylifehistorysocialstructureandbodysizeallowsmammalcommunities indifferentsitestobecomparedregardlessofdifferencesinspeciescomposition
Herewe investigate ifcamera trapsurveyscandiscerndiffer‐ences in community metrics of terrestrial larger‐bodied mammalassemblagesatdifferentsiteswithinthesameCentralAfricanpro‐tectedareaWeexaminemetricsof richness guildbody‐sizeandrelativeabundanceasmeasuredbytrappingratesandoccupancyofthetwomammalcommunitiessurveyedusingagridofcameratrapsateachsite
2emsp |emspMATERIAL S AND METHODS
Camera trap surveys were conducted at two sites approximately32km apart (at their closest proximity) within the Dja FaunalReserve(DFR)insouthernCameroonContiguousnaturalforesten‐compassesbothsitesandinterveningandsurroundinghabitat
21emsp|emspStudy area
TheDFRthelargestprotectedareainCameroon isapproximately5260km2 (3deg08prime589PrimeN 13deg00prime001PrimeE Figure 1) The Dja Riversurrounds 80 of the reserve acting as a partial buffer to humanencroachment and animal movement (Muchaal amp Ngandjui 1999)Thetopographywithinthereserveismadeupofround‐toppedhillsbetween600and800maslwithvalleysoneithersideofacentralridgelinethattraversesthereserveeasttowest(MINFOFampIUCN2015)Swampsareprevalent inthetributariesfeedingintotheDjaRiverThreemajorforesttypesoccurwithinthereserveterrafirmeforest(Sonkeacute1998)monodominantforest(Gilbertedendronsp)andseasonally inundated forests (DjuikouoDoucetNguembouLewisamp Sonkeacute 2010) There are four seasons a long rainy season fromAugusttoNovemberthelongdryseasonfromNovembertoMarchashortrainyseasonfromMarchtoMayandtheshortdryseasonis between June and July Average annual rainfall is c 1600mm(HijmansCameronParraJonesampJarvis2005)CommercialloggingwaslimitedandhasnowceasedOnlytraditionalhuntingisallowedwithin the Dja Faunal (Biosphere) Reserve and no fully protectedClassAspeciescanbetaken(RepublicofCameroon1994)However
emspensp emsp | emsp761Bruce et al
thehumanpopulationaroundthereserveisincreasingandindustriessuchasloggingrubberhydropowerandminingareproliferatingre‐sultinginincreaseddemandforbushmeatBothillegalnon‐traditionalsubsistenceandcommercialhuntingoccurwithinthereserve
22emsp|emspNorthern and southern sector sites
WesetupcameratrapgridsintheNorthern(management)Sector(centredon03deg13rsquo33rsquorsquoN12deg48rsquo18rsquorsquoE)betweenNovember2015andMay 2016 and the Southern (management) Sector (02deg59rsquo37rsquorsquoN13deg07rsquo43rsquorsquoE)oftheDFRbetweenMayandJune2017(Figure1)ThecameratrapgridwithintheNorthernSectorwasplacedusingthenorthernprotectedareaboundaryasanapproximatebaselineref‐erenceThecamerasweresetovera rangeofc31 toc159kmfromtheboundaryof the reservewithanaveragedistanceof95(SEplusmn39)kmfromtheboundaryCameraswereplacedonaverage123(SEplusmn38)kmfromthenearestsettlementswitharangeofbe‐tweenc6and188kmTheNorthernSectorof theDjapresentsagenerallyhigherandmoreuniformelevation(662ndash720masl)thanthe Southern Sector (563ndash689masl) Watercourses are sparserand swamp habitat less common within this management sectorCorrespondinglythenortherncameratrapstationswereonaver‐agemoredistantfromthenearestwatercourse(c261km)andonlytwonortherncameraswereplacedinswamphabitat
Thecameras in theSouthernSectorgridwereplacedonaver‐age123(SEplusmn38)kmoverarangeofc57ndash19kmfromthereserveboundary and were between c 77 and 22km from the nearesthuman settlementwith anaveragedistanceof155 (SEplusmn37) kmThetopographywithinthesoutherncameratrapgridismorecom‐plexwithagreaterelevationalvariationThegreaterprevalenceoflowlandareasresultedinmoreswamphabitat(fivecamerasplacedwithin 50m of swamp habitats) and cameras being on averageplacedclosertowatercourses(c06km)
23emsp|emspcamera trap surveys
Forty cameraswere placed at each localitywith a 2km spacingbetweeneachcamera(Ahumadaetal2011)(Figure1)Eachgridoperatedlongenoughtoachieveatleast1000cameratrapdaysofsamplingeffort(OrsquoBrienKinnairdampWibisono2003)WeusedGlobalPositioningSystemreceiverstolocatethegridpointsAsin‐gle camerawas positioned 30ndash45cm above ground level within200m of each point aimed at a game trail that provided suffi‐cient fieldofviewtocapture lateral full‐body imagesofsmall tomedium‐sizedmammals Siteswere selected based on the pres‐enceofagametrail(Aminetal2015)tomaximisetheprobabil‐ityofobtainingusefulphotographs(TEAM2008)andasuitabletreeallowing thecamera tobepositioned facingeithernorthor
F I G U R E 1 emspLocationoftheDjaFaunalReserveCameroon(a)andthelocationofcameratrapgridsintheNorthernandSouthernsectors(b)Managementsectorsareingrey[Colourfigurecanbeviewedatwileyonlinelibrarycom]
762emsp |emsp emspensp Bruce et al
south tominimise the impacts of sunrise and sunset on cameraperformance
We used three different camera models across the two grids(BushnellAggressorReconyxHC500 andCuddebackLong rangeIRE2)Detectionrangewasatleast25mwitheitheratwo‐seconddelay(Bushnell‐2015NorthernSectorsurvey)orone‐seconddelay(ReconyxCuddebackandBushnell‐2017SouthernSectorsurvey)ThreeconsecutiveimagesweretakenpertriggerLowglowinfraredflashlightingwasusedtominimisetheriskofstartlinganimalsThefulllistofsettingsforeachcameracanbefoundinAnnex1
24emsp|emspNatural mammal fauna
Thereserveisreportedtocontain109speciesofmammalofwhich35speciesareterrestrialandhaveabodyweightgt05kg(Kingdon2015) Currently the only baseline data for populations for thesespecieswithinthereservecomefromencounterratesfromrangerpatrolsanddistancesamplingthroughlinetransectsurveys(DupainBombomeampVanElsacker2003MINFOFampIUCN2015WilliamsonampUsongo1995)
25emsp|emspAssessment of differences in human activity
Toassesstherelativedifferencesinhumanactivityincludinghunt‐ing between theNorthern and Southern Sectorwhere the twosites were located we evaluated trends from multiple sourcesEvidence of human sign was recorded on 1‐kilometre line tran‐sectsduringafullfaunalinventoryoftheDFR(Bruceetal2018)TransectsareoftenusedtomonitorthetrendsofhumanimpactsinCentralAfricanforests(Kuumlhletal2008)Therewereatotalof86and76transectscoveringadistanceof916and807kmcom‐pleted intheNorthernSectorandSouthernSector respectivelyEncountersofhumansignbetweenJanuary2016andSeptember2017byMinistryofForestsandWildlife(MINFOF)rangerpatrolswhorecorddatausingSpatialMonitoringAndReportingToolde‐viceswerealsoused(ZSLampMINFOF2017a2017b)Abufferof2kmwassetaroundeachcameraandthesignwithinthisareawasconvertedintotheamountofhumansignperkm2Thisbufferwasusedtocounteractunequalsurveyeffortwithinthesectorspos‐siblyduetoecoguardsbeingrequiredtobepresentataresearchstation in theNorthernSectorat thebottomof thecamera trapgrid
Transects provide a more objective measure of hunting pres‐sureastheyuseastandardisedmethodologyandteamcompositioncompared to rangerpatrolsTransectsarenotbiasedby followingtrailsorotherpathsofleastresistancethataffectstheprobabilityofhumansignbeingdetected
26emsp|emspData analysis
WeusedExiv2software(Huggel2012)toextractEXIFinformationfromeachphotograph(imagenamedateandtime)SpeciesofanimalinthephotographswereidentifiedwhenpossibleThesedatawere
compiled in an Excel spreadsheet (Microsoft Office ProfessionalPlus2016Version1809)andanalysedwithsoftwaredevelopedbyat ZSL (CameraTrapAnalysis Package [CTAP]) (DaveyWacherampAmin2017)
Weonlyconsideredterrestrialmammalspeciesthathaveanesti‐matedaveragemassgreaterthan05kg(medium‐to‐largemammals)fortheanalysesbecausetheyarethemaintargetgroupforcameratrapsplacedatgroundlevelSmallermammalsinducesamplingerrorthroughareducedlikelihoodofdetectionbythecameratraprsquosther‐malsensorandaccurateidentificationofsmallmammalstospecieslevelisdifficultfromcameratrapsset‐upformedium‐to‐largemam‐mals(Tobleretal2008)
We calculated rarified species accumulation curves and esti‐matedthemedium‐to‐largeterrestrialmammalspeciesrichnessforeachsectorusingtheZSLCTAPtool
We calculated Simpsonrsquos diversity index and ShannonndashWeinerdiversity index foreach sector fromspeciesdaily trap ratesusingpackageveganinRstatisticalsoftware(Oksanen2015)Simpsonrsquosdiversityindexismostsensitivetochangesinmorecommonhighlyabundant species while ShannonndashWeiner diversity index is mostsensitivetochangesinrarelessabundantspecies(Magurran2005)
Wecalculatedthenumberofindependentphotographiceventsper100trapdaysasarelativeabundanceindex(RAI)foreachspeciesWedefinedanldquoeventrdquoasanysequenceforagivenspeciesoccurringafteranintervalofge60minfromthepreviousthree‐imagesequenceof that species to ensure that species events were independent(Aminetal2015Tobleretal2008)Theeventswereautomati‐cally screenedby theZSLCTAPsoftwareWecalculated the95confidenceintervalsusingthebootstrapmethod(EfronampTibshirani1994)andconsiderednon‐overlappingconfidenceintervalsasindic‐ativeofasignificantdifferenceinRAIbetweenmanagementsectorsWeassumethatthecameratrappingratescalculatedastheRAIre‐flectactualrelativeabundanceasinRoveroandMarshall(2009)
We used single‐season occupancy analysis (MacKenzie et al2006) where assumptions and data quality allowed to estimatethe proportion of area occupied by a species within each gridOccupancyestimateswerecorrectedbydetectionprobability (iethelikelihoodthataspecieswasdetectedwhenpresent)andthere‐foreprovideamore rigorous indexofabundance forbothwithinandbetweenspeciescomparisonsThishoweverislimitedtospe‐ciesgeneratingadequatedatasetswherecameraspacingisgreaterthanthespecieshomerangeandoccupancyisnotconfoundedbychanges in the home range (Efford ampDawson 2012) For all theoccupancyanalyseswegenerated1110‐daysamplingoccasionsThismeanttheNorthernSectordataweretruncatedtomatchthenumberofoccasionsavailableforanalysis intheSouthernSectorWetestedforsignificantdifferencesinspeciesoccupancybetweenthe Northern and Southern sectors using the ldquoWaldrdquo parametricstatisticaltestasitisknowntobeanindependentandrobustmea‐sureofdifference(Aminetal2015)withplt005consideredtobesignificant
We alsomodelled occupancy as a function of site covariatesdistance to the protected area boundary in kilometres (D) and
emspensp emsp | emsp763Bruce et al
management sector (M) using the ldquounmarkedrdquo (Fiske amp Chandler2011) software package in R We treated detection probabilityas a constant and evaluated all covariate combinations ψ ()p()ψ (D)p() ψ (M)p() ψ (DM)p() ψ (D+M) p() For covariate anal‐ysis tocompare themanagementsectorswealso implementedaRoylendashNicholsmodel(2003)whichtakesintoaccountthenumberofindividualsatasiteinfluencingdetectionprobabilityandthusoc‐cupancyTheselectionofRoylendashNicholsmodelaboveasingle‐sea‐sonmodelforaspecieswouldprovidefurthersupportthatspeciesabundance was significantly different between the managementsectorsWe rankedmodelsbyAkaikersquos informationcriteria (AIC)andmodels that had a delta AIC of lt2were considered to be acompetingmodel(BurnhamampAnderson2002)Thec‐hatandchi‐squared values to assessmodel dispersionwere generated usingtheMackenzie andBailey (2004) goodness‐of‐fit testwhichwasconducted using 1000 simulations for eachmodelModels witha c‐hatgt2were rejectedas theywere regardedasoverdispersed(Farrisetal2015)
3emsp |emspRESULTS
Weaccumulated3725operationalcameratrapdays(mean91dayscamera)intheNorthernSectorand3371operationalcameratrapdays(mean84dayscamera)intheSouthernSectorIntheNorthernSector grid ten cameras were lost or damaged by people or el‐ephants and somemalfunctioned The Southern Sector only hadeightcamerasfailduetothesameissuesaswellastoleoparddam‐age In total 16 cameraswere excluded fromoccupancy analysisduetobeingoperationalforlt80ofoccasions
31emsp|emspRelative assessment of human sign
Overallhumanpressureasmeasuredbyhumansignwithinthere‐servewasmoreabundant intheNorthernSectorcomparedtotheSouthern Sector Encounter rate of human sign on transects was154km in theNorthern Sector three times higher than 049kmintheSouthernSectorAsimilarpatternwasobserved inthedatagatheredbyMINFOF rangers TheNorthern Sector had a densityofhuntingsignof087km2 withintheareaofthegridincludingthe2km buffer compared to 008km2 in the Southern Sector Giventhatseveralsignsmeasuredarecloselyassociatedwithhuntingac‐tivitysuchassnaresandcartridgesweassumethathuntingactiv‐ityisonaveragehigherintheNorthernSectorthantheSouthernSector
32emsp|emspSpecies richness
A total of 26 medium‐to‐large terrestrial mammal species werephotographedintheNorthernSectorand31medium‐to‐largeter‐restrialmammalspeciesintheSouthernSector(Table1)Wealsore‐cordedfivearborealmammalspeciesthatwerenotthetargetofthissurvey (Table1)Fourmedium‐to‐large terrestrialmammalspecies
expected to occur in the surveyed habitats according to availableIUCN distribution maps and literature were not detected by thecameratrapsurveysineithersector(Table1)
The species accumulation curves for medium‐to‐large terres‐trialmammal species showmore species detected per unit effortin theSouthernSector (Figure2)Thediversity indicesweremar‐ginally lower in the Northern Sector (Simpsons=072 ShannonndashWeiner=179)comparedtotheSouthernSector(Simpsons=078ShannonndashWeiner=208)
33emsp|emspCommunity structure
CommunitystructureofmammalsdifferedbetweentheNorthernSectorandSouthernSectorsites(Figures3and4)withmorespe‐ciesbeingencounteredforthreeoutofthefourguilds(herbivoresinsectivoresandcarnivores)intheSouthernSectorThemostfre‐quentlyencounteredguild inbothsectorswasherbivore (14spe‐ciesintheSouthernSectorand13intheNorthernSector)followedbyomnivore(seveninbothsectors)carnivore(sixintheSouthernSector four in theNorthernSector) and insectivore (three in theSouthernSector two in theNorthernSector)Overallacross theguilds trapping rates for lowerbodymassspecieswerehigher inthe Northern Sector A marked difference was the higher trap‐pingratesofherbivoresandomnivoreswithbodymassgt10kg intheSouthernSector (Figure4) compared to theNorthernSector(Figure3)
34emsp|emspForest antelopes
Werecorded4495independentphotographiceventsoftenspe‐ciesof forest antelopesTheblueduiker (Philantomba monticolaThunberg 1789) was the most frequently encountered forestantelope species across both camera trap grids (RAI=527) fol‐lowed by Petersrsquo duiker (Cephalophus callipygus Peters 1876)(RAI=412) and Bay duiker (Cephalophus dorsalis Gray 1846)(RAI=747) The rest of the forest antelopeswere relatively in‐frequently encounteredwith a global trapping rate of less thanfiveThedisturbance‐sensitivewhite‐belliedduiker(Hart2013b)wasonlyencountered in theSouthernSector (RAI=395 [lower95 confidence limit (LCL)=214 upper 95 confidence limit(UCL)=611])TrappingratesweresignificantlyhigherforPeterrsquosduiker in the Southern Sector displaying a fivefold increase be‐tween sectors (Table 1) Peterrsquos duiker occupancy was also sig‐nificantlyhigherintheSouthernSectorcomparedtotheNorthernSector (p=002 Table 2) Therewere no significant differencesin trapping rates between the two sectors forBatersquos pygmy an‐telope (Neotragus batesi de Winton 1903) bay duiker bongo(Tragelaphus eurycerusOgilbyi1837)sitatunga (Tragelaphus spe-kiiSpeke1863)andblack‐frontedduiker(Cephalophus nigrifrons Gray1871)Occupancyvaluesforbayduikerblack‐frontedduikerandBatersquospygmyantelopedidnotdiffersignificantlybetweenthesectorsTherewereinsufficientdetectionsoftheotherspeciestomodeloccupancy
764emsp |emsp emspensp Bruce et al
TA B L E 1 emspMammalspeciespredictedtoberecordedintheNorthernandSouthern(management)sectorsofDjaFaunalReserveCameroon
Order Species IUCN Status HabitatNorthern sector RAI (LCLndashUCL)
Southern sector RAI (LCLndashUCL)
Afrosoricida Giantottershrew(Potamogale velox Du Chaillu1860)
LC Wetland Notdetected Notdetected
Carnivora Africangoldencat(Profelis aurataTemminck1827)a
VU Forest Notdetected 058(027ndash091)
Carnivora Leopard(Panthera pardusLinnaeus1758)a
NT Mixed Notdetected 083(032ndash145)
Carnivora Marshmongoose(Atilax paludinosusCuvier1829)a
LC Wetland 056(033ndash082)b 009(0ndash02)b
Carnivora Black‐leggedmongoose(Bdeogale nigripesPucheran1855)a
LC Forest 183(079ndash314) 371(263ndash484)
Carnivora Camerooncusimanse(Crossarchus platycephalusGoldman1984)a
LC Forest 183(124ndash247) 083(046ndash127)
Carnivora Long‐nosedmongoose(Herpestes nasodeWinton1901)a
LC Forest 102(053ndash160) 089(009ndash227)
Carnivora Africanpalmcivet(Nandinia binotataGray1830)a
LC Forest 113(071ndash16) 089(052ndash13)
Carnivora Servalinegenet(Genetta servalinaPucheran1855)a
LC Forest 325(239ndash416) 214(142ndash295)
Carnivora Large‐spottedgenet(Genetta maculata Gray1830)
LC Forest Notdetected Notdetected
Carnivora CentralAfricanoyan(Poiana richardsoniiThomson1842)c
LC Forest Notdetected 003(003ndash009)
Cetartiodactyla Batesspygmyantelope(Neotragus batesideWinton1903)a
LC Forest 04(011ndash078) 036(015ndash059)
Cetartiodactyla Forestbuffalo(Syncerus cafferSparrmansubspnanus1779)a
EN Forest 008(0ndash024) 006(0ndash019)
Cetartiodactyla Petersduiker(Cephalophus callipygusPeters1876)a
LC Forest 141(838ndash2071)b 7146 (4963ndash9641)b
Cetartiodactyla Bayduiker(Cephalophus dorsalisGray1846)a
LC Forest 668(44ndash935) 834(492ndash1228)
Cetartiodactyla White‐belliedduiker(Cephalophus leucogastersubsp leucogasterGray1873)
LC Forest Notdetected 395(214ndash611)
Cetartiodactyla Black‐frontedduiker(Cephalophus nigrifronsGray1871)a
LC Forest 086(003ndash246) 05(006ndash114)
Cetartiodactyla Yellow‐backedduiker(Cephalophus silvicultorAfzelius1815)a
LC Forest 37(225ndash554) 555(354ndash794)
Cetartiodactyla Blueduiker(Philantomba monticolaThunberg1789)a
LC Forest 6164(4602ndash788) 4298(315ndash5561)
Cetartiodactyla Bongo(Tragelaphus eurycerusOgilbyi1837)a
NT Forest 005(0ndash014) 006(0ndash015)
Cetartiodactyla Sitatunga(Tragelaphus spekiiSpeke1863)a
LC Wetland 024(005ndash048) 009(0ndash024)
Cetartiodactyla Redriverhog(Potamochoerus porcusLinnaeus1758)a
LC Woodland 161(102ndash228)b 7(336ndash1304)b
Cetartiodactyla Giantforesthog(Hylochoerus mein-ertzhageniThomas1904)
LC Forest Notdetected Notdetected
Cetartiodactyla Waterchevrotain(Hyemoschus aquaticusOgilby1841)a
LC Forest 03(0ndash075)b 46(192ndash799)b
(Continues)
emspensp emsp | emsp765Bruce et al
35emsp|emspCarnivore
ThecarnivorecommunitydifferedinRAIandstructurebetweenthetwosectorsFelidswerenotdetectedatallintheNorthernSectorbutboth leopard (Panthera pardusLinneaus1758)andgoldencat(Profelis aurata Temminck1827)werepresentintheSouthernSector
(Table1)AmongtheHerpestidaeblack‐leggedmongoose(Bdeogale nigripes Pucheran1855) showeda significantlyhigheroccupancy(p =gt001)intheSouthernSectorbuttrappingrateslackedsignifi‐cantdifference (RAI=371 [LCL=263UCL=484])comparedtothe Northern Sector (RAI=183 [LCL=079 UCL=314])Marshmongoose(Atilax paludinosusCuvier1829)hadsignificantlyhigher
Order Species IUCN Status HabitatNorthern sector RAI (LCLndashUCL)
Southern sector RAI (LCLndashUCL)
Hyracoidea Westerntreehyrax(Dendrohyrax dorsalis Fraser1855)
LC Forest Notdetected Detected
Pholidota White‐belliedpangolin(Phataginus tricuspisRafinesque1821)a
VU Forest 062(029ndash1) 08(044ndash121)
Pholidota Giantpangolin(Smutsia giganteaIlliger1815)a
VU Forest 027(008ndash052) 068(038ndash101)
Primates Agilemangabey(Cercocebus agilisMilne‐Edwards1886)a
LC Forest 035(013ndash059) 448(265ndash682)
Primates Moustachedguenon(Cercopithecus cephusLinnaeus1758)c
LC Forest Detected Notdetected
Primates Greaterspot‐nosedguenon(Cercopithecus nictitansLinnaeus1766)c
LC Forest Detected Detected
Primates Blackcolobus(Colobus satanasWaterhouse1838)c
VU Forest Notdetected Detected
Primates Galagospc ‐ Detected Notdetected
Primates Mandrill(Mandrillus sphinxLinnaeus1758)a
VU Forest 005(0ndash013) 006(0ndash019)
Primates Westernlowlandgorilla(Gorilla gorillaSavagesubspgorilla1847)a
CR Forest 016(003ndash031) 044(02ndash073)
Primates Centralchimpanzee(Pan troglodytesBlumenbachsubsptroglodytes1799)a
EN Forest 161(077ndash29)b 457(314ndash617)b
Proboscidea Forestelephant(Loxodonta cyclotisMatschie1900)a
VU Mixed 086(046ndash135) 19(086ndash329)
Rodentia Africanbrush‐tailedporcupine(Atherurus africanusGray1842)a
LC Forest 1753(1142ndash2446) 762(464ndash1145)
Rodentia Eminspouchedrat(Cricetomys eminiWroughton1910)a
LC Forest 32(2358ndash4141)b 756(341ndash1465)b
Rodentia Greatercanerat(Thryonomys swinderi-anus Temminck1827)
LC Wetland Notdetected Notdetected
Rodentia LadyBurtonsropesquirrel(Funisciurus isabellaGray1862)c
LC Forest Detected Detected
Rodentia Fire‐footedropesquirrel(Funisciurus pyrropusCuvier1833)c
LC Forest Detected Detected
Rodentia Africangiantsquirrel(Protoxerus stangeriWaterhouse1842)c
LC Forest Detected Detected
Tubulidentata Aardvark(Orycteropus aferPallas1766)a LC Mixed Notdetected 009(005ndash019)
NotesForeachsectorandspeciesthatwasdetectedwepresentthemeanand95confidencelimits(inbrackets)ofthenumberofindependentphotographiceventspertrapdaytimes100Trappingrateswereonlycalculatedformedium‐to‐largeterrestrialmammalsduetoinconsistentdetectionprobabilitieswithotherspeciesIUCNstatuscriticallyendangered(CR)endangered(EN)vulnerable(VU)nearthreatened(NT)leastconcern(LC)aIndicatesaspeciesthatwasincludedintherarefactionanalysisaccordingtothedefinitiongiveinthedataanalysissectionofthemethodsbIndicatesthattheRAIconfidenceintervalsdonotoverlapandcanbeconsideredsignificantlydifferentcSignifiesanarborealspecies
TA B L E 1 emsp (Continued)
766emsp |emsp emspensp Bruce et al
F I G U R E 2 emspRarefiedspeciesaccumulationcurvesformedium‐to‐largeterrestrialmammalsintheNorthernandSouthernsectorsofDjaFaunalReserveCameroon
F I G U R E 3 emspDistributionofmedium‐to‐largeterrestrialmammalspeciesintheNorthernSectoroftheDjaFaunalReserveCameroononthebasisofbodysizeandtrophiccategoryEachcirclerepresentsaspeciesinfunctionalspaceSizeofthecircleproportionaltothetrappingrateforthatspecies
emspensp emsp | emsp767Bruce et al
trappingrateintheNorthernSector(Table1)butlackedsufficientdetectionstoreliablycalculateoccupancyAbundanceofCamerooncusimanse(Crossarchus platycephalusGoldman1984)didnotdiffersignificantlybetweenthetwosectors(NorthernSectorRAI=183[LCL=124 UCL=247 ψ=075] Southern Sector RAI=083[LCL=046UCL=127]ψ=056p=028)
36emsp|emspElephants great apes and giant pangolin (illegal wildlife trade targets)
Amongtheterrestrialmammalstargetedbytheillegalwildlifetradespecifically central chimpanzee (Pan troglodytes Blumenbachsubsp troglodytes 1799) western lowland gorilla (Gorilla gorillaSavagesubsp gorilla1847)forestelephantgiantpangolin(Smutsia gigantea Illiger 1815) and white‐bellied pangolin (Phataginus tri-cuspis Rafinesque 1821) only central chimpanzee displayed asignificant difference in RAI between the management sectors(Northern Sector RAI=161 [LCL=077 UCL=29] SouthernSector RAI=457 [LCL=314 UCL=617]) However there wasnosignificantdifferenceinmeanoccupancybetweenthetwosec‐tors (p=074) Giant pangolin displayed the greatest differencewithathreefoldincreaseinRAIfrom027[LCL=008UCL=052]in the Northern Sector to 068 [LCL=038 UCL=101] in theSouthernSectorbutthiswasnotsignificantduetotheoverlapping
confidencelimitsTheRAIsandwhereappropriateoccupancyofforestelephantwesternlowlandgorillaandwhite‐belliedpangolinwerenotsignificantlyhigher intheSouthernSectorcomparedtotheNorthernSector(Tables12and12)
37emsp|emspOther bushmeat‐targeted species
Eminrsquospouchedrat(Cricetomys eminiWroughton1910)wasmoreabundantasmeasuredbybothoccupancy(pge001)andtrapratesintheNorthernSectorcomparedtotheSouthernSector(Table1)Africanbrush‐tailedporcupine(Atherurus africanusGray1842)didnothavesignificantdifferencesinRAIbetweenthemanagementsectors but occupancywas significantly higher in theNorthernSector (pge004) In comparison the larger‐bodied red river hog(Potamochoerus porcus Linneaus1758)wasmore frequentlyen‐countered as measured by both species abundance metrics intheSouthernSector(RAI=7[LCL=336UCL=1304]ψ=091)compared to the Northern Sector (RAI=161 [LCL=102UCL=228]ψ=065(p=004)
38emsp|emspSpecies occupancy with covariates
Therewasatotalof15speciesthathadsufficientdetectionstomodeloccupancywithinteractingsitecovariates(distancetoparkboundary
F I G U R E 4 emspDistributionofmedium‐to‐largeterrestrialmammalspeciesintheSouthernSectoroftheDjaFaunalReserveCameroononthebasisofbodysizeandtrophiccategoryEachcirclerepresentsaspeciesinfunctionalspaceSizeofthecircleproportionaltothetrappingrateforthatspecies
768emsp |emsp emspensp Bruce et al
TAB
LE 2
emspNullmeanoccupancy(ψ)anddetection(p)probabilitieswithstandarderrorpresentedinbracketsfortheNorthernSectorandSouthernSector
Spec
ies
Nor
ther
n se
ctor
(ψ)
Nor
ther
n se
ctor
(p)
Sout
hern
sec
tor
(ψ)
Sout
hern
sec
tor
(p)
Mod
elBe
tamdash
Para
met
er
chos
enLo
wer
95
be
taU
pper
95
be
taC‐
hat v
alue
Chi‐s
quar
ep
valu
e
Certiodactyla
Batesrsquospygmy
antelope
022(01)
015(006)
[026]
ndashNull
ndashndash
ndashndash
ndash
Bayduiker
091(006)
04(003)
087(006)
04(003)
DRN
lam(DistanceSTD)
000
6356
808
043
3356
50
930
25
Black‐fronted
duiker
01(006)
036(01)
015(006)
025(008)
Null
ndashndash
ndashndash
ndash
Blueduiker
097(003)
082(002)
1(0)
1(0)
DRN
lam(DistanceSTD)
002
0135
490
3637
492
021
024
Petersrsquoduiker
083(007)
a056(003)
1(0)a
1(0)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus07435528
003
6592
430
004
03
Waterchevrotain
[007]
ndash04(008)
045(005)
ndashndash
ndashndash
ndashndash
White‐bellied
duiker
ndashndash
072(008)
031(003)
Null
ndashndash
ndashndash
ndash
Yellow‐backed
duiker
084(008)
027(003)
086(007)
039(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
010
8837
21
0251
104
069
021
Redriverhog
065(011)
a021(003)
091(006)
a033(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus12560347
minus01352547
027
044
Proboscidae
Forestelephant
067(015)
014(004)
063(013)
014(004)
Null
ndashndash
ndashndash
ndash
Primates
Central
chimpanzee
077(014)
015(004)
082(007)
035(003)
SRN
lam(sectorSouthern)
037
3686
91
4429
314
03
039
Westernlowland
goril
la[007]
ndash045(017)
01(004)
Null
ndashndash
ndashndash
ndash
Philodota
Giantpangolin
[02]
ndash061(016)
011(004)
Null
ndashndash
ndashndash
ndash
White‐bellied
pangolin
045(016)
012(005)
063(017)
011(003)
DSoccu
psi(DistanceSTDsec
torSouthern)
minus48425115
minus1910401
022
06
Rodentia
African
brush‐tailed
porcupine
098(003)
a057(003)
084(006)
a042(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus10008123
minus01586108
042
071
Eminrsquospouched
rat
1(0)a
1(0)
079(007)
a038(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus095574568
minus01390762
021
075
Carnivora
(Con
tinue
s)
emspensp emsp | emsp769Bruce et al
and management sector Table 2) Forest elephant black‐frontedduikerand long‐nosedmongoose (Herpestes nasodeWinton1901)lackedamodel thathadanAICdifferenceofgt2 therefore theco‐variatemodelswerenotsignificantlydifferent to thenullmodel forthese species Elevenof 15 species had aRoylendashNicholsmodel se‐lectedasthelowestAICvaluesuggestingadifferenceinthenumberofindividualswassignificantlyinfluencingdetectionprobabilitiesandthereforeoccupancy
RoylendashNichols models accounted for occupancy being signifi‐cantlyhigherindifferingmanagementsectorswithnointeractionofdistancetotheprotectedareaboundaryforthreespeciesCamerooncusimanse had higher occupancy in the Northern Sector In con‐trast central chimpanzee and black‐legged mongoose had signifi‐cantlyloweroccupancywithintheNorthernSectorcomparedtotheSouthernSector(Figure5)
African brush‐tailed porcupine Eminrsquos pouched rat and servalinegenet(Genetta servalinaPucheran1855)hadasynergisticRoylendashNicholsmodelselectedasthemostsupportedTheprobabilityofsiteoccupancyslightlyincreasedwithdistancetotheboundaryandwasoverallhigherin theNorthernSector butdeclinedwithdistance to theboundary intheSouthernSector(Figure6)BothPetersrsquoduikerandredriverhogalsodisplayedthispatternofoccupancybuthadamuchgreaterincreaseinoccupancyintheNorthernSectorandhadhigheroccupancyoverallintheSouthernSector(Figure6)Incontrastyellow‐backedduiker(Cephalophus silvicultorAfezilus1815)wastheonlyspeciestodemonstrateanincreaseinoccupancywithdistancetotheboundaryintheSouthernSectorwhiledecliningintheNorthernSectorHoweversimilartootherlargerspeciesoccupancywashigherintheSouthernSector(Figure6)
With regard to the remainingduiker speciesmodelled aRoylendashNicholsmodelwithdistancetotheprotectedareaboundarywasiden‐tifiedasthemostappropriateTheprobabilityofasitebeingoccupiedbyblueduikerandbayduikerincreasedwithdistancetotheboundarywith no discernible difference betweenmanagement sectors in themodel(Figure7)
White‐belliedpangolinhadasingle‐seasonoccupancymodelse‐lectedsuggestingdifferences inabundancebetweenthemanage‐mentsectorsdidnotaffectdetectionprobabilitiesTheprobabilityofasitebeingoccupiedbywhite‐belliedpangolin increasedintheNorthernSectoranddeclinedintheSouthernSectorwithincreasingdistancetotheboundary(Figure8)
Seven speciesweredetectedonly inone sectoror lacked suffi‐cientdetectionsinonesectortoreliablymodeloccupancyacrossbothmanagement sectors Therefore only the effect of distance to theboundarycouldbemodelledThesewereAfricangoldencatwesternlowlandgorillawhite‐belliedduikergiantpangolinAfricanpalmcivet(Nandinia binotata Gray 1830) Batesrsquos pygmy antelope and waterchevrotain (Hymeoschus aquaticusOgilby 1841)African palm civetwastheonlyspeciestohavedistancetotheboundaryselectedastheoptimummodel to explain occupancy as occupancy increasedwithdistance from the boundary of the protected area (Table 2)All theremainingspecieshadthenullmodelselectedastheoptimummodelaccordingtoAICcriteria (Table2)Howeverdistancetothebound‐arywaswithinlt2AICforthesespeciessuggestingthatasignificantSp
ecie
sN
orth
ern
sect
or (ψ
)N
orth
ern
sect
or (p
)So
uthe
rn s
ecto
r (ψ
)So
uthe
rn s
ecto
r (p
)M
odel
Beta
mdashPa
ram
eter
ch
osen
Low
er 9
5
beta
Upp
er 9
5
beta
C‐ha
t val
ueCh
i‐squ
arep
va
lue
Africangolden
cat
ndashndash
041(013)
013(004)
Null
ndashndash
ndashndash
ndash
Africanpalm
civet
[047]
ndash073(017)
012(003)
DOccu
psi(DistanceSTD)
minus8177158
Inf
197
008
Black‐legged
mongoose
047(01)a
025(004)
082(008)
a031(003)
SRN
lam(sectorSouthern)
028
0266
31
4627
420
011
058
Cameroon
cusimanse
075(009)
027(004)
056(015)
012(004)
SRN
lam(sectorSouthern)
minus1808131
minus05098939
005
073
Long‐nosed
mongoose
055(012)
a02(004)
015(006)
a027(007)
Null
ndashndash
ndashndash
ndash
Servalinegenet
092(006)
035(003)
08(009)
02(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus09202819
003
5821
570
50
26
Not
esNaiumlveoccupancyvaluesarepresentedinsquarebracketsforspecieswithadetectionprobabilitylt01TheoptimummodelchosenbyAkaikersquosinformationcriteriaforeachspeciesgeneratingsuf‐
ficientoccupancyvaluesinbothsectorswiththeBetaparameteranditisrespectivelowerandupper95confidencelimitsisshownandtheassociatedc‐hatandchi‐squaredp
val
ue
DdistancetoboundarySmanagementsectorRNRoylendashNicholsmodelOccuMckenziesingle‐seasonoccupancymodesynergisticinteraction
a IndicatesasignificantdifferenceinoccupancybetweensectorsasmeasuredbytheWaldteststatistic
TAB
LE 2
emsp(Continued)
770emsp |emsp emspensp Bruce et al
relationshipwithdistancetotheboundarycouldbeinfluencingoccu‐pancyIntheSouthernSectortheoccupancyincreasedwithdistanceto theboundary forwestern lowlandgorillaandgiantpangolinbutdecreasedforAfricangoldencatwhite‐belliedduikerandwaterchev‐rotainIntheNorthernSectoroccupancyincreasedwithdistancetotheboundaryforBatesrsquospygmyantelope
4emsp |emspDISCUSSION
Thecomparisonofthetwosurveysconfirmsthatstandardcameratrap surveys and derived metrics of presenceabsence trappingrates andoccupancy candiscern confidentdifferences in ground‐dwellingmammalcommunitiesinCentralAfricanforests
41emsp|emspCamera trap surveys for documenting species
Thecomparativeefficacyofcamera traps for surveyingmediumto large ground‐dwelling mammals in the DFR is indicated byobservationratesandverifiabilityofrecordsespeciallyofelusivesmallerandnocturnalspeciesForexamplethedirectencounterraterecordedbyrangersonpatrolthroughouttheentirereserveover a nine‐month period is much lower than the combinednumberofindependentphotographiceventsinbothmanagementsectors (ZSL amp MINFOF 2017b) even for relatively largeconspicuous species such as forest elephant (96 photographiceventscomparedto29directencounters)andcentralchimpanzee(204 independent photographic events compared to 23 directencounters)Methodologiessuchascameratrapping therefore
provideimportantbaselinedatathatwhenrepeatedthroughtimeusingastandardisedprotocolcanallowatleasttrendsinrelativeabundanceindicestobemonitored
42emsp|emspCamera trap surveys for comparing assemblages among sites
Despitebeingseparatedbyonlyc32kmthemammalcommunitiesbetween the twocamera trapgridsdisplayedmarkeddifferencesThiswasthecaseeventhoughbothgridshadlowShannonndashWeinerandSimpsonsdiversityindicesduetothedominanceofthreeorfourspeciesineachcameratrapgridSignificantdifferencesamongthesiteswere observed for the trapping rates of species of differentsizesbetweensectorsSmaller‐bodiedspecieswithintheherbivoreand omnivore guilds were more prevalent within the NorthernSector (Figure 2) Trapping rates and occupancy values for smallcarnivoresarealsolowerintheSouthernSectorThiscouldbeduetothedifficultyofidentifyingmorphologicallysimilarspeciessuchasmarshmongooseandlong‐nosedmongoose(Bahaa‐el‐dinetal2013 Ray 1997) in infrared imagery with single cameras Thereweremoreunidentifiablemongooseeventsthatwereclassifiedtoafamilylevel―66224intheSouthernSectorcomparedto29156intheNorthernSectorofallcombinedmongooseevents
43emsp|emspThe potential impact of seasonality on estimates derived from camera traps
Due to logistical and financial constraints the surveys could notberuninthesameseasonThishasthepotentialtoaffecttrapping
F I G U R E 5 emspChangeintheprobabilityofoccupancyforblack‐leggedmongoosecentralchimpanzeeandCamerooncusimansewithmanagementsectoraccordingtoaRoylendashNicholsmodel
emspensp emsp | emsp771Bruce et al
rates and occupancy for specieswith larger home ranges becausewhenspeciesarewide‐rangingoccupancycanproveineffectiveformeasuring relative abundance Forest elephants (Blake 2002) andgreatapesareknowntodisplayseasonalshiftsintheirhabitatusageover great distances in response to increased fruit availability andprecipitation(HeadRobbinsMundryMakagaampBoesch2012)Thiscouldalsoinfluenceothergregariousspeciessuchasredriverhogthatarealsothoughttooccasionallydisplaysimilaraggregationsandmovementsinresponsetomastingevents(LeslieampHuffman2015)However as both red river hog and chimpanzee had significantlyhigherRAIandhigheroccupancywithvariabledetectionprobabilityaccording to the number of individuals incorporated this supports
thepossibilitythatthesespeciesarefavouringtheSouthernSectorIfmanagersareable toestablishwhetherwide‐rangingspeciesarepredictably moving to known areas within the reserve they canrespondinamannerthatprovidesenhancedprotectiontovulnerablewildlifepopulations in concentration areasAsmost species in thissurveylikelyhaveasmallerhomerangethantheinter‐trapdistanceand display fixed territories it can be regarded as appropriate tocompare occupancy values as the extent of overlap of territorieswithin the two surveys are unlikely to change in such away as toaffecttheresultsFuturestudieswouldbenefitfromtryingtomatchcameratrapsurveysseasonallytotryandclarifytheissueofseasonalshiftsinhabitatusagewithintheDFR
F I G U R E 6 emspChangeintheprobabilityofoccupancyforAfricanbrush‐tailedporcupineEminspouchedratredriverhogservalinegenetPetersrsquoduikerandyellow‐backedduikerwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
772emsp |emsp emspensp Bruce et al
F I G U R E 7 emspChangeintheprobabilityofoccupancyforblueduikerandbayduikerwithdistancetotheboundaryinkilometresacrossbothmanagementsectorsaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
F I G U R E 8 emspChangeintheprobabilityofoccupancyforwhite‐belliedpangolinwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaMackenzieoccupancymodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
emspensp emsp | emsp773Bruce et al
44emsp|emspCamera trap surveys for measuring the impacts of hunting on mammal communities
The spatial scale at which mammal communities are affected byandhowpopulationsrespondtoanthropogenicpressuressuchasbushmeat hunting is difficult to empiricallymeasure (Laurance etal2006)Thisisespeciallytrueformammalsresidingwithintropi‐cal forestswheregatheringconsistentandmeaningfulpopulation‐andcommunity‐levelmetrics ischallenging(Ahumadaetal2013)Population density of tropical mammals can vary greatly due toheterogeneity present within the environment For example for‐est elephants havedifferent distributions and aggregations inwetanddryseasonsinNouabaleacute‐Ndoki NationalParkwhichispartiallydependentonspatio‐temporalpatternsoffruitingtreesacrossthelandscape(Blake2002)
Whether the differences observed among the two sites sur‐veyedhereareattributabletodifferent levelsofhuntingpressureremains to be confirmed There are however indications thathuntingpressureanditsimpactsonmammalfaunasaregreaterintheNorthern Sector than in the Southern Sector The effects ofhuntingpressureonmammaliandeclinesinCentralAfricanforestsarewell documented The pattern in general is the largest‐bod‐ied species frugivores and thosewith high hunter or blackmar‐ketvalue(Abernethyetal2013Cardilloetal2005FaOliveroFarfaacutenMaacuterquezDuarteetal2014aFaOliveroFarfaacutenMaacuterquezVargasetal2014bPeresampPalacios2007)arethefirstspeciestoshownoticeabledeclineInthisstudythesignificantdeclineintherelativeabundance for frugivores suchasPetersʼduikerandspe‐cieswithhighhuntervalueliketheredriverhogunderincreasedhuntingpressure in theNorthernSector is reported inother sur‐veys(Abernethyetal2013)Thisisalsoreflectedinthedifferencesobserved in this study in biomass in the different guilds of eachmammalcommunityThemammalcommunitywithintheNorthernSector shows indications of a community that is disturbed and isexperiencingelevatedhuntingpressureThesearehigher(camera)trapping rates for smaller‐bodiedspecies suchasEminrsquospouchedrat and significantly fewer encounters of larger‐bodiedmammalsthataretargetsofthebushmeattradesuchasPetersʼduikerandredriverhog(FaRyanampBell2005JerozolimskiampPeres2003)Additionalindicatorsaretheabsenceinthesurveysoflargercarni‐voresintheNorthernSectorsuchasgoldencatandleopardwhicharesensitivetosnaring(Bahaa‐el‐dinetal2015)andsignificantlyreducedabundancemetricsfordisturbance‐sensitivespeciessuchasblack‐leggedmongooseandwaterchevrotain(Hart2013a)Theabsence of white‐bellied duiker in the Northern Sector also sug‐gestselevatedhumandisturbanceasthisspecieshasbeenreportedasverysensitivetoevenminorperturbationwithintheenvironment(Hart2013b)IncomparisontheSouthernSectorcontainedindica‐torfaunasuchasthewhite‐belliedduikerandhadhighertrappingratesforlarger‐bodiedspecies
WesuspectthedifferencesobservedaremostlikelyduetolowerhumandisturbanceintheSouthernSectorTheteamsdeployingand
recoveringthecamerasintheSouthernSectorcovered238kmandencountered few signs of humanperturbation (T Brucepers obs)whereashumansignwascommonlyencounteredbytheteamsintheNorthernSectorThisperceiveddifference is reflected in the2017and 2018 density of hunting signwithin each camera trap grid asdetected throughMINFOF ranger patrols (ZSL ampMINFOF 2017a2017b) and through the2018DistanceSampling inventory for theDFR (Bruce et al 2018) Higher numbers of hunting sign in theNorthernSectorwouldbeconsistentwithanelevatedhuntingpres‐sureinthatarea
45emsp|emspProtection of refugia from hunting
Though inferences made for wide‐ranging species such as forestelephantsandgreatapesusingcameratrapsaredifficultthefactthattrappingrateswerehigherinmorechallengingterrainwithassumedlower hunting pressure could be indicative of complex habitatprovidingsomelevelofprotectionfromhuntingElephantisknownto retreatwhen they aredisturbed to terrain that ismoredifficulttoaccessbyhumans (Hedges2012)Thuswithin largerprotectedareas certain zones may act as refugia for wildlife populations(Campbelletal2011)Thiscanbeduetoarangeof factorssuchas remoteanddifficult terrain forpoachers (Attum2007Hedges2012) or the regular presence of field researchers and rangers(Campbell et al 2011) The significanceof these refugia for largerprotected areas is that the populations of wildlife residing withinthem if adequately protected may provide source populations toallowrecolonisationofotherareasofthereserve(NaranjoampBodmer2007)Thereforeifadequateprotectioncanbeprovidedtorelativelysmallbutimportantareasoflargereservesthismayprovidetropicalforestswithabetterchanceofbeingecologicallyresilienttoongoingand increasing human perturbation Well‐designed camera trapsurveys may provide data on the status of wildlife populations atrelativelyfinespatialresolutionssoastoidentifyfunctionalrefugiawithgreaterconfidence
ACKNOWLEDG EMENTS
WeappreciatetheongoingsupportofCameroonrsquosMinistryofForestsandWildlife(MINFOF)andtheopportunitytocontributetobiodiver‐sityconservationthroughoutthecountryInparticularwewouldliketothanktheChefdrsquoAntenneSergeJacobMeyeforhisongoingsup‐portofconservationresearchwithintheprotectedareaWeappreci‐atethestalwarteffortsofMINFOFecoguardsandlocalporterswhoaccompaniedthesurveyteamsinthefieldWewouldalsoliketothanktheUnitedStatesFishandWildlifeService(USFWS)mdashAfricanElephantConservationandIUCNSOSmdashFondationSegreacutePangolinConservationInitiativeforsupportingthiswork
ORCID
Tom Bruce httporcidorg0000‐0001‐6958‐1657
774emsp |emsp emspensp Bruce et al
R E FE R E N C E S
AbernethyKACoad L TaylorG LeeMEampMaisels F (2013)Extent and ecological consequences of hunting in Central Africanrainforests in thetwenty‐firstcenturyPhilosophical Transactions of the Royal Society of London Biological Sciences368(1625)20120303httpsdoiorg101098rstb20120303
AbrahamsM I Peres C A amp Costa H C (2017)Measuring localdepletion of terrestrial game vertebrates by central‐place hunt‐ers in rural Amazonia PLoS ONE 12(10) e0186653 httpsdoiorg101371journalpone0186653
AhumadaJAHurtadoJampLizcanoD(2013)MonitoringthestatusandtrendsoftropicalforestterrestrialvertebratecommunitiesfromcameratrapdataAtool forconservationPLoS ONE8(9)e73707httpsdoiorg101371journalpone0073707
Ahumada J A Silva C E Gajapersad K Hallam C Hurtado JMartin E hellip Sheil D (2011) Community structure and diver‐sity of tropical forest mammals Data from a global camera trapnetwork Philosophical Transactions of the Royal Society of London Biological Sciences366(1578)2703ndash2711httpsdoiorg101098rstb20110115
AminRAndanjeSAOgwonkaBAliAHBowkettAEOmarMampWacherT(2015)ThenortherncoastalforestsofKenyaarenationally and globally important for the conservation of AdersrsquoduikerCephalophusadersiandotherantelopespeciesBiodiversity and Conservation 24(3) 641ndash658 httpsdoiorg101007s10531‐014‐0842‐z
Attum O (2007) Can landscape use be among the factors that po‐tentiallymake some ungulates speciesmore difficult to conserveJournal of Arid Environments69(3)410ndash419
Bahaa‐el‐dinLHenschelPAbaaRAbernethyKBohmTBoutNhellipLeeM (2013)NotesonthedistributionandstatusofsmallcarnivoresinGabonSmall Carnivore Conservation4819ndash29
Bahaa‐el‐dinLHenschelPButynskiTMMacdonaldDWMillsDSlotowRampHunterL (2015)TheAfricangoldencatCaracalaurataAfricasleast‐knownfelidMammal Review45(1)63ndash77
Bennett E L Blencowe E Brandon K Brown D Burn R WCowlishaw G hellip Robinson J G (2007) Hunting for consensusReconcilingbushmeatharvestconservationanddevelopmentpol‐icyinWestandCentralAfricaConservation Biology21(3)884ndash887httpsdoiorg101111j1523‐1739200600595x
BlakeSDeemSLMossimboEMaiselsFampWalshP(2009)Forestelephants Tree planters of the CongoBiotropica41(4) 459ndash468httpsdoiorg101111j1744‐7429200900512x
Blake S (2002) The ecology of forest elephant distribution and itsimplications for conservation Doctoral dissertation University ofEdinburgh
BruceTNdjassiCFowlerANdimbeMFankemOTabueRhellipOlsonD(2018)Faunal inventory of the Dja Faunal Reserve Cameroon Yaoundeacute Cameroon Ministry of Forests and Wildlife (MINFOF)Zoological Society of London ndash Cameroon Country ProgrammeAfricanWildlifeFoundation
BruceTWacherTNdingaHBidjokaVMeyongFNgoBataMampOlsonD(2017)camera trap survey for larger terrestrial wildlife in the Dja Biosphere Reserve CameroonYaoundeacuteCameroonZoologicalSocietyofLondon(ZSL)ampCameroonMinistryofForestsandWildlife(MINFOF)
BurnhamKPampAndersonDR(2002)Model selection and multimodel inferenceNewYorkNYSpringer
Campbell G Kuehl H Diarrassouba A NGoran P K amp BoeschC (2011) Long‐term research sites as refugia for threatened andover‐harvested species Biology Letters 7(5) 723ndash726 httpsdoiorg101098rsbl20110155
CardilloMMaceGMJonesKEBielbyJBininda‐EmondsORSechrestWhellipPurvisA(2005)Multiplecausesofhighextinction
riskinlargemammalspeciesScience309(5738)1239ndash1241httpsdoiorg101126science1116030
Craigie IDBaillieJEBalmfordACarboneCCollenBGreenREampHuttonJM (2010)Largemammalpopulationdeclines inAfricarsquosprotectedareasBiological Conservation143(9)2221ndash2228httpsdoiorg101016jbiocon201006007
DaveyKWacherTampAminR(2017)Analysis tool for camera-trap sur-vey data [Computer software]ZoologicalSocietyofLondonRetrievedfromhttpswwwzslorgzsl‐camera‐trap‐data‐management‐ and‐analysis‐package
Djuikouo M N K Doucet J L Nguembou C K Lewis S L ampSonkeacute B (2010) Diversity and aboveground biomass in threetropical forest types in the Dja Biosphere Reserve Cameroon African Journal of Ecology 48(4) 1053ndash1063 httpsdoiorg101111j1365‐2028201001212x
DupainJBombomeKampVanElsackerL(2003)LeschimpanzeacutesetlesgorillesdelareacuteservedefauneduDjaCanopeacutee2414ndash15
EffordMGampDawsonDK(2012)OccupancyincontinuoushabitatEcosphere3(4)1ndash15httpsdoiorg101890ES11‐003081
Efron B amp Tibshirani R J (1994) An introduction to the bootstrap WashingtonDCCRCPress
FaJEOliveroJFarfaacutenMAacuteMaacuterquezALDuarteJNackoneyJhellipMacdonaldDW(2014a)CorrelatesofbushmeatinmarketsanddepletionofwildlifeConservation Biology29(3)805ndash815
Fa J EOlivero J FarfaacutenMAacuteMaacuterquezA LVargas JMRealRampNasiR(2014b)IntegratingsustainablehuntinginbiodiversityprotectioninCentralAfricaHotspotsweakspotsandstrongspotsPLoS ONE9(11)e112367
FaJERyanSFampBellDJ (2005)Huntingvulnerabilityecolog‐ical characteristics and harvest rates of bushmeat species in afro‐tropicalforestsBiological Conservation121(2)167ndash176httpsdoiorg101016jbiocon200404016
Fa J E Seymour S Dupain J E F Amin R Albrechtsen L ampMacdonaldD (2006) Getting to gripswith themagnitude of ex‐ploitationBushmeat in theCross‐SanagariversregionNigeria and Cameroon Biological Conservation 129(4) 497ndash510 httpsdoiorg101016jbiocon200511031
Farris Z J Boone H M Karpanty S Murphy A Ratelolahy FAndrianjakariveloVampKellyMJ(2015)FeralcatsandthefitoatyFirstpopulationassessmentoftheblackforestcatinMadagascarrsquosrainforestsJournal of Mammalogy97(2)518ndash525
Fiske IampChandlerR (2011)UnmarkedAnRpackageforfittinghi‐erarchicalmodelsofwildlifeoccurrenceandabundanceJournal of Statistical Software43(10)1ndash23
HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences107(19)8650ndash8655httpsdoiorg101073pnas0912668107
HartJ(2013a)WaterchevrotainHymemoschusaquaticusInJKingdonampMHoffmann (Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp88ndash92)LondonUKBloomsbury
Hart J (2013b) White‐bellied duiker Cephalophus leucogaster In JKingdonampMHoffmann(Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp255ndash258)LondonUKBloomsbury
HeadJSRobbinsMMMundryRMakagaLampBoeschC(2012)Remotevideo‐cameratrapsmeasurehabitatuseandcompetitiveex‐clusionamongsympatricchimpanzeegorillaandelephantinLoangoNational ParkGabon Journal of Tropical Ecology28(06) 571ndash583httpsdoiorg101017S0266467412000612
HedgesS(2012)Monitoring elephant populations and assessing threats HimayatnagarTelanganaUniversitiesPress
HedwigDKienastIBonnetMCurranBKCourageABoeschChellipKingT(2018)Acameratrapassessmentoftheforestmam‐mal community within the transitional savannah‐forest mosaic oftheBateacutekeacutePlateauNationalParkGabonAfrican Journal of Ecology56(4)777ndash790httpsdoiorg101111aje12497
emspensp emsp | emsp775Bruce et al
HijmansRJCameronSEParraJLJonesPGampJarvisA(2005)Very high resolution interpolated climate surfaces for global landareasInternational Journal of Climatology25(15)1965ndash1978httpsdoiorg101002joc1276
HuggelA(2012)Exiv2softwaretool[Computersoftware]Retrievedfromhttpswwwexiv2orgindexhtml
Jerozolimski A amp Peres C A (2003) Bringing home the biggestbacon A cross‐site analysis of the structure of hunter‐kill profilesin Neotropical forests Biological Conservation 111(3) 415ndash425httpsdoiorg101016S0006‐3207(02)00310‐5
KingdonJ (2015)The Kingdon field guide to African mammalsLondonUKBloomsburyPublishing
KuumlhlHFMaiselsMAncrenazampEAWilliamson(Eds)(2008)Best practice guidelines for surveys and monitoring of great ape populations GlandSwitzerlandIUCN
LauranceWFCroesBMTchignoumbaLLahmSAAlonsoALeeMEhellipOndzeanoC(2006)ImpactsofroadsandhuntingoncentralAfrican rainforestmammalsConservation Biology20(4)1251ndash1261httpsdoiorg101111j1523‐1739200600420x
LauranceWFUsecheDCRendeiroJKalkaMBradshawCJSloan S P hellip Arroyo‐Rodriguez V (2012) Averting biodiversitycollapse in tropical forestprotectedareasNature489(7415)290httpsdoiorg101038nature11318
LeslieDMampHuffmanBA(2015)Potamochoerus porcus(ArtiodactylaSuidae)Mammalian Species4715ndash31
MacKenzieD IampBailey L L (2004)Assessing the fit of site‐occu‐pancy models Journal of Agricultural Biological and Environmental Statistics9300ndash318httpsdoiorg101198108571104X3361
MacKenzieDINicholsJDRoyleJAPollockKHBaileyLLampHinesJE (2006)Occupancy estimation and modellingBurlingtonMAAcademicPress
Magurran A E (2005) Species abundance distributions Patternor process Functional Ecology 19(1) 177ndash181 httpsdoiorg101111j0269‐8463200500930x
MaiselsFStrindbergSBlakeSWittemyerGHartJWilliamsonEAhellipWarrenY (2013)DevastatingdeclineofforestelephantsinCentralAfricaPLoS ONE8(3)e59469httpsdoiorg101371journalpone0059469
MalhiYAdu‐BreduSAsareRA LewisS LampMayauxP (2013)AfricanrainforestsPastpresentandfuturePhilosophical Transactions of the Royal Society of London Biological Sciences 368(1625)20120312
MallonDPHoffmannMGraingerMJHibertFVanVlietNampMcGowanP JK (2015)An IUCNsituationanalysisof terrestrialandfreshwaterfaunainWestandCentralAfricaOccasionalpaperoftheIUCNspeciessurvivalcommission(54)
MambeyaMMBakerFMombouaBRKoumbaPamboAFHegaMOkouyiOkouyiVJhellipAbernethyK(2018)TheemergenceofacommercialtradeinpangolinsfromGabonAfrican Journal of Ecology56(3)601ndash609httpsdoiorg101111aje12507
MINFOFampIUCN(2015)CaracteacuterisationdelapopulationdegrandsetmoyensmammifegraveresdanslaReservedeFauneduDjaPotentieletmenacesYaoundeacuteCameroun
Muchaal P K amp Ngandjui G (1999) Impact of village hunt‐ing on wildlife populations in the western Dja ReserveCameroon Conservation Biology 13(2) 385ndash396 httpsdoiorg101046j1523‐17391999013002385x
NaranjoEJampBodmerRE (2007) Sourcendashsink systemsandconser‐vationofhuntedungulatesintheLacandonForestMexico Biological Conservation 138(3ndash4) 412ndash420 httpsdoiorg101016jbiocon 200705010
NielsenMR(2006)ImportancecauseandeffectofbushmeathuntingintheUdzungwaMountainsTanzania ImplicationsforcommunitybasedwildlifemanagementBiological Conservation128(4)509ndash516httpsdoiorg101016jbiocon200510017
OBrienTGKinnairdMFampWibisonoHT (2003)Crouching ti‐gers hiddenprey Sumatran tiger andprey populations in a tropi‐calforestlandscapeAnimal Conservation6(2)131ndash139httpsdoiorg101017S1367943003003172
OksanenJ(2015)VegananintroductiontoordinationVol8(p19)Retrieved from httpscranr‐projectorgwebpackagesveganvi‐gnettesintroveganpdf
PeresCAampPalaciosE(2007)Basin‐wideeffectsofgameharvestonvertebrate populationdensities inAmazonian forests Implicationsfor animal‐mediated seed dispersal Biotropica 39(3) 304ndash315httpsdoiorg101111j1744‐7429200700272x
PotapovPVTurubanovaSAHansenMCAduseiBBroichMAltstattAhellipJusticeCO(2012)QuantifyingforestcoverlossinDemocraticRepublicoftheCongo2000ndash2010withLandsatETM+data Remote Sensing of Environment 122 106ndash116 httpsdoiorg101016jrse201108027
PoulsenJRKoernerSEMooreSMedjibeVPBlakeSClarkC JhellipRosinC (2017) Poaching empties criticalCentralAfricanwilderness of forest elephants Current Biology 27(4) 134ndashR135httpsdoiorg101016jcub201701023
PurvisAGittlemanJlCowlishawGampMaceGM(2000)PredictingextinctionriskindecliningspeciesProceedings of the Royal Society B Biological Sciences267(1456) 1947ndash1952 httpsdoiorg101098rspb20001234
RayJ(1997)ComparativeecologyoftwoAfricanforestmongoosesHerpestesnasoandAtilaxpaludinosusAfrican Journal of Ecology35(3)237ndash253httpsdoiorg101111j1365‐20281997086‐ 89086x
Redford K H (1992) The empty forest BioScience 42(6) 412ndash422httpsdoiorg1023071311860
RepublicofCameroon(1994)Lawno9401du20janvier1994portantreacutegimedesforecirctsdelafauneetdelapecirccheRepublicofCameroon
RoveroFampMarshallAR(2009)CameratrappingphotographicrateasanindexofdensityinforestungulatesJournal of Applied Ecology46(5)1011ndash1017httpsdoiorg101111j1365‐2664200901705x
Royle J A amp Nichols J D (2003) Estimating abundance from re‐peated presence‐absence data or point counts Ecology 84(3)777ndash790 httpsdoiorg1018900012‐9658(2003)084[0777EAFRPA]20CO2
Seddon P J Griffiths C J Soorae P S ampArmstrongD P (2014)ReversingdefaunationRestoringspeciesinachangingworldScience345(6195)406ndash412httpsdoiorg101126science1251818
Silveira L Jacomo A T amp Diniz‐Filho J A F (2003) Camera trapline transect census and track surveys A comparative evaluationBiological Conservation 114(3) 351ndash355 httpsdoiorg101016S0006‐3207(03)00063‐6
Sonkeacute B (1998) Etudes floristiques et structurales des forecircts de laReacuteserve de Faune du Dja (Cameroun) Laboratoire de BotaniqueSysteacutematique et de Phytosociologie Universiteacute Libre de Bruxelles(ULB)
Srbek‐AraujoACampChiarelloAG(2005)Iscameratrappinganeffi‐cientmethodforsurveyingmammalsinNeotropicalforestsAcasestudyinsouth‐easternBrazilJournal of Tropical Ecology21(1)121ndash125httpsdoiorg101017S0266467404001956
Stiles D (2011) Elephant meat and ivory trade in Central AfricaPachyderm5026ndash36
TEAMNetwork(2008)Terrestrialvertebrateprotocol implementationmanualv30(p56)WashingtonDCTropicalEcologyAssessmentandMonitoringNetworkCenter forAppliedBiodiversity ScienceConservationInternational
Tobler M W Carrillo‐Percastegui S E Leite Pitman R MaresR amp Powell G (2008) An evaluation of camera traps for in‐ventorying large‐and medium‐sized terrestrial rainforestmammals Animal Conservation 11(3) 169ndash178 httpsdoiorg101111j1469‐1795200800169x
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
760emsp |emsp emspensp Bruce et al
1emsp |emspINTRODUC TION
WildlifeinCentralAfricanforestsisunderincreasingpressurefromhabitatlosshabitatfragmentationandintensivehuntingforbush‐meatandwildlifeparts(HansenStehmanampPotapov2010Mallonet al 2015Mambeya et al 2018 Potapov et al 2012 Poulsenet al 2017) Hunting is a daily occurrence in Central African vil‐lages(AbernethyCoadTaylorLeeampMaisels2013Ziegleretal2016) and is an important factor contributing to the distributionof mammal species within protected areas (Muchaal amp Ngandjui1999) and around settlements (Abrahams Peres amp Costa 2017)BushmeatmarketsurveyswithinCentralAfricahavedemonstratedthatmammalsrepresentgt90ofthecarcassessold(Faetal2006)Themotivesbehindhuntingrangefromtraditionalsubsistenceandcommercialhunting forbushmeat to targetingspecies for the ille‐galwildlifetradesuchasgreatapesforbodypartsforestelephant(Loxodonta cyclotisMatschie1900)forivoryandpangolinsfortheirscales(Craigieetal2010Stiles2011)
Reduction and extirpation of mammal populations in CentralAfrican forests have cascading ecological impacts on forest eco‐systemsInparticularthelossoftoppredators(MalhiAdu‐BreduAsareLewisampMayaux2013)keyseeddispersersincludinggreatapes and forest elephants (Blake Deem Mossimbo Maisels ampWalsh2009)andlandscapearchitectssuchaselephantsthatkeepclearingsopeninCentralAfricanforests(Maiselsetal2013)canhavelong‐termandfar‐reachingimpactsonforestcommunitiesandprocesses(Abernethyetal2013Lauranceetal2012)
Understanding the interplay of patterns of hunting (for exam‐ple distribution intensity target species frequency and huntingmethods)amajordriverofmammaliandefaunationand resultantimpactsonthecompositionstructureanddistributionofmedium‐to larger‐bodied terrestrialmammals in Central Africa forests caninform management actions (Abernethy et al 2013 Bennett etal 2007 Laurance et al 2006Nielsen 2006 SeddonGriffithsSooraeampArmstrong2014)
Forexample can regular effectivepatrollingby rangersmain‐tain robust wildlife communities within ldquodefendedrdquo zones whensurroundingareasareexperiencinghigherlevelsofhuntingThean‐swerwilldependinpartonthelong‐termreachofhuntingimpactsonmammalcommunitiesacrossforestlandscapesAslarger‐bodiedmammalsareusuallymorewide‐rangingoccuratlowdensitiesandhavelonggestationperiodsthismakesthemparticularlyvulnerabletoextinction(PurvisGittlemanCowlishawampMace2000TuckerOrdampRogers2014)whereasspecieswithsmallerhomerangesandhigherdensitiesonaveragemaybemoreresilientastheminimumareaneededtomaintainviablepopulationsissmallerThusarefinedunderstandingoftheprocessofdefaunationacrossforestedCentralAfrican landscapeswill help identifymanagement actions and thescales atwhich they aremost effective for slowing and reversingit (Bruce et al 2017 Campbell Kuehl Diarrassouba NrsquoGoran ampBoesch2011Redford1992)
Camera trap surveys arewell‐suitedas amethodology todoc‐umenttherichnessoffaunasandunderstanddielactivitypatterns
andhabitatpreferencesofmediumtolargeterrestrialmammalspe‐cies in dense forests (Ahumada et al 2011 Hedwig et al 2018Silveira Jacomo amp Diniz‐Filho 2003 Tobler Carrillo‐PercasteguiLeitePitmanMaresampPowell2008)Theyprovideacost‐effectiveefficient non‐invasive and replicable surveymethod (Ahumada etal2011RoveroampMarshall2009Tobleretal2008)Importantlythey removemuchof thehumanerror anduncertaintyassociatedwithothersurveytypessuchasdistancesamplingthroughlinetran‐sectsandinterviewswiththelocalpopulations(AhumadaHurtadoampLizcano2013Hedwigetal2018)thatareoftenbiasedtowardslarger‐bodied diurnal species and fail to detect rare and elusivenocturnalspecies(Srbek‐AraujoampChiarello2005)Theuseofstan‐dardisedcameratrappingmethodsandclassifyingspeciesintofunc‐tionalgroupssuchasbytrophiccategorylifehistorysocialstructureandbodysizeallowsmammalcommunities indifferentsitestobecomparedregardlessofdifferencesinspeciescomposition
Herewe investigate ifcamera trapsurveyscandiscerndiffer‐ences in community metrics of terrestrial larger‐bodied mammalassemblagesatdifferentsiteswithinthesameCentralAfricanpro‐tectedareaWeexaminemetricsof richness guildbody‐sizeandrelativeabundanceasmeasuredbytrappingratesandoccupancyofthetwomammalcommunitiessurveyedusingagridofcameratrapsateachsite
2emsp |emspMATERIAL S AND METHODS
Camera trap surveys were conducted at two sites approximately32km apart (at their closest proximity) within the Dja FaunalReserve(DFR)insouthernCameroonContiguousnaturalforesten‐compassesbothsitesandinterveningandsurroundinghabitat
21emsp|emspStudy area
TheDFRthelargestprotectedareainCameroon isapproximately5260km2 (3deg08prime589PrimeN 13deg00prime001PrimeE Figure 1) The Dja Riversurrounds 80 of the reserve acting as a partial buffer to humanencroachment and animal movement (Muchaal amp Ngandjui 1999)Thetopographywithinthereserveismadeupofround‐toppedhillsbetween600and800maslwithvalleysoneithersideofacentralridgelinethattraversesthereserveeasttowest(MINFOFampIUCN2015)Swampsareprevalent inthetributariesfeedingintotheDjaRiverThreemajorforesttypesoccurwithinthereserveterrafirmeforest(Sonkeacute1998)monodominantforest(Gilbertedendronsp)andseasonally inundated forests (DjuikouoDoucetNguembouLewisamp Sonkeacute 2010) There are four seasons a long rainy season fromAugusttoNovemberthelongdryseasonfromNovembertoMarchashortrainyseasonfromMarchtoMayandtheshortdryseasonis between June and July Average annual rainfall is c 1600mm(HijmansCameronParraJonesampJarvis2005)CommercialloggingwaslimitedandhasnowceasedOnlytraditionalhuntingisallowedwithin the Dja Faunal (Biosphere) Reserve and no fully protectedClassAspeciescanbetaken(RepublicofCameroon1994)However
emspensp emsp | emsp761Bruce et al
thehumanpopulationaroundthereserveisincreasingandindustriessuchasloggingrubberhydropowerandminingareproliferatingre‐sultinginincreaseddemandforbushmeatBothillegalnon‐traditionalsubsistenceandcommercialhuntingoccurwithinthereserve
22emsp|emspNorthern and southern sector sites
WesetupcameratrapgridsintheNorthern(management)Sector(centredon03deg13rsquo33rsquorsquoN12deg48rsquo18rsquorsquoE)betweenNovember2015andMay 2016 and the Southern (management) Sector (02deg59rsquo37rsquorsquoN13deg07rsquo43rsquorsquoE)oftheDFRbetweenMayandJune2017(Figure1)ThecameratrapgridwithintheNorthernSectorwasplacedusingthenorthernprotectedareaboundaryasanapproximatebaselineref‐erenceThecamerasweresetovera rangeofc31 toc159kmfromtheboundaryof the reservewithanaveragedistanceof95(SEplusmn39)kmfromtheboundaryCameraswereplacedonaverage123(SEplusmn38)kmfromthenearestsettlementswitharangeofbe‐tweenc6and188kmTheNorthernSectorof theDjapresentsagenerallyhigherandmoreuniformelevation(662ndash720masl)thanthe Southern Sector (563ndash689masl) Watercourses are sparserand swamp habitat less common within this management sectorCorrespondinglythenortherncameratrapstationswereonaver‐agemoredistantfromthenearestwatercourse(c261km)andonlytwonortherncameraswereplacedinswamphabitat
Thecameras in theSouthernSectorgridwereplacedonaver‐age123(SEplusmn38)kmoverarangeofc57ndash19kmfromthereserveboundary and were between c 77 and 22km from the nearesthuman settlementwith anaveragedistanceof155 (SEplusmn37) kmThetopographywithinthesoutherncameratrapgridismorecom‐plexwithagreaterelevationalvariationThegreaterprevalenceoflowlandareasresultedinmoreswamphabitat(fivecamerasplacedwithin 50m of swamp habitats) and cameras being on averageplacedclosertowatercourses(c06km)
23emsp|emspcamera trap surveys
Forty cameraswere placed at each localitywith a 2km spacingbetweeneachcamera(Ahumadaetal2011)(Figure1)Eachgridoperatedlongenoughtoachieveatleast1000cameratrapdaysofsamplingeffort(OrsquoBrienKinnairdampWibisono2003)WeusedGlobalPositioningSystemreceiverstolocatethegridpointsAsin‐gle camerawas positioned 30ndash45cm above ground level within200m of each point aimed at a game trail that provided suffi‐cient fieldofviewtocapture lateral full‐body imagesofsmall tomedium‐sizedmammals Siteswere selected based on the pres‐enceofagametrail(Aminetal2015)tomaximisetheprobabil‐ityofobtainingusefulphotographs(TEAM2008)andasuitabletreeallowing thecamera tobepositioned facingeithernorthor
F I G U R E 1 emspLocationoftheDjaFaunalReserveCameroon(a)andthelocationofcameratrapgridsintheNorthernandSouthernsectors(b)Managementsectorsareingrey[Colourfigurecanbeviewedatwileyonlinelibrarycom]
762emsp |emsp emspensp Bruce et al
south tominimise the impacts of sunrise and sunset on cameraperformance
We used three different camera models across the two grids(BushnellAggressorReconyxHC500 andCuddebackLong rangeIRE2)Detectionrangewasatleast25mwitheitheratwo‐seconddelay(Bushnell‐2015NorthernSectorsurvey)orone‐seconddelay(ReconyxCuddebackandBushnell‐2017SouthernSectorsurvey)ThreeconsecutiveimagesweretakenpertriggerLowglowinfraredflashlightingwasusedtominimisetheriskofstartlinganimalsThefulllistofsettingsforeachcameracanbefoundinAnnex1
24emsp|emspNatural mammal fauna
Thereserveisreportedtocontain109speciesofmammalofwhich35speciesareterrestrialandhaveabodyweightgt05kg(Kingdon2015) Currently the only baseline data for populations for thesespecieswithinthereservecomefromencounterratesfromrangerpatrolsanddistancesamplingthroughlinetransectsurveys(DupainBombomeampVanElsacker2003MINFOFampIUCN2015WilliamsonampUsongo1995)
25emsp|emspAssessment of differences in human activity
Toassesstherelativedifferencesinhumanactivityincludinghunt‐ing between theNorthern and Southern Sectorwhere the twosites were located we evaluated trends from multiple sourcesEvidence of human sign was recorded on 1‐kilometre line tran‐sectsduringafullfaunalinventoryoftheDFR(Bruceetal2018)TransectsareoftenusedtomonitorthetrendsofhumanimpactsinCentralAfricanforests(Kuumlhletal2008)Therewereatotalof86and76transectscoveringadistanceof916and807kmcom‐pleted intheNorthernSectorandSouthernSector respectivelyEncountersofhumansignbetweenJanuary2016andSeptember2017byMinistryofForestsandWildlife(MINFOF)rangerpatrolswhorecorddatausingSpatialMonitoringAndReportingToolde‐viceswerealsoused(ZSLampMINFOF2017a2017b)Abufferof2kmwassetaroundeachcameraandthesignwithinthisareawasconvertedintotheamountofhumansignperkm2Thisbufferwasusedtocounteractunequalsurveyeffortwithinthesectorspos‐siblyduetoecoguardsbeingrequiredtobepresentataresearchstation in theNorthernSectorat thebottomof thecamera trapgrid
Transects provide a more objective measure of hunting pres‐sureastheyuseastandardisedmethodologyandteamcompositioncompared to rangerpatrolsTransectsarenotbiasedby followingtrailsorotherpathsofleastresistancethataffectstheprobabilityofhumansignbeingdetected
26emsp|emspData analysis
WeusedExiv2software(Huggel2012)toextractEXIFinformationfromeachphotograph(imagenamedateandtime)SpeciesofanimalinthephotographswereidentifiedwhenpossibleThesedatawere
compiled in an Excel spreadsheet (Microsoft Office ProfessionalPlus2016Version1809)andanalysedwithsoftwaredevelopedbyat ZSL (CameraTrapAnalysis Package [CTAP]) (DaveyWacherampAmin2017)
Weonlyconsideredterrestrialmammalspeciesthathaveanesti‐matedaveragemassgreaterthan05kg(medium‐to‐largemammals)fortheanalysesbecausetheyarethemaintargetgroupforcameratrapsplacedatgroundlevelSmallermammalsinducesamplingerrorthroughareducedlikelihoodofdetectionbythecameratraprsquosther‐malsensorandaccurateidentificationofsmallmammalstospecieslevelisdifficultfromcameratrapsset‐upformedium‐to‐largemam‐mals(Tobleretal2008)
We calculated rarified species accumulation curves and esti‐matedthemedium‐to‐largeterrestrialmammalspeciesrichnessforeachsectorusingtheZSLCTAPtool
We calculated Simpsonrsquos diversity index and ShannonndashWeinerdiversity index foreach sector fromspeciesdaily trap ratesusingpackageveganinRstatisticalsoftware(Oksanen2015)Simpsonrsquosdiversityindexismostsensitivetochangesinmorecommonhighlyabundant species while ShannonndashWeiner diversity index is mostsensitivetochangesinrarelessabundantspecies(Magurran2005)
Wecalculatedthenumberofindependentphotographiceventsper100trapdaysasarelativeabundanceindex(RAI)foreachspeciesWedefinedanldquoeventrdquoasanysequenceforagivenspeciesoccurringafteranintervalofge60minfromthepreviousthree‐imagesequenceof that species to ensure that species events were independent(Aminetal2015Tobleretal2008)Theeventswereautomati‐cally screenedby theZSLCTAPsoftwareWecalculated the95confidenceintervalsusingthebootstrapmethod(EfronampTibshirani1994)andconsiderednon‐overlappingconfidenceintervalsasindic‐ativeofasignificantdifferenceinRAIbetweenmanagementsectorsWeassumethatthecameratrappingratescalculatedastheRAIre‐flectactualrelativeabundanceasinRoveroandMarshall(2009)
We used single‐season occupancy analysis (MacKenzie et al2006) where assumptions and data quality allowed to estimatethe proportion of area occupied by a species within each gridOccupancyestimateswerecorrectedbydetectionprobability (iethelikelihoodthataspecieswasdetectedwhenpresent)andthere‐foreprovideamore rigorous indexofabundance forbothwithinandbetweenspeciescomparisonsThishoweverislimitedtospe‐ciesgeneratingadequatedatasetswherecameraspacingisgreaterthanthespecieshomerangeandoccupancyisnotconfoundedbychanges in the home range (Efford ampDawson 2012) For all theoccupancyanalyseswegenerated1110‐daysamplingoccasionsThismeanttheNorthernSectordataweretruncatedtomatchthenumberofoccasionsavailableforanalysis intheSouthernSectorWetestedforsignificantdifferencesinspeciesoccupancybetweenthe Northern and Southern sectors using the ldquoWaldrdquo parametricstatisticaltestasitisknowntobeanindependentandrobustmea‐sureofdifference(Aminetal2015)withplt005consideredtobesignificant
We alsomodelled occupancy as a function of site covariatesdistance to the protected area boundary in kilometres (D) and
emspensp emsp | emsp763Bruce et al
management sector (M) using the ldquounmarkedrdquo (Fiske amp Chandler2011) software package in R We treated detection probabilityas a constant and evaluated all covariate combinations ψ ()p()ψ (D)p() ψ (M)p() ψ (DM)p() ψ (D+M) p() For covariate anal‐ysis tocompare themanagementsectorswealso implementedaRoylendashNicholsmodel(2003)whichtakesintoaccountthenumberofindividualsatasiteinfluencingdetectionprobabilityandthusoc‐cupancyTheselectionofRoylendashNicholsmodelaboveasingle‐sea‐sonmodelforaspecieswouldprovidefurthersupportthatspeciesabundance was significantly different between the managementsectorsWe rankedmodelsbyAkaikersquos informationcriteria (AIC)andmodels that had a delta AIC of lt2were considered to be acompetingmodel(BurnhamampAnderson2002)Thec‐hatandchi‐squared values to assessmodel dispersionwere generated usingtheMackenzie andBailey (2004) goodness‐of‐fit testwhichwasconducted using 1000 simulations for eachmodelModels witha c‐hatgt2were rejectedas theywere regardedasoverdispersed(Farrisetal2015)
3emsp |emspRESULTS
Weaccumulated3725operationalcameratrapdays(mean91dayscamera)intheNorthernSectorand3371operationalcameratrapdays(mean84dayscamera)intheSouthernSectorIntheNorthernSector grid ten cameras were lost or damaged by people or el‐ephants and somemalfunctioned The Southern Sector only hadeightcamerasfailduetothesameissuesaswellastoleoparddam‐age In total 16 cameraswere excluded fromoccupancy analysisduetobeingoperationalforlt80ofoccasions
31emsp|emspRelative assessment of human sign
Overallhumanpressureasmeasuredbyhumansignwithinthere‐servewasmoreabundant intheNorthernSectorcomparedtotheSouthern Sector Encounter rate of human sign on transects was154km in theNorthern Sector three times higher than 049kmintheSouthernSectorAsimilarpatternwasobserved inthedatagatheredbyMINFOF rangers TheNorthern Sector had a densityofhuntingsignof087km2 withintheareaofthegridincludingthe2km buffer compared to 008km2 in the Southern Sector Giventhatseveralsignsmeasuredarecloselyassociatedwithhuntingac‐tivitysuchassnaresandcartridgesweassumethathuntingactiv‐ityisonaveragehigherintheNorthernSectorthantheSouthernSector
32emsp|emspSpecies richness
A total of 26 medium‐to‐large terrestrial mammal species werephotographedintheNorthernSectorand31medium‐to‐largeter‐restrialmammalspeciesintheSouthernSector(Table1)Wealsore‐cordedfivearborealmammalspeciesthatwerenotthetargetofthissurvey (Table1)Fourmedium‐to‐large terrestrialmammalspecies
expected to occur in the surveyed habitats according to availableIUCN distribution maps and literature were not detected by thecameratrapsurveysineithersector(Table1)
The species accumulation curves for medium‐to‐large terres‐trialmammal species showmore species detected per unit effortin theSouthernSector (Figure2)Thediversity indicesweremar‐ginally lower in the Northern Sector (Simpsons=072 ShannonndashWeiner=179)comparedtotheSouthernSector(Simpsons=078ShannonndashWeiner=208)
33emsp|emspCommunity structure
CommunitystructureofmammalsdifferedbetweentheNorthernSectorandSouthernSectorsites(Figures3and4)withmorespe‐ciesbeingencounteredforthreeoutofthefourguilds(herbivoresinsectivoresandcarnivores)intheSouthernSectorThemostfre‐quentlyencounteredguild inbothsectorswasherbivore (14spe‐ciesintheSouthernSectorand13intheNorthernSector)followedbyomnivore(seveninbothsectors)carnivore(sixintheSouthernSector four in theNorthernSector) and insectivore (three in theSouthernSector two in theNorthernSector)Overallacross theguilds trapping rates for lowerbodymassspecieswerehigher inthe Northern Sector A marked difference was the higher trap‐pingratesofherbivoresandomnivoreswithbodymassgt10kg intheSouthernSector (Figure4) compared to theNorthernSector(Figure3)
34emsp|emspForest antelopes
Werecorded4495independentphotographiceventsoftenspe‐ciesof forest antelopesTheblueduiker (Philantomba monticolaThunberg 1789) was the most frequently encountered forestantelope species across both camera trap grids (RAI=527) fol‐lowed by Petersrsquo duiker (Cephalophus callipygus Peters 1876)(RAI=412) and Bay duiker (Cephalophus dorsalis Gray 1846)(RAI=747) The rest of the forest antelopeswere relatively in‐frequently encounteredwith a global trapping rate of less thanfiveThedisturbance‐sensitivewhite‐belliedduiker(Hart2013b)wasonlyencountered in theSouthernSector (RAI=395 [lower95 confidence limit (LCL)=214 upper 95 confidence limit(UCL)=611])TrappingratesweresignificantlyhigherforPeterrsquosduiker in the Southern Sector displaying a fivefold increase be‐tween sectors (Table 1) Peterrsquos duiker occupancy was also sig‐nificantlyhigherintheSouthernSectorcomparedtotheNorthernSector (p=002 Table 2) Therewere no significant differencesin trapping rates between the two sectors forBatersquos pygmy an‐telope (Neotragus batesi de Winton 1903) bay duiker bongo(Tragelaphus eurycerusOgilbyi1837)sitatunga (Tragelaphus spe-kiiSpeke1863)andblack‐frontedduiker(Cephalophus nigrifrons Gray1871)Occupancyvaluesforbayduikerblack‐frontedduikerandBatersquospygmyantelopedidnotdiffersignificantlybetweenthesectorsTherewereinsufficientdetectionsoftheotherspeciestomodeloccupancy
764emsp |emsp emspensp Bruce et al
TA B L E 1 emspMammalspeciespredictedtoberecordedintheNorthernandSouthern(management)sectorsofDjaFaunalReserveCameroon
Order Species IUCN Status HabitatNorthern sector RAI (LCLndashUCL)
Southern sector RAI (LCLndashUCL)
Afrosoricida Giantottershrew(Potamogale velox Du Chaillu1860)
LC Wetland Notdetected Notdetected
Carnivora Africangoldencat(Profelis aurataTemminck1827)a
VU Forest Notdetected 058(027ndash091)
Carnivora Leopard(Panthera pardusLinnaeus1758)a
NT Mixed Notdetected 083(032ndash145)
Carnivora Marshmongoose(Atilax paludinosusCuvier1829)a
LC Wetland 056(033ndash082)b 009(0ndash02)b
Carnivora Black‐leggedmongoose(Bdeogale nigripesPucheran1855)a
LC Forest 183(079ndash314) 371(263ndash484)
Carnivora Camerooncusimanse(Crossarchus platycephalusGoldman1984)a
LC Forest 183(124ndash247) 083(046ndash127)
Carnivora Long‐nosedmongoose(Herpestes nasodeWinton1901)a
LC Forest 102(053ndash160) 089(009ndash227)
Carnivora Africanpalmcivet(Nandinia binotataGray1830)a
LC Forest 113(071ndash16) 089(052ndash13)
Carnivora Servalinegenet(Genetta servalinaPucheran1855)a
LC Forest 325(239ndash416) 214(142ndash295)
Carnivora Large‐spottedgenet(Genetta maculata Gray1830)
LC Forest Notdetected Notdetected
Carnivora CentralAfricanoyan(Poiana richardsoniiThomson1842)c
LC Forest Notdetected 003(003ndash009)
Cetartiodactyla Batesspygmyantelope(Neotragus batesideWinton1903)a
LC Forest 04(011ndash078) 036(015ndash059)
Cetartiodactyla Forestbuffalo(Syncerus cafferSparrmansubspnanus1779)a
EN Forest 008(0ndash024) 006(0ndash019)
Cetartiodactyla Petersduiker(Cephalophus callipygusPeters1876)a
LC Forest 141(838ndash2071)b 7146 (4963ndash9641)b
Cetartiodactyla Bayduiker(Cephalophus dorsalisGray1846)a
LC Forest 668(44ndash935) 834(492ndash1228)
Cetartiodactyla White‐belliedduiker(Cephalophus leucogastersubsp leucogasterGray1873)
LC Forest Notdetected 395(214ndash611)
Cetartiodactyla Black‐frontedduiker(Cephalophus nigrifronsGray1871)a
LC Forest 086(003ndash246) 05(006ndash114)
Cetartiodactyla Yellow‐backedduiker(Cephalophus silvicultorAfzelius1815)a
LC Forest 37(225ndash554) 555(354ndash794)
Cetartiodactyla Blueduiker(Philantomba monticolaThunberg1789)a
LC Forest 6164(4602ndash788) 4298(315ndash5561)
Cetartiodactyla Bongo(Tragelaphus eurycerusOgilbyi1837)a
NT Forest 005(0ndash014) 006(0ndash015)
Cetartiodactyla Sitatunga(Tragelaphus spekiiSpeke1863)a
LC Wetland 024(005ndash048) 009(0ndash024)
Cetartiodactyla Redriverhog(Potamochoerus porcusLinnaeus1758)a
LC Woodland 161(102ndash228)b 7(336ndash1304)b
Cetartiodactyla Giantforesthog(Hylochoerus mein-ertzhageniThomas1904)
LC Forest Notdetected Notdetected
Cetartiodactyla Waterchevrotain(Hyemoschus aquaticusOgilby1841)a
LC Forest 03(0ndash075)b 46(192ndash799)b
(Continues)
emspensp emsp | emsp765Bruce et al
35emsp|emspCarnivore
ThecarnivorecommunitydifferedinRAIandstructurebetweenthetwosectorsFelidswerenotdetectedatallintheNorthernSectorbutboth leopard (Panthera pardusLinneaus1758)andgoldencat(Profelis aurata Temminck1827)werepresentintheSouthernSector
(Table1)AmongtheHerpestidaeblack‐leggedmongoose(Bdeogale nigripes Pucheran1855) showeda significantlyhigheroccupancy(p =gt001)intheSouthernSectorbuttrappingrateslackedsignifi‐cantdifference (RAI=371 [LCL=263UCL=484])comparedtothe Northern Sector (RAI=183 [LCL=079 UCL=314])Marshmongoose(Atilax paludinosusCuvier1829)hadsignificantlyhigher
Order Species IUCN Status HabitatNorthern sector RAI (LCLndashUCL)
Southern sector RAI (LCLndashUCL)
Hyracoidea Westerntreehyrax(Dendrohyrax dorsalis Fraser1855)
LC Forest Notdetected Detected
Pholidota White‐belliedpangolin(Phataginus tricuspisRafinesque1821)a
VU Forest 062(029ndash1) 08(044ndash121)
Pholidota Giantpangolin(Smutsia giganteaIlliger1815)a
VU Forest 027(008ndash052) 068(038ndash101)
Primates Agilemangabey(Cercocebus agilisMilne‐Edwards1886)a
LC Forest 035(013ndash059) 448(265ndash682)
Primates Moustachedguenon(Cercopithecus cephusLinnaeus1758)c
LC Forest Detected Notdetected
Primates Greaterspot‐nosedguenon(Cercopithecus nictitansLinnaeus1766)c
LC Forest Detected Detected
Primates Blackcolobus(Colobus satanasWaterhouse1838)c
VU Forest Notdetected Detected
Primates Galagospc ‐ Detected Notdetected
Primates Mandrill(Mandrillus sphinxLinnaeus1758)a
VU Forest 005(0ndash013) 006(0ndash019)
Primates Westernlowlandgorilla(Gorilla gorillaSavagesubspgorilla1847)a
CR Forest 016(003ndash031) 044(02ndash073)
Primates Centralchimpanzee(Pan troglodytesBlumenbachsubsptroglodytes1799)a
EN Forest 161(077ndash29)b 457(314ndash617)b
Proboscidea Forestelephant(Loxodonta cyclotisMatschie1900)a
VU Mixed 086(046ndash135) 19(086ndash329)
Rodentia Africanbrush‐tailedporcupine(Atherurus africanusGray1842)a
LC Forest 1753(1142ndash2446) 762(464ndash1145)
Rodentia Eminspouchedrat(Cricetomys eminiWroughton1910)a
LC Forest 32(2358ndash4141)b 756(341ndash1465)b
Rodentia Greatercanerat(Thryonomys swinderi-anus Temminck1827)
LC Wetland Notdetected Notdetected
Rodentia LadyBurtonsropesquirrel(Funisciurus isabellaGray1862)c
LC Forest Detected Detected
Rodentia Fire‐footedropesquirrel(Funisciurus pyrropusCuvier1833)c
LC Forest Detected Detected
Rodentia Africangiantsquirrel(Protoxerus stangeriWaterhouse1842)c
LC Forest Detected Detected
Tubulidentata Aardvark(Orycteropus aferPallas1766)a LC Mixed Notdetected 009(005ndash019)
NotesForeachsectorandspeciesthatwasdetectedwepresentthemeanand95confidencelimits(inbrackets)ofthenumberofindependentphotographiceventspertrapdaytimes100Trappingrateswereonlycalculatedformedium‐to‐largeterrestrialmammalsduetoinconsistentdetectionprobabilitieswithotherspeciesIUCNstatuscriticallyendangered(CR)endangered(EN)vulnerable(VU)nearthreatened(NT)leastconcern(LC)aIndicatesaspeciesthatwasincludedintherarefactionanalysisaccordingtothedefinitiongiveinthedataanalysissectionofthemethodsbIndicatesthattheRAIconfidenceintervalsdonotoverlapandcanbeconsideredsignificantlydifferentcSignifiesanarborealspecies
TA B L E 1 emsp (Continued)
766emsp |emsp emspensp Bruce et al
F I G U R E 2 emspRarefiedspeciesaccumulationcurvesformedium‐to‐largeterrestrialmammalsintheNorthernandSouthernsectorsofDjaFaunalReserveCameroon
F I G U R E 3 emspDistributionofmedium‐to‐largeterrestrialmammalspeciesintheNorthernSectoroftheDjaFaunalReserveCameroononthebasisofbodysizeandtrophiccategoryEachcirclerepresentsaspeciesinfunctionalspaceSizeofthecircleproportionaltothetrappingrateforthatspecies
emspensp emsp | emsp767Bruce et al
trappingrateintheNorthernSector(Table1)butlackedsufficientdetectionstoreliablycalculateoccupancyAbundanceofCamerooncusimanse(Crossarchus platycephalusGoldman1984)didnotdiffersignificantlybetweenthetwosectors(NorthernSectorRAI=183[LCL=124 UCL=247 ψ=075] Southern Sector RAI=083[LCL=046UCL=127]ψ=056p=028)
36emsp|emspElephants great apes and giant pangolin (illegal wildlife trade targets)
Amongtheterrestrialmammalstargetedbytheillegalwildlifetradespecifically central chimpanzee (Pan troglodytes Blumenbachsubsp troglodytes 1799) western lowland gorilla (Gorilla gorillaSavagesubsp gorilla1847)forestelephantgiantpangolin(Smutsia gigantea Illiger 1815) and white‐bellied pangolin (Phataginus tri-cuspis Rafinesque 1821) only central chimpanzee displayed asignificant difference in RAI between the management sectors(Northern Sector RAI=161 [LCL=077 UCL=29] SouthernSector RAI=457 [LCL=314 UCL=617]) However there wasnosignificantdifferenceinmeanoccupancybetweenthetwosec‐tors (p=074) Giant pangolin displayed the greatest differencewithathreefoldincreaseinRAIfrom027[LCL=008UCL=052]in the Northern Sector to 068 [LCL=038 UCL=101] in theSouthernSectorbutthiswasnotsignificantduetotheoverlapping
confidencelimitsTheRAIsandwhereappropriateoccupancyofforestelephantwesternlowlandgorillaandwhite‐belliedpangolinwerenotsignificantlyhigher intheSouthernSectorcomparedtotheNorthernSector(Tables12and12)
37emsp|emspOther bushmeat‐targeted species
Eminrsquospouchedrat(Cricetomys eminiWroughton1910)wasmoreabundantasmeasuredbybothoccupancy(pge001)andtrapratesintheNorthernSectorcomparedtotheSouthernSector(Table1)Africanbrush‐tailedporcupine(Atherurus africanusGray1842)didnothavesignificantdifferencesinRAIbetweenthemanagementsectors but occupancywas significantly higher in theNorthernSector (pge004) In comparison the larger‐bodied red river hog(Potamochoerus porcus Linneaus1758)wasmore frequentlyen‐countered as measured by both species abundance metrics intheSouthernSector(RAI=7[LCL=336UCL=1304]ψ=091)compared to the Northern Sector (RAI=161 [LCL=102UCL=228]ψ=065(p=004)
38emsp|emspSpecies occupancy with covariates
Therewasatotalof15speciesthathadsufficientdetectionstomodeloccupancywithinteractingsitecovariates(distancetoparkboundary
F I G U R E 4 emspDistributionofmedium‐to‐largeterrestrialmammalspeciesintheSouthernSectoroftheDjaFaunalReserveCameroononthebasisofbodysizeandtrophiccategoryEachcirclerepresentsaspeciesinfunctionalspaceSizeofthecircleproportionaltothetrappingrateforthatspecies
768emsp |emsp emspensp Bruce et al
TAB
LE 2
emspNullmeanoccupancy(ψ)anddetection(p)probabilitieswithstandarderrorpresentedinbracketsfortheNorthernSectorandSouthernSector
Spec
ies
Nor
ther
n se
ctor
(ψ)
Nor
ther
n se
ctor
(p)
Sout
hern
sec
tor
(ψ)
Sout
hern
sec
tor
(p)
Mod
elBe
tamdash
Para
met
er
chos
enLo
wer
95
be
taU
pper
95
be
taC‐
hat v
alue
Chi‐s
quar
ep
valu
e
Certiodactyla
Batesrsquospygmy
antelope
022(01)
015(006)
[026]
ndashNull
ndashndash
ndashndash
ndash
Bayduiker
091(006)
04(003)
087(006)
04(003)
DRN
lam(DistanceSTD)
000
6356
808
043
3356
50
930
25
Black‐fronted
duiker
01(006)
036(01)
015(006)
025(008)
Null
ndashndash
ndashndash
ndash
Blueduiker
097(003)
082(002)
1(0)
1(0)
DRN
lam(DistanceSTD)
002
0135
490
3637
492
021
024
Petersrsquoduiker
083(007)
a056(003)
1(0)a
1(0)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus07435528
003
6592
430
004
03
Waterchevrotain
[007]
ndash04(008)
045(005)
ndashndash
ndashndash
ndashndash
White‐bellied
duiker
ndashndash
072(008)
031(003)
Null
ndashndash
ndashndash
ndash
Yellow‐backed
duiker
084(008)
027(003)
086(007)
039(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
010
8837
21
0251
104
069
021
Redriverhog
065(011)
a021(003)
091(006)
a033(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus12560347
minus01352547
027
044
Proboscidae
Forestelephant
067(015)
014(004)
063(013)
014(004)
Null
ndashndash
ndashndash
ndash
Primates
Central
chimpanzee
077(014)
015(004)
082(007)
035(003)
SRN
lam(sectorSouthern)
037
3686
91
4429
314
03
039
Westernlowland
goril
la[007]
ndash045(017)
01(004)
Null
ndashndash
ndashndash
ndash
Philodota
Giantpangolin
[02]
ndash061(016)
011(004)
Null
ndashndash
ndashndash
ndash
White‐bellied
pangolin
045(016)
012(005)
063(017)
011(003)
DSoccu
psi(DistanceSTDsec
torSouthern)
minus48425115
minus1910401
022
06
Rodentia
African
brush‐tailed
porcupine
098(003)
a057(003)
084(006)
a042(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus10008123
minus01586108
042
071
Eminrsquospouched
rat
1(0)a
1(0)
079(007)
a038(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus095574568
minus01390762
021
075
Carnivora
(Con
tinue
s)
emspensp emsp | emsp769Bruce et al
and management sector Table 2) Forest elephant black‐frontedduikerand long‐nosedmongoose (Herpestes nasodeWinton1901)lackedamodel thathadanAICdifferenceofgt2 therefore theco‐variatemodelswerenotsignificantlydifferent to thenullmodel forthese species Elevenof 15 species had aRoylendashNicholsmodel se‐lectedasthelowestAICvaluesuggestingadifferenceinthenumberofindividualswassignificantlyinfluencingdetectionprobabilitiesandthereforeoccupancy
RoylendashNichols models accounted for occupancy being signifi‐cantlyhigherindifferingmanagementsectorswithnointeractionofdistancetotheprotectedareaboundaryforthreespeciesCamerooncusimanse had higher occupancy in the Northern Sector In con‐trast central chimpanzee and black‐legged mongoose had signifi‐cantlyloweroccupancywithintheNorthernSectorcomparedtotheSouthernSector(Figure5)
African brush‐tailed porcupine Eminrsquos pouched rat and servalinegenet(Genetta servalinaPucheran1855)hadasynergisticRoylendashNicholsmodelselectedasthemostsupportedTheprobabilityofsiteoccupancyslightlyincreasedwithdistancetotheboundaryandwasoverallhigherin theNorthernSector butdeclinedwithdistance to theboundary intheSouthernSector(Figure6)BothPetersrsquoduikerandredriverhogalsodisplayedthispatternofoccupancybuthadamuchgreaterincreaseinoccupancyintheNorthernSectorandhadhigheroccupancyoverallintheSouthernSector(Figure6)Incontrastyellow‐backedduiker(Cephalophus silvicultorAfezilus1815)wastheonlyspeciestodemonstrateanincreaseinoccupancywithdistancetotheboundaryintheSouthernSectorwhiledecliningintheNorthernSectorHoweversimilartootherlargerspeciesoccupancywashigherintheSouthernSector(Figure6)
With regard to the remainingduiker speciesmodelled aRoylendashNicholsmodelwithdistancetotheprotectedareaboundarywasiden‐tifiedasthemostappropriateTheprobabilityofasitebeingoccupiedbyblueduikerandbayduikerincreasedwithdistancetotheboundarywith no discernible difference betweenmanagement sectors in themodel(Figure7)
White‐belliedpangolinhadasingle‐seasonoccupancymodelse‐lectedsuggestingdifferences inabundancebetweenthemanage‐mentsectorsdidnotaffectdetectionprobabilitiesTheprobabilityofasitebeingoccupiedbywhite‐belliedpangolin increasedintheNorthernSectoranddeclinedintheSouthernSectorwithincreasingdistancetotheboundary(Figure8)
Seven speciesweredetectedonly inone sectoror lacked suffi‐cientdetectionsinonesectortoreliablymodeloccupancyacrossbothmanagement sectors Therefore only the effect of distance to theboundarycouldbemodelledThesewereAfricangoldencatwesternlowlandgorillawhite‐belliedduikergiantpangolinAfricanpalmcivet(Nandinia binotata Gray 1830) Batesrsquos pygmy antelope and waterchevrotain (Hymeoschus aquaticusOgilby 1841)African palm civetwastheonlyspeciestohavedistancetotheboundaryselectedastheoptimummodel to explain occupancy as occupancy increasedwithdistance from the boundary of the protected area (Table 2)All theremainingspecieshadthenullmodelselectedastheoptimummodelaccordingtoAICcriteria (Table2)Howeverdistancetothebound‐arywaswithinlt2AICforthesespeciessuggestingthatasignificantSp
ecie
sN
orth
ern
sect
or (ψ
)N
orth
ern
sect
or (p
)So
uthe
rn s
ecto
r (ψ
)So
uthe
rn s
ecto
r (p
)M
odel
Beta
mdashPa
ram
eter
ch
osen
Low
er 9
5
beta
Upp
er 9
5
beta
C‐ha
t val
ueCh
i‐squ
arep
va
lue
Africangolden
cat
ndashndash
041(013)
013(004)
Null
ndashndash
ndashndash
ndash
Africanpalm
civet
[047]
ndash073(017)
012(003)
DOccu
psi(DistanceSTD)
minus8177158
Inf
197
008
Black‐legged
mongoose
047(01)a
025(004)
082(008)
a031(003)
SRN
lam(sectorSouthern)
028
0266
31
4627
420
011
058
Cameroon
cusimanse
075(009)
027(004)
056(015)
012(004)
SRN
lam(sectorSouthern)
minus1808131
minus05098939
005
073
Long‐nosed
mongoose
055(012)
a02(004)
015(006)
a027(007)
Null
ndashndash
ndashndash
ndash
Servalinegenet
092(006)
035(003)
08(009)
02(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus09202819
003
5821
570
50
26
Not
esNaiumlveoccupancyvaluesarepresentedinsquarebracketsforspecieswithadetectionprobabilitylt01TheoptimummodelchosenbyAkaikersquosinformationcriteriaforeachspeciesgeneratingsuf‐
ficientoccupancyvaluesinbothsectorswiththeBetaparameteranditisrespectivelowerandupper95confidencelimitsisshownandtheassociatedc‐hatandchi‐squaredp
val
ue
DdistancetoboundarySmanagementsectorRNRoylendashNicholsmodelOccuMckenziesingle‐seasonoccupancymodesynergisticinteraction
a IndicatesasignificantdifferenceinoccupancybetweensectorsasmeasuredbytheWaldteststatistic
TAB
LE 2
emsp(Continued)
770emsp |emsp emspensp Bruce et al
relationshipwithdistancetotheboundarycouldbeinfluencingoccu‐pancyIntheSouthernSectortheoccupancyincreasedwithdistanceto theboundary forwestern lowlandgorillaandgiantpangolinbutdecreasedforAfricangoldencatwhite‐belliedduikerandwaterchev‐rotainIntheNorthernSectoroccupancyincreasedwithdistancetotheboundaryforBatesrsquospygmyantelope
4emsp |emspDISCUSSION
Thecomparisonofthetwosurveysconfirmsthatstandardcameratrap surveys and derived metrics of presenceabsence trappingrates andoccupancy candiscern confidentdifferences in ground‐dwellingmammalcommunitiesinCentralAfricanforests
41emsp|emspCamera trap surveys for documenting species
Thecomparativeefficacyofcamera traps for surveyingmediumto large ground‐dwelling mammals in the DFR is indicated byobservationratesandverifiabilityofrecordsespeciallyofelusivesmallerandnocturnalspeciesForexamplethedirectencounterraterecordedbyrangersonpatrolthroughouttheentirereserveover a nine‐month period is much lower than the combinednumberofindependentphotographiceventsinbothmanagementsectors (ZSL amp MINFOF 2017b) even for relatively largeconspicuous species such as forest elephant (96 photographiceventscomparedto29directencounters)andcentralchimpanzee(204 independent photographic events compared to 23 directencounters)Methodologiessuchascameratrapping therefore
provideimportantbaselinedatathatwhenrepeatedthroughtimeusingastandardisedprotocolcanallowatleasttrendsinrelativeabundanceindicestobemonitored
42emsp|emspCamera trap surveys for comparing assemblages among sites
Despitebeingseparatedbyonlyc32kmthemammalcommunitiesbetween the twocamera trapgridsdisplayedmarkeddifferencesThiswasthecaseeventhoughbothgridshadlowShannonndashWeinerandSimpsonsdiversityindicesduetothedominanceofthreeorfourspeciesineachcameratrapgridSignificantdifferencesamongthesiteswere observed for the trapping rates of species of differentsizesbetweensectorsSmaller‐bodiedspecieswithintheherbivoreand omnivore guilds were more prevalent within the NorthernSector (Figure 2) Trapping rates and occupancy values for smallcarnivoresarealsolowerintheSouthernSectorThiscouldbeduetothedifficultyofidentifyingmorphologicallysimilarspeciessuchasmarshmongooseandlong‐nosedmongoose(Bahaa‐el‐dinetal2013 Ray 1997) in infrared imagery with single cameras Thereweremoreunidentifiablemongooseeventsthatwereclassifiedtoafamilylevel―66224intheSouthernSectorcomparedto29156intheNorthernSectorofallcombinedmongooseevents
43emsp|emspThe potential impact of seasonality on estimates derived from camera traps
Due to logistical and financial constraints the surveys could notberuninthesameseasonThishasthepotentialtoaffecttrapping
F I G U R E 5 emspChangeintheprobabilityofoccupancyforblack‐leggedmongoosecentralchimpanzeeandCamerooncusimansewithmanagementsectoraccordingtoaRoylendashNicholsmodel
emspensp emsp | emsp771Bruce et al
rates and occupancy for specieswith larger home ranges becausewhenspeciesarewide‐rangingoccupancycanproveineffectiveformeasuring relative abundance Forest elephants (Blake 2002) andgreatapesareknowntodisplayseasonalshiftsintheirhabitatusageover great distances in response to increased fruit availability andprecipitation(HeadRobbinsMundryMakagaampBoesch2012)Thiscouldalsoinfluenceothergregariousspeciessuchasredriverhogthatarealsothoughttooccasionallydisplaysimilaraggregationsandmovementsinresponsetomastingevents(LeslieampHuffman2015)However as both red river hog and chimpanzee had significantlyhigherRAIandhigheroccupancywithvariabledetectionprobabilityaccording to the number of individuals incorporated this supports
thepossibilitythatthesespeciesarefavouringtheSouthernSectorIfmanagersareable toestablishwhetherwide‐rangingspeciesarepredictably moving to known areas within the reserve they canrespondinamannerthatprovidesenhancedprotectiontovulnerablewildlifepopulations in concentration areasAsmost species in thissurveylikelyhaveasmallerhomerangethantheinter‐trapdistanceand display fixed territories it can be regarded as appropriate tocompare occupancy values as the extent of overlap of territorieswithin the two surveys are unlikely to change in such away as toaffecttheresultsFuturestudieswouldbenefitfromtryingtomatchcameratrapsurveysseasonallytotryandclarifytheissueofseasonalshiftsinhabitatusagewithintheDFR
F I G U R E 6 emspChangeintheprobabilityofoccupancyforAfricanbrush‐tailedporcupineEminspouchedratredriverhogservalinegenetPetersrsquoduikerandyellow‐backedduikerwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
772emsp |emsp emspensp Bruce et al
F I G U R E 7 emspChangeintheprobabilityofoccupancyforblueduikerandbayduikerwithdistancetotheboundaryinkilometresacrossbothmanagementsectorsaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
F I G U R E 8 emspChangeintheprobabilityofoccupancyforwhite‐belliedpangolinwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaMackenzieoccupancymodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
emspensp emsp | emsp773Bruce et al
44emsp|emspCamera trap surveys for measuring the impacts of hunting on mammal communities
The spatial scale at which mammal communities are affected byandhowpopulationsrespondtoanthropogenicpressuressuchasbushmeat hunting is difficult to empiricallymeasure (Laurance etal2006)Thisisespeciallytrueformammalsresidingwithintropi‐cal forestswheregatheringconsistentandmeaningfulpopulation‐andcommunity‐levelmetrics ischallenging(Ahumadaetal2013)Population density of tropical mammals can vary greatly due toheterogeneity present within the environment For example for‐est elephants havedifferent distributions and aggregations inwetanddryseasonsinNouabaleacute‐Ndoki NationalParkwhichispartiallydependentonspatio‐temporalpatternsoffruitingtreesacrossthelandscape(Blake2002)
Whether the differences observed among the two sites sur‐veyedhereareattributabletodifferent levelsofhuntingpressureremains to be confirmed There are however indications thathuntingpressureanditsimpactsonmammalfaunasaregreaterintheNorthern Sector than in the Southern Sector The effects ofhuntingpressureonmammaliandeclinesinCentralAfricanforestsarewell documented The pattern in general is the largest‐bod‐ied species frugivores and thosewith high hunter or blackmar‐ketvalue(Abernethyetal2013Cardilloetal2005FaOliveroFarfaacutenMaacuterquezDuarteetal2014aFaOliveroFarfaacutenMaacuterquezVargasetal2014bPeresampPalacios2007)arethefirstspeciestoshownoticeabledeclineInthisstudythesignificantdeclineintherelativeabundance for frugivores suchasPetersʼduikerandspe‐cieswithhighhuntervalueliketheredriverhogunderincreasedhuntingpressure in theNorthernSector is reported inother sur‐veys(Abernethyetal2013)Thisisalsoreflectedinthedifferencesobserved in this study in biomass in the different guilds of eachmammalcommunityThemammalcommunitywithintheNorthernSector shows indications of a community that is disturbed and isexperiencingelevatedhuntingpressureThesearehigher(camera)trapping rates for smaller‐bodiedspecies suchasEminrsquospouchedrat and significantly fewer encounters of larger‐bodiedmammalsthataretargetsofthebushmeattradesuchasPetersʼduikerandredriverhog(FaRyanampBell2005JerozolimskiampPeres2003)Additionalindicatorsaretheabsenceinthesurveysoflargercarni‐voresintheNorthernSectorsuchasgoldencatandleopardwhicharesensitivetosnaring(Bahaa‐el‐dinetal2015)andsignificantlyreducedabundancemetricsfordisturbance‐sensitivespeciessuchasblack‐leggedmongooseandwaterchevrotain(Hart2013a)Theabsence of white‐bellied duiker in the Northern Sector also sug‐gestselevatedhumandisturbanceasthisspecieshasbeenreportedasverysensitivetoevenminorperturbationwithintheenvironment(Hart2013b)IncomparisontheSouthernSectorcontainedindica‐torfaunasuchasthewhite‐belliedduikerandhadhighertrappingratesforlarger‐bodiedspecies
WesuspectthedifferencesobservedaremostlikelyduetolowerhumandisturbanceintheSouthernSectorTheteamsdeployingand
recoveringthecamerasintheSouthernSectorcovered238kmandencountered few signs of humanperturbation (T Brucepers obs)whereashumansignwascommonlyencounteredbytheteamsintheNorthernSectorThisperceiveddifference is reflected in the2017and 2018 density of hunting signwithin each camera trap grid asdetected throughMINFOF ranger patrols (ZSL ampMINFOF 2017a2017b) and through the2018DistanceSampling inventory for theDFR (Bruce et al 2018) Higher numbers of hunting sign in theNorthernSectorwouldbeconsistentwithanelevatedhuntingpres‐sureinthatarea
45emsp|emspProtection of refugia from hunting
Though inferences made for wide‐ranging species such as forestelephantsandgreatapesusingcameratrapsaredifficultthefactthattrappingrateswerehigherinmorechallengingterrainwithassumedlower hunting pressure could be indicative of complex habitatprovidingsomelevelofprotectionfromhuntingElephantisknownto retreatwhen they aredisturbed to terrain that ismoredifficulttoaccessbyhumans (Hedges2012)Thuswithin largerprotectedareas certain zones may act as refugia for wildlife populations(Campbelletal2011)Thiscanbeduetoarangeof factorssuchas remoteanddifficult terrain forpoachers (Attum2007Hedges2012) or the regular presence of field researchers and rangers(Campbell et al 2011) The significanceof these refugia for largerprotected areas is that the populations of wildlife residing withinthem if adequately protected may provide source populations toallowrecolonisationofotherareasofthereserve(NaranjoampBodmer2007)Thereforeifadequateprotectioncanbeprovidedtorelativelysmallbutimportantareasoflargereservesthismayprovidetropicalforestswithabetterchanceofbeingecologicallyresilienttoongoingand increasing human perturbation Well‐designed camera trapsurveys may provide data on the status of wildlife populations atrelativelyfinespatialresolutionssoastoidentifyfunctionalrefugiawithgreaterconfidence
ACKNOWLEDG EMENTS
WeappreciatetheongoingsupportofCameroonrsquosMinistryofForestsandWildlife(MINFOF)andtheopportunitytocontributetobiodiver‐sityconservationthroughoutthecountryInparticularwewouldliketothanktheChefdrsquoAntenneSergeJacobMeyeforhisongoingsup‐portofconservationresearchwithintheprotectedareaWeappreci‐atethestalwarteffortsofMINFOFecoguardsandlocalporterswhoaccompaniedthesurveyteamsinthefieldWewouldalsoliketothanktheUnitedStatesFishandWildlifeService(USFWS)mdashAfricanElephantConservationandIUCNSOSmdashFondationSegreacutePangolinConservationInitiativeforsupportingthiswork
ORCID
Tom Bruce httporcidorg0000‐0001‐6958‐1657
774emsp |emsp emspensp Bruce et al
R E FE R E N C E S
AbernethyKACoad L TaylorG LeeMEampMaisels F (2013)Extent and ecological consequences of hunting in Central Africanrainforests in thetwenty‐firstcenturyPhilosophical Transactions of the Royal Society of London Biological Sciences368(1625)20120303httpsdoiorg101098rstb20120303
AbrahamsM I Peres C A amp Costa H C (2017)Measuring localdepletion of terrestrial game vertebrates by central‐place hunt‐ers in rural Amazonia PLoS ONE 12(10) e0186653 httpsdoiorg101371journalpone0186653
AhumadaJAHurtadoJampLizcanoD(2013)MonitoringthestatusandtrendsoftropicalforestterrestrialvertebratecommunitiesfromcameratrapdataAtool forconservationPLoS ONE8(9)e73707httpsdoiorg101371journalpone0073707
Ahumada J A Silva C E Gajapersad K Hallam C Hurtado JMartin E hellip Sheil D (2011) Community structure and diver‐sity of tropical forest mammals Data from a global camera trapnetwork Philosophical Transactions of the Royal Society of London Biological Sciences366(1578)2703ndash2711httpsdoiorg101098rstb20110115
AminRAndanjeSAOgwonkaBAliAHBowkettAEOmarMampWacherT(2015)ThenortherncoastalforestsofKenyaarenationally and globally important for the conservation of AdersrsquoduikerCephalophusadersiandotherantelopespeciesBiodiversity and Conservation 24(3) 641ndash658 httpsdoiorg101007s10531‐014‐0842‐z
Attum O (2007) Can landscape use be among the factors that po‐tentiallymake some ungulates speciesmore difficult to conserveJournal of Arid Environments69(3)410ndash419
Bahaa‐el‐dinLHenschelPAbaaRAbernethyKBohmTBoutNhellipLeeM (2013)NotesonthedistributionandstatusofsmallcarnivoresinGabonSmall Carnivore Conservation4819ndash29
Bahaa‐el‐dinLHenschelPButynskiTMMacdonaldDWMillsDSlotowRampHunterL (2015)TheAfricangoldencatCaracalaurataAfricasleast‐knownfelidMammal Review45(1)63ndash77
Bennett E L Blencowe E Brandon K Brown D Burn R WCowlishaw G hellip Robinson J G (2007) Hunting for consensusReconcilingbushmeatharvestconservationanddevelopmentpol‐icyinWestandCentralAfricaConservation Biology21(3)884ndash887httpsdoiorg101111j1523‐1739200600595x
BlakeSDeemSLMossimboEMaiselsFampWalshP(2009)Forestelephants Tree planters of the CongoBiotropica41(4) 459ndash468httpsdoiorg101111j1744‐7429200900512x
Blake S (2002) The ecology of forest elephant distribution and itsimplications for conservation Doctoral dissertation University ofEdinburgh
BruceTNdjassiCFowlerANdimbeMFankemOTabueRhellipOlsonD(2018)Faunal inventory of the Dja Faunal Reserve Cameroon Yaoundeacute Cameroon Ministry of Forests and Wildlife (MINFOF)Zoological Society of London ndash Cameroon Country ProgrammeAfricanWildlifeFoundation
BruceTWacherTNdingaHBidjokaVMeyongFNgoBataMampOlsonD(2017)camera trap survey for larger terrestrial wildlife in the Dja Biosphere Reserve CameroonYaoundeacuteCameroonZoologicalSocietyofLondon(ZSL)ampCameroonMinistryofForestsandWildlife(MINFOF)
BurnhamKPampAndersonDR(2002)Model selection and multimodel inferenceNewYorkNYSpringer
Campbell G Kuehl H Diarrassouba A NGoran P K amp BoeschC (2011) Long‐term research sites as refugia for threatened andover‐harvested species Biology Letters 7(5) 723ndash726 httpsdoiorg101098rsbl20110155
CardilloMMaceGMJonesKEBielbyJBininda‐EmondsORSechrestWhellipPurvisA(2005)Multiplecausesofhighextinction
riskinlargemammalspeciesScience309(5738)1239ndash1241httpsdoiorg101126science1116030
Craigie IDBaillieJEBalmfordACarboneCCollenBGreenREampHuttonJM (2010)Largemammalpopulationdeclines inAfricarsquosprotectedareasBiological Conservation143(9)2221ndash2228httpsdoiorg101016jbiocon201006007
DaveyKWacherTampAminR(2017)Analysis tool for camera-trap sur-vey data [Computer software]ZoologicalSocietyofLondonRetrievedfromhttpswwwzslorgzsl‐camera‐trap‐data‐management‐ and‐analysis‐package
Djuikouo M N K Doucet J L Nguembou C K Lewis S L ampSonkeacute B (2010) Diversity and aboveground biomass in threetropical forest types in the Dja Biosphere Reserve Cameroon African Journal of Ecology 48(4) 1053ndash1063 httpsdoiorg101111j1365‐2028201001212x
DupainJBombomeKampVanElsackerL(2003)LeschimpanzeacutesetlesgorillesdelareacuteservedefauneduDjaCanopeacutee2414ndash15
EffordMGampDawsonDK(2012)OccupancyincontinuoushabitatEcosphere3(4)1ndash15httpsdoiorg101890ES11‐003081
Efron B amp Tibshirani R J (1994) An introduction to the bootstrap WashingtonDCCRCPress
FaJEOliveroJFarfaacutenMAacuteMaacuterquezALDuarteJNackoneyJhellipMacdonaldDW(2014a)CorrelatesofbushmeatinmarketsanddepletionofwildlifeConservation Biology29(3)805ndash815
Fa J EOlivero J FarfaacutenMAacuteMaacuterquezA LVargas JMRealRampNasiR(2014b)IntegratingsustainablehuntinginbiodiversityprotectioninCentralAfricaHotspotsweakspotsandstrongspotsPLoS ONE9(11)e112367
FaJERyanSFampBellDJ (2005)Huntingvulnerabilityecolog‐ical characteristics and harvest rates of bushmeat species in afro‐tropicalforestsBiological Conservation121(2)167ndash176httpsdoiorg101016jbiocon200404016
Fa J E Seymour S Dupain J E F Amin R Albrechtsen L ampMacdonaldD (2006) Getting to gripswith themagnitude of ex‐ploitationBushmeat in theCross‐SanagariversregionNigeria and Cameroon Biological Conservation 129(4) 497ndash510 httpsdoiorg101016jbiocon200511031
Farris Z J Boone H M Karpanty S Murphy A Ratelolahy FAndrianjakariveloVampKellyMJ(2015)FeralcatsandthefitoatyFirstpopulationassessmentoftheblackforestcatinMadagascarrsquosrainforestsJournal of Mammalogy97(2)518ndash525
Fiske IampChandlerR (2011)UnmarkedAnRpackageforfittinghi‐erarchicalmodelsofwildlifeoccurrenceandabundanceJournal of Statistical Software43(10)1ndash23
HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences107(19)8650ndash8655httpsdoiorg101073pnas0912668107
HartJ(2013a)WaterchevrotainHymemoschusaquaticusInJKingdonampMHoffmann (Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp88ndash92)LondonUKBloomsbury
Hart J (2013b) White‐bellied duiker Cephalophus leucogaster In JKingdonampMHoffmann(Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp255ndash258)LondonUKBloomsbury
HeadJSRobbinsMMMundryRMakagaLampBoeschC(2012)Remotevideo‐cameratrapsmeasurehabitatuseandcompetitiveex‐clusionamongsympatricchimpanzeegorillaandelephantinLoangoNational ParkGabon Journal of Tropical Ecology28(06) 571ndash583httpsdoiorg101017S0266467412000612
HedgesS(2012)Monitoring elephant populations and assessing threats HimayatnagarTelanganaUniversitiesPress
HedwigDKienastIBonnetMCurranBKCourageABoeschChellipKingT(2018)Acameratrapassessmentoftheforestmam‐mal community within the transitional savannah‐forest mosaic oftheBateacutekeacutePlateauNationalParkGabonAfrican Journal of Ecology56(4)777ndash790httpsdoiorg101111aje12497
emspensp emsp | emsp775Bruce et al
HijmansRJCameronSEParraJLJonesPGampJarvisA(2005)Very high resolution interpolated climate surfaces for global landareasInternational Journal of Climatology25(15)1965ndash1978httpsdoiorg101002joc1276
HuggelA(2012)Exiv2softwaretool[Computersoftware]Retrievedfromhttpswwwexiv2orgindexhtml
Jerozolimski A amp Peres C A (2003) Bringing home the biggestbacon A cross‐site analysis of the structure of hunter‐kill profilesin Neotropical forests Biological Conservation 111(3) 415ndash425httpsdoiorg101016S0006‐3207(02)00310‐5
KingdonJ (2015)The Kingdon field guide to African mammalsLondonUKBloomsburyPublishing
KuumlhlHFMaiselsMAncrenazampEAWilliamson(Eds)(2008)Best practice guidelines for surveys and monitoring of great ape populations GlandSwitzerlandIUCN
LauranceWFCroesBMTchignoumbaLLahmSAAlonsoALeeMEhellipOndzeanoC(2006)ImpactsofroadsandhuntingoncentralAfrican rainforestmammalsConservation Biology20(4)1251ndash1261httpsdoiorg101111j1523‐1739200600420x
LauranceWFUsecheDCRendeiroJKalkaMBradshawCJSloan S P hellip Arroyo‐Rodriguez V (2012) Averting biodiversitycollapse in tropical forestprotectedareasNature489(7415)290httpsdoiorg101038nature11318
LeslieDMampHuffmanBA(2015)Potamochoerus porcus(ArtiodactylaSuidae)Mammalian Species4715ndash31
MacKenzieD IampBailey L L (2004)Assessing the fit of site‐occu‐pancy models Journal of Agricultural Biological and Environmental Statistics9300ndash318httpsdoiorg101198108571104X3361
MacKenzieDINicholsJDRoyleJAPollockKHBaileyLLampHinesJE (2006)Occupancy estimation and modellingBurlingtonMAAcademicPress
Magurran A E (2005) Species abundance distributions Patternor process Functional Ecology 19(1) 177ndash181 httpsdoiorg101111j0269‐8463200500930x
MaiselsFStrindbergSBlakeSWittemyerGHartJWilliamsonEAhellipWarrenY (2013)DevastatingdeclineofforestelephantsinCentralAfricaPLoS ONE8(3)e59469httpsdoiorg101371journalpone0059469
MalhiYAdu‐BreduSAsareRA LewisS LampMayauxP (2013)AfricanrainforestsPastpresentandfuturePhilosophical Transactions of the Royal Society of London Biological Sciences 368(1625)20120312
MallonDPHoffmannMGraingerMJHibertFVanVlietNampMcGowanP JK (2015)An IUCNsituationanalysisof terrestrialandfreshwaterfaunainWestandCentralAfricaOccasionalpaperoftheIUCNspeciessurvivalcommission(54)
MambeyaMMBakerFMombouaBRKoumbaPamboAFHegaMOkouyiOkouyiVJhellipAbernethyK(2018)TheemergenceofacommercialtradeinpangolinsfromGabonAfrican Journal of Ecology56(3)601ndash609httpsdoiorg101111aje12507
MINFOFampIUCN(2015)CaracteacuterisationdelapopulationdegrandsetmoyensmammifegraveresdanslaReservedeFauneduDjaPotentieletmenacesYaoundeacuteCameroun
Muchaal P K amp Ngandjui G (1999) Impact of village hunt‐ing on wildlife populations in the western Dja ReserveCameroon Conservation Biology 13(2) 385ndash396 httpsdoiorg101046j1523‐17391999013002385x
NaranjoEJampBodmerRE (2007) Sourcendashsink systemsandconser‐vationofhuntedungulatesintheLacandonForestMexico Biological Conservation 138(3ndash4) 412ndash420 httpsdoiorg101016jbiocon 200705010
NielsenMR(2006)ImportancecauseandeffectofbushmeathuntingintheUdzungwaMountainsTanzania ImplicationsforcommunitybasedwildlifemanagementBiological Conservation128(4)509ndash516httpsdoiorg101016jbiocon200510017
OBrienTGKinnairdMFampWibisonoHT (2003)Crouching ti‐gers hiddenprey Sumatran tiger andprey populations in a tropi‐calforestlandscapeAnimal Conservation6(2)131ndash139httpsdoiorg101017S1367943003003172
OksanenJ(2015)VegananintroductiontoordinationVol8(p19)Retrieved from httpscranr‐projectorgwebpackagesveganvi‐gnettesintroveganpdf
PeresCAampPalaciosE(2007)Basin‐wideeffectsofgameharvestonvertebrate populationdensities inAmazonian forests Implicationsfor animal‐mediated seed dispersal Biotropica 39(3) 304ndash315httpsdoiorg101111j1744‐7429200700272x
PotapovPVTurubanovaSAHansenMCAduseiBBroichMAltstattAhellipJusticeCO(2012)QuantifyingforestcoverlossinDemocraticRepublicoftheCongo2000ndash2010withLandsatETM+data Remote Sensing of Environment 122 106ndash116 httpsdoiorg101016jrse201108027
PoulsenJRKoernerSEMooreSMedjibeVPBlakeSClarkC JhellipRosinC (2017) Poaching empties criticalCentralAfricanwilderness of forest elephants Current Biology 27(4) 134ndashR135httpsdoiorg101016jcub201701023
PurvisAGittlemanJlCowlishawGampMaceGM(2000)PredictingextinctionriskindecliningspeciesProceedings of the Royal Society B Biological Sciences267(1456) 1947ndash1952 httpsdoiorg101098rspb20001234
RayJ(1997)ComparativeecologyoftwoAfricanforestmongoosesHerpestesnasoandAtilaxpaludinosusAfrican Journal of Ecology35(3)237ndash253httpsdoiorg101111j1365‐20281997086‐ 89086x
Redford K H (1992) The empty forest BioScience 42(6) 412ndash422httpsdoiorg1023071311860
RepublicofCameroon(1994)Lawno9401du20janvier1994portantreacutegimedesforecirctsdelafauneetdelapecirccheRepublicofCameroon
RoveroFampMarshallAR(2009)CameratrappingphotographicrateasanindexofdensityinforestungulatesJournal of Applied Ecology46(5)1011ndash1017httpsdoiorg101111j1365‐2664200901705x
Royle J A amp Nichols J D (2003) Estimating abundance from re‐peated presence‐absence data or point counts Ecology 84(3)777ndash790 httpsdoiorg1018900012‐9658(2003)084[0777EAFRPA]20CO2
Seddon P J Griffiths C J Soorae P S ampArmstrongD P (2014)ReversingdefaunationRestoringspeciesinachangingworldScience345(6195)406ndash412httpsdoiorg101126science1251818
Silveira L Jacomo A T amp Diniz‐Filho J A F (2003) Camera trapline transect census and track surveys A comparative evaluationBiological Conservation 114(3) 351ndash355 httpsdoiorg101016S0006‐3207(03)00063‐6
Sonkeacute B (1998) Etudes floristiques et structurales des forecircts de laReacuteserve de Faune du Dja (Cameroun) Laboratoire de BotaniqueSysteacutematique et de Phytosociologie Universiteacute Libre de Bruxelles(ULB)
Srbek‐AraujoACampChiarelloAG(2005)Iscameratrappinganeffi‐cientmethodforsurveyingmammalsinNeotropicalforestsAcasestudyinsouth‐easternBrazilJournal of Tropical Ecology21(1)121ndash125httpsdoiorg101017S0266467404001956
Stiles D (2011) Elephant meat and ivory trade in Central AfricaPachyderm5026ndash36
TEAMNetwork(2008)Terrestrialvertebrateprotocol implementationmanualv30(p56)WashingtonDCTropicalEcologyAssessmentandMonitoringNetworkCenter forAppliedBiodiversity ScienceConservationInternational
Tobler M W Carrillo‐Percastegui S E Leite Pitman R MaresR amp Powell G (2008) An evaluation of camera traps for in‐ventorying large‐and medium‐sized terrestrial rainforestmammals Animal Conservation 11(3) 169ndash178 httpsdoiorg101111j1469‐1795200800169x
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
emspensp emsp | emsp761Bruce et al
thehumanpopulationaroundthereserveisincreasingandindustriessuchasloggingrubberhydropowerandminingareproliferatingre‐sultinginincreaseddemandforbushmeatBothillegalnon‐traditionalsubsistenceandcommercialhuntingoccurwithinthereserve
22emsp|emspNorthern and southern sector sites
WesetupcameratrapgridsintheNorthern(management)Sector(centredon03deg13rsquo33rsquorsquoN12deg48rsquo18rsquorsquoE)betweenNovember2015andMay 2016 and the Southern (management) Sector (02deg59rsquo37rsquorsquoN13deg07rsquo43rsquorsquoE)oftheDFRbetweenMayandJune2017(Figure1)ThecameratrapgridwithintheNorthernSectorwasplacedusingthenorthernprotectedareaboundaryasanapproximatebaselineref‐erenceThecamerasweresetovera rangeofc31 toc159kmfromtheboundaryof the reservewithanaveragedistanceof95(SEplusmn39)kmfromtheboundaryCameraswereplacedonaverage123(SEplusmn38)kmfromthenearestsettlementswitharangeofbe‐tweenc6and188kmTheNorthernSectorof theDjapresentsagenerallyhigherandmoreuniformelevation(662ndash720masl)thanthe Southern Sector (563ndash689masl) Watercourses are sparserand swamp habitat less common within this management sectorCorrespondinglythenortherncameratrapstationswereonaver‐agemoredistantfromthenearestwatercourse(c261km)andonlytwonortherncameraswereplacedinswamphabitat
Thecameras in theSouthernSectorgridwereplacedonaver‐age123(SEplusmn38)kmoverarangeofc57ndash19kmfromthereserveboundary and were between c 77 and 22km from the nearesthuman settlementwith anaveragedistanceof155 (SEplusmn37) kmThetopographywithinthesoutherncameratrapgridismorecom‐plexwithagreaterelevationalvariationThegreaterprevalenceoflowlandareasresultedinmoreswamphabitat(fivecamerasplacedwithin 50m of swamp habitats) and cameras being on averageplacedclosertowatercourses(c06km)
23emsp|emspcamera trap surveys
Forty cameraswere placed at each localitywith a 2km spacingbetweeneachcamera(Ahumadaetal2011)(Figure1)Eachgridoperatedlongenoughtoachieveatleast1000cameratrapdaysofsamplingeffort(OrsquoBrienKinnairdampWibisono2003)WeusedGlobalPositioningSystemreceiverstolocatethegridpointsAsin‐gle camerawas positioned 30ndash45cm above ground level within200m of each point aimed at a game trail that provided suffi‐cient fieldofviewtocapture lateral full‐body imagesofsmall tomedium‐sizedmammals Siteswere selected based on the pres‐enceofagametrail(Aminetal2015)tomaximisetheprobabil‐ityofobtainingusefulphotographs(TEAM2008)andasuitabletreeallowing thecamera tobepositioned facingeithernorthor
F I G U R E 1 emspLocationoftheDjaFaunalReserveCameroon(a)andthelocationofcameratrapgridsintheNorthernandSouthernsectors(b)Managementsectorsareingrey[Colourfigurecanbeviewedatwileyonlinelibrarycom]
762emsp |emsp emspensp Bruce et al
south tominimise the impacts of sunrise and sunset on cameraperformance
We used three different camera models across the two grids(BushnellAggressorReconyxHC500 andCuddebackLong rangeIRE2)Detectionrangewasatleast25mwitheitheratwo‐seconddelay(Bushnell‐2015NorthernSectorsurvey)orone‐seconddelay(ReconyxCuddebackandBushnell‐2017SouthernSectorsurvey)ThreeconsecutiveimagesweretakenpertriggerLowglowinfraredflashlightingwasusedtominimisetheriskofstartlinganimalsThefulllistofsettingsforeachcameracanbefoundinAnnex1
24emsp|emspNatural mammal fauna
Thereserveisreportedtocontain109speciesofmammalofwhich35speciesareterrestrialandhaveabodyweightgt05kg(Kingdon2015) Currently the only baseline data for populations for thesespecieswithinthereservecomefromencounterratesfromrangerpatrolsanddistancesamplingthroughlinetransectsurveys(DupainBombomeampVanElsacker2003MINFOFampIUCN2015WilliamsonampUsongo1995)
25emsp|emspAssessment of differences in human activity
Toassesstherelativedifferencesinhumanactivityincludinghunt‐ing between theNorthern and Southern Sectorwhere the twosites were located we evaluated trends from multiple sourcesEvidence of human sign was recorded on 1‐kilometre line tran‐sectsduringafullfaunalinventoryoftheDFR(Bruceetal2018)TransectsareoftenusedtomonitorthetrendsofhumanimpactsinCentralAfricanforests(Kuumlhletal2008)Therewereatotalof86and76transectscoveringadistanceof916and807kmcom‐pleted intheNorthernSectorandSouthernSector respectivelyEncountersofhumansignbetweenJanuary2016andSeptember2017byMinistryofForestsandWildlife(MINFOF)rangerpatrolswhorecorddatausingSpatialMonitoringAndReportingToolde‐viceswerealsoused(ZSLampMINFOF2017a2017b)Abufferof2kmwassetaroundeachcameraandthesignwithinthisareawasconvertedintotheamountofhumansignperkm2Thisbufferwasusedtocounteractunequalsurveyeffortwithinthesectorspos‐siblyduetoecoguardsbeingrequiredtobepresentataresearchstation in theNorthernSectorat thebottomof thecamera trapgrid
Transects provide a more objective measure of hunting pres‐sureastheyuseastandardisedmethodologyandteamcompositioncompared to rangerpatrolsTransectsarenotbiasedby followingtrailsorotherpathsofleastresistancethataffectstheprobabilityofhumansignbeingdetected
26emsp|emspData analysis
WeusedExiv2software(Huggel2012)toextractEXIFinformationfromeachphotograph(imagenamedateandtime)SpeciesofanimalinthephotographswereidentifiedwhenpossibleThesedatawere
compiled in an Excel spreadsheet (Microsoft Office ProfessionalPlus2016Version1809)andanalysedwithsoftwaredevelopedbyat ZSL (CameraTrapAnalysis Package [CTAP]) (DaveyWacherampAmin2017)
Weonlyconsideredterrestrialmammalspeciesthathaveanesti‐matedaveragemassgreaterthan05kg(medium‐to‐largemammals)fortheanalysesbecausetheyarethemaintargetgroupforcameratrapsplacedatgroundlevelSmallermammalsinducesamplingerrorthroughareducedlikelihoodofdetectionbythecameratraprsquosther‐malsensorandaccurateidentificationofsmallmammalstospecieslevelisdifficultfromcameratrapsset‐upformedium‐to‐largemam‐mals(Tobleretal2008)
We calculated rarified species accumulation curves and esti‐matedthemedium‐to‐largeterrestrialmammalspeciesrichnessforeachsectorusingtheZSLCTAPtool
We calculated Simpsonrsquos diversity index and ShannonndashWeinerdiversity index foreach sector fromspeciesdaily trap ratesusingpackageveganinRstatisticalsoftware(Oksanen2015)Simpsonrsquosdiversityindexismostsensitivetochangesinmorecommonhighlyabundant species while ShannonndashWeiner diversity index is mostsensitivetochangesinrarelessabundantspecies(Magurran2005)
Wecalculatedthenumberofindependentphotographiceventsper100trapdaysasarelativeabundanceindex(RAI)foreachspeciesWedefinedanldquoeventrdquoasanysequenceforagivenspeciesoccurringafteranintervalofge60minfromthepreviousthree‐imagesequenceof that species to ensure that species events were independent(Aminetal2015Tobleretal2008)Theeventswereautomati‐cally screenedby theZSLCTAPsoftwareWecalculated the95confidenceintervalsusingthebootstrapmethod(EfronampTibshirani1994)andconsiderednon‐overlappingconfidenceintervalsasindic‐ativeofasignificantdifferenceinRAIbetweenmanagementsectorsWeassumethatthecameratrappingratescalculatedastheRAIre‐flectactualrelativeabundanceasinRoveroandMarshall(2009)
We used single‐season occupancy analysis (MacKenzie et al2006) where assumptions and data quality allowed to estimatethe proportion of area occupied by a species within each gridOccupancyestimateswerecorrectedbydetectionprobability (iethelikelihoodthataspecieswasdetectedwhenpresent)andthere‐foreprovideamore rigorous indexofabundance forbothwithinandbetweenspeciescomparisonsThishoweverislimitedtospe‐ciesgeneratingadequatedatasetswherecameraspacingisgreaterthanthespecieshomerangeandoccupancyisnotconfoundedbychanges in the home range (Efford ampDawson 2012) For all theoccupancyanalyseswegenerated1110‐daysamplingoccasionsThismeanttheNorthernSectordataweretruncatedtomatchthenumberofoccasionsavailableforanalysis intheSouthernSectorWetestedforsignificantdifferencesinspeciesoccupancybetweenthe Northern and Southern sectors using the ldquoWaldrdquo parametricstatisticaltestasitisknowntobeanindependentandrobustmea‐sureofdifference(Aminetal2015)withplt005consideredtobesignificant
We alsomodelled occupancy as a function of site covariatesdistance to the protected area boundary in kilometres (D) and
emspensp emsp | emsp763Bruce et al
management sector (M) using the ldquounmarkedrdquo (Fiske amp Chandler2011) software package in R We treated detection probabilityas a constant and evaluated all covariate combinations ψ ()p()ψ (D)p() ψ (M)p() ψ (DM)p() ψ (D+M) p() For covariate anal‐ysis tocompare themanagementsectorswealso implementedaRoylendashNicholsmodel(2003)whichtakesintoaccountthenumberofindividualsatasiteinfluencingdetectionprobabilityandthusoc‐cupancyTheselectionofRoylendashNicholsmodelaboveasingle‐sea‐sonmodelforaspecieswouldprovidefurthersupportthatspeciesabundance was significantly different between the managementsectorsWe rankedmodelsbyAkaikersquos informationcriteria (AIC)andmodels that had a delta AIC of lt2were considered to be acompetingmodel(BurnhamampAnderson2002)Thec‐hatandchi‐squared values to assessmodel dispersionwere generated usingtheMackenzie andBailey (2004) goodness‐of‐fit testwhichwasconducted using 1000 simulations for eachmodelModels witha c‐hatgt2were rejectedas theywere regardedasoverdispersed(Farrisetal2015)
3emsp |emspRESULTS
Weaccumulated3725operationalcameratrapdays(mean91dayscamera)intheNorthernSectorand3371operationalcameratrapdays(mean84dayscamera)intheSouthernSectorIntheNorthernSector grid ten cameras were lost or damaged by people or el‐ephants and somemalfunctioned The Southern Sector only hadeightcamerasfailduetothesameissuesaswellastoleoparddam‐age In total 16 cameraswere excluded fromoccupancy analysisduetobeingoperationalforlt80ofoccasions
31emsp|emspRelative assessment of human sign
Overallhumanpressureasmeasuredbyhumansignwithinthere‐servewasmoreabundant intheNorthernSectorcomparedtotheSouthern Sector Encounter rate of human sign on transects was154km in theNorthern Sector three times higher than 049kmintheSouthernSectorAsimilarpatternwasobserved inthedatagatheredbyMINFOF rangers TheNorthern Sector had a densityofhuntingsignof087km2 withintheareaofthegridincludingthe2km buffer compared to 008km2 in the Southern Sector Giventhatseveralsignsmeasuredarecloselyassociatedwithhuntingac‐tivitysuchassnaresandcartridgesweassumethathuntingactiv‐ityisonaveragehigherintheNorthernSectorthantheSouthernSector
32emsp|emspSpecies richness
A total of 26 medium‐to‐large terrestrial mammal species werephotographedintheNorthernSectorand31medium‐to‐largeter‐restrialmammalspeciesintheSouthernSector(Table1)Wealsore‐cordedfivearborealmammalspeciesthatwerenotthetargetofthissurvey (Table1)Fourmedium‐to‐large terrestrialmammalspecies
expected to occur in the surveyed habitats according to availableIUCN distribution maps and literature were not detected by thecameratrapsurveysineithersector(Table1)
The species accumulation curves for medium‐to‐large terres‐trialmammal species showmore species detected per unit effortin theSouthernSector (Figure2)Thediversity indicesweremar‐ginally lower in the Northern Sector (Simpsons=072 ShannonndashWeiner=179)comparedtotheSouthernSector(Simpsons=078ShannonndashWeiner=208)
33emsp|emspCommunity structure
CommunitystructureofmammalsdifferedbetweentheNorthernSectorandSouthernSectorsites(Figures3and4)withmorespe‐ciesbeingencounteredforthreeoutofthefourguilds(herbivoresinsectivoresandcarnivores)intheSouthernSectorThemostfre‐quentlyencounteredguild inbothsectorswasherbivore (14spe‐ciesintheSouthernSectorand13intheNorthernSector)followedbyomnivore(seveninbothsectors)carnivore(sixintheSouthernSector four in theNorthernSector) and insectivore (three in theSouthernSector two in theNorthernSector)Overallacross theguilds trapping rates for lowerbodymassspecieswerehigher inthe Northern Sector A marked difference was the higher trap‐pingratesofherbivoresandomnivoreswithbodymassgt10kg intheSouthernSector (Figure4) compared to theNorthernSector(Figure3)
34emsp|emspForest antelopes
Werecorded4495independentphotographiceventsoftenspe‐ciesof forest antelopesTheblueduiker (Philantomba monticolaThunberg 1789) was the most frequently encountered forestantelope species across both camera trap grids (RAI=527) fol‐lowed by Petersrsquo duiker (Cephalophus callipygus Peters 1876)(RAI=412) and Bay duiker (Cephalophus dorsalis Gray 1846)(RAI=747) The rest of the forest antelopeswere relatively in‐frequently encounteredwith a global trapping rate of less thanfiveThedisturbance‐sensitivewhite‐belliedduiker(Hart2013b)wasonlyencountered in theSouthernSector (RAI=395 [lower95 confidence limit (LCL)=214 upper 95 confidence limit(UCL)=611])TrappingratesweresignificantlyhigherforPeterrsquosduiker in the Southern Sector displaying a fivefold increase be‐tween sectors (Table 1) Peterrsquos duiker occupancy was also sig‐nificantlyhigherintheSouthernSectorcomparedtotheNorthernSector (p=002 Table 2) Therewere no significant differencesin trapping rates between the two sectors forBatersquos pygmy an‐telope (Neotragus batesi de Winton 1903) bay duiker bongo(Tragelaphus eurycerusOgilbyi1837)sitatunga (Tragelaphus spe-kiiSpeke1863)andblack‐frontedduiker(Cephalophus nigrifrons Gray1871)Occupancyvaluesforbayduikerblack‐frontedduikerandBatersquospygmyantelopedidnotdiffersignificantlybetweenthesectorsTherewereinsufficientdetectionsoftheotherspeciestomodeloccupancy
764emsp |emsp emspensp Bruce et al
TA B L E 1 emspMammalspeciespredictedtoberecordedintheNorthernandSouthern(management)sectorsofDjaFaunalReserveCameroon
Order Species IUCN Status HabitatNorthern sector RAI (LCLndashUCL)
Southern sector RAI (LCLndashUCL)
Afrosoricida Giantottershrew(Potamogale velox Du Chaillu1860)
LC Wetland Notdetected Notdetected
Carnivora Africangoldencat(Profelis aurataTemminck1827)a
VU Forest Notdetected 058(027ndash091)
Carnivora Leopard(Panthera pardusLinnaeus1758)a
NT Mixed Notdetected 083(032ndash145)
Carnivora Marshmongoose(Atilax paludinosusCuvier1829)a
LC Wetland 056(033ndash082)b 009(0ndash02)b
Carnivora Black‐leggedmongoose(Bdeogale nigripesPucheran1855)a
LC Forest 183(079ndash314) 371(263ndash484)
Carnivora Camerooncusimanse(Crossarchus platycephalusGoldman1984)a
LC Forest 183(124ndash247) 083(046ndash127)
Carnivora Long‐nosedmongoose(Herpestes nasodeWinton1901)a
LC Forest 102(053ndash160) 089(009ndash227)
Carnivora Africanpalmcivet(Nandinia binotataGray1830)a
LC Forest 113(071ndash16) 089(052ndash13)
Carnivora Servalinegenet(Genetta servalinaPucheran1855)a
LC Forest 325(239ndash416) 214(142ndash295)
Carnivora Large‐spottedgenet(Genetta maculata Gray1830)
LC Forest Notdetected Notdetected
Carnivora CentralAfricanoyan(Poiana richardsoniiThomson1842)c
LC Forest Notdetected 003(003ndash009)
Cetartiodactyla Batesspygmyantelope(Neotragus batesideWinton1903)a
LC Forest 04(011ndash078) 036(015ndash059)
Cetartiodactyla Forestbuffalo(Syncerus cafferSparrmansubspnanus1779)a
EN Forest 008(0ndash024) 006(0ndash019)
Cetartiodactyla Petersduiker(Cephalophus callipygusPeters1876)a
LC Forest 141(838ndash2071)b 7146 (4963ndash9641)b
Cetartiodactyla Bayduiker(Cephalophus dorsalisGray1846)a
LC Forest 668(44ndash935) 834(492ndash1228)
Cetartiodactyla White‐belliedduiker(Cephalophus leucogastersubsp leucogasterGray1873)
LC Forest Notdetected 395(214ndash611)
Cetartiodactyla Black‐frontedduiker(Cephalophus nigrifronsGray1871)a
LC Forest 086(003ndash246) 05(006ndash114)
Cetartiodactyla Yellow‐backedduiker(Cephalophus silvicultorAfzelius1815)a
LC Forest 37(225ndash554) 555(354ndash794)
Cetartiodactyla Blueduiker(Philantomba monticolaThunberg1789)a
LC Forest 6164(4602ndash788) 4298(315ndash5561)
Cetartiodactyla Bongo(Tragelaphus eurycerusOgilbyi1837)a
NT Forest 005(0ndash014) 006(0ndash015)
Cetartiodactyla Sitatunga(Tragelaphus spekiiSpeke1863)a
LC Wetland 024(005ndash048) 009(0ndash024)
Cetartiodactyla Redriverhog(Potamochoerus porcusLinnaeus1758)a
LC Woodland 161(102ndash228)b 7(336ndash1304)b
Cetartiodactyla Giantforesthog(Hylochoerus mein-ertzhageniThomas1904)
LC Forest Notdetected Notdetected
Cetartiodactyla Waterchevrotain(Hyemoschus aquaticusOgilby1841)a
LC Forest 03(0ndash075)b 46(192ndash799)b
(Continues)
emspensp emsp | emsp765Bruce et al
35emsp|emspCarnivore
ThecarnivorecommunitydifferedinRAIandstructurebetweenthetwosectorsFelidswerenotdetectedatallintheNorthernSectorbutboth leopard (Panthera pardusLinneaus1758)andgoldencat(Profelis aurata Temminck1827)werepresentintheSouthernSector
(Table1)AmongtheHerpestidaeblack‐leggedmongoose(Bdeogale nigripes Pucheran1855) showeda significantlyhigheroccupancy(p =gt001)intheSouthernSectorbuttrappingrateslackedsignifi‐cantdifference (RAI=371 [LCL=263UCL=484])comparedtothe Northern Sector (RAI=183 [LCL=079 UCL=314])Marshmongoose(Atilax paludinosusCuvier1829)hadsignificantlyhigher
Order Species IUCN Status HabitatNorthern sector RAI (LCLndashUCL)
Southern sector RAI (LCLndashUCL)
Hyracoidea Westerntreehyrax(Dendrohyrax dorsalis Fraser1855)
LC Forest Notdetected Detected
Pholidota White‐belliedpangolin(Phataginus tricuspisRafinesque1821)a
VU Forest 062(029ndash1) 08(044ndash121)
Pholidota Giantpangolin(Smutsia giganteaIlliger1815)a
VU Forest 027(008ndash052) 068(038ndash101)
Primates Agilemangabey(Cercocebus agilisMilne‐Edwards1886)a
LC Forest 035(013ndash059) 448(265ndash682)
Primates Moustachedguenon(Cercopithecus cephusLinnaeus1758)c
LC Forest Detected Notdetected
Primates Greaterspot‐nosedguenon(Cercopithecus nictitansLinnaeus1766)c
LC Forest Detected Detected
Primates Blackcolobus(Colobus satanasWaterhouse1838)c
VU Forest Notdetected Detected
Primates Galagospc ‐ Detected Notdetected
Primates Mandrill(Mandrillus sphinxLinnaeus1758)a
VU Forest 005(0ndash013) 006(0ndash019)
Primates Westernlowlandgorilla(Gorilla gorillaSavagesubspgorilla1847)a
CR Forest 016(003ndash031) 044(02ndash073)
Primates Centralchimpanzee(Pan troglodytesBlumenbachsubsptroglodytes1799)a
EN Forest 161(077ndash29)b 457(314ndash617)b
Proboscidea Forestelephant(Loxodonta cyclotisMatschie1900)a
VU Mixed 086(046ndash135) 19(086ndash329)
Rodentia Africanbrush‐tailedporcupine(Atherurus africanusGray1842)a
LC Forest 1753(1142ndash2446) 762(464ndash1145)
Rodentia Eminspouchedrat(Cricetomys eminiWroughton1910)a
LC Forest 32(2358ndash4141)b 756(341ndash1465)b
Rodentia Greatercanerat(Thryonomys swinderi-anus Temminck1827)
LC Wetland Notdetected Notdetected
Rodentia LadyBurtonsropesquirrel(Funisciurus isabellaGray1862)c
LC Forest Detected Detected
Rodentia Fire‐footedropesquirrel(Funisciurus pyrropusCuvier1833)c
LC Forest Detected Detected
Rodentia Africangiantsquirrel(Protoxerus stangeriWaterhouse1842)c
LC Forest Detected Detected
Tubulidentata Aardvark(Orycteropus aferPallas1766)a LC Mixed Notdetected 009(005ndash019)
NotesForeachsectorandspeciesthatwasdetectedwepresentthemeanand95confidencelimits(inbrackets)ofthenumberofindependentphotographiceventspertrapdaytimes100Trappingrateswereonlycalculatedformedium‐to‐largeterrestrialmammalsduetoinconsistentdetectionprobabilitieswithotherspeciesIUCNstatuscriticallyendangered(CR)endangered(EN)vulnerable(VU)nearthreatened(NT)leastconcern(LC)aIndicatesaspeciesthatwasincludedintherarefactionanalysisaccordingtothedefinitiongiveinthedataanalysissectionofthemethodsbIndicatesthattheRAIconfidenceintervalsdonotoverlapandcanbeconsideredsignificantlydifferentcSignifiesanarborealspecies
TA B L E 1 emsp (Continued)
766emsp |emsp emspensp Bruce et al
F I G U R E 2 emspRarefiedspeciesaccumulationcurvesformedium‐to‐largeterrestrialmammalsintheNorthernandSouthernsectorsofDjaFaunalReserveCameroon
F I G U R E 3 emspDistributionofmedium‐to‐largeterrestrialmammalspeciesintheNorthernSectoroftheDjaFaunalReserveCameroononthebasisofbodysizeandtrophiccategoryEachcirclerepresentsaspeciesinfunctionalspaceSizeofthecircleproportionaltothetrappingrateforthatspecies
emspensp emsp | emsp767Bruce et al
trappingrateintheNorthernSector(Table1)butlackedsufficientdetectionstoreliablycalculateoccupancyAbundanceofCamerooncusimanse(Crossarchus platycephalusGoldman1984)didnotdiffersignificantlybetweenthetwosectors(NorthernSectorRAI=183[LCL=124 UCL=247 ψ=075] Southern Sector RAI=083[LCL=046UCL=127]ψ=056p=028)
36emsp|emspElephants great apes and giant pangolin (illegal wildlife trade targets)
Amongtheterrestrialmammalstargetedbytheillegalwildlifetradespecifically central chimpanzee (Pan troglodytes Blumenbachsubsp troglodytes 1799) western lowland gorilla (Gorilla gorillaSavagesubsp gorilla1847)forestelephantgiantpangolin(Smutsia gigantea Illiger 1815) and white‐bellied pangolin (Phataginus tri-cuspis Rafinesque 1821) only central chimpanzee displayed asignificant difference in RAI between the management sectors(Northern Sector RAI=161 [LCL=077 UCL=29] SouthernSector RAI=457 [LCL=314 UCL=617]) However there wasnosignificantdifferenceinmeanoccupancybetweenthetwosec‐tors (p=074) Giant pangolin displayed the greatest differencewithathreefoldincreaseinRAIfrom027[LCL=008UCL=052]in the Northern Sector to 068 [LCL=038 UCL=101] in theSouthernSectorbutthiswasnotsignificantduetotheoverlapping
confidencelimitsTheRAIsandwhereappropriateoccupancyofforestelephantwesternlowlandgorillaandwhite‐belliedpangolinwerenotsignificantlyhigher intheSouthernSectorcomparedtotheNorthernSector(Tables12and12)
37emsp|emspOther bushmeat‐targeted species
Eminrsquospouchedrat(Cricetomys eminiWroughton1910)wasmoreabundantasmeasuredbybothoccupancy(pge001)andtrapratesintheNorthernSectorcomparedtotheSouthernSector(Table1)Africanbrush‐tailedporcupine(Atherurus africanusGray1842)didnothavesignificantdifferencesinRAIbetweenthemanagementsectors but occupancywas significantly higher in theNorthernSector (pge004) In comparison the larger‐bodied red river hog(Potamochoerus porcus Linneaus1758)wasmore frequentlyen‐countered as measured by both species abundance metrics intheSouthernSector(RAI=7[LCL=336UCL=1304]ψ=091)compared to the Northern Sector (RAI=161 [LCL=102UCL=228]ψ=065(p=004)
38emsp|emspSpecies occupancy with covariates
Therewasatotalof15speciesthathadsufficientdetectionstomodeloccupancywithinteractingsitecovariates(distancetoparkboundary
F I G U R E 4 emspDistributionofmedium‐to‐largeterrestrialmammalspeciesintheSouthernSectoroftheDjaFaunalReserveCameroononthebasisofbodysizeandtrophiccategoryEachcirclerepresentsaspeciesinfunctionalspaceSizeofthecircleproportionaltothetrappingrateforthatspecies
768emsp |emsp emspensp Bruce et al
TAB
LE 2
emspNullmeanoccupancy(ψ)anddetection(p)probabilitieswithstandarderrorpresentedinbracketsfortheNorthernSectorandSouthernSector
Spec
ies
Nor
ther
n se
ctor
(ψ)
Nor
ther
n se
ctor
(p)
Sout
hern
sec
tor
(ψ)
Sout
hern
sec
tor
(p)
Mod
elBe
tamdash
Para
met
er
chos
enLo
wer
95
be
taU
pper
95
be
taC‐
hat v
alue
Chi‐s
quar
ep
valu
e
Certiodactyla
Batesrsquospygmy
antelope
022(01)
015(006)
[026]
ndashNull
ndashndash
ndashndash
ndash
Bayduiker
091(006)
04(003)
087(006)
04(003)
DRN
lam(DistanceSTD)
000
6356
808
043
3356
50
930
25
Black‐fronted
duiker
01(006)
036(01)
015(006)
025(008)
Null
ndashndash
ndashndash
ndash
Blueduiker
097(003)
082(002)
1(0)
1(0)
DRN
lam(DistanceSTD)
002
0135
490
3637
492
021
024
Petersrsquoduiker
083(007)
a056(003)
1(0)a
1(0)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus07435528
003
6592
430
004
03
Waterchevrotain
[007]
ndash04(008)
045(005)
ndashndash
ndashndash
ndashndash
White‐bellied
duiker
ndashndash
072(008)
031(003)
Null
ndashndash
ndashndash
ndash
Yellow‐backed
duiker
084(008)
027(003)
086(007)
039(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
010
8837
21
0251
104
069
021
Redriverhog
065(011)
a021(003)
091(006)
a033(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus12560347
minus01352547
027
044
Proboscidae
Forestelephant
067(015)
014(004)
063(013)
014(004)
Null
ndashndash
ndashndash
ndash
Primates
Central
chimpanzee
077(014)
015(004)
082(007)
035(003)
SRN
lam(sectorSouthern)
037
3686
91
4429
314
03
039
Westernlowland
goril
la[007]
ndash045(017)
01(004)
Null
ndashndash
ndashndash
ndash
Philodota
Giantpangolin
[02]
ndash061(016)
011(004)
Null
ndashndash
ndashndash
ndash
White‐bellied
pangolin
045(016)
012(005)
063(017)
011(003)
DSoccu
psi(DistanceSTDsec
torSouthern)
minus48425115
minus1910401
022
06
Rodentia
African
brush‐tailed
porcupine
098(003)
a057(003)
084(006)
a042(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus10008123
minus01586108
042
071
Eminrsquospouched
rat
1(0)a
1(0)
079(007)
a038(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus095574568
minus01390762
021
075
Carnivora
(Con
tinue
s)
emspensp emsp | emsp769Bruce et al
and management sector Table 2) Forest elephant black‐frontedduikerand long‐nosedmongoose (Herpestes nasodeWinton1901)lackedamodel thathadanAICdifferenceofgt2 therefore theco‐variatemodelswerenotsignificantlydifferent to thenullmodel forthese species Elevenof 15 species had aRoylendashNicholsmodel se‐lectedasthelowestAICvaluesuggestingadifferenceinthenumberofindividualswassignificantlyinfluencingdetectionprobabilitiesandthereforeoccupancy
RoylendashNichols models accounted for occupancy being signifi‐cantlyhigherindifferingmanagementsectorswithnointeractionofdistancetotheprotectedareaboundaryforthreespeciesCamerooncusimanse had higher occupancy in the Northern Sector In con‐trast central chimpanzee and black‐legged mongoose had signifi‐cantlyloweroccupancywithintheNorthernSectorcomparedtotheSouthernSector(Figure5)
African brush‐tailed porcupine Eminrsquos pouched rat and servalinegenet(Genetta servalinaPucheran1855)hadasynergisticRoylendashNicholsmodelselectedasthemostsupportedTheprobabilityofsiteoccupancyslightlyincreasedwithdistancetotheboundaryandwasoverallhigherin theNorthernSector butdeclinedwithdistance to theboundary intheSouthernSector(Figure6)BothPetersrsquoduikerandredriverhogalsodisplayedthispatternofoccupancybuthadamuchgreaterincreaseinoccupancyintheNorthernSectorandhadhigheroccupancyoverallintheSouthernSector(Figure6)Incontrastyellow‐backedduiker(Cephalophus silvicultorAfezilus1815)wastheonlyspeciestodemonstrateanincreaseinoccupancywithdistancetotheboundaryintheSouthernSectorwhiledecliningintheNorthernSectorHoweversimilartootherlargerspeciesoccupancywashigherintheSouthernSector(Figure6)
With regard to the remainingduiker speciesmodelled aRoylendashNicholsmodelwithdistancetotheprotectedareaboundarywasiden‐tifiedasthemostappropriateTheprobabilityofasitebeingoccupiedbyblueduikerandbayduikerincreasedwithdistancetotheboundarywith no discernible difference betweenmanagement sectors in themodel(Figure7)
White‐belliedpangolinhadasingle‐seasonoccupancymodelse‐lectedsuggestingdifferences inabundancebetweenthemanage‐mentsectorsdidnotaffectdetectionprobabilitiesTheprobabilityofasitebeingoccupiedbywhite‐belliedpangolin increasedintheNorthernSectoranddeclinedintheSouthernSectorwithincreasingdistancetotheboundary(Figure8)
Seven speciesweredetectedonly inone sectoror lacked suffi‐cientdetectionsinonesectortoreliablymodeloccupancyacrossbothmanagement sectors Therefore only the effect of distance to theboundarycouldbemodelledThesewereAfricangoldencatwesternlowlandgorillawhite‐belliedduikergiantpangolinAfricanpalmcivet(Nandinia binotata Gray 1830) Batesrsquos pygmy antelope and waterchevrotain (Hymeoschus aquaticusOgilby 1841)African palm civetwastheonlyspeciestohavedistancetotheboundaryselectedastheoptimummodel to explain occupancy as occupancy increasedwithdistance from the boundary of the protected area (Table 2)All theremainingspecieshadthenullmodelselectedastheoptimummodelaccordingtoAICcriteria (Table2)Howeverdistancetothebound‐arywaswithinlt2AICforthesespeciessuggestingthatasignificantSp
ecie
sN
orth
ern
sect
or (ψ
)N
orth
ern
sect
or (p
)So
uthe
rn s
ecto
r (ψ
)So
uthe
rn s
ecto
r (p
)M
odel
Beta
mdashPa
ram
eter
ch
osen
Low
er 9
5
beta
Upp
er 9
5
beta
C‐ha
t val
ueCh
i‐squ
arep
va
lue
Africangolden
cat
ndashndash
041(013)
013(004)
Null
ndashndash
ndashndash
ndash
Africanpalm
civet
[047]
ndash073(017)
012(003)
DOccu
psi(DistanceSTD)
minus8177158
Inf
197
008
Black‐legged
mongoose
047(01)a
025(004)
082(008)
a031(003)
SRN
lam(sectorSouthern)
028
0266
31
4627
420
011
058
Cameroon
cusimanse
075(009)
027(004)
056(015)
012(004)
SRN
lam(sectorSouthern)
minus1808131
minus05098939
005
073
Long‐nosed
mongoose
055(012)
a02(004)
015(006)
a027(007)
Null
ndashndash
ndashndash
ndash
Servalinegenet
092(006)
035(003)
08(009)
02(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus09202819
003
5821
570
50
26
Not
esNaiumlveoccupancyvaluesarepresentedinsquarebracketsforspecieswithadetectionprobabilitylt01TheoptimummodelchosenbyAkaikersquosinformationcriteriaforeachspeciesgeneratingsuf‐
ficientoccupancyvaluesinbothsectorswiththeBetaparameteranditisrespectivelowerandupper95confidencelimitsisshownandtheassociatedc‐hatandchi‐squaredp
val
ue
DdistancetoboundarySmanagementsectorRNRoylendashNicholsmodelOccuMckenziesingle‐seasonoccupancymodesynergisticinteraction
a IndicatesasignificantdifferenceinoccupancybetweensectorsasmeasuredbytheWaldteststatistic
TAB
LE 2
emsp(Continued)
770emsp |emsp emspensp Bruce et al
relationshipwithdistancetotheboundarycouldbeinfluencingoccu‐pancyIntheSouthernSectortheoccupancyincreasedwithdistanceto theboundary forwestern lowlandgorillaandgiantpangolinbutdecreasedforAfricangoldencatwhite‐belliedduikerandwaterchev‐rotainIntheNorthernSectoroccupancyincreasedwithdistancetotheboundaryforBatesrsquospygmyantelope
4emsp |emspDISCUSSION
Thecomparisonofthetwosurveysconfirmsthatstandardcameratrap surveys and derived metrics of presenceabsence trappingrates andoccupancy candiscern confidentdifferences in ground‐dwellingmammalcommunitiesinCentralAfricanforests
41emsp|emspCamera trap surveys for documenting species
Thecomparativeefficacyofcamera traps for surveyingmediumto large ground‐dwelling mammals in the DFR is indicated byobservationratesandverifiabilityofrecordsespeciallyofelusivesmallerandnocturnalspeciesForexamplethedirectencounterraterecordedbyrangersonpatrolthroughouttheentirereserveover a nine‐month period is much lower than the combinednumberofindependentphotographiceventsinbothmanagementsectors (ZSL amp MINFOF 2017b) even for relatively largeconspicuous species such as forest elephant (96 photographiceventscomparedto29directencounters)andcentralchimpanzee(204 independent photographic events compared to 23 directencounters)Methodologiessuchascameratrapping therefore
provideimportantbaselinedatathatwhenrepeatedthroughtimeusingastandardisedprotocolcanallowatleasttrendsinrelativeabundanceindicestobemonitored
42emsp|emspCamera trap surveys for comparing assemblages among sites
Despitebeingseparatedbyonlyc32kmthemammalcommunitiesbetween the twocamera trapgridsdisplayedmarkeddifferencesThiswasthecaseeventhoughbothgridshadlowShannonndashWeinerandSimpsonsdiversityindicesduetothedominanceofthreeorfourspeciesineachcameratrapgridSignificantdifferencesamongthesiteswere observed for the trapping rates of species of differentsizesbetweensectorsSmaller‐bodiedspecieswithintheherbivoreand omnivore guilds were more prevalent within the NorthernSector (Figure 2) Trapping rates and occupancy values for smallcarnivoresarealsolowerintheSouthernSectorThiscouldbeduetothedifficultyofidentifyingmorphologicallysimilarspeciessuchasmarshmongooseandlong‐nosedmongoose(Bahaa‐el‐dinetal2013 Ray 1997) in infrared imagery with single cameras Thereweremoreunidentifiablemongooseeventsthatwereclassifiedtoafamilylevel―66224intheSouthernSectorcomparedto29156intheNorthernSectorofallcombinedmongooseevents
43emsp|emspThe potential impact of seasonality on estimates derived from camera traps
Due to logistical and financial constraints the surveys could notberuninthesameseasonThishasthepotentialtoaffecttrapping
F I G U R E 5 emspChangeintheprobabilityofoccupancyforblack‐leggedmongoosecentralchimpanzeeandCamerooncusimansewithmanagementsectoraccordingtoaRoylendashNicholsmodel
emspensp emsp | emsp771Bruce et al
rates and occupancy for specieswith larger home ranges becausewhenspeciesarewide‐rangingoccupancycanproveineffectiveformeasuring relative abundance Forest elephants (Blake 2002) andgreatapesareknowntodisplayseasonalshiftsintheirhabitatusageover great distances in response to increased fruit availability andprecipitation(HeadRobbinsMundryMakagaampBoesch2012)Thiscouldalsoinfluenceothergregariousspeciessuchasredriverhogthatarealsothoughttooccasionallydisplaysimilaraggregationsandmovementsinresponsetomastingevents(LeslieampHuffman2015)However as both red river hog and chimpanzee had significantlyhigherRAIandhigheroccupancywithvariabledetectionprobabilityaccording to the number of individuals incorporated this supports
thepossibilitythatthesespeciesarefavouringtheSouthernSectorIfmanagersareable toestablishwhetherwide‐rangingspeciesarepredictably moving to known areas within the reserve they canrespondinamannerthatprovidesenhancedprotectiontovulnerablewildlifepopulations in concentration areasAsmost species in thissurveylikelyhaveasmallerhomerangethantheinter‐trapdistanceand display fixed territories it can be regarded as appropriate tocompare occupancy values as the extent of overlap of territorieswithin the two surveys are unlikely to change in such away as toaffecttheresultsFuturestudieswouldbenefitfromtryingtomatchcameratrapsurveysseasonallytotryandclarifytheissueofseasonalshiftsinhabitatusagewithintheDFR
F I G U R E 6 emspChangeintheprobabilityofoccupancyforAfricanbrush‐tailedporcupineEminspouchedratredriverhogservalinegenetPetersrsquoduikerandyellow‐backedduikerwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
772emsp |emsp emspensp Bruce et al
F I G U R E 7 emspChangeintheprobabilityofoccupancyforblueduikerandbayduikerwithdistancetotheboundaryinkilometresacrossbothmanagementsectorsaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
F I G U R E 8 emspChangeintheprobabilityofoccupancyforwhite‐belliedpangolinwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaMackenzieoccupancymodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
emspensp emsp | emsp773Bruce et al
44emsp|emspCamera trap surveys for measuring the impacts of hunting on mammal communities
The spatial scale at which mammal communities are affected byandhowpopulationsrespondtoanthropogenicpressuressuchasbushmeat hunting is difficult to empiricallymeasure (Laurance etal2006)Thisisespeciallytrueformammalsresidingwithintropi‐cal forestswheregatheringconsistentandmeaningfulpopulation‐andcommunity‐levelmetrics ischallenging(Ahumadaetal2013)Population density of tropical mammals can vary greatly due toheterogeneity present within the environment For example for‐est elephants havedifferent distributions and aggregations inwetanddryseasonsinNouabaleacute‐Ndoki NationalParkwhichispartiallydependentonspatio‐temporalpatternsoffruitingtreesacrossthelandscape(Blake2002)
Whether the differences observed among the two sites sur‐veyedhereareattributabletodifferent levelsofhuntingpressureremains to be confirmed There are however indications thathuntingpressureanditsimpactsonmammalfaunasaregreaterintheNorthern Sector than in the Southern Sector The effects ofhuntingpressureonmammaliandeclinesinCentralAfricanforestsarewell documented The pattern in general is the largest‐bod‐ied species frugivores and thosewith high hunter or blackmar‐ketvalue(Abernethyetal2013Cardilloetal2005FaOliveroFarfaacutenMaacuterquezDuarteetal2014aFaOliveroFarfaacutenMaacuterquezVargasetal2014bPeresampPalacios2007)arethefirstspeciestoshownoticeabledeclineInthisstudythesignificantdeclineintherelativeabundance for frugivores suchasPetersʼduikerandspe‐cieswithhighhuntervalueliketheredriverhogunderincreasedhuntingpressure in theNorthernSector is reported inother sur‐veys(Abernethyetal2013)Thisisalsoreflectedinthedifferencesobserved in this study in biomass in the different guilds of eachmammalcommunityThemammalcommunitywithintheNorthernSector shows indications of a community that is disturbed and isexperiencingelevatedhuntingpressureThesearehigher(camera)trapping rates for smaller‐bodiedspecies suchasEminrsquospouchedrat and significantly fewer encounters of larger‐bodiedmammalsthataretargetsofthebushmeattradesuchasPetersʼduikerandredriverhog(FaRyanampBell2005JerozolimskiampPeres2003)Additionalindicatorsaretheabsenceinthesurveysoflargercarni‐voresintheNorthernSectorsuchasgoldencatandleopardwhicharesensitivetosnaring(Bahaa‐el‐dinetal2015)andsignificantlyreducedabundancemetricsfordisturbance‐sensitivespeciessuchasblack‐leggedmongooseandwaterchevrotain(Hart2013a)Theabsence of white‐bellied duiker in the Northern Sector also sug‐gestselevatedhumandisturbanceasthisspecieshasbeenreportedasverysensitivetoevenminorperturbationwithintheenvironment(Hart2013b)IncomparisontheSouthernSectorcontainedindica‐torfaunasuchasthewhite‐belliedduikerandhadhighertrappingratesforlarger‐bodiedspecies
WesuspectthedifferencesobservedaremostlikelyduetolowerhumandisturbanceintheSouthernSectorTheteamsdeployingand
recoveringthecamerasintheSouthernSectorcovered238kmandencountered few signs of humanperturbation (T Brucepers obs)whereashumansignwascommonlyencounteredbytheteamsintheNorthernSectorThisperceiveddifference is reflected in the2017and 2018 density of hunting signwithin each camera trap grid asdetected throughMINFOF ranger patrols (ZSL ampMINFOF 2017a2017b) and through the2018DistanceSampling inventory for theDFR (Bruce et al 2018) Higher numbers of hunting sign in theNorthernSectorwouldbeconsistentwithanelevatedhuntingpres‐sureinthatarea
45emsp|emspProtection of refugia from hunting
Though inferences made for wide‐ranging species such as forestelephantsandgreatapesusingcameratrapsaredifficultthefactthattrappingrateswerehigherinmorechallengingterrainwithassumedlower hunting pressure could be indicative of complex habitatprovidingsomelevelofprotectionfromhuntingElephantisknownto retreatwhen they aredisturbed to terrain that ismoredifficulttoaccessbyhumans (Hedges2012)Thuswithin largerprotectedareas certain zones may act as refugia for wildlife populations(Campbelletal2011)Thiscanbeduetoarangeof factorssuchas remoteanddifficult terrain forpoachers (Attum2007Hedges2012) or the regular presence of field researchers and rangers(Campbell et al 2011) The significanceof these refugia for largerprotected areas is that the populations of wildlife residing withinthem if adequately protected may provide source populations toallowrecolonisationofotherareasofthereserve(NaranjoampBodmer2007)Thereforeifadequateprotectioncanbeprovidedtorelativelysmallbutimportantareasoflargereservesthismayprovidetropicalforestswithabetterchanceofbeingecologicallyresilienttoongoingand increasing human perturbation Well‐designed camera trapsurveys may provide data on the status of wildlife populations atrelativelyfinespatialresolutionssoastoidentifyfunctionalrefugiawithgreaterconfidence
ACKNOWLEDG EMENTS
WeappreciatetheongoingsupportofCameroonrsquosMinistryofForestsandWildlife(MINFOF)andtheopportunitytocontributetobiodiver‐sityconservationthroughoutthecountryInparticularwewouldliketothanktheChefdrsquoAntenneSergeJacobMeyeforhisongoingsup‐portofconservationresearchwithintheprotectedareaWeappreci‐atethestalwarteffortsofMINFOFecoguardsandlocalporterswhoaccompaniedthesurveyteamsinthefieldWewouldalsoliketothanktheUnitedStatesFishandWildlifeService(USFWS)mdashAfricanElephantConservationandIUCNSOSmdashFondationSegreacutePangolinConservationInitiativeforsupportingthiswork
ORCID
Tom Bruce httporcidorg0000‐0001‐6958‐1657
774emsp |emsp emspensp Bruce et al
R E FE R E N C E S
AbernethyKACoad L TaylorG LeeMEampMaisels F (2013)Extent and ecological consequences of hunting in Central Africanrainforests in thetwenty‐firstcenturyPhilosophical Transactions of the Royal Society of London Biological Sciences368(1625)20120303httpsdoiorg101098rstb20120303
AbrahamsM I Peres C A amp Costa H C (2017)Measuring localdepletion of terrestrial game vertebrates by central‐place hunt‐ers in rural Amazonia PLoS ONE 12(10) e0186653 httpsdoiorg101371journalpone0186653
AhumadaJAHurtadoJampLizcanoD(2013)MonitoringthestatusandtrendsoftropicalforestterrestrialvertebratecommunitiesfromcameratrapdataAtool forconservationPLoS ONE8(9)e73707httpsdoiorg101371journalpone0073707
Ahumada J A Silva C E Gajapersad K Hallam C Hurtado JMartin E hellip Sheil D (2011) Community structure and diver‐sity of tropical forest mammals Data from a global camera trapnetwork Philosophical Transactions of the Royal Society of London Biological Sciences366(1578)2703ndash2711httpsdoiorg101098rstb20110115
AminRAndanjeSAOgwonkaBAliAHBowkettAEOmarMampWacherT(2015)ThenortherncoastalforestsofKenyaarenationally and globally important for the conservation of AdersrsquoduikerCephalophusadersiandotherantelopespeciesBiodiversity and Conservation 24(3) 641ndash658 httpsdoiorg101007s10531‐014‐0842‐z
Attum O (2007) Can landscape use be among the factors that po‐tentiallymake some ungulates speciesmore difficult to conserveJournal of Arid Environments69(3)410ndash419
Bahaa‐el‐dinLHenschelPAbaaRAbernethyKBohmTBoutNhellipLeeM (2013)NotesonthedistributionandstatusofsmallcarnivoresinGabonSmall Carnivore Conservation4819ndash29
Bahaa‐el‐dinLHenschelPButynskiTMMacdonaldDWMillsDSlotowRampHunterL (2015)TheAfricangoldencatCaracalaurataAfricasleast‐knownfelidMammal Review45(1)63ndash77
Bennett E L Blencowe E Brandon K Brown D Burn R WCowlishaw G hellip Robinson J G (2007) Hunting for consensusReconcilingbushmeatharvestconservationanddevelopmentpol‐icyinWestandCentralAfricaConservation Biology21(3)884ndash887httpsdoiorg101111j1523‐1739200600595x
BlakeSDeemSLMossimboEMaiselsFampWalshP(2009)Forestelephants Tree planters of the CongoBiotropica41(4) 459ndash468httpsdoiorg101111j1744‐7429200900512x
Blake S (2002) The ecology of forest elephant distribution and itsimplications for conservation Doctoral dissertation University ofEdinburgh
BruceTNdjassiCFowlerANdimbeMFankemOTabueRhellipOlsonD(2018)Faunal inventory of the Dja Faunal Reserve Cameroon Yaoundeacute Cameroon Ministry of Forests and Wildlife (MINFOF)Zoological Society of London ndash Cameroon Country ProgrammeAfricanWildlifeFoundation
BruceTWacherTNdingaHBidjokaVMeyongFNgoBataMampOlsonD(2017)camera trap survey for larger terrestrial wildlife in the Dja Biosphere Reserve CameroonYaoundeacuteCameroonZoologicalSocietyofLondon(ZSL)ampCameroonMinistryofForestsandWildlife(MINFOF)
BurnhamKPampAndersonDR(2002)Model selection and multimodel inferenceNewYorkNYSpringer
Campbell G Kuehl H Diarrassouba A NGoran P K amp BoeschC (2011) Long‐term research sites as refugia for threatened andover‐harvested species Biology Letters 7(5) 723ndash726 httpsdoiorg101098rsbl20110155
CardilloMMaceGMJonesKEBielbyJBininda‐EmondsORSechrestWhellipPurvisA(2005)Multiplecausesofhighextinction
riskinlargemammalspeciesScience309(5738)1239ndash1241httpsdoiorg101126science1116030
Craigie IDBaillieJEBalmfordACarboneCCollenBGreenREampHuttonJM (2010)Largemammalpopulationdeclines inAfricarsquosprotectedareasBiological Conservation143(9)2221ndash2228httpsdoiorg101016jbiocon201006007
DaveyKWacherTampAminR(2017)Analysis tool for camera-trap sur-vey data [Computer software]ZoologicalSocietyofLondonRetrievedfromhttpswwwzslorgzsl‐camera‐trap‐data‐management‐ and‐analysis‐package
Djuikouo M N K Doucet J L Nguembou C K Lewis S L ampSonkeacute B (2010) Diversity and aboveground biomass in threetropical forest types in the Dja Biosphere Reserve Cameroon African Journal of Ecology 48(4) 1053ndash1063 httpsdoiorg101111j1365‐2028201001212x
DupainJBombomeKampVanElsackerL(2003)LeschimpanzeacutesetlesgorillesdelareacuteservedefauneduDjaCanopeacutee2414ndash15
EffordMGampDawsonDK(2012)OccupancyincontinuoushabitatEcosphere3(4)1ndash15httpsdoiorg101890ES11‐003081
Efron B amp Tibshirani R J (1994) An introduction to the bootstrap WashingtonDCCRCPress
FaJEOliveroJFarfaacutenMAacuteMaacuterquezALDuarteJNackoneyJhellipMacdonaldDW(2014a)CorrelatesofbushmeatinmarketsanddepletionofwildlifeConservation Biology29(3)805ndash815
Fa J EOlivero J FarfaacutenMAacuteMaacuterquezA LVargas JMRealRampNasiR(2014b)IntegratingsustainablehuntinginbiodiversityprotectioninCentralAfricaHotspotsweakspotsandstrongspotsPLoS ONE9(11)e112367
FaJERyanSFampBellDJ (2005)Huntingvulnerabilityecolog‐ical characteristics and harvest rates of bushmeat species in afro‐tropicalforestsBiological Conservation121(2)167ndash176httpsdoiorg101016jbiocon200404016
Fa J E Seymour S Dupain J E F Amin R Albrechtsen L ampMacdonaldD (2006) Getting to gripswith themagnitude of ex‐ploitationBushmeat in theCross‐SanagariversregionNigeria and Cameroon Biological Conservation 129(4) 497ndash510 httpsdoiorg101016jbiocon200511031
Farris Z J Boone H M Karpanty S Murphy A Ratelolahy FAndrianjakariveloVampKellyMJ(2015)FeralcatsandthefitoatyFirstpopulationassessmentoftheblackforestcatinMadagascarrsquosrainforestsJournal of Mammalogy97(2)518ndash525
Fiske IampChandlerR (2011)UnmarkedAnRpackageforfittinghi‐erarchicalmodelsofwildlifeoccurrenceandabundanceJournal of Statistical Software43(10)1ndash23
HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences107(19)8650ndash8655httpsdoiorg101073pnas0912668107
HartJ(2013a)WaterchevrotainHymemoschusaquaticusInJKingdonampMHoffmann (Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp88ndash92)LondonUKBloomsbury
Hart J (2013b) White‐bellied duiker Cephalophus leucogaster In JKingdonampMHoffmann(Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp255ndash258)LondonUKBloomsbury
HeadJSRobbinsMMMundryRMakagaLampBoeschC(2012)Remotevideo‐cameratrapsmeasurehabitatuseandcompetitiveex‐clusionamongsympatricchimpanzeegorillaandelephantinLoangoNational ParkGabon Journal of Tropical Ecology28(06) 571ndash583httpsdoiorg101017S0266467412000612
HedgesS(2012)Monitoring elephant populations and assessing threats HimayatnagarTelanganaUniversitiesPress
HedwigDKienastIBonnetMCurranBKCourageABoeschChellipKingT(2018)Acameratrapassessmentoftheforestmam‐mal community within the transitional savannah‐forest mosaic oftheBateacutekeacutePlateauNationalParkGabonAfrican Journal of Ecology56(4)777ndash790httpsdoiorg101111aje12497
emspensp emsp | emsp775Bruce et al
HijmansRJCameronSEParraJLJonesPGampJarvisA(2005)Very high resolution interpolated climate surfaces for global landareasInternational Journal of Climatology25(15)1965ndash1978httpsdoiorg101002joc1276
HuggelA(2012)Exiv2softwaretool[Computersoftware]Retrievedfromhttpswwwexiv2orgindexhtml
Jerozolimski A amp Peres C A (2003) Bringing home the biggestbacon A cross‐site analysis of the structure of hunter‐kill profilesin Neotropical forests Biological Conservation 111(3) 415ndash425httpsdoiorg101016S0006‐3207(02)00310‐5
KingdonJ (2015)The Kingdon field guide to African mammalsLondonUKBloomsburyPublishing
KuumlhlHFMaiselsMAncrenazampEAWilliamson(Eds)(2008)Best practice guidelines for surveys and monitoring of great ape populations GlandSwitzerlandIUCN
LauranceWFCroesBMTchignoumbaLLahmSAAlonsoALeeMEhellipOndzeanoC(2006)ImpactsofroadsandhuntingoncentralAfrican rainforestmammalsConservation Biology20(4)1251ndash1261httpsdoiorg101111j1523‐1739200600420x
LauranceWFUsecheDCRendeiroJKalkaMBradshawCJSloan S P hellip Arroyo‐Rodriguez V (2012) Averting biodiversitycollapse in tropical forestprotectedareasNature489(7415)290httpsdoiorg101038nature11318
LeslieDMampHuffmanBA(2015)Potamochoerus porcus(ArtiodactylaSuidae)Mammalian Species4715ndash31
MacKenzieD IampBailey L L (2004)Assessing the fit of site‐occu‐pancy models Journal of Agricultural Biological and Environmental Statistics9300ndash318httpsdoiorg101198108571104X3361
MacKenzieDINicholsJDRoyleJAPollockKHBaileyLLampHinesJE (2006)Occupancy estimation and modellingBurlingtonMAAcademicPress
Magurran A E (2005) Species abundance distributions Patternor process Functional Ecology 19(1) 177ndash181 httpsdoiorg101111j0269‐8463200500930x
MaiselsFStrindbergSBlakeSWittemyerGHartJWilliamsonEAhellipWarrenY (2013)DevastatingdeclineofforestelephantsinCentralAfricaPLoS ONE8(3)e59469httpsdoiorg101371journalpone0059469
MalhiYAdu‐BreduSAsareRA LewisS LampMayauxP (2013)AfricanrainforestsPastpresentandfuturePhilosophical Transactions of the Royal Society of London Biological Sciences 368(1625)20120312
MallonDPHoffmannMGraingerMJHibertFVanVlietNampMcGowanP JK (2015)An IUCNsituationanalysisof terrestrialandfreshwaterfaunainWestandCentralAfricaOccasionalpaperoftheIUCNspeciessurvivalcommission(54)
MambeyaMMBakerFMombouaBRKoumbaPamboAFHegaMOkouyiOkouyiVJhellipAbernethyK(2018)TheemergenceofacommercialtradeinpangolinsfromGabonAfrican Journal of Ecology56(3)601ndash609httpsdoiorg101111aje12507
MINFOFampIUCN(2015)CaracteacuterisationdelapopulationdegrandsetmoyensmammifegraveresdanslaReservedeFauneduDjaPotentieletmenacesYaoundeacuteCameroun
Muchaal P K amp Ngandjui G (1999) Impact of village hunt‐ing on wildlife populations in the western Dja ReserveCameroon Conservation Biology 13(2) 385ndash396 httpsdoiorg101046j1523‐17391999013002385x
NaranjoEJampBodmerRE (2007) Sourcendashsink systemsandconser‐vationofhuntedungulatesintheLacandonForestMexico Biological Conservation 138(3ndash4) 412ndash420 httpsdoiorg101016jbiocon 200705010
NielsenMR(2006)ImportancecauseandeffectofbushmeathuntingintheUdzungwaMountainsTanzania ImplicationsforcommunitybasedwildlifemanagementBiological Conservation128(4)509ndash516httpsdoiorg101016jbiocon200510017
OBrienTGKinnairdMFampWibisonoHT (2003)Crouching ti‐gers hiddenprey Sumatran tiger andprey populations in a tropi‐calforestlandscapeAnimal Conservation6(2)131ndash139httpsdoiorg101017S1367943003003172
OksanenJ(2015)VegananintroductiontoordinationVol8(p19)Retrieved from httpscranr‐projectorgwebpackagesveganvi‐gnettesintroveganpdf
PeresCAampPalaciosE(2007)Basin‐wideeffectsofgameharvestonvertebrate populationdensities inAmazonian forests Implicationsfor animal‐mediated seed dispersal Biotropica 39(3) 304ndash315httpsdoiorg101111j1744‐7429200700272x
PotapovPVTurubanovaSAHansenMCAduseiBBroichMAltstattAhellipJusticeCO(2012)QuantifyingforestcoverlossinDemocraticRepublicoftheCongo2000ndash2010withLandsatETM+data Remote Sensing of Environment 122 106ndash116 httpsdoiorg101016jrse201108027
PoulsenJRKoernerSEMooreSMedjibeVPBlakeSClarkC JhellipRosinC (2017) Poaching empties criticalCentralAfricanwilderness of forest elephants Current Biology 27(4) 134ndashR135httpsdoiorg101016jcub201701023
PurvisAGittlemanJlCowlishawGampMaceGM(2000)PredictingextinctionriskindecliningspeciesProceedings of the Royal Society B Biological Sciences267(1456) 1947ndash1952 httpsdoiorg101098rspb20001234
RayJ(1997)ComparativeecologyoftwoAfricanforestmongoosesHerpestesnasoandAtilaxpaludinosusAfrican Journal of Ecology35(3)237ndash253httpsdoiorg101111j1365‐20281997086‐ 89086x
Redford K H (1992) The empty forest BioScience 42(6) 412ndash422httpsdoiorg1023071311860
RepublicofCameroon(1994)Lawno9401du20janvier1994portantreacutegimedesforecirctsdelafauneetdelapecirccheRepublicofCameroon
RoveroFampMarshallAR(2009)CameratrappingphotographicrateasanindexofdensityinforestungulatesJournal of Applied Ecology46(5)1011ndash1017httpsdoiorg101111j1365‐2664200901705x
Royle J A amp Nichols J D (2003) Estimating abundance from re‐peated presence‐absence data or point counts Ecology 84(3)777ndash790 httpsdoiorg1018900012‐9658(2003)084[0777EAFRPA]20CO2
Seddon P J Griffiths C J Soorae P S ampArmstrongD P (2014)ReversingdefaunationRestoringspeciesinachangingworldScience345(6195)406ndash412httpsdoiorg101126science1251818
Silveira L Jacomo A T amp Diniz‐Filho J A F (2003) Camera trapline transect census and track surveys A comparative evaluationBiological Conservation 114(3) 351ndash355 httpsdoiorg101016S0006‐3207(03)00063‐6
Sonkeacute B (1998) Etudes floristiques et structurales des forecircts de laReacuteserve de Faune du Dja (Cameroun) Laboratoire de BotaniqueSysteacutematique et de Phytosociologie Universiteacute Libre de Bruxelles(ULB)
Srbek‐AraujoACampChiarelloAG(2005)Iscameratrappinganeffi‐cientmethodforsurveyingmammalsinNeotropicalforestsAcasestudyinsouth‐easternBrazilJournal of Tropical Ecology21(1)121ndash125httpsdoiorg101017S0266467404001956
Stiles D (2011) Elephant meat and ivory trade in Central AfricaPachyderm5026ndash36
TEAMNetwork(2008)Terrestrialvertebrateprotocol implementationmanualv30(p56)WashingtonDCTropicalEcologyAssessmentandMonitoringNetworkCenter forAppliedBiodiversity ScienceConservationInternational
Tobler M W Carrillo‐Percastegui S E Leite Pitman R MaresR amp Powell G (2008) An evaluation of camera traps for in‐ventorying large‐and medium‐sized terrestrial rainforestmammals Animal Conservation 11(3) 169ndash178 httpsdoiorg101111j1469‐1795200800169x
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
762emsp |emsp emspensp Bruce et al
south tominimise the impacts of sunrise and sunset on cameraperformance
We used three different camera models across the two grids(BushnellAggressorReconyxHC500 andCuddebackLong rangeIRE2)Detectionrangewasatleast25mwitheitheratwo‐seconddelay(Bushnell‐2015NorthernSectorsurvey)orone‐seconddelay(ReconyxCuddebackandBushnell‐2017SouthernSectorsurvey)ThreeconsecutiveimagesweretakenpertriggerLowglowinfraredflashlightingwasusedtominimisetheriskofstartlinganimalsThefulllistofsettingsforeachcameracanbefoundinAnnex1
24emsp|emspNatural mammal fauna
Thereserveisreportedtocontain109speciesofmammalofwhich35speciesareterrestrialandhaveabodyweightgt05kg(Kingdon2015) Currently the only baseline data for populations for thesespecieswithinthereservecomefromencounterratesfromrangerpatrolsanddistancesamplingthroughlinetransectsurveys(DupainBombomeampVanElsacker2003MINFOFampIUCN2015WilliamsonampUsongo1995)
25emsp|emspAssessment of differences in human activity
Toassesstherelativedifferencesinhumanactivityincludinghunt‐ing between theNorthern and Southern Sectorwhere the twosites were located we evaluated trends from multiple sourcesEvidence of human sign was recorded on 1‐kilometre line tran‐sectsduringafullfaunalinventoryoftheDFR(Bruceetal2018)TransectsareoftenusedtomonitorthetrendsofhumanimpactsinCentralAfricanforests(Kuumlhletal2008)Therewereatotalof86and76transectscoveringadistanceof916and807kmcom‐pleted intheNorthernSectorandSouthernSector respectivelyEncountersofhumansignbetweenJanuary2016andSeptember2017byMinistryofForestsandWildlife(MINFOF)rangerpatrolswhorecorddatausingSpatialMonitoringAndReportingToolde‐viceswerealsoused(ZSLampMINFOF2017a2017b)Abufferof2kmwassetaroundeachcameraandthesignwithinthisareawasconvertedintotheamountofhumansignperkm2Thisbufferwasusedtocounteractunequalsurveyeffortwithinthesectorspos‐siblyduetoecoguardsbeingrequiredtobepresentataresearchstation in theNorthernSectorat thebottomof thecamera trapgrid
Transects provide a more objective measure of hunting pres‐sureastheyuseastandardisedmethodologyandteamcompositioncompared to rangerpatrolsTransectsarenotbiasedby followingtrailsorotherpathsofleastresistancethataffectstheprobabilityofhumansignbeingdetected
26emsp|emspData analysis
WeusedExiv2software(Huggel2012)toextractEXIFinformationfromeachphotograph(imagenamedateandtime)SpeciesofanimalinthephotographswereidentifiedwhenpossibleThesedatawere
compiled in an Excel spreadsheet (Microsoft Office ProfessionalPlus2016Version1809)andanalysedwithsoftwaredevelopedbyat ZSL (CameraTrapAnalysis Package [CTAP]) (DaveyWacherampAmin2017)
Weonlyconsideredterrestrialmammalspeciesthathaveanesti‐matedaveragemassgreaterthan05kg(medium‐to‐largemammals)fortheanalysesbecausetheyarethemaintargetgroupforcameratrapsplacedatgroundlevelSmallermammalsinducesamplingerrorthroughareducedlikelihoodofdetectionbythecameratraprsquosther‐malsensorandaccurateidentificationofsmallmammalstospecieslevelisdifficultfromcameratrapsset‐upformedium‐to‐largemam‐mals(Tobleretal2008)
We calculated rarified species accumulation curves and esti‐matedthemedium‐to‐largeterrestrialmammalspeciesrichnessforeachsectorusingtheZSLCTAPtool
We calculated Simpsonrsquos diversity index and ShannonndashWeinerdiversity index foreach sector fromspeciesdaily trap ratesusingpackageveganinRstatisticalsoftware(Oksanen2015)Simpsonrsquosdiversityindexismostsensitivetochangesinmorecommonhighlyabundant species while ShannonndashWeiner diversity index is mostsensitivetochangesinrarelessabundantspecies(Magurran2005)
Wecalculatedthenumberofindependentphotographiceventsper100trapdaysasarelativeabundanceindex(RAI)foreachspeciesWedefinedanldquoeventrdquoasanysequenceforagivenspeciesoccurringafteranintervalofge60minfromthepreviousthree‐imagesequenceof that species to ensure that species events were independent(Aminetal2015Tobleretal2008)Theeventswereautomati‐cally screenedby theZSLCTAPsoftwareWecalculated the95confidenceintervalsusingthebootstrapmethod(EfronampTibshirani1994)andconsiderednon‐overlappingconfidenceintervalsasindic‐ativeofasignificantdifferenceinRAIbetweenmanagementsectorsWeassumethatthecameratrappingratescalculatedastheRAIre‐flectactualrelativeabundanceasinRoveroandMarshall(2009)
We used single‐season occupancy analysis (MacKenzie et al2006) where assumptions and data quality allowed to estimatethe proportion of area occupied by a species within each gridOccupancyestimateswerecorrectedbydetectionprobability (iethelikelihoodthataspecieswasdetectedwhenpresent)andthere‐foreprovideamore rigorous indexofabundance forbothwithinandbetweenspeciescomparisonsThishoweverislimitedtospe‐ciesgeneratingadequatedatasetswherecameraspacingisgreaterthanthespecieshomerangeandoccupancyisnotconfoundedbychanges in the home range (Efford ampDawson 2012) For all theoccupancyanalyseswegenerated1110‐daysamplingoccasionsThismeanttheNorthernSectordataweretruncatedtomatchthenumberofoccasionsavailableforanalysis intheSouthernSectorWetestedforsignificantdifferencesinspeciesoccupancybetweenthe Northern and Southern sectors using the ldquoWaldrdquo parametricstatisticaltestasitisknowntobeanindependentandrobustmea‐sureofdifference(Aminetal2015)withplt005consideredtobesignificant
We alsomodelled occupancy as a function of site covariatesdistance to the protected area boundary in kilometres (D) and
emspensp emsp | emsp763Bruce et al
management sector (M) using the ldquounmarkedrdquo (Fiske amp Chandler2011) software package in R We treated detection probabilityas a constant and evaluated all covariate combinations ψ ()p()ψ (D)p() ψ (M)p() ψ (DM)p() ψ (D+M) p() For covariate anal‐ysis tocompare themanagementsectorswealso implementedaRoylendashNicholsmodel(2003)whichtakesintoaccountthenumberofindividualsatasiteinfluencingdetectionprobabilityandthusoc‐cupancyTheselectionofRoylendashNicholsmodelaboveasingle‐sea‐sonmodelforaspecieswouldprovidefurthersupportthatspeciesabundance was significantly different between the managementsectorsWe rankedmodelsbyAkaikersquos informationcriteria (AIC)andmodels that had a delta AIC of lt2were considered to be acompetingmodel(BurnhamampAnderson2002)Thec‐hatandchi‐squared values to assessmodel dispersionwere generated usingtheMackenzie andBailey (2004) goodness‐of‐fit testwhichwasconducted using 1000 simulations for eachmodelModels witha c‐hatgt2were rejectedas theywere regardedasoverdispersed(Farrisetal2015)
3emsp |emspRESULTS
Weaccumulated3725operationalcameratrapdays(mean91dayscamera)intheNorthernSectorand3371operationalcameratrapdays(mean84dayscamera)intheSouthernSectorIntheNorthernSector grid ten cameras were lost or damaged by people or el‐ephants and somemalfunctioned The Southern Sector only hadeightcamerasfailduetothesameissuesaswellastoleoparddam‐age In total 16 cameraswere excluded fromoccupancy analysisduetobeingoperationalforlt80ofoccasions
31emsp|emspRelative assessment of human sign
Overallhumanpressureasmeasuredbyhumansignwithinthere‐servewasmoreabundant intheNorthernSectorcomparedtotheSouthern Sector Encounter rate of human sign on transects was154km in theNorthern Sector three times higher than 049kmintheSouthernSectorAsimilarpatternwasobserved inthedatagatheredbyMINFOF rangers TheNorthern Sector had a densityofhuntingsignof087km2 withintheareaofthegridincludingthe2km buffer compared to 008km2 in the Southern Sector Giventhatseveralsignsmeasuredarecloselyassociatedwithhuntingac‐tivitysuchassnaresandcartridgesweassumethathuntingactiv‐ityisonaveragehigherintheNorthernSectorthantheSouthernSector
32emsp|emspSpecies richness
A total of 26 medium‐to‐large terrestrial mammal species werephotographedintheNorthernSectorand31medium‐to‐largeter‐restrialmammalspeciesintheSouthernSector(Table1)Wealsore‐cordedfivearborealmammalspeciesthatwerenotthetargetofthissurvey (Table1)Fourmedium‐to‐large terrestrialmammalspecies
expected to occur in the surveyed habitats according to availableIUCN distribution maps and literature were not detected by thecameratrapsurveysineithersector(Table1)
The species accumulation curves for medium‐to‐large terres‐trialmammal species showmore species detected per unit effortin theSouthernSector (Figure2)Thediversity indicesweremar‐ginally lower in the Northern Sector (Simpsons=072 ShannonndashWeiner=179)comparedtotheSouthernSector(Simpsons=078ShannonndashWeiner=208)
33emsp|emspCommunity structure
CommunitystructureofmammalsdifferedbetweentheNorthernSectorandSouthernSectorsites(Figures3and4)withmorespe‐ciesbeingencounteredforthreeoutofthefourguilds(herbivoresinsectivoresandcarnivores)intheSouthernSectorThemostfre‐quentlyencounteredguild inbothsectorswasherbivore (14spe‐ciesintheSouthernSectorand13intheNorthernSector)followedbyomnivore(seveninbothsectors)carnivore(sixintheSouthernSector four in theNorthernSector) and insectivore (three in theSouthernSector two in theNorthernSector)Overallacross theguilds trapping rates for lowerbodymassspecieswerehigher inthe Northern Sector A marked difference was the higher trap‐pingratesofherbivoresandomnivoreswithbodymassgt10kg intheSouthernSector (Figure4) compared to theNorthernSector(Figure3)
34emsp|emspForest antelopes
Werecorded4495independentphotographiceventsoftenspe‐ciesof forest antelopesTheblueduiker (Philantomba monticolaThunberg 1789) was the most frequently encountered forestantelope species across both camera trap grids (RAI=527) fol‐lowed by Petersrsquo duiker (Cephalophus callipygus Peters 1876)(RAI=412) and Bay duiker (Cephalophus dorsalis Gray 1846)(RAI=747) The rest of the forest antelopeswere relatively in‐frequently encounteredwith a global trapping rate of less thanfiveThedisturbance‐sensitivewhite‐belliedduiker(Hart2013b)wasonlyencountered in theSouthernSector (RAI=395 [lower95 confidence limit (LCL)=214 upper 95 confidence limit(UCL)=611])TrappingratesweresignificantlyhigherforPeterrsquosduiker in the Southern Sector displaying a fivefold increase be‐tween sectors (Table 1) Peterrsquos duiker occupancy was also sig‐nificantlyhigherintheSouthernSectorcomparedtotheNorthernSector (p=002 Table 2) Therewere no significant differencesin trapping rates between the two sectors forBatersquos pygmy an‐telope (Neotragus batesi de Winton 1903) bay duiker bongo(Tragelaphus eurycerusOgilbyi1837)sitatunga (Tragelaphus spe-kiiSpeke1863)andblack‐frontedduiker(Cephalophus nigrifrons Gray1871)Occupancyvaluesforbayduikerblack‐frontedduikerandBatersquospygmyantelopedidnotdiffersignificantlybetweenthesectorsTherewereinsufficientdetectionsoftheotherspeciestomodeloccupancy
764emsp |emsp emspensp Bruce et al
TA B L E 1 emspMammalspeciespredictedtoberecordedintheNorthernandSouthern(management)sectorsofDjaFaunalReserveCameroon
Order Species IUCN Status HabitatNorthern sector RAI (LCLndashUCL)
Southern sector RAI (LCLndashUCL)
Afrosoricida Giantottershrew(Potamogale velox Du Chaillu1860)
LC Wetland Notdetected Notdetected
Carnivora Africangoldencat(Profelis aurataTemminck1827)a
VU Forest Notdetected 058(027ndash091)
Carnivora Leopard(Panthera pardusLinnaeus1758)a
NT Mixed Notdetected 083(032ndash145)
Carnivora Marshmongoose(Atilax paludinosusCuvier1829)a
LC Wetland 056(033ndash082)b 009(0ndash02)b
Carnivora Black‐leggedmongoose(Bdeogale nigripesPucheran1855)a
LC Forest 183(079ndash314) 371(263ndash484)
Carnivora Camerooncusimanse(Crossarchus platycephalusGoldman1984)a
LC Forest 183(124ndash247) 083(046ndash127)
Carnivora Long‐nosedmongoose(Herpestes nasodeWinton1901)a
LC Forest 102(053ndash160) 089(009ndash227)
Carnivora Africanpalmcivet(Nandinia binotataGray1830)a
LC Forest 113(071ndash16) 089(052ndash13)
Carnivora Servalinegenet(Genetta servalinaPucheran1855)a
LC Forest 325(239ndash416) 214(142ndash295)
Carnivora Large‐spottedgenet(Genetta maculata Gray1830)
LC Forest Notdetected Notdetected
Carnivora CentralAfricanoyan(Poiana richardsoniiThomson1842)c
LC Forest Notdetected 003(003ndash009)
Cetartiodactyla Batesspygmyantelope(Neotragus batesideWinton1903)a
LC Forest 04(011ndash078) 036(015ndash059)
Cetartiodactyla Forestbuffalo(Syncerus cafferSparrmansubspnanus1779)a
EN Forest 008(0ndash024) 006(0ndash019)
Cetartiodactyla Petersduiker(Cephalophus callipygusPeters1876)a
LC Forest 141(838ndash2071)b 7146 (4963ndash9641)b
Cetartiodactyla Bayduiker(Cephalophus dorsalisGray1846)a
LC Forest 668(44ndash935) 834(492ndash1228)
Cetartiodactyla White‐belliedduiker(Cephalophus leucogastersubsp leucogasterGray1873)
LC Forest Notdetected 395(214ndash611)
Cetartiodactyla Black‐frontedduiker(Cephalophus nigrifronsGray1871)a
LC Forest 086(003ndash246) 05(006ndash114)
Cetartiodactyla Yellow‐backedduiker(Cephalophus silvicultorAfzelius1815)a
LC Forest 37(225ndash554) 555(354ndash794)
Cetartiodactyla Blueduiker(Philantomba monticolaThunberg1789)a
LC Forest 6164(4602ndash788) 4298(315ndash5561)
Cetartiodactyla Bongo(Tragelaphus eurycerusOgilbyi1837)a
NT Forest 005(0ndash014) 006(0ndash015)
Cetartiodactyla Sitatunga(Tragelaphus spekiiSpeke1863)a
LC Wetland 024(005ndash048) 009(0ndash024)
Cetartiodactyla Redriverhog(Potamochoerus porcusLinnaeus1758)a
LC Woodland 161(102ndash228)b 7(336ndash1304)b
Cetartiodactyla Giantforesthog(Hylochoerus mein-ertzhageniThomas1904)
LC Forest Notdetected Notdetected
Cetartiodactyla Waterchevrotain(Hyemoschus aquaticusOgilby1841)a
LC Forest 03(0ndash075)b 46(192ndash799)b
(Continues)
emspensp emsp | emsp765Bruce et al
35emsp|emspCarnivore
ThecarnivorecommunitydifferedinRAIandstructurebetweenthetwosectorsFelidswerenotdetectedatallintheNorthernSectorbutboth leopard (Panthera pardusLinneaus1758)andgoldencat(Profelis aurata Temminck1827)werepresentintheSouthernSector
(Table1)AmongtheHerpestidaeblack‐leggedmongoose(Bdeogale nigripes Pucheran1855) showeda significantlyhigheroccupancy(p =gt001)intheSouthernSectorbuttrappingrateslackedsignifi‐cantdifference (RAI=371 [LCL=263UCL=484])comparedtothe Northern Sector (RAI=183 [LCL=079 UCL=314])Marshmongoose(Atilax paludinosusCuvier1829)hadsignificantlyhigher
Order Species IUCN Status HabitatNorthern sector RAI (LCLndashUCL)
Southern sector RAI (LCLndashUCL)
Hyracoidea Westerntreehyrax(Dendrohyrax dorsalis Fraser1855)
LC Forest Notdetected Detected
Pholidota White‐belliedpangolin(Phataginus tricuspisRafinesque1821)a
VU Forest 062(029ndash1) 08(044ndash121)
Pholidota Giantpangolin(Smutsia giganteaIlliger1815)a
VU Forest 027(008ndash052) 068(038ndash101)
Primates Agilemangabey(Cercocebus agilisMilne‐Edwards1886)a
LC Forest 035(013ndash059) 448(265ndash682)
Primates Moustachedguenon(Cercopithecus cephusLinnaeus1758)c
LC Forest Detected Notdetected
Primates Greaterspot‐nosedguenon(Cercopithecus nictitansLinnaeus1766)c
LC Forest Detected Detected
Primates Blackcolobus(Colobus satanasWaterhouse1838)c
VU Forest Notdetected Detected
Primates Galagospc ‐ Detected Notdetected
Primates Mandrill(Mandrillus sphinxLinnaeus1758)a
VU Forest 005(0ndash013) 006(0ndash019)
Primates Westernlowlandgorilla(Gorilla gorillaSavagesubspgorilla1847)a
CR Forest 016(003ndash031) 044(02ndash073)
Primates Centralchimpanzee(Pan troglodytesBlumenbachsubsptroglodytes1799)a
EN Forest 161(077ndash29)b 457(314ndash617)b
Proboscidea Forestelephant(Loxodonta cyclotisMatschie1900)a
VU Mixed 086(046ndash135) 19(086ndash329)
Rodentia Africanbrush‐tailedporcupine(Atherurus africanusGray1842)a
LC Forest 1753(1142ndash2446) 762(464ndash1145)
Rodentia Eminspouchedrat(Cricetomys eminiWroughton1910)a
LC Forest 32(2358ndash4141)b 756(341ndash1465)b
Rodentia Greatercanerat(Thryonomys swinderi-anus Temminck1827)
LC Wetland Notdetected Notdetected
Rodentia LadyBurtonsropesquirrel(Funisciurus isabellaGray1862)c
LC Forest Detected Detected
Rodentia Fire‐footedropesquirrel(Funisciurus pyrropusCuvier1833)c
LC Forest Detected Detected
Rodentia Africangiantsquirrel(Protoxerus stangeriWaterhouse1842)c
LC Forest Detected Detected
Tubulidentata Aardvark(Orycteropus aferPallas1766)a LC Mixed Notdetected 009(005ndash019)
NotesForeachsectorandspeciesthatwasdetectedwepresentthemeanand95confidencelimits(inbrackets)ofthenumberofindependentphotographiceventspertrapdaytimes100Trappingrateswereonlycalculatedformedium‐to‐largeterrestrialmammalsduetoinconsistentdetectionprobabilitieswithotherspeciesIUCNstatuscriticallyendangered(CR)endangered(EN)vulnerable(VU)nearthreatened(NT)leastconcern(LC)aIndicatesaspeciesthatwasincludedintherarefactionanalysisaccordingtothedefinitiongiveinthedataanalysissectionofthemethodsbIndicatesthattheRAIconfidenceintervalsdonotoverlapandcanbeconsideredsignificantlydifferentcSignifiesanarborealspecies
TA B L E 1 emsp (Continued)
766emsp |emsp emspensp Bruce et al
F I G U R E 2 emspRarefiedspeciesaccumulationcurvesformedium‐to‐largeterrestrialmammalsintheNorthernandSouthernsectorsofDjaFaunalReserveCameroon
F I G U R E 3 emspDistributionofmedium‐to‐largeterrestrialmammalspeciesintheNorthernSectoroftheDjaFaunalReserveCameroononthebasisofbodysizeandtrophiccategoryEachcirclerepresentsaspeciesinfunctionalspaceSizeofthecircleproportionaltothetrappingrateforthatspecies
emspensp emsp | emsp767Bruce et al
trappingrateintheNorthernSector(Table1)butlackedsufficientdetectionstoreliablycalculateoccupancyAbundanceofCamerooncusimanse(Crossarchus platycephalusGoldman1984)didnotdiffersignificantlybetweenthetwosectors(NorthernSectorRAI=183[LCL=124 UCL=247 ψ=075] Southern Sector RAI=083[LCL=046UCL=127]ψ=056p=028)
36emsp|emspElephants great apes and giant pangolin (illegal wildlife trade targets)
Amongtheterrestrialmammalstargetedbytheillegalwildlifetradespecifically central chimpanzee (Pan troglodytes Blumenbachsubsp troglodytes 1799) western lowland gorilla (Gorilla gorillaSavagesubsp gorilla1847)forestelephantgiantpangolin(Smutsia gigantea Illiger 1815) and white‐bellied pangolin (Phataginus tri-cuspis Rafinesque 1821) only central chimpanzee displayed asignificant difference in RAI between the management sectors(Northern Sector RAI=161 [LCL=077 UCL=29] SouthernSector RAI=457 [LCL=314 UCL=617]) However there wasnosignificantdifferenceinmeanoccupancybetweenthetwosec‐tors (p=074) Giant pangolin displayed the greatest differencewithathreefoldincreaseinRAIfrom027[LCL=008UCL=052]in the Northern Sector to 068 [LCL=038 UCL=101] in theSouthernSectorbutthiswasnotsignificantduetotheoverlapping
confidencelimitsTheRAIsandwhereappropriateoccupancyofforestelephantwesternlowlandgorillaandwhite‐belliedpangolinwerenotsignificantlyhigher intheSouthernSectorcomparedtotheNorthernSector(Tables12and12)
37emsp|emspOther bushmeat‐targeted species
Eminrsquospouchedrat(Cricetomys eminiWroughton1910)wasmoreabundantasmeasuredbybothoccupancy(pge001)andtrapratesintheNorthernSectorcomparedtotheSouthernSector(Table1)Africanbrush‐tailedporcupine(Atherurus africanusGray1842)didnothavesignificantdifferencesinRAIbetweenthemanagementsectors but occupancywas significantly higher in theNorthernSector (pge004) In comparison the larger‐bodied red river hog(Potamochoerus porcus Linneaus1758)wasmore frequentlyen‐countered as measured by both species abundance metrics intheSouthernSector(RAI=7[LCL=336UCL=1304]ψ=091)compared to the Northern Sector (RAI=161 [LCL=102UCL=228]ψ=065(p=004)
38emsp|emspSpecies occupancy with covariates
Therewasatotalof15speciesthathadsufficientdetectionstomodeloccupancywithinteractingsitecovariates(distancetoparkboundary
F I G U R E 4 emspDistributionofmedium‐to‐largeterrestrialmammalspeciesintheSouthernSectoroftheDjaFaunalReserveCameroononthebasisofbodysizeandtrophiccategoryEachcirclerepresentsaspeciesinfunctionalspaceSizeofthecircleproportionaltothetrappingrateforthatspecies
768emsp |emsp emspensp Bruce et al
TAB
LE 2
emspNullmeanoccupancy(ψ)anddetection(p)probabilitieswithstandarderrorpresentedinbracketsfortheNorthernSectorandSouthernSector
Spec
ies
Nor
ther
n se
ctor
(ψ)
Nor
ther
n se
ctor
(p)
Sout
hern
sec
tor
(ψ)
Sout
hern
sec
tor
(p)
Mod
elBe
tamdash
Para
met
er
chos
enLo
wer
95
be
taU
pper
95
be
taC‐
hat v
alue
Chi‐s
quar
ep
valu
e
Certiodactyla
Batesrsquospygmy
antelope
022(01)
015(006)
[026]
ndashNull
ndashndash
ndashndash
ndash
Bayduiker
091(006)
04(003)
087(006)
04(003)
DRN
lam(DistanceSTD)
000
6356
808
043
3356
50
930
25
Black‐fronted
duiker
01(006)
036(01)
015(006)
025(008)
Null
ndashndash
ndashndash
ndash
Blueduiker
097(003)
082(002)
1(0)
1(0)
DRN
lam(DistanceSTD)
002
0135
490
3637
492
021
024
Petersrsquoduiker
083(007)
a056(003)
1(0)a
1(0)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus07435528
003
6592
430
004
03
Waterchevrotain
[007]
ndash04(008)
045(005)
ndashndash
ndashndash
ndashndash
White‐bellied
duiker
ndashndash
072(008)
031(003)
Null
ndashndash
ndashndash
ndash
Yellow‐backed
duiker
084(008)
027(003)
086(007)
039(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
010
8837
21
0251
104
069
021
Redriverhog
065(011)
a021(003)
091(006)
a033(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus12560347
minus01352547
027
044
Proboscidae
Forestelephant
067(015)
014(004)
063(013)
014(004)
Null
ndashndash
ndashndash
ndash
Primates
Central
chimpanzee
077(014)
015(004)
082(007)
035(003)
SRN
lam(sectorSouthern)
037
3686
91
4429
314
03
039
Westernlowland
goril
la[007]
ndash045(017)
01(004)
Null
ndashndash
ndashndash
ndash
Philodota
Giantpangolin
[02]
ndash061(016)
011(004)
Null
ndashndash
ndashndash
ndash
White‐bellied
pangolin
045(016)
012(005)
063(017)
011(003)
DSoccu
psi(DistanceSTDsec
torSouthern)
minus48425115
minus1910401
022
06
Rodentia
African
brush‐tailed
porcupine
098(003)
a057(003)
084(006)
a042(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus10008123
minus01586108
042
071
Eminrsquospouched
rat
1(0)a
1(0)
079(007)
a038(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus095574568
minus01390762
021
075
Carnivora
(Con
tinue
s)
emspensp emsp | emsp769Bruce et al
and management sector Table 2) Forest elephant black‐frontedduikerand long‐nosedmongoose (Herpestes nasodeWinton1901)lackedamodel thathadanAICdifferenceofgt2 therefore theco‐variatemodelswerenotsignificantlydifferent to thenullmodel forthese species Elevenof 15 species had aRoylendashNicholsmodel se‐lectedasthelowestAICvaluesuggestingadifferenceinthenumberofindividualswassignificantlyinfluencingdetectionprobabilitiesandthereforeoccupancy
RoylendashNichols models accounted for occupancy being signifi‐cantlyhigherindifferingmanagementsectorswithnointeractionofdistancetotheprotectedareaboundaryforthreespeciesCamerooncusimanse had higher occupancy in the Northern Sector In con‐trast central chimpanzee and black‐legged mongoose had signifi‐cantlyloweroccupancywithintheNorthernSectorcomparedtotheSouthernSector(Figure5)
African brush‐tailed porcupine Eminrsquos pouched rat and servalinegenet(Genetta servalinaPucheran1855)hadasynergisticRoylendashNicholsmodelselectedasthemostsupportedTheprobabilityofsiteoccupancyslightlyincreasedwithdistancetotheboundaryandwasoverallhigherin theNorthernSector butdeclinedwithdistance to theboundary intheSouthernSector(Figure6)BothPetersrsquoduikerandredriverhogalsodisplayedthispatternofoccupancybuthadamuchgreaterincreaseinoccupancyintheNorthernSectorandhadhigheroccupancyoverallintheSouthernSector(Figure6)Incontrastyellow‐backedduiker(Cephalophus silvicultorAfezilus1815)wastheonlyspeciestodemonstrateanincreaseinoccupancywithdistancetotheboundaryintheSouthernSectorwhiledecliningintheNorthernSectorHoweversimilartootherlargerspeciesoccupancywashigherintheSouthernSector(Figure6)
With regard to the remainingduiker speciesmodelled aRoylendashNicholsmodelwithdistancetotheprotectedareaboundarywasiden‐tifiedasthemostappropriateTheprobabilityofasitebeingoccupiedbyblueduikerandbayduikerincreasedwithdistancetotheboundarywith no discernible difference betweenmanagement sectors in themodel(Figure7)
White‐belliedpangolinhadasingle‐seasonoccupancymodelse‐lectedsuggestingdifferences inabundancebetweenthemanage‐mentsectorsdidnotaffectdetectionprobabilitiesTheprobabilityofasitebeingoccupiedbywhite‐belliedpangolin increasedintheNorthernSectoranddeclinedintheSouthernSectorwithincreasingdistancetotheboundary(Figure8)
Seven speciesweredetectedonly inone sectoror lacked suffi‐cientdetectionsinonesectortoreliablymodeloccupancyacrossbothmanagement sectors Therefore only the effect of distance to theboundarycouldbemodelledThesewereAfricangoldencatwesternlowlandgorillawhite‐belliedduikergiantpangolinAfricanpalmcivet(Nandinia binotata Gray 1830) Batesrsquos pygmy antelope and waterchevrotain (Hymeoschus aquaticusOgilby 1841)African palm civetwastheonlyspeciestohavedistancetotheboundaryselectedastheoptimummodel to explain occupancy as occupancy increasedwithdistance from the boundary of the protected area (Table 2)All theremainingspecieshadthenullmodelselectedastheoptimummodelaccordingtoAICcriteria (Table2)Howeverdistancetothebound‐arywaswithinlt2AICforthesespeciessuggestingthatasignificantSp
ecie
sN
orth
ern
sect
or (ψ
)N
orth
ern
sect
or (p
)So
uthe
rn s
ecto
r (ψ
)So
uthe
rn s
ecto
r (p
)M
odel
Beta
mdashPa
ram
eter
ch
osen
Low
er 9
5
beta
Upp
er 9
5
beta
C‐ha
t val
ueCh
i‐squ
arep
va
lue
Africangolden
cat
ndashndash
041(013)
013(004)
Null
ndashndash
ndashndash
ndash
Africanpalm
civet
[047]
ndash073(017)
012(003)
DOccu
psi(DistanceSTD)
minus8177158
Inf
197
008
Black‐legged
mongoose
047(01)a
025(004)
082(008)
a031(003)
SRN
lam(sectorSouthern)
028
0266
31
4627
420
011
058
Cameroon
cusimanse
075(009)
027(004)
056(015)
012(004)
SRN
lam(sectorSouthern)
minus1808131
minus05098939
005
073
Long‐nosed
mongoose
055(012)
a02(004)
015(006)
a027(007)
Null
ndashndash
ndashndash
ndash
Servalinegenet
092(006)
035(003)
08(009)
02(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus09202819
003
5821
570
50
26
Not
esNaiumlveoccupancyvaluesarepresentedinsquarebracketsforspecieswithadetectionprobabilitylt01TheoptimummodelchosenbyAkaikersquosinformationcriteriaforeachspeciesgeneratingsuf‐
ficientoccupancyvaluesinbothsectorswiththeBetaparameteranditisrespectivelowerandupper95confidencelimitsisshownandtheassociatedc‐hatandchi‐squaredp
val
ue
DdistancetoboundarySmanagementsectorRNRoylendashNicholsmodelOccuMckenziesingle‐seasonoccupancymodesynergisticinteraction
a IndicatesasignificantdifferenceinoccupancybetweensectorsasmeasuredbytheWaldteststatistic
TAB
LE 2
emsp(Continued)
770emsp |emsp emspensp Bruce et al
relationshipwithdistancetotheboundarycouldbeinfluencingoccu‐pancyIntheSouthernSectortheoccupancyincreasedwithdistanceto theboundary forwestern lowlandgorillaandgiantpangolinbutdecreasedforAfricangoldencatwhite‐belliedduikerandwaterchev‐rotainIntheNorthernSectoroccupancyincreasedwithdistancetotheboundaryforBatesrsquospygmyantelope
4emsp |emspDISCUSSION
Thecomparisonofthetwosurveysconfirmsthatstandardcameratrap surveys and derived metrics of presenceabsence trappingrates andoccupancy candiscern confidentdifferences in ground‐dwellingmammalcommunitiesinCentralAfricanforests
41emsp|emspCamera trap surveys for documenting species
Thecomparativeefficacyofcamera traps for surveyingmediumto large ground‐dwelling mammals in the DFR is indicated byobservationratesandverifiabilityofrecordsespeciallyofelusivesmallerandnocturnalspeciesForexamplethedirectencounterraterecordedbyrangersonpatrolthroughouttheentirereserveover a nine‐month period is much lower than the combinednumberofindependentphotographiceventsinbothmanagementsectors (ZSL amp MINFOF 2017b) even for relatively largeconspicuous species such as forest elephant (96 photographiceventscomparedto29directencounters)andcentralchimpanzee(204 independent photographic events compared to 23 directencounters)Methodologiessuchascameratrapping therefore
provideimportantbaselinedatathatwhenrepeatedthroughtimeusingastandardisedprotocolcanallowatleasttrendsinrelativeabundanceindicestobemonitored
42emsp|emspCamera trap surveys for comparing assemblages among sites
Despitebeingseparatedbyonlyc32kmthemammalcommunitiesbetween the twocamera trapgridsdisplayedmarkeddifferencesThiswasthecaseeventhoughbothgridshadlowShannonndashWeinerandSimpsonsdiversityindicesduetothedominanceofthreeorfourspeciesineachcameratrapgridSignificantdifferencesamongthesiteswere observed for the trapping rates of species of differentsizesbetweensectorsSmaller‐bodiedspecieswithintheherbivoreand omnivore guilds were more prevalent within the NorthernSector (Figure 2) Trapping rates and occupancy values for smallcarnivoresarealsolowerintheSouthernSectorThiscouldbeduetothedifficultyofidentifyingmorphologicallysimilarspeciessuchasmarshmongooseandlong‐nosedmongoose(Bahaa‐el‐dinetal2013 Ray 1997) in infrared imagery with single cameras Thereweremoreunidentifiablemongooseeventsthatwereclassifiedtoafamilylevel―66224intheSouthernSectorcomparedto29156intheNorthernSectorofallcombinedmongooseevents
43emsp|emspThe potential impact of seasonality on estimates derived from camera traps
Due to logistical and financial constraints the surveys could notberuninthesameseasonThishasthepotentialtoaffecttrapping
F I G U R E 5 emspChangeintheprobabilityofoccupancyforblack‐leggedmongoosecentralchimpanzeeandCamerooncusimansewithmanagementsectoraccordingtoaRoylendashNicholsmodel
emspensp emsp | emsp771Bruce et al
rates and occupancy for specieswith larger home ranges becausewhenspeciesarewide‐rangingoccupancycanproveineffectiveformeasuring relative abundance Forest elephants (Blake 2002) andgreatapesareknowntodisplayseasonalshiftsintheirhabitatusageover great distances in response to increased fruit availability andprecipitation(HeadRobbinsMundryMakagaampBoesch2012)Thiscouldalsoinfluenceothergregariousspeciessuchasredriverhogthatarealsothoughttooccasionallydisplaysimilaraggregationsandmovementsinresponsetomastingevents(LeslieampHuffman2015)However as both red river hog and chimpanzee had significantlyhigherRAIandhigheroccupancywithvariabledetectionprobabilityaccording to the number of individuals incorporated this supports
thepossibilitythatthesespeciesarefavouringtheSouthernSectorIfmanagersareable toestablishwhetherwide‐rangingspeciesarepredictably moving to known areas within the reserve they canrespondinamannerthatprovidesenhancedprotectiontovulnerablewildlifepopulations in concentration areasAsmost species in thissurveylikelyhaveasmallerhomerangethantheinter‐trapdistanceand display fixed territories it can be regarded as appropriate tocompare occupancy values as the extent of overlap of territorieswithin the two surveys are unlikely to change in such away as toaffecttheresultsFuturestudieswouldbenefitfromtryingtomatchcameratrapsurveysseasonallytotryandclarifytheissueofseasonalshiftsinhabitatusagewithintheDFR
F I G U R E 6 emspChangeintheprobabilityofoccupancyforAfricanbrush‐tailedporcupineEminspouchedratredriverhogservalinegenetPetersrsquoduikerandyellow‐backedduikerwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
772emsp |emsp emspensp Bruce et al
F I G U R E 7 emspChangeintheprobabilityofoccupancyforblueduikerandbayduikerwithdistancetotheboundaryinkilometresacrossbothmanagementsectorsaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
F I G U R E 8 emspChangeintheprobabilityofoccupancyforwhite‐belliedpangolinwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaMackenzieoccupancymodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
emspensp emsp | emsp773Bruce et al
44emsp|emspCamera trap surveys for measuring the impacts of hunting on mammal communities
The spatial scale at which mammal communities are affected byandhowpopulationsrespondtoanthropogenicpressuressuchasbushmeat hunting is difficult to empiricallymeasure (Laurance etal2006)Thisisespeciallytrueformammalsresidingwithintropi‐cal forestswheregatheringconsistentandmeaningfulpopulation‐andcommunity‐levelmetrics ischallenging(Ahumadaetal2013)Population density of tropical mammals can vary greatly due toheterogeneity present within the environment For example for‐est elephants havedifferent distributions and aggregations inwetanddryseasonsinNouabaleacute‐Ndoki NationalParkwhichispartiallydependentonspatio‐temporalpatternsoffruitingtreesacrossthelandscape(Blake2002)
Whether the differences observed among the two sites sur‐veyedhereareattributabletodifferent levelsofhuntingpressureremains to be confirmed There are however indications thathuntingpressureanditsimpactsonmammalfaunasaregreaterintheNorthern Sector than in the Southern Sector The effects ofhuntingpressureonmammaliandeclinesinCentralAfricanforestsarewell documented The pattern in general is the largest‐bod‐ied species frugivores and thosewith high hunter or blackmar‐ketvalue(Abernethyetal2013Cardilloetal2005FaOliveroFarfaacutenMaacuterquezDuarteetal2014aFaOliveroFarfaacutenMaacuterquezVargasetal2014bPeresampPalacios2007)arethefirstspeciestoshownoticeabledeclineInthisstudythesignificantdeclineintherelativeabundance for frugivores suchasPetersʼduikerandspe‐cieswithhighhuntervalueliketheredriverhogunderincreasedhuntingpressure in theNorthernSector is reported inother sur‐veys(Abernethyetal2013)Thisisalsoreflectedinthedifferencesobserved in this study in biomass in the different guilds of eachmammalcommunityThemammalcommunitywithintheNorthernSector shows indications of a community that is disturbed and isexperiencingelevatedhuntingpressureThesearehigher(camera)trapping rates for smaller‐bodiedspecies suchasEminrsquospouchedrat and significantly fewer encounters of larger‐bodiedmammalsthataretargetsofthebushmeattradesuchasPetersʼduikerandredriverhog(FaRyanampBell2005JerozolimskiampPeres2003)Additionalindicatorsaretheabsenceinthesurveysoflargercarni‐voresintheNorthernSectorsuchasgoldencatandleopardwhicharesensitivetosnaring(Bahaa‐el‐dinetal2015)andsignificantlyreducedabundancemetricsfordisturbance‐sensitivespeciessuchasblack‐leggedmongooseandwaterchevrotain(Hart2013a)Theabsence of white‐bellied duiker in the Northern Sector also sug‐gestselevatedhumandisturbanceasthisspecieshasbeenreportedasverysensitivetoevenminorperturbationwithintheenvironment(Hart2013b)IncomparisontheSouthernSectorcontainedindica‐torfaunasuchasthewhite‐belliedduikerandhadhighertrappingratesforlarger‐bodiedspecies
WesuspectthedifferencesobservedaremostlikelyduetolowerhumandisturbanceintheSouthernSectorTheteamsdeployingand
recoveringthecamerasintheSouthernSectorcovered238kmandencountered few signs of humanperturbation (T Brucepers obs)whereashumansignwascommonlyencounteredbytheteamsintheNorthernSectorThisperceiveddifference is reflected in the2017and 2018 density of hunting signwithin each camera trap grid asdetected throughMINFOF ranger patrols (ZSL ampMINFOF 2017a2017b) and through the2018DistanceSampling inventory for theDFR (Bruce et al 2018) Higher numbers of hunting sign in theNorthernSectorwouldbeconsistentwithanelevatedhuntingpres‐sureinthatarea
45emsp|emspProtection of refugia from hunting
Though inferences made for wide‐ranging species such as forestelephantsandgreatapesusingcameratrapsaredifficultthefactthattrappingrateswerehigherinmorechallengingterrainwithassumedlower hunting pressure could be indicative of complex habitatprovidingsomelevelofprotectionfromhuntingElephantisknownto retreatwhen they aredisturbed to terrain that ismoredifficulttoaccessbyhumans (Hedges2012)Thuswithin largerprotectedareas certain zones may act as refugia for wildlife populations(Campbelletal2011)Thiscanbeduetoarangeof factorssuchas remoteanddifficult terrain forpoachers (Attum2007Hedges2012) or the regular presence of field researchers and rangers(Campbell et al 2011) The significanceof these refugia for largerprotected areas is that the populations of wildlife residing withinthem if adequately protected may provide source populations toallowrecolonisationofotherareasofthereserve(NaranjoampBodmer2007)Thereforeifadequateprotectioncanbeprovidedtorelativelysmallbutimportantareasoflargereservesthismayprovidetropicalforestswithabetterchanceofbeingecologicallyresilienttoongoingand increasing human perturbation Well‐designed camera trapsurveys may provide data on the status of wildlife populations atrelativelyfinespatialresolutionssoastoidentifyfunctionalrefugiawithgreaterconfidence
ACKNOWLEDG EMENTS
WeappreciatetheongoingsupportofCameroonrsquosMinistryofForestsandWildlife(MINFOF)andtheopportunitytocontributetobiodiver‐sityconservationthroughoutthecountryInparticularwewouldliketothanktheChefdrsquoAntenneSergeJacobMeyeforhisongoingsup‐portofconservationresearchwithintheprotectedareaWeappreci‐atethestalwarteffortsofMINFOFecoguardsandlocalporterswhoaccompaniedthesurveyteamsinthefieldWewouldalsoliketothanktheUnitedStatesFishandWildlifeService(USFWS)mdashAfricanElephantConservationandIUCNSOSmdashFondationSegreacutePangolinConservationInitiativeforsupportingthiswork
ORCID
Tom Bruce httporcidorg0000‐0001‐6958‐1657
774emsp |emsp emspensp Bruce et al
R E FE R E N C E S
AbernethyKACoad L TaylorG LeeMEampMaisels F (2013)Extent and ecological consequences of hunting in Central Africanrainforests in thetwenty‐firstcenturyPhilosophical Transactions of the Royal Society of London Biological Sciences368(1625)20120303httpsdoiorg101098rstb20120303
AbrahamsM I Peres C A amp Costa H C (2017)Measuring localdepletion of terrestrial game vertebrates by central‐place hunt‐ers in rural Amazonia PLoS ONE 12(10) e0186653 httpsdoiorg101371journalpone0186653
AhumadaJAHurtadoJampLizcanoD(2013)MonitoringthestatusandtrendsoftropicalforestterrestrialvertebratecommunitiesfromcameratrapdataAtool forconservationPLoS ONE8(9)e73707httpsdoiorg101371journalpone0073707
Ahumada J A Silva C E Gajapersad K Hallam C Hurtado JMartin E hellip Sheil D (2011) Community structure and diver‐sity of tropical forest mammals Data from a global camera trapnetwork Philosophical Transactions of the Royal Society of London Biological Sciences366(1578)2703ndash2711httpsdoiorg101098rstb20110115
AminRAndanjeSAOgwonkaBAliAHBowkettAEOmarMampWacherT(2015)ThenortherncoastalforestsofKenyaarenationally and globally important for the conservation of AdersrsquoduikerCephalophusadersiandotherantelopespeciesBiodiversity and Conservation 24(3) 641ndash658 httpsdoiorg101007s10531‐014‐0842‐z
Attum O (2007) Can landscape use be among the factors that po‐tentiallymake some ungulates speciesmore difficult to conserveJournal of Arid Environments69(3)410ndash419
Bahaa‐el‐dinLHenschelPAbaaRAbernethyKBohmTBoutNhellipLeeM (2013)NotesonthedistributionandstatusofsmallcarnivoresinGabonSmall Carnivore Conservation4819ndash29
Bahaa‐el‐dinLHenschelPButynskiTMMacdonaldDWMillsDSlotowRampHunterL (2015)TheAfricangoldencatCaracalaurataAfricasleast‐knownfelidMammal Review45(1)63ndash77
Bennett E L Blencowe E Brandon K Brown D Burn R WCowlishaw G hellip Robinson J G (2007) Hunting for consensusReconcilingbushmeatharvestconservationanddevelopmentpol‐icyinWestandCentralAfricaConservation Biology21(3)884ndash887httpsdoiorg101111j1523‐1739200600595x
BlakeSDeemSLMossimboEMaiselsFampWalshP(2009)Forestelephants Tree planters of the CongoBiotropica41(4) 459ndash468httpsdoiorg101111j1744‐7429200900512x
Blake S (2002) The ecology of forest elephant distribution and itsimplications for conservation Doctoral dissertation University ofEdinburgh
BruceTNdjassiCFowlerANdimbeMFankemOTabueRhellipOlsonD(2018)Faunal inventory of the Dja Faunal Reserve Cameroon Yaoundeacute Cameroon Ministry of Forests and Wildlife (MINFOF)Zoological Society of London ndash Cameroon Country ProgrammeAfricanWildlifeFoundation
BruceTWacherTNdingaHBidjokaVMeyongFNgoBataMampOlsonD(2017)camera trap survey for larger terrestrial wildlife in the Dja Biosphere Reserve CameroonYaoundeacuteCameroonZoologicalSocietyofLondon(ZSL)ampCameroonMinistryofForestsandWildlife(MINFOF)
BurnhamKPampAndersonDR(2002)Model selection and multimodel inferenceNewYorkNYSpringer
Campbell G Kuehl H Diarrassouba A NGoran P K amp BoeschC (2011) Long‐term research sites as refugia for threatened andover‐harvested species Biology Letters 7(5) 723ndash726 httpsdoiorg101098rsbl20110155
CardilloMMaceGMJonesKEBielbyJBininda‐EmondsORSechrestWhellipPurvisA(2005)Multiplecausesofhighextinction
riskinlargemammalspeciesScience309(5738)1239ndash1241httpsdoiorg101126science1116030
Craigie IDBaillieJEBalmfordACarboneCCollenBGreenREampHuttonJM (2010)Largemammalpopulationdeclines inAfricarsquosprotectedareasBiological Conservation143(9)2221ndash2228httpsdoiorg101016jbiocon201006007
DaveyKWacherTampAminR(2017)Analysis tool for camera-trap sur-vey data [Computer software]ZoologicalSocietyofLondonRetrievedfromhttpswwwzslorgzsl‐camera‐trap‐data‐management‐ and‐analysis‐package
Djuikouo M N K Doucet J L Nguembou C K Lewis S L ampSonkeacute B (2010) Diversity and aboveground biomass in threetropical forest types in the Dja Biosphere Reserve Cameroon African Journal of Ecology 48(4) 1053ndash1063 httpsdoiorg101111j1365‐2028201001212x
DupainJBombomeKampVanElsackerL(2003)LeschimpanzeacutesetlesgorillesdelareacuteservedefauneduDjaCanopeacutee2414ndash15
EffordMGampDawsonDK(2012)OccupancyincontinuoushabitatEcosphere3(4)1ndash15httpsdoiorg101890ES11‐003081
Efron B amp Tibshirani R J (1994) An introduction to the bootstrap WashingtonDCCRCPress
FaJEOliveroJFarfaacutenMAacuteMaacuterquezALDuarteJNackoneyJhellipMacdonaldDW(2014a)CorrelatesofbushmeatinmarketsanddepletionofwildlifeConservation Biology29(3)805ndash815
Fa J EOlivero J FarfaacutenMAacuteMaacuterquezA LVargas JMRealRampNasiR(2014b)IntegratingsustainablehuntinginbiodiversityprotectioninCentralAfricaHotspotsweakspotsandstrongspotsPLoS ONE9(11)e112367
FaJERyanSFampBellDJ (2005)Huntingvulnerabilityecolog‐ical characteristics and harvest rates of bushmeat species in afro‐tropicalforestsBiological Conservation121(2)167ndash176httpsdoiorg101016jbiocon200404016
Fa J E Seymour S Dupain J E F Amin R Albrechtsen L ampMacdonaldD (2006) Getting to gripswith themagnitude of ex‐ploitationBushmeat in theCross‐SanagariversregionNigeria and Cameroon Biological Conservation 129(4) 497ndash510 httpsdoiorg101016jbiocon200511031
Farris Z J Boone H M Karpanty S Murphy A Ratelolahy FAndrianjakariveloVampKellyMJ(2015)FeralcatsandthefitoatyFirstpopulationassessmentoftheblackforestcatinMadagascarrsquosrainforestsJournal of Mammalogy97(2)518ndash525
Fiske IampChandlerR (2011)UnmarkedAnRpackageforfittinghi‐erarchicalmodelsofwildlifeoccurrenceandabundanceJournal of Statistical Software43(10)1ndash23
HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences107(19)8650ndash8655httpsdoiorg101073pnas0912668107
HartJ(2013a)WaterchevrotainHymemoschusaquaticusInJKingdonampMHoffmann (Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp88ndash92)LondonUKBloomsbury
Hart J (2013b) White‐bellied duiker Cephalophus leucogaster In JKingdonampMHoffmann(Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp255ndash258)LondonUKBloomsbury
HeadJSRobbinsMMMundryRMakagaLampBoeschC(2012)Remotevideo‐cameratrapsmeasurehabitatuseandcompetitiveex‐clusionamongsympatricchimpanzeegorillaandelephantinLoangoNational ParkGabon Journal of Tropical Ecology28(06) 571ndash583httpsdoiorg101017S0266467412000612
HedgesS(2012)Monitoring elephant populations and assessing threats HimayatnagarTelanganaUniversitiesPress
HedwigDKienastIBonnetMCurranBKCourageABoeschChellipKingT(2018)Acameratrapassessmentoftheforestmam‐mal community within the transitional savannah‐forest mosaic oftheBateacutekeacutePlateauNationalParkGabonAfrican Journal of Ecology56(4)777ndash790httpsdoiorg101111aje12497
emspensp emsp | emsp775Bruce et al
HijmansRJCameronSEParraJLJonesPGampJarvisA(2005)Very high resolution interpolated climate surfaces for global landareasInternational Journal of Climatology25(15)1965ndash1978httpsdoiorg101002joc1276
HuggelA(2012)Exiv2softwaretool[Computersoftware]Retrievedfromhttpswwwexiv2orgindexhtml
Jerozolimski A amp Peres C A (2003) Bringing home the biggestbacon A cross‐site analysis of the structure of hunter‐kill profilesin Neotropical forests Biological Conservation 111(3) 415ndash425httpsdoiorg101016S0006‐3207(02)00310‐5
KingdonJ (2015)The Kingdon field guide to African mammalsLondonUKBloomsburyPublishing
KuumlhlHFMaiselsMAncrenazampEAWilliamson(Eds)(2008)Best practice guidelines for surveys and monitoring of great ape populations GlandSwitzerlandIUCN
LauranceWFCroesBMTchignoumbaLLahmSAAlonsoALeeMEhellipOndzeanoC(2006)ImpactsofroadsandhuntingoncentralAfrican rainforestmammalsConservation Biology20(4)1251ndash1261httpsdoiorg101111j1523‐1739200600420x
LauranceWFUsecheDCRendeiroJKalkaMBradshawCJSloan S P hellip Arroyo‐Rodriguez V (2012) Averting biodiversitycollapse in tropical forestprotectedareasNature489(7415)290httpsdoiorg101038nature11318
LeslieDMampHuffmanBA(2015)Potamochoerus porcus(ArtiodactylaSuidae)Mammalian Species4715ndash31
MacKenzieD IampBailey L L (2004)Assessing the fit of site‐occu‐pancy models Journal of Agricultural Biological and Environmental Statistics9300ndash318httpsdoiorg101198108571104X3361
MacKenzieDINicholsJDRoyleJAPollockKHBaileyLLampHinesJE (2006)Occupancy estimation and modellingBurlingtonMAAcademicPress
Magurran A E (2005) Species abundance distributions Patternor process Functional Ecology 19(1) 177ndash181 httpsdoiorg101111j0269‐8463200500930x
MaiselsFStrindbergSBlakeSWittemyerGHartJWilliamsonEAhellipWarrenY (2013)DevastatingdeclineofforestelephantsinCentralAfricaPLoS ONE8(3)e59469httpsdoiorg101371journalpone0059469
MalhiYAdu‐BreduSAsareRA LewisS LampMayauxP (2013)AfricanrainforestsPastpresentandfuturePhilosophical Transactions of the Royal Society of London Biological Sciences 368(1625)20120312
MallonDPHoffmannMGraingerMJHibertFVanVlietNampMcGowanP JK (2015)An IUCNsituationanalysisof terrestrialandfreshwaterfaunainWestandCentralAfricaOccasionalpaperoftheIUCNspeciessurvivalcommission(54)
MambeyaMMBakerFMombouaBRKoumbaPamboAFHegaMOkouyiOkouyiVJhellipAbernethyK(2018)TheemergenceofacommercialtradeinpangolinsfromGabonAfrican Journal of Ecology56(3)601ndash609httpsdoiorg101111aje12507
MINFOFampIUCN(2015)CaracteacuterisationdelapopulationdegrandsetmoyensmammifegraveresdanslaReservedeFauneduDjaPotentieletmenacesYaoundeacuteCameroun
Muchaal P K amp Ngandjui G (1999) Impact of village hunt‐ing on wildlife populations in the western Dja ReserveCameroon Conservation Biology 13(2) 385ndash396 httpsdoiorg101046j1523‐17391999013002385x
NaranjoEJampBodmerRE (2007) Sourcendashsink systemsandconser‐vationofhuntedungulatesintheLacandonForestMexico Biological Conservation 138(3ndash4) 412ndash420 httpsdoiorg101016jbiocon 200705010
NielsenMR(2006)ImportancecauseandeffectofbushmeathuntingintheUdzungwaMountainsTanzania ImplicationsforcommunitybasedwildlifemanagementBiological Conservation128(4)509ndash516httpsdoiorg101016jbiocon200510017
OBrienTGKinnairdMFampWibisonoHT (2003)Crouching ti‐gers hiddenprey Sumatran tiger andprey populations in a tropi‐calforestlandscapeAnimal Conservation6(2)131ndash139httpsdoiorg101017S1367943003003172
OksanenJ(2015)VegananintroductiontoordinationVol8(p19)Retrieved from httpscranr‐projectorgwebpackagesveganvi‐gnettesintroveganpdf
PeresCAampPalaciosE(2007)Basin‐wideeffectsofgameharvestonvertebrate populationdensities inAmazonian forests Implicationsfor animal‐mediated seed dispersal Biotropica 39(3) 304ndash315httpsdoiorg101111j1744‐7429200700272x
PotapovPVTurubanovaSAHansenMCAduseiBBroichMAltstattAhellipJusticeCO(2012)QuantifyingforestcoverlossinDemocraticRepublicoftheCongo2000ndash2010withLandsatETM+data Remote Sensing of Environment 122 106ndash116 httpsdoiorg101016jrse201108027
PoulsenJRKoernerSEMooreSMedjibeVPBlakeSClarkC JhellipRosinC (2017) Poaching empties criticalCentralAfricanwilderness of forest elephants Current Biology 27(4) 134ndashR135httpsdoiorg101016jcub201701023
PurvisAGittlemanJlCowlishawGampMaceGM(2000)PredictingextinctionriskindecliningspeciesProceedings of the Royal Society B Biological Sciences267(1456) 1947ndash1952 httpsdoiorg101098rspb20001234
RayJ(1997)ComparativeecologyoftwoAfricanforestmongoosesHerpestesnasoandAtilaxpaludinosusAfrican Journal of Ecology35(3)237ndash253httpsdoiorg101111j1365‐20281997086‐ 89086x
Redford K H (1992) The empty forest BioScience 42(6) 412ndash422httpsdoiorg1023071311860
RepublicofCameroon(1994)Lawno9401du20janvier1994portantreacutegimedesforecirctsdelafauneetdelapecirccheRepublicofCameroon
RoveroFampMarshallAR(2009)CameratrappingphotographicrateasanindexofdensityinforestungulatesJournal of Applied Ecology46(5)1011ndash1017httpsdoiorg101111j1365‐2664200901705x
Royle J A amp Nichols J D (2003) Estimating abundance from re‐peated presence‐absence data or point counts Ecology 84(3)777ndash790 httpsdoiorg1018900012‐9658(2003)084[0777EAFRPA]20CO2
Seddon P J Griffiths C J Soorae P S ampArmstrongD P (2014)ReversingdefaunationRestoringspeciesinachangingworldScience345(6195)406ndash412httpsdoiorg101126science1251818
Silveira L Jacomo A T amp Diniz‐Filho J A F (2003) Camera trapline transect census and track surveys A comparative evaluationBiological Conservation 114(3) 351ndash355 httpsdoiorg101016S0006‐3207(03)00063‐6
Sonkeacute B (1998) Etudes floristiques et structurales des forecircts de laReacuteserve de Faune du Dja (Cameroun) Laboratoire de BotaniqueSysteacutematique et de Phytosociologie Universiteacute Libre de Bruxelles(ULB)
Srbek‐AraujoACampChiarelloAG(2005)Iscameratrappinganeffi‐cientmethodforsurveyingmammalsinNeotropicalforestsAcasestudyinsouth‐easternBrazilJournal of Tropical Ecology21(1)121ndash125httpsdoiorg101017S0266467404001956
Stiles D (2011) Elephant meat and ivory trade in Central AfricaPachyderm5026ndash36
TEAMNetwork(2008)Terrestrialvertebrateprotocol implementationmanualv30(p56)WashingtonDCTropicalEcologyAssessmentandMonitoringNetworkCenter forAppliedBiodiversity ScienceConservationInternational
Tobler M W Carrillo‐Percastegui S E Leite Pitman R MaresR amp Powell G (2008) An evaluation of camera traps for in‐ventorying large‐and medium‐sized terrestrial rainforestmammals Animal Conservation 11(3) 169ndash178 httpsdoiorg101111j1469‐1795200800169x
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
emspensp emsp | emsp763Bruce et al
management sector (M) using the ldquounmarkedrdquo (Fiske amp Chandler2011) software package in R We treated detection probabilityas a constant and evaluated all covariate combinations ψ ()p()ψ (D)p() ψ (M)p() ψ (DM)p() ψ (D+M) p() For covariate anal‐ysis tocompare themanagementsectorswealso implementedaRoylendashNicholsmodel(2003)whichtakesintoaccountthenumberofindividualsatasiteinfluencingdetectionprobabilityandthusoc‐cupancyTheselectionofRoylendashNicholsmodelaboveasingle‐sea‐sonmodelforaspecieswouldprovidefurthersupportthatspeciesabundance was significantly different between the managementsectorsWe rankedmodelsbyAkaikersquos informationcriteria (AIC)andmodels that had a delta AIC of lt2were considered to be acompetingmodel(BurnhamampAnderson2002)Thec‐hatandchi‐squared values to assessmodel dispersionwere generated usingtheMackenzie andBailey (2004) goodness‐of‐fit testwhichwasconducted using 1000 simulations for eachmodelModels witha c‐hatgt2were rejectedas theywere regardedasoverdispersed(Farrisetal2015)
3emsp |emspRESULTS
Weaccumulated3725operationalcameratrapdays(mean91dayscamera)intheNorthernSectorand3371operationalcameratrapdays(mean84dayscamera)intheSouthernSectorIntheNorthernSector grid ten cameras were lost or damaged by people or el‐ephants and somemalfunctioned The Southern Sector only hadeightcamerasfailduetothesameissuesaswellastoleoparddam‐age In total 16 cameraswere excluded fromoccupancy analysisduetobeingoperationalforlt80ofoccasions
31emsp|emspRelative assessment of human sign
Overallhumanpressureasmeasuredbyhumansignwithinthere‐servewasmoreabundant intheNorthernSectorcomparedtotheSouthern Sector Encounter rate of human sign on transects was154km in theNorthern Sector three times higher than 049kmintheSouthernSectorAsimilarpatternwasobserved inthedatagatheredbyMINFOF rangers TheNorthern Sector had a densityofhuntingsignof087km2 withintheareaofthegridincludingthe2km buffer compared to 008km2 in the Southern Sector Giventhatseveralsignsmeasuredarecloselyassociatedwithhuntingac‐tivitysuchassnaresandcartridgesweassumethathuntingactiv‐ityisonaveragehigherintheNorthernSectorthantheSouthernSector
32emsp|emspSpecies richness
A total of 26 medium‐to‐large terrestrial mammal species werephotographedintheNorthernSectorand31medium‐to‐largeter‐restrialmammalspeciesintheSouthernSector(Table1)Wealsore‐cordedfivearborealmammalspeciesthatwerenotthetargetofthissurvey (Table1)Fourmedium‐to‐large terrestrialmammalspecies
expected to occur in the surveyed habitats according to availableIUCN distribution maps and literature were not detected by thecameratrapsurveysineithersector(Table1)
The species accumulation curves for medium‐to‐large terres‐trialmammal species showmore species detected per unit effortin theSouthernSector (Figure2)Thediversity indicesweremar‐ginally lower in the Northern Sector (Simpsons=072 ShannonndashWeiner=179)comparedtotheSouthernSector(Simpsons=078ShannonndashWeiner=208)
33emsp|emspCommunity structure
CommunitystructureofmammalsdifferedbetweentheNorthernSectorandSouthernSectorsites(Figures3and4)withmorespe‐ciesbeingencounteredforthreeoutofthefourguilds(herbivoresinsectivoresandcarnivores)intheSouthernSectorThemostfre‐quentlyencounteredguild inbothsectorswasherbivore (14spe‐ciesintheSouthernSectorand13intheNorthernSector)followedbyomnivore(seveninbothsectors)carnivore(sixintheSouthernSector four in theNorthernSector) and insectivore (three in theSouthernSector two in theNorthernSector)Overallacross theguilds trapping rates for lowerbodymassspecieswerehigher inthe Northern Sector A marked difference was the higher trap‐pingratesofherbivoresandomnivoreswithbodymassgt10kg intheSouthernSector (Figure4) compared to theNorthernSector(Figure3)
34emsp|emspForest antelopes
Werecorded4495independentphotographiceventsoftenspe‐ciesof forest antelopesTheblueduiker (Philantomba monticolaThunberg 1789) was the most frequently encountered forestantelope species across both camera trap grids (RAI=527) fol‐lowed by Petersrsquo duiker (Cephalophus callipygus Peters 1876)(RAI=412) and Bay duiker (Cephalophus dorsalis Gray 1846)(RAI=747) The rest of the forest antelopeswere relatively in‐frequently encounteredwith a global trapping rate of less thanfiveThedisturbance‐sensitivewhite‐belliedduiker(Hart2013b)wasonlyencountered in theSouthernSector (RAI=395 [lower95 confidence limit (LCL)=214 upper 95 confidence limit(UCL)=611])TrappingratesweresignificantlyhigherforPeterrsquosduiker in the Southern Sector displaying a fivefold increase be‐tween sectors (Table 1) Peterrsquos duiker occupancy was also sig‐nificantlyhigherintheSouthernSectorcomparedtotheNorthernSector (p=002 Table 2) Therewere no significant differencesin trapping rates between the two sectors forBatersquos pygmy an‐telope (Neotragus batesi de Winton 1903) bay duiker bongo(Tragelaphus eurycerusOgilbyi1837)sitatunga (Tragelaphus spe-kiiSpeke1863)andblack‐frontedduiker(Cephalophus nigrifrons Gray1871)Occupancyvaluesforbayduikerblack‐frontedduikerandBatersquospygmyantelopedidnotdiffersignificantlybetweenthesectorsTherewereinsufficientdetectionsoftheotherspeciestomodeloccupancy
764emsp |emsp emspensp Bruce et al
TA B L E 1 emspMammalspeciespredictedtoberecordedintheNorthernandSouthern(management)sectorsofDjaFaunalReserveCameroon
Order Species IUCN Status HabitatNorthern sector RAI (LCLndashUCL)
Southern sector RAI (LCLndashUCL)
Afrosoricida Giantottershrew(Potamogale velox Du Chaillu1860)
LC Wetland Notdetected Notdetected
Carnivora Africangoldencat(Profelis aurataTemminck1827)a
VU Forest Notdetected 058(027ndash091)
Carnivora Leopard(Panthera pardusLinnaeus1758)a
NT Mixed Notdetected 083(032ndash145)
Carnivora Marshmongoose(Atilax paludinosusCuvier1829)a
LC Wetland 056(033ndash082)b 009(0ndash02)b
Carnivora Black‐leggedmongoose(Bdeogale nigripesPucheran1855)a
LC Forest 183(079ndash314) 371(263ndash484)
Carnivora Camerooncusimanse(Crossarchus platycephalusGoldman1984)a
LC Forest 183(124ndash247) 083(046ndash127)
Carnivora Long‐nosedmongoose(Herpestes nasodeWinton1901)a
LC Forest 102(053ndash160) 089(009ndash227)
Carnivora Africanpalmcivet(Nandinia binotataGray1830)a
LC Forest 113(071ndash16) 089(052ndash13)
Carnivora Servalinegenet(Genetta servalinaPucheran1855)a
LC Forest 325(239ndash416) 214(142ndash295)
Carnivora Large‐spottedgenet(Genetta maculata Gray1830)
LC Forest Notdetected Notdetected
Carnivora CentralAfricanoyan(Poiana richardsoniiThomson1842)c
LC Forest Notdetected 003(003ndash009)
Cetartiodactyla Batesspygmyantelope(Neotragus batesideWinton1903)a
LC Forest 04(011ndash078) 036(015ndash059)
Cetartiodactyla Forestbuffalo(Syncerus cafferSparrmansubspnanus1779)a
EN Forest 008(0ndash024) 006(0ndash019)
Cetartiodactyla Petersduiker(Cephalophus callipygusPeters1876)a
LC Forest 141(838ndash2071)b 7146 (4963ndash9641)b
Cetartiodactyla Bayduiker(Cephalophus dorsalisGray1846)a
LC Forest 668(44ndash935) 834(492ndash1228)
Cetartiodactyla White‐belliedduiker(Cephalophus leucogastersubsp leucogasterGray1873)
LC Forest Notdetected 395(214ndash611)
Cetartiodactyla Black‐frontedduiker(Cephalophus nigrifronsGray1871)a
LC Forest 086(003ndash246) 05(006ndash114)
Cetartiodactyla Yellow‐backedduiker(Cephalophus silvicultorAfzelius1815)a
LC Forest 37(225ndash554) 555(354ndash794)
Cetartiodactyla Blueduiker(Philantomba monticolaThunberg1789)a
LC Forest 6164(4602ndash788) 4298(315ndash5561)
Cetartiodactyla Bongo(Tragelaphus eurycerusOgilbyi1837)a
NT Forest 005(0ndash014) 006(0ndash015)
Cetartiodactyla Sitatunga(Tragelaphus spekiiSpeke1863)a
LC Wetland 024(005ndash048) 009(0ndash024)
Cetartiodactyla Redriverhog(Potamochoerus porcusLinnaeus1758)a
LC Woodland 161(102ndash228)b 7(336ndash1304)b
Cetartiodactyla Giantforesthog(Hylochoerus mein-ertzhageniThomas1904)
LC Forest Notdetected Notdetected
Cetartiodactyla Waterchevrotain(Hyemoschus aquaticusOgilby1841)a
LC Forest 03(0ndash075)b 46(192ndash799)b
(Continues)
emspensp emsp | emsp765Bruce et al
35emsp|emspCarnivore
ThecarnivorecommunitydifferedinRAIandstructurebetweenthetwosectorsFelidswerenotdetectedatallintheNorthernSectorbutboth leopard (Panthera pardusLinneaus1758)andgoldencat(Profelis aurata Temminck1827)werepresentintheSouthernSector
(Table1)AmongtheHerpestidaeblack‐leggedmongoose(Bdeogale nigripes Pucheran1855) showeda significantlyhigheroccupancy(p =gt001)intheSouthernSectorbuttrappingrateslackedsignifi‐cantdifference (RAI=371 [LCL=263UCL=484])comparedtothe Northern Sector (RAI=183 [LCL=079 UCL=314])Marshmongoose(Atilax paludinosusCuvier1829)hadsignificantlyhigher
Order Species IUCN Status HabitatNorthern sector RAI (LCLndashUCL)
Southern sector RAI (LCLndashUCL)
Hyracoidea Westerntreehyrax(Dendrohyrax dorsalis Fraser1855)
LC Forest Notdetected Detected
Pholidota White‐belliedpangolin(Phataginus tricuspisRafinesque1821)a
VU Forest 062(029ndash1) 08(044ndash121)
Pholidota Giantpangolin(Smutsia giganteaIlliger1815)a
VU Forest 027(008ndash052) 068(038ndash101)
Primates Agilemangabey(Cercocebus agilisMilne‐Edwards1886)a
LC Forest 035(013ndash059) 448(265ndash682)
Primates Moustachedguenon(Cercopithecus cephusLinnaeus1758)c
LC Forest Detected Notdetected
Primates Greaterspot‐nosedguenon(Cercopithecus nictitansLinnaeus1766)c
LC Forest Detected Detected
Primates Blackcolobus(Colobus satanasWaterhouse1838)c
VU Forest Notdetected Detected
Primates Galagospc ‐ Detected Notdetected
Primates Mandrill(Mandrillus sphinxLinnaeus1758)a
VU Forest 005(0ndash013) 006(0ndash019)
Primates Westernlowlandgorilla(Gorilla gorillaSavagesubspgorilla1847)a
CR Forest 016(003ndash031) 044(02ndash073)
Primates Centralchimpanzee(Pan troglodytesBlumenbachsubsptroglodytes1799)a
EN Forest 161(077ndash29)b 457(314ndash617)b
Proboscidea Forestelephant(Loxodonta cyclotisMatschie1900)a
VU Mixed 086(046ndash135) 19(086ndash329)
Rodentia Africanbrush‐tailedporcupine(Atherurus africanusGray1842)a
LC Forest 1753(1142ndash2446) 762(464ndash1145)
Rodentia Eminspouchedrat(Cricetomys eminiWroughton1910)a
LC Forest 32(2358ndash4141)b 756(341ndash1465)b
Rodentia Greatercanerat(Thryonomys swinderi-anus Temminck1827)
LC Wetland Notdetected Notdetected
Rodentia LadyBurtonsropesquirrel(Funisciurus isabellaGray1862)c
LC Forest Detected Detected
Rodentia Fire‐footedropesquirrel(Funisciurus pyrropusCuvier1833)c
LC Forest Detected Detected
Rodentia Africangiantsquirrel(Protoxerus stangeriWaterhouse1842)c
LC Forest Detected Detected
Tubulidentata Aardvark(Orycteropus aferPallas1766)a LC Mixed Notdetected 009(005ndash019)
NotesForeachsectorandspeciesthatwasdetectedwepresentthemeanand95confidencelimits(inbrackets)ofthenumberofindependentphotographiceventspertrapdaytimes100Trappingrateswereonlycalculatedformedium‐to‐largeterrestrialmammalsduetoinconsistentdetectionprobabilitieswithotherspeciesIUCNstatuscriticallyendangered(CR)endangered(EN)vulnerable(VU)nearthreatened(NT)leastconcern(LC)aIndicatesaspeciesthatwasincludedintherarefactionanalysisaccordingtothedefinitiongiveinthedataanalysissectionofthemethodsbIndicatesthattheRAIconfidenceintervalsdonotoverlapandcanbeconsideredsignificantlydifferentcSignifiesanarborealspecies
TA B L E 1 emsp (Continued)
766emsp |emsp emspensp Bruce et al
F I G U R E 2 emspRarefiedspeciesaccumulationcurvesformedium‐to‐largeterrestrialmammalsintheNorthernandSouthernsectorsofDjaFaunalReserveCameroon
F I G U R E 3 emspDistributionofmedium‐to‐largeterrestrialmammalspeciesintheNorthernSectoroftheDjaFaunalReserveCameroononthebasisofbodysizeandtrophiccategoryEachcirclerepresentsaspeciesinfunctionalspaceSizeofthecircleproportionaltothetrappingrateforthatspecies
emspensp emsp | emsp767Bruce et al
trappingrateintheNorthernSector(Table1)butlackedsufficientdetectionstoreliablycalculateoccupancyAbundanceofCamerooncusimanse(Crossarchus platycephalusGoldman1984)didnotdiffersignificantlybetweenthetwosectors(NorthernSectorRAI=183[LCL=124 UCL=247 ψ=075] Southern Sector RAI=083[LCL=046UCL=127]ψ=056p=028)
36emsp|emspElephants great apes and giant pangolin (illegal wildlife trade targets)
Amongtheterrestrialmammalstargetedbytheillegalwildlifetradespecifically central chimpanzee (Pan troglodytes Blumenbachsubsp troglodytes 1799) western lowland gorilla (Gorilla gorillaSavagesubsp gorilla1847)forestelephantgiantpangolin(Smutsia gigantea Illiger 1815) and white‐bellied pangolin (Phataginus tri-cuspis Rafinesque 1821) only central chimpanzee displayed asignificant difference in RAI between the management sectors(Northern Sector RAI=161 [LCL=077 UCL=29] SouthernSector RAI=457 [LCL=314 UCL=617]) However there wasnosignificantdifferenceinmeanoccupancybetweenthetwosec‐tors (p=074) Giant pangolin displayed the greatest differencewithathreefoldincreaseinRAIfrom027[LCL=008UCL=052]in the Northern Sector to 068 [LCL=038 UCL=101] in theSouthernSectorbutthiswasnotsignificantduetotheoverlapping
confidencelimitsTheRAIsandwhereappropriateoccupancyofforestelephantwesternlowlandgorillaandwhite‐belliedpangolinwerenotsignificantlyhigher intheSouthernSectorcomparedtotheNorthernSector(Tables12and12)
37emsp|emspOther bushmeat‐targeted species
Eminrsquospouchedrat(Cricetomys eminiWroughton1910)wasmoreabundantasmeasuredbybothoccupancy(pge001)andtrapratesintheNorthernSectorcomparedtotheSouthernSector(Table1)Africanbrush‐tailedporcupine(Atherurus africanusGray1842)didnothavesignificantdifferencesinRAIbetweenthemanagementsectors but occupancywas significantly higher in theNorthernSector (pge004) In comparison the larger‐bodied red river hog(Potamochoerus porcus Linneaus1758)wasmore frequentlyen‐countered as measured by both species abundance metrics intheSouthernSector(RAI=7[LCL=336UCL=1304]ψ=091)compared to the Northern Sector (RAI=161 [LCL=102UCL=228]ψ=065(p=004)
38emsp|emspSpecies occupancy with covariates
Therewasatotalof15speciesthathadsufficientdetectionstomodeloccupancywithinteractingsitecovariates(distancetoparkboundary
F I G U R E 4 emspDistributionofmedium‐to‐largeterrestrialmammalspeciesintheSouthernSectoroftheDjaFaunalReserveCameroononthebasisofbodysizeandtrophiccategoryEachcirclerepresentsaspeciesinfunctionalspaceSizeofthecircleproportionaltothetrappingrateforthatspecies
768emsp |emsp emspensp Bruce et al
TAB
LE 2
emspNullmeanoccupancy(ψ)anddetection(p)probabilitieswithstandarderrorpresentedinbracketsfortheNorthernSectorandSouthernSector
Spec
ies
Nor
ther
n se
ctor
(ψ)
Nor
ther
n se
ctor
(p)
Sout
hern
sec
tor
(ψ)
Sout
hern
sec
tor
(p)
Mod
elBe
tamdash
Para
met
er
chos
enLo
wer
95
be
taU
pper
95
be
taC‐
hat v
alue
Chi‐s
quar
ep
valu
e
Certiodactyla
Batesrsquospygmy
antelope
022(01)
015(006)
[026]
ndashNull
ndashndash
ndashndash
ndash
Bayduiker
091(006)
04(003)
087(006)
04(003)
DRN
lam(DistanceSTD)
000
6356
808
043
3356
50
930
25
Black‐fronted
duiker
01(006)
036(01)
015(006)
025(008)
Null
ndashndash
ndashndash
ndash
Blueduiker
097(003)
082(002)
1(0)
1(0)
DRN
lam(DistanceSTD)
002
0135
490
3637
492
021
024
Petersrsquoduiker
083(007)
a056(003)
1(0)a
1(0)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus07435528
003
6592
430
004
03
Waterchevrotain
[007]
ndash04(008)
045(005)
ndashndash
ndashndash
ndashndash
White‐bellied
duiker
ndashndash
072(008)
031(003)
Null
ndashndash
ndashndash
ndash
Yellow‐backed
duiker
084(008)
027(003)
086(007)
039(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
010
8837
21
0251
104
069
021
Redriverhog
065(011)
a021(003)
091(006)
a033(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus12560347
minus01352547
027
044
Proboscidae
Forestelephant
067(015)
014(004)
063(013)
014(004)
Null
ndashndash
ndashndash
ndash
Primates
Central
chimpanzee
077(014)
015(004)
082(007)
035(003)
SRN
lam(sectorSouthern)
037
3686
91
4429
314
03
039
Westernlowland
goril
la[007]
ndash045(017)
01(004)
Null
ndashndash
ndashndash
ndash
Philodota
Giantpangolin
[02]
ndash061(016)
011(004)
Null
ndashndash
ndashndash
ndash
White‐bellied
pangolin
045(016)
012(005)
063(017)
011(003)
DSoccu
psi(DistanceSTDsec
torSouthern)
minus48425115
minus1910401
022
06
Rodentia
African
brush‐tailed
porcupine
098(003)
a057(003)
084(006)
a042(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus10008123
minus01586108
042
071
Eminrsquospouched
rat
1(0)a
1(0)
079(007)
a038(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus095574568
minus01390762
021
075
Carnivora
(Con
tinue
s)
emspensp emsp | emsp769Bruce et al
and management sector Table 2) Forest elephant black‐frontedduikerand long‐nosedmongoose (Herpestes nasodeWinton1901)lackedamodel thathadanAICdifferenceofgt2 therefore theco‐variatemodelswerenotsignificantlydifferent to thenullmodel forthese species Elevenof 15 species had aRoylendashNicholsmodel se‐lectedasthelowestAICvaluesuggestingadifferenceinthenumberofindividualswassignificantlyinfluencingdetectionprobabilitiesandthereforeoccupancy
RoylendashNichols models accounted for occupancy being signifi‐cantlyhigherindifferingmanagementsectorswithnointeractionofdistancetotheprotectedareaboundaryforthreespeciesCamerooncusimanse had higher occupancy in the Northern Sector In con‐trast central chimpanzee and black‐legged mongoose had signifi‐cantlyloweroccupancywithintheNorthernSectorcomparedtotheSouthernSector(Figure5)
African brush‐tailed porcupine Eminrsquos pouched rat and servalinegenet(Genetta servalinaPucheran1855)hadasynergisticRoylendashNicholsmodelselectedasthemostsupportedTheprobabilityofsiteoccupancyslightlyincreasedwithdistancetotheboundaryandwasoverallhigherin theNorthernSector butdeclinedwithdistance to theboundary intheSouthernSector(Figure6)BothPetersrsquoduikerandredriverhogalsodisplayedthispatternofoccupancybuthadamuchgreaterincreaseinoccupancyintheNorthernSectorandhadhigheroccupancyoverallintheSouthernSector(Figure6)Incontrastyellow‐backedduiker(Cephalophus silvicultorAfezilus1815)wastheonlyspeciestodemonstrateanincreaseinoccupancywithdistancetotheboundaryintheSouthernSectorwhiledecliningintheNorthernSectorHoweversimilartootherlargerspeciesoccupancywashigherintheSouthernSector(Figure6)
With regard to the remainingduiker speciesmodelled aRoylendashNicholsmodelwithdistancetotheprotectedareaboundarywasiden‐tifiedasthemostappropriateTheprobabilityofasitebeingoccupiedbyblueduikerandbayduikerincreasedwithdistancetotheboundarywith no discernible difference betweenmanagement sectors in themodel(Figure7)
White‐belliedpangolinhadasingle‐seasonoccupancymodelse‐lectedsuggestingdifferences inabundancebetweenthemanage‐mentsectorsdidnotaffectdetectionprobabilitiesTheprobabilityofasitebeingoccupiedbywhite‐belliedpangolin increasedintheNorthernSectoranddeclinedintheSouthernSectorwithincreasingdistancetotheboundary(Figure8)
Seven speciesweredetectedonly inone sectoror lacked suffi‐cientdetectionsinonesectortoreliablymodeloccupancyacrossbothmanagement sectors Therefore only the effect of distance to theboundarycouldbemodelledThesewereAfricangoldencatwesternlowlandgorillawhite‐belliedduikergiantpangolinAfricanpalmcivet(Nandinia binotata Gray 1830) Batesrsquos pygmy antelope and waterchevrotain (Hymeoschus aquaticusOgilby 1841)African palm civetwastheonlyspeciestohavedistancetotheboundaryselectedastheoptimummodel to explain occupancy as occupancy increasedwithdistance from the boundary of the protected area (Table 2)All theremainingspecieshadthenullmodelselectedastheoptimummodelaccordingtoAICcriteria (Table2)Howeverdistancetothebound‐arywaswithinlt2AICforthesespeciessuggestingthatasignificantSp
ecie
sN
orth
ern
sect
or (ψ
)N
orth
ern
sect
or (p
)So
uthe
rn s
ecto
r (ψ
)So
uthe
rn s
ecto
r (p
)M
odel
Beta
mdashPa
ram
eter
ch
osen
Low
er 9
5
beta
Upp
er 9
5
beta
C‐ha
t val
ueCh
i‐squ
arep
va
lue
Africangolden
cat
ndashndash
041(013)
013(004)
Null
ndashndash
ndashndash
ndash
Africanpalm
civet
[047]
ndash073(017)
012(003)
DOccu
psi(DistanceSTD)
minus8177158
Inf
197
008
Black‐legged
mongoose
047(01)a
025(004)
082(008)
a031(003)
SRN
lam(sectorSouthern)
028
0266
31
4627
420
011
058
Cameroon
cusimanse
075(009)
027(004)
056(015)
012(004)
SRN
lam(sectorSouthern)
minus1808131
minus05098939
005
073
Long‐nosed
mongoose
055(012)
a02(004)
015(006)
a027(007)
Null
ndashndash
ndashndash
ndash
Servalinegenet
092(006)
035(003)
08(009)
02(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus09202819
003
5821
570
50
26
Not
esNaiumlveoccupancyvaluesarepresentedinsquarebracketsforspecieswithadetectionprobabilitylt01TheoptimummodelchosenbyAkaikersquosinformationcriteriaforeachspeciesgeneratingsuf‐
ficientoccupancyvaluesinbothsectorswiththeBetaparameteranditisrespectivelowerandupper95confidencelimitsisshownandtheassociatedc‐hatandchi‐squaredp
val
ue
DdistancetoboundarySmanagementsectorRNRoylendashNicholsmodelOccuMckenziesingle‐seasonoccupancymodesynergisticinteraction
a IndicatesasignificantdifferenceinoccupancybetweensectorsasmeasuredbytheWaldteststatistic
TAB
LE 2
emsp(Continued)
770emsp |emsp emspensp Bruce et al
relationshipwithdistancetotheboundarycouldbeinfluencingoccu‐pancyIntheSouthernSectortheoccupancyincreasedwithdistanceto theboundary forwestern lowlandgorillaandgiantpangolinbutdecreasedforAfricangoldencatwhite‐belliedduikerandwaterchev‐rotainIntheNorthernSectoroccupancyincreasedwithdistancetotheboundaryforBatesrsquospygmyantelope
4emsp |emspDISCUSSION
Thecomparisonofthetwosurveysconfirmsthatstandardcameratrap surveys and derived metrics of presenceabsence trappingrates andoccupancy candiscern confidentdifferences in ground‐dwellingmammalcommunitiesinCentralAfricanforests
41emsp|emspCamera trap surveys for documenting species
Thecomparativeefficacyofcamera traps for surveyingmediumto large ground‐dwelling mammals in the DFR is indicated byobservationratesandverifiabilityofrecordsespeciallyofelusivesmallerandnocturnalspeciesForexamplethedirectencounterraterecordedbyrangersonpatrolthroughouttheentirereserveover a nine‐month period is much lower than the combinednumberofindependentphotographiceventsinbothmanagementsectors (ZSL amp MINFOF 2017b) even for relatively largeconspicuous species such as forest elephant (96 photographiceventscomparedto29directencounters)andcentralchimpanzee(204 independent photographic events compared to 23 directencounters)Methodologiessuchascameratrapping therefore
provideimportantbaselinedatathatwhenrepeatedthroughtimeusingastandardisedprotocolcanallowatleasttrendsinrelativeabundanceindicestobemonitored
42emsp|emspCamera trap surveys for comparing assemblages among sites
Despitebeingseparatedbyonlyc32kmthemammalcommunitiesbetween the twocamera trapgridsdisplayedmarkeddifferencesThiswasthecaseeventhoughbothgridshadlowShannonndashWeinerandSimpsonsdiversityindicesduetothedominanceofthreeorfourspeciesineachcameratrapgridSignificantdifferencesamongthesiteswere observed for the trapping rates of species of differentsizesbetweensectorsSmaller‐bodiedspecieswithintheherbivoreand omnivore guilds were more prevalent within the NorthernSector (Figure 2) Trapping rates and occupancy values for smallcarnivoresarealsolowerintheSouthernSectorThiscouldbeduetothedifficultyofidentifyingmorphologicallysimilarspeciessuchasmarshmongooseandlong‐nosedmongoose(Bahaa‐el‐dinetal2013 Ray 1997) in infrared imagery with single cameras Thereweremoreunidentifiablemongooseeventsthatwereclassifiedtoafamilylevel―66224intheSouthernSectorcomparedto29156intheNorthernSectorofallcombinedmongooseevents
43emsp|emspThe potential impact of seasonality on estimates derived from camera traps
Due to logistical and financial constraints the surveys could notberuninthesameseasonThishasthepotentialtoaffecttrapping
F I G U R E 5 emspChangeintheprobabilityofoccupancyforblack‐leggedmongoosecentralchimpanzeeandCamerooncusimansewithmanagementsectoraccordingtoaRoylendashNicholsmodel
emspensp emsp | emsp771Bruce et al
rates and occupancy for specieswith larger home ranges becausewhenspeciesarewide‐rangingoccupancycanproveineffectiveformeasuring relative abundance Forest elephants (Blake 2002) andgreatapesareknowntodisplayseasonalshiftsintheirhabitatusageover great distances in response to increased fruit availability andprecipitation(HeadRobbinsMundryMakagaampBoesch2012)Thiscouldalsoinfluenceothergregariousspeciessuchasredriverhogthatarealsothoughttooccasionallydisplaysimilaraggregationsandmovementsinresponsetomastingevents(LeslieampHuffman2015)However as both red river hog and chimpanzee had significantlyhigherRAIandhigheroccupancywithvariabledetectionprobabilityaccording to the number of individuals incorporated this supports
thepossibilitythatthesespeciesarefavouringtheSouthernSectorIfmanagersareable toestablishwhetherwide‐rangingspeciesarepredictably moving to known areas within the reserve they canrespondinamannerthatprovidesenhancedprotectiontovulnerablewildlifepopulations in concentration areasAsmost species in thissurveylikelyhaveasmallerhomerangethantheinter‐trapdistanceand display fixed territories it can be regarded as appropriate tocompare occupancy values as the extent of overlap of territorieswithin the two surveys are unlikely to change in such away as toaffecttheresultsFuturestudieswouldbenefitfromtryingtomatchcameratrapsurveysseasonallytotryandclarifytheissueofseasonalshiftsinhabitatusagewithintheDFR
F I G U R E 6 emspChangeintheprobabilityofoccupancyforAfricanbrush‐tailedporcupineEminspouchedratredriverhogservalinegenetPetersrsquoduikerandyellow‐backedduikerwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
772emsp |emsp emspensp Bruce et al
F I G U R E 7 emspChangeintheprobabilityofoccupancyforblueduikerandbayduikerwithdistancetotheboundaryinkilometresacrossbothmanagementsectorsaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
F I G U R E 8 emspChangeintheprobabilityofoccupancyforwhite‐belliedpangolinwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaMackenzieoccupancymodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
emspensp emsp | emsp773Bruce et al
44emsp|emspCamera trap surveys for measuring the impacts of hunting on mammal communities
The spatial scale at which mammal communities are affected byandhowpopulationsrespondtoanthropogenicpressuressuchasbushmeat hunting is difficult to empiricallymeasure (Laurance etal2006)Thisisespeciallytrueformammalsresidingwithintropi‐cal forestswheregatheringconsistentandmeaningfulpopulation‐andcommunity‐levelmetrics ischallenging(Ahumadaetal2013)Population density of tropical mammals can vary greatly due toheterogeneity present within the environment For example for‐est elephants havedifferent distributions and aggregations inwetanddryseasonsinNouabaleacute‐Ndoki NationalParkwhichispartiallydependentonspatio‐temporalpatternsoffruitingtreesacrossthelandscape(Blake2002)
Whether the differences observed among the two sites sur‐veyedhereareattributabletodifferent levelsofhuntingpressureremains to be confirmed There are however indications thathuntingpressureanditsimpactsonmammalfaunasaregreaterintheNorthern Sector than in the Southern Sector The effects ofhuntingpressureonmammaliandeclinesinCentralAfricanforestsarewell documented The pattern in general is the largest‐bod‐ied species frugivores and thosewith high hunter or blackmar‐ketvalue(Abernethyetal2013Cardilloetal2005FaOliveroFarfaacutenMaacuterquezDuarteetal2014aFaOliveroFarfaacutenMaacuterquezVargasetal2014bPeresampPalacios2007)arethefirstspeciestoshownoticeabledeclineInthisstudythesignificantdeclineintherelativeabundance for frugivores suchasPetersʼduikerandspe‐cieswithhighhuntervalueliketheredriverhogunderincreasedhuntingpressure in theNorthernSector is reported inother sur‐veys(Abernethyetal2013)Thisisalsoreflectedinthedifferencesobserved in this study in biomass in the different guilds of eachmammalcommunityThemammalcommunitywithintheNorthernSector shows indications of a community that is disturbed and isexperiencingelevatedhuntingpressureThesearehigher(camera)trapping rates for smaller‐bodiedspecies suchasEminrsquospouchedrat and significantly fewer encounters of larger‐bodiedmammalsthataretargetsofthebushmeattradesuchasPetersʼduikerandredriverhog(FaRyanampBell2005JerozolimskiampPeres2003)Additionalindicatorsaretheabsenceinthesurveysoflargercarni‐voresintheNorthernSectorsuchasgoldencatandleopardwhicharesensitivetosnaring(Bahaa‐el‐dinetal2015)andsignificantlyreducedabundancemetricsfordisturbance‐sensitivespeciessuchasblack‐leggedmongooseandwaterchevrotain(Hart2013a)Theabsence of white‐bellied duiker in the Northern Sector also sug‐gestselevatedhumandisturbanceasthisspecieshasbeenreportedasverysensitivetoevenminorperturbationwithintheenvironment(Hart2013b)IncomparisontheSouthernSectorcontainedindica‐torfaunasuchasthewhite‐belliedduikerandhadhighertrappingratesforlarger‐bodiedspecies
WesuspectthedifferencesobservedaremostlikelyduetolowerhumandisturbanceintheSouthernSectorTheteamsdeployingand
recoveringthecamerasintheSouthernSectorcovered238kmandencountered few signs of humanperturbation (T Brucepers obs)whereashumansignwascommonlyencounteredbytheteamsintheNorthernSectorThisperceiveddifference is reflected in the2017and 2018 density of hunting signwithin each camera trap grid asdetected throughMINFOF ranger patrols (ZSL ampMINFOF 2017a2017b) and through the2018DistanceSampling inventory for theDFR (Bruce et al 2018) Higher numbers of hunting sign in theNorthernSectorwouldbeconsistentwithanelevatedhuntingpres‐sureinthatarea
45emsp|emspProtection of refugia from hunting
Though inferences made for wide‐ranging species such as forestelephantsandgreatapesusingcameratrapsaredifficultthefactthattrappingrateswerehigherinmorechallengingterrainwithassumedlower hunting pressure could be indicative of complex habitatprovidingsomelevelofprotectionfromhuntingElephantisknownto retreatwhen they aredisturbed to terrain that ismoredifficulttoaccessbyhumans (Hedges2012)Thuswithin largerprotectedareas certain zones may act as refugia for wildlife populations(Campbelletal2011)Thiscanbeduetoarangeof factorssuchas remoteanddifficult terrain forpoachers (Attum2007Hedges2012) or the regular presence of field researchers and rangers(Campbell et al 2011) The significanceof these refugia for largerprotected areas is that the populations of wildlife residing withinthem if adequately protected may provide source populations toallowrecolonisationofotherareasofthereserve(NaranjoampBodmer2007)Thereforeifadequateprotectioncanbeprovidedtorelativelysmallbutimportantareasoflargereservesthismayprovidetropicalforestswithabetterchanceofbeingecologicallyresilienttoongoingand increasing human perturbation Well‐designed camera trapsurveys may provide data on the status of wildlife populations atrelativelyfinespatialresolutionssoastoidentifyfunctionalrefugiawithgreaterconfidence
ACKNOWLEDG EMENTS
WeappreciatetheongoingsupportofCameroonrsquosMinistryofForestsandWildlife(MINFOF)andtheopportunitytocontributetobiodiver‐sityconservationthroughoutthecountryInparticularwewouldliketothanktheChefdrsquoAntenneSergeJacobMeyeforhisongoingsup‐portofconservationresearchwithintheprotectedareaWeappreci‐atethestalwarteffortsofMINFOFecoguardsandlocalporterswhoaccompaniedthesurveyteamsinthefieldWewouldalsoliketothanktheUnitedStatesFishandWildlifeService(USFWS)mdashAfricanElephantConservationandIUCNSOSmdashFondationSegreacutePangolinConservationInitiativeforsupportingthiswork
ORCID
Tom Bruce httporcidorg0000‐0001‐6958‐1657
774emsp |emsp emspensp Bruce et al
R E FE R E N C E S
AbernethyKACoad L TaylorG LeeMEampMaisels F (2013)Extent and ecological consequences of hunting in Central Africanrainforests in thetwenty‐firstcenturyPhilosophical Transactions of the Royal Society of London Biological Sciences368(1625)20120303httpsdoiorg101098rstb20120303
AbrahamsM I Peres C A amp Costa H C (2017)Measuring localdepletion of terrestrial game vertebrates by central‐place hunt‐ers in rural Amazonia PLoS ONE 12(10) e0186653 httpsdoiorg101371journalpone0186653
AhumadaJAHurtadoJampLizcanoD(2013)MonitoringthestatusandtrendsoftropicalforestterrestrialvertebratecommunitiesfromcameratrapdataAtool forconservationPLoS ONE8(9)e73707httpsdoiorg101371journalpone0073707
Ahumada J A Silva C E Gajapersad K Hallam C Hurtado JMartin E hellip Sheil D (2011) Community structure and diver‐sity of tropical forest mammals Data from a global camera trapnetwork Philosophical Transactions of the Royal Society of London Biological Sciences366(1578)2703ndash2711httpsdoiorg101098rstb20110115
AminRAndanjeSAOgwonkaBAliAHBowkettAEOmarMampWacherT(2015)ThenortherncoastalforestsofKenyaarenationally and globally important for the conservation of AdersrsquoduikerCephalophusadersiandotherantelopespeciesBiodiversity and Conservation 24(3) 641ndash658 httpsdoiorg101007s10531‐014‐0842‐z
Attum O (2007) Can landscape use be among the factors that po‐tentiallymake some ungulates speciesmore difficult to conserveJournal of Arid Environments69(3)410ndash419
Bahaa‐el‐dinLHenschelPAbaaRAbernethyKBohmTBoutNhellipLeeM (2013)NotesonthedistributionandstatusofsmallcarnivoresinGabonSmall Carnivore Conservation4819ndash29
Bahaa‐el‐dinLHenschelPButynskiTMMacdonaldDWMillsDSlotowRampHunterL (2015)TheAfricangoldencatCaracalaurataAfricasleast‐knownfelidMammal Review45(1)63ndash77
Bennett E L Blencowe E Brandon K Brown D Burn R WCowlishaw G hellip Robinson J G (2007) Hunting for consensusReconcilingbushmeatharvestconservationanddevelopmentpol‐icyinWestandCentralAfricaConservation Biology21(3)884ndash887httpsdoiorg101111j1523‐1739200600595x
BlakeSDeemSLMossimboEMaiselsFampWalshP(2009)Forestelephants Tree planters of the CongoBiotropica41(4) 459ndash468httpsdoiorg101111j1744‐7429200900512x
Blake S (2002) The ecology of forest elephant distribution and itsimplications for conservation Doctoral dissertation University ofEdinburgh
BruceTNdjassiCFowlerANdimbeMFankemOTabueRhellipOlsonD(2018)Faunal inventory of the Dja Faunal Reserve Cameroon Yaoundeacute Cameroon Ministry of Forests and Wildlife (MINFOF)Zoological Society of London ndash Cameroon Country ProgrammeAfricanWildlifeFoundation
BruceTWacherTNdingaHBidjokaVMeyongFNgoBataMampOlsonD(2017)camera trap survey for larger terrestrial wildlife in the Dja Biosphere Reserve CameroonYaoundeacuteCameroonZoologicalSocietyofLondon(ZSL)ampCameroonMinistryofForestsandWildlife(MINFOF)
BurnhamKPampAndersonDR(2002)Model selection and multimodel inferenceNewYorkNYSpringer
Campbell G Kuehl H Diarrassouba A NGoran P K amp BoeschC (2011) Long‐term research sites as refugia for threatened andover‐harvested species Biology Letters 7(5) 723ndash726 httpsdoiorg101098rsbl20110155
CardilloMMaceGMJonesKEBielbyJBininda‐EmondsORSechrestWhellipPurvisA(2005)Multiplecausesofhighextinction
riskinlargemammalspeciesScience309(5738)1239ndash1241httpsdoiorg101126science1116030
Craigie IDBaillieJEBalmfordACarboneCCollenBGreenREampHuttonJM (2010)Largemammalpopulationdeclines inAfricarsquosprotectedareasBiological Conservation143(9)2221ndash2228httpsdoiorg101016jbiocon201006007
DaveyKWacherTampAminR(2017)Analysis tool for camera-trap sur-vey data [Computer software]ZoologicalSocietyofLondonRetrievedfromhttpswwwzslorgzsl‐camera‐trap‐data‐management‐ and‐analysis‐package
Djuikouo M N K Doucet J L Nguembou C K Lewis S L ampSonkeacute B (2010) Diversity and aboveground biomass in threetropical forest types in the Dja Biosphere Reserve Cameroon African Journal of Ecology 48(4) 1053ndash1063 httpsdoiorg101111j1365‐2028201001212x
DupainJBombomeKampVanElsackerL(2003)LeschimpanzeacutesetlesgorillesdelareacuteservedefauneduDjaCanopeacutee2414ndash15
EffordMGampDawsonDK(2012)OccupancyincontinuoushabitatEcosphere3(4)1ndash15httpsdoiorg101890ES11‐003081
Efron B amp Tibshirani R J (1994) An introduction to the bootstrap WashingtonDCCRCPress
FaJEOliveroJFarfaacutenMAacuteMaacuterquezALDuarteJNackoneyJhellipMacdonaldDW(2014a)CorrelatesofbushmeatinmarketsanddepletionofwildlifeConservation Biology29(3)805ndash815
Fa J EOlivero J FarfaacutenMAacuteMaacuterquezA LVargas JMRealRampNasiR(2014b)IntegratingsustainablehuntinginbiodiversityprotectioninCentralAfricaHotspotsweakspotsandstrongspotsPLoS ONE9(11)e112367
FaJERyanSFampBellDJ (2005)Huntingvulnerabilityecolog‐ical characteristics and harvest rates of bushmeat species in afro‐tropicalforestsBiological Conservation121(2)167ndash176httpsdoiorg101016jbiocon200404016
Fa J E Seymour S Dupain J E F Amin R Albrechtsen L ampMacdonaldD (2006) Getting to gripswith themagnitude of ex‐ploitationBushmeat in theCross‐SanagariversregionNigeria and Cameroon Biological Conservation 129(4) 497ndash510 httpsdoiorg101016jbiocon200511031
Farris Z J Boone H M Karpanty S Murphy A Ratelolahy FAndrianjakariveloVampKellyMJ(2015)FeralcatsandthefitoatyFirstpopulationassessmentoftheblackforestcatinMadagascarrsquosrainforestsJournal of Mammalogy97(2)518ndash525
Fiske IampChandlerR (2011)UnmarkedAnRpackageforfittinghi‐erarchicalmodelsofwildlifeoccurrenceandabundanceJournal of Statistical Software43(10)1ndash23
HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences107(19)8650ndash8655httpsdoiorg101073pnas0912668107
HartJ(2013a)WaterchevrotainHymemoschusaquaticusInJKingdonampMHoffmann (Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp88ndash92)LondonUKBloomsbury
Hart J (2013b) White‐bellied duiker Cephalophus leucogaster In JKingdonampMHoffmann(Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp255ndash258)LondonUKBloomsbury
HeadJSRobbinsMMMundryRMakagaLampBoeschC(2012)Remotevideo‐cameratrapsmeasurehabitatuseandcompetitiveex‐clusionamongsympatricchimpanzeegorillaandelephantinLoangoNational ParkGabon Journal of Tropical Ecology28(06) 571ndash583httpsdoiorg101017S0266467412000612
HedgesS(2012)Monitoring elephant populations and assessing threats HimayatnagarTelanganaUniversitiesPress
HedwigDKienastIBonnetMCurranBKCourageABoeschChellipKingT(2018)Acameratrapassessmentoftheforestmam‐mal community within the transitional savannah‐forest mosaic oftheBateacutekeacutePlateauNationalParkGabonAfrican Journal of Ecology56(4)777ndash790httpsdoiorg101111aje12497
emspensp emsp | emsp775Bruce et al
HijmansRJCameronSEParraJLJonesPGampJarvisA(2005)Very high resolution interpolated climate surfaces for global landareasInternational Journal of Climatology25(15)1965ndash1978httpsdoiorg101002joc1276
HuggelA(2012)Exiv2softwaretool[Computersoftware]Retrievedfromhttpswwwexiv2orgindexhtml
Jerozolimski A amp Peres C A (2003) Bringing home the biggestbacon A cross‐site analysis of the structure of hunter‐kill profilesin Neotropical forests Biological Conservation 111(3) 415ndash425httpsdoiorg101016S0006‐3207(02)00310‐5
KingdonJ (2015)The Kingdon field guide to African mammalsLondonUKBloomsburyPublishing
KuumlhlHFMaiselsMAncrenazampEAWilliamson(Eds)(2008)Best practice guidelines for surveys and monitoring of great ape populations GlandSwitzerlandIUCN
LauranceWFCroesBMTchignoumbaLLahmSAAlonsoALeeMEhellipOndzeanoC(2006)ImpactsofroadsandhuntingoncentralAfrican rainforestmammalsConservation Biology20(4)1251ndash1261httpsdoiorg101111j1523‐1739200600420x
LauranceWFUsecheDCRendeiroJKalkaMBradshawCJSloan S P hellip Arroyo‐Rodriguez V (2012) Averting biodiversitycollapse in tropical forestprotectedareasNature489(7415)290httpsdoiorg101038nature11318
LeslieDMampHuffmanBA(2015)Potamochoerus porcus(ArtiodactylaSuidae)Mammalian Species4715ndash31
MacKenzieD IampBailey L L (2004)Assessing the fit of site‐occu‐pancy models Journal of Agricultural Biological and Environmental Statistics9300ndash318httpsdoiorg101198108571104X3361
MacKenzieDINicholsJDRoyleJAPollockKHBaileyLLampHinesJE (2006)Occupancy estimation and modellingBurlingtonMAAcademicPress
Magurran A E (2005) Species abundance distributions Patternor process Functional Ecology 19(1) 177ndash181 httpsdoiorg101111j0269‐8463200500930x
MaiselsFStrindbergSBlakeSWittemyerGHartJWilliamsonEAhellipWarrenY (2013)DevastatingdeclineofforestelephantsinCentralAfricaPLoS ONE8(3)e59469httpsdoiorg101371journalpone0059469
MalhiYAdu‐BreduSAsareRA LewisS LampMayauxP (2013)AfricanrainforestsPastpresentandfuturePhilosophical Transactions of the Royal Society of London Biological Sciences 368(1625)20120312
MallonDPHoffmannMGraingerMJHibertFVanVlietNampMcGowanP JK (2015)An IUCNsituationanalysisof terrestrialandfreshwaterfaunainWestandCentralAfricaOccasionalpaperoftheIUCNspeciessurvivalcommission(54)
MambeyaMMBakerFMombouaBRKoumbaPamboAFHegaMOkouyiOkouyiVJhellipAbernethyK(2018)TheemergenceofacommercialtradeinpangolinsfromGabonAfrican Journal of Ecology56(3)601ndash609httpsdoiorg101111aje12507
MINFOFampIUCN(2015)CaracteacuterisationdelapopulationdegrandsetmoyensmammifegraveresdanslaReservedeFauneduDjaPotentieletmenacesYaoundeacuteCameroun
Muchaal P K amp Ngandjui G (1999) Impact of village hunt‐ing on wildlife populations in the western Dja ReserveCameroon Conservation Biology 13(2) 385ndash396 httpsdoiorg101046j1523‐17391999013002385x
NaranjoEJampBodmerRE (2007) Sourcendashsink systemsandconser‐vationofhuntedungulatesintheLacandonForestMexico Biological Conservation 138(3ndash4) 412ndash420 httpsdoiorg101016jbiocon 200705010
NielsenMR(2006)ImportancecauseandeffectofbushmeathuntingintheUdzungwaMountainsTanzania ImplicationsforcommunitybasedwildlifemanagementBiological Conservation128(4)509ndash516httpsdoiorg101016jbiocon200510017
OBrienTGKinnairdMFampWibisonoHT (2003)Crouching ti‐gers hiddenprey Sumatran tiger andprey populations in a tropi‐calforestlandscapeAnimal Conservation6(2)131ndash139httpsdoiorg101017S1367943003003172
OksanenJ(2015)VegananintroductiontoordinationVol8(p19)Retrieved from httpscranr‐projectorgwebpackagesveganvi‐gnettesintroveganpdf
PeresCAampPalaciosE(2007)Basin‐wideeffectsofgameharvestonvertebrate populationdensities inAmazonian forests Implicationsfor animal‐mediated seed dispersal Biotropica 39(3) 304ndash315httpsdoiorg101111j1744‐7429200700272x
PotapovPVTurubanovaSAHansenMCAduseiBBroichMAltstattAhellipJusticeCO(2012)QuantifyingforestcoverlossinDemocraticRepublicoftheCongo2000ndash2010withLandsatETM+data Remote Sensing of Environment 122 106ndash116 httpsdoiorg101016jrse201108027
PoulsenJRKoernerSEMooreSMedjibeVPBlakeSClarkC JhellipRosinC (2017) Poaching empties criticalCentralAfricanwilderness of forest elephants Current Biology 27(4) 134ndashR135httpsdoiorg101016jcub201701023
PurvisAGittlemanJlCowlishawGampMaceGM(2000)PredictingextinctionriskindecliningspeciesProceedings of the Royal Society B Biological Sciences267(1456) 1947ndash1952 httpsdoiorg101098rspb20001234
RayJ(1997)ComparativeecologyoftwoAfricanforestmongoosesHerpestesnasoandAtilaxpaludinosusAfrican Journal of Ecology35(3)237ndash253httpsdoiorg101111j1365‐20281997086‐ 89086x
Redford K H (1992) The empty forest BioScience 42(6) 412ndash422httpsdoiorg1023071311860
RepublicofCameroon(1994)Lawno9401du20janvier1994portantreacutegimedesforecirctsdelafauneetdelapecirccheRepublicofCameroon
RoveroFampMarshallAR(2009)CameratrappingphotographicrateasanindexofdensityinforestungulatesJournal of Applied Ecology46(5)1011ndash1017httpsdoiorg101111j1365‐2664200901705x
Royle J A amp Nichols J D (2003) Estimating abundance from re‐peated presence‐absence data or point counts Ecology 84(3)777ndash790 httpsdoiorg1018900012‐9658(2003)084[0777EAFRPA]20CO2
Seddon P J Griffiths C J Soorae P S ampArmstrongD P (2014)ReversingdefaunationRestoringspeciesinachangingworldScience345(6195)406ndash412httpsdoiorg101126science1251818
Silveira L Jacomo A T amp Diniz‐Filho J A F (2003) Camera trapline transect census and track surveys A comparative evaluationBiological Conservation 114(3) 351ndash355 httpsdoiorg101016S0006‐3207(03)00063‐6
Sonkeacute B (1998) Etudes floristiques et structurales des forecircts de laReacuteserve de Faune du Dja (Cameroun) Laboratoire de BotaniqueSysteacutematique et de Phytosociologie Universiteacute Libre de Bruxelles(ULB)
Srbek‐AraujoACampChiarelloAG(2005)Iscameratrappinganeffi‐cientmethodforsurveyingmammalsinNeotropicalforestsAcasestudyinsouth‐easternBrazilJournal of Tropical Ecology21(1)121ndash125httpsdoiorg101017S0266467404001956
Stiles D (2011) Elephant meat and ivory trade in Central AfricaPachyderm5026ndash36
TEAMNetwork(2008)Terrestrialvertebrateprotocol implementationmanualv30(p56)WashingtonDCTropicalEcologyAssessmentandMonitoringNetworkCenter forAppliedBiodiversity ScienceConservationInternational
Tobler M W Carrillo‐Percastegui S E Leite Pitman R MaresR amp Powell G (2008) An evaluation of camera traps for in‐ventorying large‐and medium‐sized terrestrial rainforestmammals Animal Conservation 11(3) 169ndash178 httpsdoiorg101111j1469‐1795200800169x
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
764emsp |emsp emspensp Bruce et al
TA B L E 1 emspMammalspeciespredictedtoberecordedintheNorthernandSouthern(management)sectorsofDjaFaunalReserveCameroon
Order Species IUCN Status HabitatNorthern sector RAI (LCLndashUCL)
Southern sector RAI (LCLndashUCL)
Afrosoricida Giantottershrew(Potamogale velox Du Chaillu1860)
LC Wetland Notdetected Notdetected
Carnivora Africangoldencat(Profelis aurataTemminck1827)a
VU Forest Notdetected 058(027ndash091)
Carnivora Leopard(Panthera pardusLinnaeus1758)a
NT Mixed Notdetected 083(032ndash145)
Carnivora Marshmongoose(Atilax paludinosusCuvier1829)a
LC Wetland 056(033ndash082)b 009(0ndash02)b
Carnivora Black‐leggedmongoose(Bdeogale nigripesPucheran1855)a
LC Forest 183(079ndash314) 371(263ndash484)
Carnivora Camerooncusimanse(Crossarchus platycephalusGoldman1984)a
LC Forest 183(124ndash247) 083(046ndash127)
Carnivora Long‐nosedmongoose(Herpestes nasodeWinton1901)a
LC Forest 102(053ndash160) 089(009ndash227)
Carnivora Africanpalmcivet(Nandinia binotataGray1830)a
LC Forest 113(071ndash16) 089(052ndash13)
Carnivora Servalinegenet(Genetta servalinaPucheran1855)a
LC Forest 325(239ndash416) 214(142ndash295)
Carnivora Large‐spottedgenet(Genetta maculata Gray1830)
LC Forest Notdetected Notdetected
Carnivora CentralAfricanoyan(Poiana richardsoniiThomson1842)c
LC Forest Notdetected 003(003ndash009)
Cetartiodactyla Batesspygmyantelope(Neotragus batesideWinton1903)a
LC Forest 04(011ndash078) 036(015ndash059)
Cetartiodactyla Forestbuffalo(Syncerus cafferSparrmansubspnanus1779)a
EN Forest 008(0ndash024) 006(0ndash019)
Cetartiodactyla Petersduiker(Cephalophus callipygusPeters1876)a
LC Forest 141(838ndash2071)b 7146 (4963ndash9641)b
Cetartiodactyla Bayduiker(Cephalophus dorsalisGray1846)a
LC Forest 668(44ndash935) 834(492ndash1228)
Cetartiodactyla White‐belliedduiker(Cephalophus leucogastersubsp leucogasterGray1873)
LC Forest Notdetected 395(214ndash611)
Cetartiodactyla Black‐frontedduiker(Cephalophus nigrifronsGray1871)a
LC Forest 086(003ndash246) 05(006ndash114)
Cetartiodactyla Yellow‐backedduiker(Cephalophus silvicultorAfzelius1815)a
LC Forest 37(225ndash554) 555(354ndash794)
Cetartiodactyla Blueduiker(Philantomba monticolaThunberg1789)a
LC Forest 6164(4602ndash788) 4298(315ndash5561)
Cetartiodactyla Bongo(Tragelaphus eurycerusOgilbyi1837)a
NT Forest 005(0ndash014) 006(0ndash015)
Cetartiodactyla Sitatunga(Tragelaphus spekiiSpeke1863)a
LC Wetland 024(005ndash048) 009(0ndash024)
Cetartiodactyla Redriverhog(Potamochoerus porcusLinnaeus1758)a
LC Woodland 161(102ndash228)b 7(336ndash1304)b
Cetartiodactyla Giantforesthog(Hylochoerus mein-ertzhageniThomas1904)
LC Forest Notdetected Notdetected
Cetartiodactyla Waterchevrotain(Hyemoschus aquaticusOgilby1841)a
LC Forest 03(0ndash075)b 46(192ndash799)b
(Continues)
emspensp emsp | emsp765Bruce et al
35emsp|emspCarnivore
ThecarnivorecommunitydifferedinRAIandstructurebetweenthetwosectorsFelidswerenotdetectedatallintheNorthernSectorbutboth leopard (Panthera pardusLinneaus1758)andgoldencat(Profelis aurata Temminck1827)werepresentintheSouthernSector
(Table1)AmongtheHerpestidaeblack‐leggedmongoose(Bdeogale nigripes Pucheran1855) showeda significantlyhigheroccupancy(p =gt001)intheSouthernSectorbuttrappingrateslackedsignifi‐cantdifference (RAI=371 [LCL=263UCL=484])comparedtothe Northern Sector (RAI=183 [LCL=079 UCL=314])Marshmongoose(Atilax paludinosusCuvier1829)hadsignificantlyhigher
Order Species IUCN Status HabitatNorthern sector RAI (LCLndashUCL)
Southern sector RAI (LCLndashUCL)
Hyracoidea Westerntreehyrax(Dendrohyrax dorsalis Fraser1855)
LC Forest Notdetected Detected
Pholidota White‐belliedpangolin(Phataginus tricuspisRafinesque1821)a
VU Forest 062(029ndash1) 08(044ndash121)
Pholidota Giantpangolin(Smutsia giganteaIlliger1815)a
VU Forest 027(008ndash052) 068(038ndash101)
Primates Agilemangabey(Cercocebus agilisMilne‐Edwards1886)a
LC Forest 035(013ndash059) 448(265ndash682)
Primates Moustachedguenon(Cercopithecus cephusLinnaeus1758)c
LC Forest Detected Notdetected
Primates Greaterspot‐nosedguenon(Cercopithecus nictitansLinnaeus1766)c
LC Forest Detected Detected
Primates Blackcolobus(Colobus satanasWaterhouse1838)c
VU Forest Notdetected Detected
Primates Galagospc ‐ Detected Notdetected
Primates Mandrill(Mandrillus sphinxLinnaeus1758)a
VU Forest 005(0ndash013) 006(0ndash019)
Primates Westernlowlandgorilla(Gorilla gorillaSavagesubspgorilla1847)a
CR Forest 016(003ndash031) 044(02ndash073)
Primates Centralchimpanzee(Pan troglodytesBlumenbachsubsptroglodytes1799)a
EN Forest 161(077ndash29)b 457(314ndash617)b
Proboscidea Forestelephant(Loxodonta cyclotisMatschie1900)a
VU Mixed 086(046ndash135) 19(086ndash329)
Rodentia Africanbrush‐tailedporcupine(Atherurus africanusGray1842)a
LC Forest 1753(1142ndash2446) 762(464ndash1145)
Rodentia Eminspouchedrat(Cricetomys eminiWroughton1910)a
LC Forest 32(2358ndash4141)b 756(341ndash1465)b
Rodentia Greatercanerat(Thryonomys swinderi-anus Temminck1827)
LC Wetland Notdetected Notdetected
Rodentia LadyBurtonsropesquirrel(Funisciurus isabellaGray1862)c
LC Forest Detected Detected
Rodentia Fire‐footedropesquirrel(Funisciurus pyrropusCuvier1833)c
LC Forest Detected Detected
Rodentia Africangiantsquirrel(Protoxerus stangeriWaterhouse1842)c
LC Forest Detected Detected
Tubulidentata Aardvark(Orycteropus aferPallas1766)a LC Mixed Notdetected 009(005ndash019)
NotesForeachsectorandspeciesthatwasdetectedwepresentthemeanand95confidencelimits(inbrackets)ofthenumberofindependentphotographiceventspertrapdaytimes100Trappingrateswereonlycalculatedformedium‐to‐largeterrestrialmammalsduetoinconsistentdetectionprobabilitieswithotherspeciesIUCNstatuscriticallyendangered(CR)endangered(EN)vulnerable(VU)nearthreatened(NT)leastconcern(LC)aIndicatesaspeciesthatwasincludedintherarefactionanalysisaccordingtothedefinitiongiveinthedataanalysissectionofthemethodsbIndicatesthattheRAIconfidenceintervalsdonotoverlapandcanbeconsideredsignificantlydifferentcSignifiesanarborealspecies
TA B L E 1 emsp (Continued)
766emsp |emsp emspensp Bruce et al
F I G U R E 2 emspRarefiedspeciesaccumulationcurvesformedium‐to‐largeterrestrialmammalsintheNorthernandSouthernsectorsofDjaFaunalReserveCameroon
F I G U R E 3 emspDistributionofmedium‐to‐largeterrestrialmammalspeciesintheNorthernSectoroftheDjaFaunalReserveCameroononthebasisofbodysizeandtrophiccategoryEachcirclerepresentsaspeciesinfunctionalspaceSizeofthecircleproportionaltothetrappingrateforthatspecies
emspensp emsp | emsp767Bruce et al
trappingrateintheNorthernSector(Table1)butlackedsufficientdetectionstoreliablycalculateoccupancyAbundanceofCamerooncusimanse(Crossarchus platycephalusGoldman1984)didnotdiffersignificantlybetweenthetwosectors(NorthernSectorRAI=183[LCL=124 UCL=247 ψ=075] Southern Sector RAI=083[LCL=046UCL=127]ψ=056p=028)
36emsp|emspElephants great apes and giant pangolin (illegal wildlife trade targets)
Amongtheterrestrialmammalstargetedbytheillegalwildlifetradespecifically central chimpanzee (Pan troglodytes Blumenbachsubsp troglodytes 1799) western lowland gorilla (Gorilla gorillaSavagesubsp gorilla1847)forestelephantgiantpangolin(Smutsia gigantea Illiger 1815) and white‐bellied pangolin (Phataginus tri-cuspis Rafinesque 1821) only central chimpanzee displayed asignificant difference in RAI between the management sectors(Northern Sector RAI=161 [LCL=077 UCL=29] SouthernSector RAI=457 [LCL=314 UCL=617]) However there wasnosignificantdifferenceinmeanoccupancybetweenthetwosec‐tors (p=074) Giant pangolin displayed the greatest differencewithathreefoldincreaseinRAIfrom027[LCL=008UCL=052]in the Northern Sector to 068 [LCL=038 UCL=101] in theSouthernSectorbutthiswasnotsignificantduetotheoverlapping
confidencelimitsTheRAIsandwhereappropriateoccupancyofforestelephantwesternlowlandgorillaandwhite‐belliedpangolinwerenotsignificantlyhigher intheSouthernSectorcomparedtotheNorthernSector(Tables12and12)
37emsp|emspOther bushmeat‐targeted species
Eminrsquospouchedrat(Cricetomys eminiWroughton1910)wasmoreabundantasmeasuredbybothoccupancy(pge001)andtrapratesintheNorthernSectorcomparedtotheSouthernSector(Table1)Africanbrush‐tailedporcupine(Atherurus africanusGray1842)didnothavesignificantdifferencesinRAIbetweenthemanagementsectors but occupancywas significantly higher in theNorthernSector (pge004) In comparison the larger‐bodied red river hog(Potamochoerus porcus Linneaus1758)wasmore frequentlyen‐countered as measured by both species abundance metrics intheSouthernSector(RAI=7[LCL=336UCL=1304]ψ=091)compared to the Northern Sector (RAI=161 [LCL=102UCL=228]ψ=065(p=004)
38emsp|emspSpecies occupancy with covariates
Therewasatotalof15speciesthathadsufficientdetectionstomodeloccupancywithinteractingsitecovariates(distancetoparkboundary
F I G U R E 4 emspDistributionofmedium‐to‐largeterrestrialmammalspeciesintheSouthernSectoroftheDjaFaunalReserveCameroononthebasisofbodysizeandtrophiccategoryEachcirclerepresentsaspeciesinfunctionalspaceSizeofthecircleproportionaltothetrappingrateforthatspecies
768emsp |emsp emspensp Bruce et al
TAB
LE 2
emspNullmeanoccupancy(ψ)anddetection(p)probabilitieswithstandarderrorpresentedinbracketsfortheNorthernSectorandSouthernSector
Spec
ies
Nor
ther
n se
ctor
(ψ)
Nor
ther
n se
ctor
(p)
Sout
hern
sec
tor
(ψ)
Sout
hern
sec
tor
(p)
Mod
elBe
tamdash
Para
met
er
chos
enLo
wer
95
be
taU
pper
95
be
taC‐
hat v
alue
Chi‐s
quar
ep
valu
e
Certiodactyla
Batesrsquospygmy
antelope
022(01)
015(006)
[026]
ndashNull
ndashndash
ndashndash
ndash
Bayduiker
091(006)
04(003)
087(006)
04(003)
DRN
lam(DistanceSTD)
000
6356
808
043
3356
50
930
25
Black‐fronted
duiker
01(006)
036(01)
015(006)
025(008)
Null
ndashndash
ndashndash
ndash
Blueduiker
097(003)
082(002)
1(0)
1(0)
DRN
lam(DistanceSTD)
002
0135
490
3637
492
021
024
Petersrsquoduiker
083(007)
a056(003)
1(0)a
1(0)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus07435528
003
6592
430
004
03
Waterchevrotain
[007]
ndash04(008)
045(005)
ndashndash
ndashndash
ndashndash
White‐bellied
duiker
ndashndash
072(008)
031(003)
Null
ndashndash
ndashndash
ndash
Yellow‐backed
duiker
084(008)
027(003)
086(007)
039(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
010
8837
21
0251
104
069
021
Redriverhog
065(011)
a021(003)
091(006)
a033(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus12560347
minus01352547
027
044
Proboscidae
Forestelephant
067(015)
014(004)
063(013)
014(004)
Null
ndashndash
ndashndash
ndash
Primates
Central
chimpanzee
077(014)
015(004)
082(007)
035(003)
SRN
lam(sectorSouthern)
037
3686
91
4429
314
03
039
Westernlowland
goril
la[007]
ndash045(017)
01(004)
Null
ndashndash
ndashndash
ndash
Philodota
Giantpangolin
[02]
ndash061(016)
011(004)
Null
ndashndash
ndashndash
ndash
White‐bellied
pangolin
045(016)
012(005)
063(017)
011(003)
DSoccu
psi(DistanceSTDsec
torSouthern)
minus48425115
minus1910401
022
06
Rodentia
African
brush‐tailed
porcupine
098(003)
a057(003)
084(006)
a042(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus10008123
minus01586108
042
071
Eminrsquospouched
rat
1(0)a
1(0)
079(007)
a038(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus095574568
minus01390762
021
075
Carnivora
(Con
tinue
s)
emspensp emsp | emsp769Bruce et al
and management sector Table 2) Forest elephant black‐frontedduikerand long‐nosedmongoose (Herpestes nasodeWinton1901)lackedamodel thathadanAICdifferenceofgt2 therefore theco‐variatemodelswerenotsignificantlydifferent to thenullmodel forthese species Elevenof 15 species had aRoylendashNicholsmodel se‐lectedasthelowestAICvaluesuggestingadifferenceinthenumberofindividualswassignificantlyinfluencingdetectionprobabilitiesandthereforeoccupancy
RoylendashNichols models accounted for occupancy being signifi‐cantlyhigherindifferingmanagementsectorswithnointeractionofdistancetotheprotectedareaboundaryforthreespeciesCamerooncusimanse had higher occupancy in the Northern Sector In con‐trast central chimpanzee and black‐legged mongoose had signifi‐cantlyloweroccupancywithintheNorthernSectorcomparedtotheSouthernSector(Figure5)
African brush‐tailed porcupine Eminrsquos pouched rat and servalinegenet(Genetta servalinaPucheran1855)hadasynergisticRoylendashNicholsmodelselectedasthemostsupportedTheprobabilityofsiteoccupancyslightlyincreasedwithdistancetotheboundaryandwasoverallhigherin theNorthernSector butdeclinedwithdistance to theboundary intheSouthernSector(Figure6)BothPetersrsquoduikerandredriverhogalsodisplayedthispatternofoccupancybuthadamuchgreaterincreaseinoccupancyintheNorthernSectorandhadhigheroccupancyoverallintheSouthernSector(Figure6)Incontrastyellow‐backedduiker(Cephalophus silvicultorAfezilus1815)wastheonlyspeciestodemonstrateanincreaseinoccupancywithdistancetotheboundaryintheSouthernSectorwhiledecliningintheNorthernSectorHoweversimilartootherlargerspeciesoccupancywashigherintheSouthernSector(Figure6)
With regard to the remainingduiker speciesmodelled aRoylendashNicholsmodelwithdistancetotheprotectedareaboundarywasiden‐tifiedasthemostappropriateTheprobabilityofasitebeingoccupiedbyblueduikerandbayduikerincreasedwithdistancetotheboundarywith no discernible difference betweenmanagement sectors in themodel(Figure7)
White‐belliedpangolinhadasingle‐seasonoccupancymodelse‐lectedsuggestingdifferences inabundancebetweenthemanage‐mentsectorsdidnotaffectdetectionprobabilitiesTheprobabilityofasitebeingoccupiedbywhite‐belliedpangolin increasedintheNorthernSectoranddeclinedintheSouthernSectorwithincreasingdistancetotheboundary(Figure8)
Seven speciesweredetectedonly inone sectoror lacked suffi‐cientdetectionsinonesectortoreliablymodeloccupancyacrossbothmanagement sectors Therefore only the effect of distance to theboundarycouldbemodelledThesewereAfricangoldencatwesternlowlandgorillawhite‐belliedduikergiantpangolinAfricanpalmcivet(Nandinia binotata Gray 1830) Batesrsquos pygmy antelope and waterchevrotain (Hymeoschus aquaticusOgilby 1841)African palm civetwastheonlyspeciestohavedistancetotheboundaryselectedastheoptimummodel to explain occupancy as occupancy increasedwithdistance from the boundary of the protected area (Table 2)All theremainingspecieshadthenullmodelselectedastheoptimummodelaccordingtoAICcriteria (Table2)Howeverdistancetothebound‐arywaswithinlt2AICforthesespeciessuggestingthatasignificantSp
ecie
sN
orth
ern
sect
or (ψ
)N
orth
ern
sect
or (p
)So
uthe
rn s
ecto
r (ψ
)So
uthe
rn s
ecto
r (p
)M
odel
Beta
mdashPa
ram
eter
ch
osen
Low
er 9
5
beta
Upp
er 9
5
beta
C‐ha
t val
ueCh
i‐squ
arep
va
lue
Africangolden
cat
ndashndash
041(013)
013(004)
Null
ndashndash
ndashndash
ndash
Africanpalm
civet
[047]
ndash073(017)
012(003)
DOccu
psi(DistanceSTD)
minus8177158
Inf
197
008
Black‐legged
mongoose
047(01)a
025(004)
082(008)
a031(003)
SRN
lam(sectorSouthern)
028
0266
31
4627
420
011
058
Cameroon
cusimanse
075(009)
027(004)
056(015)
012(004)
SRN
lam(sectorSouthern)
minus1808131
minus05098939
005
073
Long‐nosed
mongoose
055(012)
a02(004)
015(006)
a027(007)
Null
ndashndash
ndashndash
ndash
Servalinegenet
092(006)
035(003)
08(009)
02(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus09202819
003
5821
570
50
26
Not
esNaiumlveoccupancyvaluesarepresentedinsquarebracketsforspecieswithadetectionprobabilitylt01TheoptimummodelchosenbyAkaikersquosinformationcriteriaforeachspeciesgeneratingsuf‐
ficientoccupancyvaluesinbothsectorswiththeBetaparameteranditisrespectivelowerandupper95confidencelimitsisshownandtheassociatedc‐hatandchi‐squaredp
val
ue
DdistancetoboundarySmanagementsectorRNRoylendashNicholsmodelOccuMckenziesingle‐seasonoccupancymodesynergisticinteraction
a IndicatesasignificantdifferenceinoccupancybetweensectorsasmeasuredbytheWaldteststatistic
TAB
LE 2
emsp(Continued)
770emsp |emsp emspensp Bruce et al
relationshipwithdistancetotheboundarycouldbeinfluencingoccu‐pancyIntheSouthernSectortheoccupancyincreasedwithdistanceto theboundary forwestern lowlandgorillaandgiantpangolinbutdecreasedforAfricangoldencatwhite‐belliedduikerandwaterchev‐rotainIntheNorthernSectoroccupancyincreasedwithdistancetotheboundaryforBatesrsquospygmyantelope
4emsp |emspDISCUSSION
Thecomparisonofthetwosurveysconfirmsthatstandardcameratrap surveys and derived metrics of presenceabsence trappingrates andoccupancy candiscern confidentdifferences in ground‐dwellingmammalcommunitiesinCentralAfricanforests
41emsp|emspCamera trap surveys for documenting species
Thecomparativeefficacyofcamera traps for surveyingmediumto large ground‐dwelling mammals in the DFR is indicated byobservationratesandverifiabilityofrecordsespeciallyofelusivesmallerandnocturnalspeciesForexamplethedirectencounterraterecordedbyrangersonpatrolthroughouttheentirereserveover a nine‐month period is much lower than the combinednumberofindependentphotographiceventsinbothmanagementsectors (ZSL amp MINFOF 2017b) even for relatively largeconspicuous species such as forest elephant (96 photographiceventscomparedto29directencounters)andcentralchimpanzee(204 independent photographic events compared to 23 directencounters)Methodologiessuchascameratrapping therefore
provideimportantbaselinedatathatwhenrepeatedthroughtimeusingastandardisedprotocolcanallowatleasttrendsinrelativeabundanceindicestobemonitored
42emsp|emspCamera trap surveys for comparing assemblages among sites
Despitebeingseparatedbyonlyc32kmthemammalcommunitiesbetween the twocamera trapgridsdisplayedmarkeddifferencesThiswasthecaseeventhoughbothgridshadlowShannonndashWeinerandSimpsonsdiversityindicesduetothedominanceofthreeorfourspeciesineachcameratrapgridSignificantdifferencesamongthesiteswere observed for the trapping rates of species of differentsizesbetweensectorsSmaller‐bodiedspecieswithintheherbivoreand omnivore guilds were more prevalent within the NorthernSector (Figure 2) Trapping rates and occupancy values for smallcarnivoresarealsolowerintheSouthernSectorThiscouldbeduetothedifficultyofidentifyingmorphologicallysimilarspeciessuchasmarshmongooseandlong‐nosedmongoose(Bahaa‐el‐dinetal2013 Ray 1997) in infrared imagery with single cameras Thereweremoreunidentifiablemongooseeventsthatwereclassifiedtoafamilylevel―66224intheSouthernSectorcomparedto29156intheNorthernSectorofallcombinedmongooseevents
43emsp|emspThe potential impact of seasonality on estimates derived from camera traps
Due to logistical and financial constraints the surveys could notberuninthesameseasonThishasthepotentialtoaffecttrapping
F I G U R E 5 emspChangeintheprobabilityofoccupancyforblack‐leggedmongoosecentralchimpanzeeandCamerooncusimansewithmanagementsectoraccordingtoaRoylendashNicholsmodel
emspensp emsp | emsp771Bruce et al
rates and occupancy for specieswith larger home ranges becausewhenspeciesarewide‐rangingoccupancycanproveineffectiveformeasuring relative abundance Forest elephants (Blake 2002) andgreatapesareknowntodisplayseasonalshiftsintheirhabitatusageover great distances in response to increased fruit availability andprecipitation(HeadRobbinsMundryMakagaampBoesch2012)Thiscouldalsoinfluenceothergregariousspeciessuchasredriverhogthatarealsothoughttooccasionallydisplaysimilaraggregationsandmovementsinresponsetomastingevents(LeslieampHuffman2015)However as both red river hog and chimpanzee had significantlyhigherRAIandhigheroccupancywithvariabledetectionprobabilityaccording to the number of individuals incorporated this supports
thepossibilitythatthesespeciesarefavouringtheSouthernSectorIfmanagersareable toestablishwhetherwide‐rangingspeciesarepredictably moving to known areas within the reserve they canrespondinamannerthatprovidesenhancedprotectiontovulnerablewildlifepopulations in concentration areasAsmost species in thissurveylikelyhaveasmallerhomerangethantheinter‐trapdistanceand display fixed territories it can be regarded as appropriate tocompare occupancy values as the extent of overlap of territorieswithin the two surveys are unlikely to change in such away as toaffecttheresultsFuturestudieswouldbenefitfromtryingtomatchcameratrapsurveysseasonallytotryandclarifytheissueofseasonalshiftsinhabitatusagewithintheDFR
F I G U R E 6 emspChangeintheprobabilityofoccupancyforAfricanbrush‐tailedporcupineEminspouchedratredriverhogservalinegenetPetersrsquoduikerandyellow‐backedduikerwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
772emsp |emsp emspensp Bruce et al
F I G U R E 7 emspChangeintheprobabilityofoccupancyforblueduikerandbayduikerwithdistancetotheboundaryinkilometresacrossbothmanagementsectorsaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
F I G U R E 8 emspChangeintheprobabilityofoccupancyforwhite‐belliedpangolinwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaMackenzieoccupancymodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
emspensp emsp | emsp773Bruce et al
44emsp|emspCamera trap surveys for measuring the impacts of hunting on mammal communities
The spatial scale at which mammal communities are affected byandhowpopulationsrespondtoanthropogenicpressuressuchasbushmeat hunting is difficult to empiricallymeasure (Laurance etal2006)Thisisespeciallytrueformammalsresidingwithintropi‐cal forestswheregatheringconsistentandmeaningfulpopulation‐andcommunity‐levelmetrics ischallenging(Ahumadaetal2013)Population density of tropical mammals can vary greatly due toheterogeneity present within the environment For example for‐est elephants havedifferent distributions and aggregations inwetanddryseasonsinNouabaleacute‐Ndoki NationalParkwhichispartiallydependentonspatio‐temporalpatternsoffruitingtreesacrossthelandscape(Blake2002)
Whether the differences observed among the two sites sur‐veyedhereareattributabletodifferent levelsofhuntingpressureremains to be confirmed There are however indications thathuntingpressureanditsimpactsonmammalfaunasaregreaterintheNorthern Sector than in the Southern Sector The effects ofhuntingpressureonmammaliandeclinesinCentralAfricanforestsarewell documented The pattern in general is the largest‐bod‐ied species frugivores and thosewith high hunter or blackmar‐ketvalue(Abernethyetal2013Cardilloetal2005FaOliveroFarfaacutenMaacuterquezDuarteetal2014aFaOliveroFarfaacutenMaacuterquezVargasetal2014bPeresampPalacios2007)arethefirstspeciestoshownoticeabledeclineInthisstudythesignificantdeclineintherelativeabundance for frugivores suchasPetersʼduikerandspe‐cieswithhighhuntervalueliketheredriverhogunderincreasedhuntingpressure in theNorthernSector is reported inother sur‐veys(Abernethyetal2013)Thisisalsoreflectedinthedifferencesobserved in this study in biomass in the different guilds of eachmammalcommunityThemammalcommunitywithintheNorthernSector shows indications of a community that is disturbed and isexperiencingelevatedhuntingpressureThesearehigher(camera)trapping rates for smaller‐bodiedspecies suchasEminrsquospouchedrat and significantly fewer encounters of larger‐bodiedmammalsthataretargetsofthebushmeattradesuchasPetersʼduikerandredriverhog(FaRyanampBell2005JerozolimskiampPeres2003)Additionalindicatorsaretheabsenceinthesurveysoflargercarni‐voresintheNorthernSectorsuchasgoldencatandleopardwhicharesensitivetosnaring(Bahaa‐el‐dinetal2015)andsignificantlyreducedabundancemetricsfordisturbance‐sensitivespeciessuchasblack‐leggedmongooseandwaterchevrotain(Hart2013a)Theabsence of white‐bellied duiker in the Northern Sector also sug‐gestselevatedhumandisturbanceasthisspecieshasbeenreportedasverysensitivetoevenminorperturbationwithintheenvironment(Hart2013b)IncomparisontheSouthernSectorcontainedindica‐torfaunasuchasthewhite‐belliedduikerandhadhighertrappingratesforlarger‐bodiedspecies
WesuspectthedifferencesobservedaremostlikelyduetolowerhumandisturbanceintheSouthernSectorTheteamsdeployingand
recoveringthecamerasintheSouthernSectorcovered238kmandencountered few signs of humanperturbation (T Brucepers obs)whereashumansignwascommonlyencounteredbytheteamsintheNorthernSectorThisperceiveddifference is reflected in the2017and 2018 density of hunting signwithin each camera trap grid asdetected throughMINFOF ranger patrols (ZSL ampMINFOF 2017a2017b) and through the2018DistanceSampling inventory for theDFR (Bruce et al 2018) Higher numbers of hunting sign in theNorthernSectorwouldbeconsistentwithanelevatedhuntingpres‐sureinthatarea
45emsp|emspProtection of refugia from hunting
Though inferences made for wide‐ranging species such as forestelephantsandgreatapesusingcameratrapsaredifficultthefactthattrappingrateswerehigherinmorechallengingterrainwithassumedlower hunting pressure could be indicative of complex habitatprovidingsomelevelofprotectionfromhuntingElephantisknownto retreatwhen they aredisturbed to terrain that ismoredifficulttoaccessbyhumans (Hedges2012)Thuswithin largerprotectedareas certain zones may act as refugia for wildlife populations(Campbelletal2011)Thiscanbeduetoarangeof factorssuchas remoteanddifficult terrain forpoachers (Attum2007Hedges2012) or the regular presence of field researchers and rangers(Campbell et al 2011) The significanceof these refugia for largerprotected areas is that the populations of wildlife residing withinthem if adequately protected may provide source populations toallowrecolonisationofotherareasofthereserve(NaranjoampBodmer2007)Thereforeifadequateprotectioncanbeprovidedtorelativelysmallbutimportantareasoflargereservesthismayprovidetropicalforestswithabetterchanceofbeingecologicallyresilienttoongoingand increasing human perturbation Well‐designed camera trapsurveys may provide data on the status of wildlife populations atrelativelyfinespatialresolutionssoastoidentifyfunctionalrefugiawithgreaterconfidence
ACKNOWLEDG EMENTS
WeappreciatetheongoingsupportofCameroonrsquosMinistryofForestsandWildlife(MINFOF)andtheopportunitytocontributetobiodiver‐sityconservationthroughoutthecountryInparticularwewouldliketothanktheChefdrsquoAntenneSergeJacobMeyeforhisongoingsup‐portofconservationresearchwithintheprotectedareaWeappreci‐atethestalwarteffortsofMINFOFecoguardsandlocalporterswhoaccompaniedthesurveyteamsinthefieldWewouldalsoliketothanktheUnitedStatesFishandWildlifeService(USFWS)mdashAfricanElephantConservationandIUCNSOSmdashFondationSegreacutePangolinConservationInitiativeforsupportingthiswork
ORCID
Tom Bruce httporcidorg0000‐0001‐6958‐1657
774emsp |emsp emspensp Bruce et al
R E FE R E N C E S
AbernethyKACoad L TaylorG LeeMEampMaisels F (2013)Extent and ecological consequences of hunting in Central Africanrainforests in thetwenty‐firstcenturyPhilosophical Transactions of the Royal Society of London Biological Sciences368(1625)20120303httpsdoiorg101098rstb20120303
AbrahamsM I Peres C A amp Costa H C (2017)Measuring localdepletion of terrestrial game vertebrates by central‐place hunt‐ers in rural Amazonia PLoS ONE 12(10) e0186653 httpsdoiorg101371journalpone0186653
AhumadaJAHurtadoJampLizcanoD(2013)MonitoringthestatusandtrendsoftropicalforestterrestrialvertebratecommunitiesfromcameratrapdataAtool forconservationPLoS ONE8(9)e73707httpsdoiorg101371journalpone0073707
Ahumada J A Silva C E Gajapersad K Hallam C Hurtado JMartin E hellip Sheil D (2011) Community structure and diver‐sity of tropical forest mammals Data from a global camera trapnetwork Philosophical Transactions of the Royal Society of London Biological Sciences366(1578)2703ndash2711httpsdoiorg101098rstb20110115
AminRAndanjeSAOgwonkaBAliAHBowkettAEOmarMampWacherT(2015)ThenortherncoastalforestsofKenyaarenationally and globally important for the conservation of AdersrsquoduikerCephalophusadersiandotherantelopespeciesBiodiversity and Conservation 24(3) 641ndash658 httpsdoiorg101007s10531‐014‐0842‐z
Attum O (2007) Can landscape use be among the factors that po‐tentiallymake some ungulates speciesmore difficult to conserveJournal of Arid Environments69(3)410ndash419
Bahaa‐el‐dinLHenschelPAbaaRAbernethyKBohmTBoutNhellipLeeM (2013)NotesonthedistributionandstatusofsmallcarnivoresinGabonSmall Carnivore Conservation4819ndash29
Bahaa‐el‐dinLHenschelPButynskiTMMacdonaldDWMillsDSlotowRampHunterL (2015)TheAfricangoldencatCaracalaurataAfricasleast‐knownfelidMammal Review45(1)63ndash77
Bennett E L Blencowe E Brandon K Brown D Burn R WCowlishaw G hellip Robinson J G (2007) Hunting for consensusReconcilingbushmeatharvestconservationanddevelopmentpol‐icyinWestandCentralAfricaConservation Biology21(3)884ndash887httpsdoiorg101111j1523‐1739200600595x
BlakeSDeemSLMossimboEMaiselsFampWalshP(2009)Forestelephants Tree planters of the CongoBiotropica41(4) 459ndash468httpsdoiorg101111j1744‐7429200900512x
Blake S (2002) The ecology of forest elephant distribution and itsimplications for conservation Doctoral dissertation University ofEdinburgh
BruceTNdjassiCFowlerANdimbeMFankemOTabueRhellipOlsonD(2018)Faunal inventory of the Dja Faunal Reserve Cameroon Yaoundeacute Cameroon Ministry of Forests and Wildlife (MINFOF)Zoological Society of London ndash Cameroon Country ProgrammeAfricanWildlifeFoundation
BruceTWacherTNdingaHBidjokaVMeyongFNgoBataMampOlsonD(2017)camera trap survey for larger terrestrial wildlife in the Dja Biosphere Reserve CameroonYaoundeacuteCameroonZoologicalSocietyofLondon(ZSL)ampCameroonMinistryofForestsandWildlife(MINFOF)
BurnhamKPampAndersonDR(2002)Model selection and multimodel inferenceNewYorkNYSpringer
Campbell G Kuehl H Diarrassouba A NGoran P K amp BoeschC (2011) Long‐term research sites as refugia for threatened andover‐harvested species Biology Letters 7(5) 723ndash726 httpsdoiorg101098rsbl20110155
CardilloMMaceGMJonesKEBielbyJBininda‐EmondsORSechrestWhellipPurvisA(2005)Multiplecausesofhighextinction
riskinlargemammalspeciesScience309(5738)1239ndash1241httpsdoiorg101126science1116030
Craigie IDBaillieJEBalmfordACarboneCCollenBGreenREampHuttonJM (2010)Largemammalpopulationdeclines inAfricarsquosprotectedareasBiological Conservation143(9)2221ndash2228httpsdoiorg101016jbiocon201006007
DaveyKWacherTampAminR(2017)Analysis tool for camera-trap sur-vey data [Computer software]ZoologicalSocietyofLondonRetrievedfromhttpswwwzslorgzsl‐camera‐trap‐data‐management‐ and‐analysis‐package
Djuikouo M N K Doucet J L Nguembou C K Lewis S L ampSonkeacute B (2010) Diversity and aboveground biomass in threetropical forest types in the Dja Biosphere Reserve Cameroon African Journal of Ecology 48(4) 1053ndash1063 httpsdoiorg101111j1365‐2028201001212x
DupainJBombomeKampVanElsackerL(2003)LeschimpanzeacutesetlesgorillesdelareacuteservedefauneduDjaCanopeacutee2414ndash15
EffordMGampDawsonDK(2012)OccupancyincontinuoushabitatEcosphere3(4)1ndash15httpsdoiorg101890ES11‐003081
Efron B amp Tibshirani R J (1994) An introduction to the bootstrap WashingtonDCCRCPress
FaJEOliveroJFarfaacutenMAacuteMaacuterquezALDuarteJNackoneyJhellipMacdonaldDW(2014a)CorrelatesofbushmeatinmarketsanddepletionofwildlifeConservation Biology29(3)805ndash815
Fa J EOlivero J FarfaacutenMAacuteMaacuterquezA LVargas JMRealRampNasiR(2014b)IntegratingsustainablehuntinginbiodiversityprotectioninCentralAfricaHotspotsweakspotsandstrongspotsPLoS ONE9(11)e112367
FaJERyanSFampBellDJ (2005)Huntingvulnerabilityecolog‐ical characteristics and harvest rates of bushmeat species in afro‐tropicalforestsBiological Conservation121(2)167ndash176httpsdoiorg101016jbiocon200404016
Fa J E Seymour S Dupain J E F Amin R Albrechtsen L ampMacdonaldD (2006) Getting to gripswith themagnitude of ex‐ploitationBushmeat in theCross‐SanagariversregionNigeria and Cameroon Biological Conservation 129(4) 497ndash510 httpsdoiorg101016jbiocon200511031
Farris Z J Boone H M Karpanty S Murphy A Ratelolahy FAndrianjakariveloVampKellyMJ(2015)FeralcatsandthefitoatyFirstpopulationassessmentoftheblackforestcatinMadagascarrsquosrainforestsJournal of Mammalogy97(2)518ndash525
Fiske IampChandlerR (2011)UnmarkedAnRpackageforfittinghi‐erarchicalmodelsofwildlifeoccurrenceandabundanceJournal of Statistical Software43(10)1ndash23
HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences107(19)8650ndash8655httpsdoiorg101073pnas0912668107
HartJ(2013a)WaterchevrotainHymemoschusaquaticusInJKingdonampMHoffmann (Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp88ndash92)LondonUKBloomsbury
Hart J (2013b) White‐bellied duiker Cephalophus leucogaster In JKingdonampMHoffmann(Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp255ndash258)LondonUKBloomsbury
HeadJSRobbinsMMMundryRMakagaLampBoeschC(2012)Remotevideo‐cameratrapsmeasurehabitatuseandcompetitiveex‐clusionamongsympatricchimpanzeegorillaandelephantinLoangoNational ParkGabon Journal of Tropical Ecology28(06) 571ndash583httpsdoiorg101017S0266467412000612
HedgesS(2012)Monitoring elephant populations and assessing threats HimayatnagarTelanganaUniversitiesPress
HedwigDKienastIBonnetMCurranBKCourageABoeschChellipKingT(2018)Acameratrapassessmentoftheforestmam‐mal community within the transitional savannah‐forest mosaic oftheBateacutekeacutePlateauNationalParkGabonAfrican Journal of Ecology56(4)777ndash790httpsdoiorg101111aje12497
emspensp emsp | emsp775Bruce et al
HijmansRJCameronSEParraJLJonesPGampJarvisA(2005)Very high resolution interpolated climate surfaces for global landareasInternational Journal of Climatology25(15)1965ndash1978httpsdoiorg101002joc1276
HuggelA(2012)Exiv2softwaretool[Computersoftware]Retrievedfromhttpswwwexiv2orgindexhtml
Jerozolimski A amp Peres C A (2003) Bringing home the biggestbacon A cross‐site analysis of the structure of hunter‐kill profilesin Neotropical forests Biological Conservation 111(3) 415ndash425httpsdoiorg101016S0006‐3207(02)00310‐5
KingdonJ (2015)The Kingdon field guide to African mammalsLondonUKBloomsburyPublishing
KuumlhlHFMaiselsMAncrenazampEAWilliamson(Eds)(2008)Best practice guidelines for surveys and monitoring of great ape populations GlandSwitzerlandIUCN
LauranceWFCroesBMTchignoumbaLLahmSAAlonsoALeeMEhellipOndzeanoC(2006)ImpactsofroadsandhuntingoncentralAfrican rainforestmammalsConservation Biology20(4)1251ndash1261httpsdoiorg101111j1523‐1739200600420x
LauranceWFUsecheDCRendeiroJKalkaMBradshawCJSloan S P hellip Arroyo‐Rodriguez V (2012) Averting biodiversitycollapse in tropical forestprotectedareasNature489(7415)290httpsdoiorg101038nature11318
LeslieDMampHuffmanBA(2015)Potamochoerus porcus(ArtiodactylaSuidae)Mammalian Species4715ndash31
MacKenzieD IampBailey L L (2004)Assessing the fit of site‐occu‐pancy models Journal of Agricultural Biological and Environmental Statistics9300ndash318httpsdoiorg101198108571104X3361
MacKenzieDINicholsJDRoyleJAPollockKHBaileyLLampHinesJE (2006)Occupancy estimation and modellingBurlingtonMAAcademicPress
Magurran A E (2005) Species abundance distributions Patternor process Functional Ecology 19(1) 177ndash181 httpsdoiorg101111j0269‐8463200500930x
MaiselsFStrindbergSBlakeSWittemyerGHartJWilliamsonEAhellipWarrenY (2013)DevastatingdeclineofforestelephantsinCentralAfricaPLoS ONE8(3)e59469httpsdoiorg101371journalpone0059469
MalhiYAdu‐BreduSAsareRA LewisS LampMayauxP (2013)AfricanrainforestsPastpresentandfuturePhilosophical Transactions of the Royal Society of London Biological Sciences 368(1625)20120312
MallonDPHoffmannMGraingerMJHibertFVanVlietNampMcGowanP JK (2015)An IUCNsituationanalysisof terrestrialandfreshwaterfaunainWestandCentralAfricaOccasionalpaperoftheIUCNspeciessurvivalcommission(54)
MambeyaMMBakerFMombouaBRKoumbaPamboAFHegaMOkouyiOkouyiVJhellipAbernethyK(2018)TheemergenceofacommercialtradeinpangolinsfromGabonAfrican Journal of Ecology56(3)601ndash609httpsdoiorg101111aje12507
MINFOFampIUCN(2015)CaracteacuterisationdelapopulationdegrandsetmoyensmammifegraveresdanslaReservedeFauneduDjaPotentieletmenacesYaoundeacuteCameroun
Muchaal P K amp Ngandjui G (1999) Impact of village hunt‐ing on wildlife populations in the western Dja ReserveCameroon Conservation Biology 13(2) 385ndash396 httpsdoiorg101046j1523‐17391999013002385x
NaranjoEJampBodmerRE (2007) Sourcendashsink systemsandconser‐vationofhuntedungulatesintheLacandonForestMexico Biological Conservation 138(3ndash4) 412ndash420 httpsdoiorg101016jbiocon 200705010
NielsenMR(2006)ImportancecauseandeffectofbushmeathuntingintheUdzungwaMountainsTanzania ImplicationsforcommunitybasedwildlifemanagementBiological Conservation128(4)509ndash516httpsdoiorg101016jbiocon200510017
OBrienTGKinnairdMFampWibisonoHT (2003)Crouching ti‐gers hiddenprey Sumatran tiger andprey populations in a tropi‐calforestlandscapeAnimal Conservation6(2)131ndash139httpsdoiorg101017S1367943003003172
OksanenJ(2015)VegananintroductiontoordinationVol8(p19)Retrieved from httpscranr‐projectorgwebpackagesveganvi‐gnettesintroveganpdf
PeresCAampPalaciosE(2007)Basin‐wideeffectsofgameharvestonvertebrate populationdensities inAmazonian forests Implicationsfor animal‐mediated seed dispersal Biotropica 39(3) 304ndash315httpsdoiorg101111j1744‐7429200700272x
PotapovPVTurubanovaSAHansenMCAduseiBBroichMAltstattAhellipJusticeCO(2012)QuantifyingforestcoverlossinDemocraticRepublicoftheCongo2000ndash2010withLandsatETM+data Remote Sensing of Environment 122 106ndash116 httpsdoiorg101016jrse201108027
PoulsenJRKoernerSEMooreSMedjibeVPBlakeSClarkC JhellipRosinC (2017) Poaching empties criticalCentralAfricanwilderness of forest elephants Current Biology 27(4) 134ndashR135httpsdoiorg101016jcub201701023
PurvisAGittlemanJlCowlishawGampMaceGM(2000)PredictingextinctionriskindecliningspeciesProceedings of the Royal Society B Biological Sciences267(1456) 1947ndash1952 httpsdoiorg101098rspb20001234
RayJ(1997)ComparativeecologyoftwoAfricanforestmongoosesHerpestesnasoandAtilaxpaludinosusAfrican Journal of Ecology35(3)237ndash253httpsdoiorg101111j1365‐20281997086‐ 89086x
Redford K H (1992) The empty forest BioScience 42(6) 412ndash422httpsdoiorg1023071311860
RepublicofCameroon(1994)Lawno9401du20janvier1994portantreacutegimedesforecirctsdelafauneetdelapecirccheRepublicofCameroon
RoveroFampMarshallAR(2009)CameratrappingphotographicrateasanindexofdensityinforestungulatesJournal of Applied Ecology46(5)1011ndash1017httpsdoiorg101111j1365‐2664200901705x
Royle J A amp Nichols J D (2003) Estimating abundance from re‐peated presence‐absence data or point counts Ecology 84(3)777ndash790 httpsdoiorg1018900012‐9658(2003)084[0777EAFRPA]20CO2
Seddon P J Griffiths C J Soorae P S ampArmstrongD P (2014)ReversingdefaunationRestoringspeciesinachangingworldScience345(6195)406ndash412httpsdoiorg101126science1251818
Silveira L Jacomo A T amp Diniz‐Filho J A F (2003) Camera trapline transect census and track surveys A comparative evaluationBiological Conservation 114(3) 351ndash355 httpsdoiorg101016S0006‐3207(03)00063‐6
Sonkeacute B (1998) Etudes floristiques et structurales des forecircts de laReacuteserve de Faune du Dja (Cameroun) Laboratoire de BotaniqueSysteacutematique et de Phytosociologie Universiteacute Libre de Bruxelles(ULB)
Srbek‐AraujoACampChiarelloAG(2005)Iscameratrappinganeffi‐cientmethodforsurveyingmammalsinNeotropicalforestsAcasestudyinsouth‐easternBrazilJournal of Tropical Ecology21(1)121ndash125httpsdoiorg101017S0266467404001956
Stiles D (2011) Elephant meat and ivory trade in Central AfricaPachyderm5026ndash36
TEAMNetwork(2008)Terrestrialvertebrateprotocol implementationmanualv30(p56)WashingtonDCTropicalEcologyAssessmentandMonitoringNetworkCenter forAppliedBiodiversity ScienceConservationInternational
Tobler M W Carrillo‐Percastegui S E Leite Pitman R MaresR amp Powell G (2008) An evaluation of camera traps for in‐ventorying large‐and medium‐sized terrestrial rainforestmammals Animal Conservation 11(3) 169ndash178 httpsdoiorg101111j1469‐1795200800169x
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
emspensp emsp | emsp765Bruce et al
35emsp|emspCarnivore
ThecarnivorecommunitydifferedinRAIandstructurebetweenthetwosectorsFelidswerenotdetectedatallintheNorthernSectorbutboth leopard (Panthera pardusLinneaus1758)andgoldencat(Profelis aurata Temminck1827)werepresentintheSouthernSector
(Table1)AmongtheHerpestidaeblack‐leggedmongoose(Bdeogale nigripes Pucheran1855) showeda significantlyhigheroccupancy(p =gt001)intheSouthernSectorbuttrappingrateslackedsignifi‐cantdifference (RAI=371 [LCL=263UCL=484])comparedtothe Northern Sector (RAI=183 [LCL=079 UCL=314])Marshmongoose(Atilax paludinosusCuvier1829)hadsignificantlyhigher
Order Species IUCN Status HabitatNorthern sector RAI (LCLndashUCL)
Southern sector RAI (LCLndashUCL)
Hyracoidea Westerntreehyrax(Dendrohyrax dorsalis Fraser1855)
LC Forest Notdetected Detected
Pholidota White‐belliedpangolin(Phataginus tricuspisRafinesque1821)a
VU Forest 062(029ndash1) 08(044ndash121)
Pholidota Giantpangolin(Smutsia giganteaIlliger1815)a
VU Forest 027(008ndash052) 068(038ndash101)
Primates Agilemangabey(Cercocebus agilisMilne‐Edwards1886)a
LC Forest 035(013ndash059) 448(265ndash682)
Primates Moustachedguenon(Cercopithecus cephusLinnaeus1758)c
LC Forest Detected Notdetected
Primates Greaterspot‐nosedguenon(Cercopithecus nictitansLinnaeus1766)c
LC Forest Detected Detected
Primates Blackcolobus(Colobus satanasWaterhouse1838)c
VU Forest Notdetected Detected
Primates Galagospc ‐ Detected Notdetected
Primates Mandrill(Mandrillus sphinxLinnaeus1758)a
VU Forest 005(0ndash013) 006(0ndash019)
Primates Westernlowlandgorilla(Gorilla gorillaSavagesubspgorilla1847)a
CR Forest 016(003ndash031) 044(02ndash073)
Primates Centralchimpanzee(Pan troglodytesBlumenbachsubsptroglodytes1799)a
EN Forest 161(077ndash29)b 457(314ndash617)b
Proboscidea Forestelephant(Loxodonta cyclotisMatschie1900)a
VU Mixed 086(046ndash135) 19(086ndash329)
Rodentia Africanbrush‐tailedporcupine(Atherurus africanusGray1842)a
LC Forest 1753(1142ndash2446) 762(464ndash1145)
Rodentia Eminspouchedrat(Cricetomys eminiWroughton1910)a
LC Forest 32(2358ndash4141)b 756(341ndash1465)b
Rodentia Greatercanerat(Thryonomys swinderi-anus Temminck1827)
LC Wetland Notdetected Notdetected
Rodentia LadyBurtonsropesquirrel(Funisciurus isabellaGray1862)c
LC Forest Detected Detected
Rodentia Fire‐footedropesquirrel(Funisciurus pyrropusCuvier1833)c
LC Forest Detected Detected
Rodentia Africangiantsquirrel(Protoxerus stangeriWaterhouse1842)c
LC Forest Detected Detected
Tubulidentata Aardvark(Orycteropus aferPallas1766)a LC Mixed Notdetected 009(005ndash019)
NotesForeachsectorandspeciesthatwasdetectedwepresentthemeanand95confidencelimits(inbrackets)ofthenumberofindependentphotographiceventspertrapdaytimes100Trappingrateswereonlycalculatedformedium‐to‐largeterrestrialmammalsduetoinconsistentdetectionprobabilitieswithotherspeciesIUCNstatuscriticallyendangered(CR)endangered(EN)vulnerable(VU)nearthreatened(NT)leastconcern(LC)aIndicatesaspeciesthatwasincludedintherarefactionanalysisaccordingtothedefinitiongiveinthedataanalysissectionofthemethodsbIndicatesthattheRAIconfidenceintervalsdonotoverlapandcanbeconsideredsignificantlydifferentcSignifiesanarborealspecies
TA B L E 1 emsp (Continued)
766emsp |emsp emspensp Bruce et al
F I G U R E 2 emspRarefiedspeciesaccumulationcurvesformedium‐to‐largeterrestrialmammalsintheNorthernandSouthernsectorsofDjaFaunalReserveCameroon
F I G U R E 3 emspDistributionofmedium‐to‐largeterrestrialmammalspeciesintheNorthernSectoroftheDjaFaunalReserveCameroononthebasisofbodysizeandtrophiccategoryEachcirclerepresentsaspeciesinfunctionalspaceSizeofthecircleproportionaltothetrappingrateforthatspecies
emspensp emsp | emsp767Bruce et al
trappingrateintheNorthernSector(Table1)butlackedsufficientdetectionstoreliablycalculateoccupancyAbundanceofCamerooncusimanse(Crossarchus platycephalusGoldman1984)didnotdiffersignificantlybetweenthetwosectors(NorthernSectorRAI=183[LCL=124 UCL=247 ψ=075] Southern Sector RAI=083[LCL=046UCL=127]ψ=056p=028)
36emsp|emspElephants great apes and giant pangolin (illegal wildlife trade targets)
Amongtheterrestrialmammalstargetedbytheillegalwildlifetradespecifically central chimpanzee (Pan troglodytes Blumenbachsubsp troglodytes 1799) western lowland gorilla (Gorilla gorillaSavagesubsp gorilla1847)forestelephantgiantpangolin(Smutsia gigantea Illiger 1815) and white‐bellied pangolin (Phataginus tri-cuspis Rafinesque 1821) only central chimpanzee displayed asignificant difference in RAI between the management sectors(Northern Sector RAI=161 [LCL=077 UCL=29] SouthernSector RAI=457 [LCL=314 UCL=617]) However there wasnosignificantdifferenceinmeanoccupancybetweenthetwosec‐tors (p=074) Giant pangolin displayed the greatest differencewithathreefoldincreaseinRAIfrom027[LCL=008UCL=052]in the Northern Sector to 068 [LCL=038 UCL=101] in theSouthernSectorbutthiswasnotsignificantduetotheoverlapping
confidencelimitsTheRAIsandwhereappropriateoccupancyofforestelephantwesternlowlandgorillaandwhite‐belliedpangolinwerenotsignificantlyhigher intheSouthernSectorcomparedtotheNorthernSector(Tables12and12)
37emsp|emspOther bushmeat‐targeted species
Eminrsquospouchedrat(Cricetomys eminiWroughton1910)wasmoreabundantasmeasuredbybothoccupancy(pge001)andtrapratesintheNorthernSectorcomparedtotheSouthernSector(Table1)Africanbrush‐tailedporcupine(Atherurus africanusGray1842)didnothavesignificantdifferencesinRAIbetweenthemanagementsectors but occupancywas significantly higher in theNorthernSector (pge004) In comparison the larger‐bodied red river hog(Potamochoerus porcus Linneaus1758)wasmore frequentlyen‐countered as measured by both species abundance metrics intheSouthernSector(RAI=7[LCL=336UCL=1304]ψ=091)compared to the Northern Sector (RAI=161 [LCL=102UCL=228]ψ=065(p=004)
38emsp|emspSpecies occupancy with covariates
Therewasatotalof15speciesthathadsufficientdetectionstomodeloccupancywithinteractingsitecovariates(distancetoparkboundary
F I G U R E 4 emspDistributionofmedium‐to‐largeterrestrialmammalspeciesintheSouthernSectoroftheDjaFaunalReserveCameroononthebasisofbodysizeandtrophiccategoryEachcirclerepresentsaspeciesinfunctionalspaceSizeofthecircleproportionaltothetrappingrateforthatspecies
768emsp |emsp emspensp Bruce et al
TAB
LE 2
emspNullmeanoccupancy(ψ)anddetection(p)probabilitieswithstandarderrorpresentedinbracketsfortheNorthernSectorandSouthernSector
Spec
ies
Nor
ther
n se
ctor
(ψ)
Nor
ther
n se
ctor
(p)
Sout
hern
sec
tor
(ψ)
Sout
hern
sec
tor
(p)
Mod
elBe
tamdash
Para
met
er
chos
enLo
wer
95
be
taU
pper
95
be
taC‐
hat v
alue
Chi‐s
quar
ep
valu
e
Certiodactyla
Batesrsquospygmy
antelope
022(01)
015(006)
[026]
ndashNull
ndashndash
ndashndash
ndash
Bayduiker
091(006)
04(003)
087(006)
04(003)
DRN
lam(DistanceSTD)
000
6356
808
043
3356
50
930
25
Black‐fronted
duiker
01(006)
036(01)
015(006)
025(008)
Null
ndashndash
ndashndash
ndash
Blueduiker
097(003)
082(002)
1(0)
1(0)
DRN
lam(DistanceSTD)
002
0135
490
3637
492
021
024
Petersrsquoduiker
083(007)
a056(003)
1(0)a
1(0)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus07435528
003
6592
430
004
03
Waterchevrotain
[007]
ndash04(008)
045(005)
ndashndash
ndashndash
ndashndash
White‐bellied
duiker
ndashndash
072(008)
031(003)
Null
ndashndash
ndashndash
ndash
Yellow‐backed
duiker
084(008)
027(003)
086(007)
039(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
010
8837
21
0251
104
069
021
Redriverhog
065(011)
a021(003)
091(006)
a033(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus12560347
minus01352547
027
044
Proboscidae
Forestelephant
067(015)
014(004)
063(013)
014(004)
Null
ndashndash
ndashndash
ndash
Primates
Central
chimpanzee
077(014)
015(004)
082(007)
035(003)
SRN
lam(sectorSouthern)
037
3686
91
4429
314
03
039
Westernlowland
goril
la[007]
ndash045(017)
01(004)
Null
ndashndash
ndashndash
ndash
Philodota
Giantpangolin
[02]
ndash061(016)
011(004)
Null
ndashndash
ndashndash
ndash
White‐bellied
pangolin
045(016)
012(005)
063(017)
011(003)
DSoccu
psi(DistanceSTDsec
torSouthern)
minus48425115
minus1910401
022
06
Rodentia
African
brush‐tailed
porcupine
098(003)
a057(003)
084(006)
a042(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus10008123
minus01586108
042
071
Eminrsquospouched
rat
1(0)a
1(0)
079(007)
a038(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus095574568
minus01390762
021
075
Carnivora
(Con
tinue
s)
emspensp emsp | emsp769Bruce et al
and management sector Table 2) Forest elephant black‐frontedduikerand long‐nosedmongoose (Herpestes nasodeWinton1901)lackedamodel thathadanAICdifferenceofgt2 therefore theco‐variatemodelswerenotsignificantlydifferent to thenullmodel forthese species Elevenof 15 species had aRoylendashNicholsmodel se‐lectedasthelowestAICvaluesuggestingadifferenceinthenumberofindividualswassignificantlyinfluencingdetectionprobabilitiesandthereforeoccupancy
RoylendashNichols models accounted for occupancy being signifi‐cantlyhigherindifferingmanagementsectorswithnointeractionofdistancetotheprotectedareaboundaryforthreespeciesCamerooncusimanse had higher occupancy in the Northern Sector In con‐trast central chimpanzee and black‐legged mongoose had signifi‐cantlyloweroccupancywithintheNorthernSectorcomparedtotheSouthernSector(Figure5)
African brush‐tailed porcupine Eminrsquos pouched rat and servalinegenet(Genetta servalinaPucheran1855)hadasynergisticRoylendashNicholsmodelselectedasthemostsupportedTheprobabilityofsiteoccupancyslightlyincreasedwithdistancetotheboundaryandwasoverallhigherin theNorthernSector butdeclinedwithdistance to theboundary intheSouthernSector(Figure6)BothPetersrsquoduikerandredriverhogalsodisplayedthispatternofoccupancybuthadamuchgreaterincreaseinoccupancyintheNorthernSectorandhadhigheroccupancyoverallintheSouthernSector(Figure6)Incontrastyellow‐backedduiker(Cephalophus silvicultorAfezilus1815)wastheonlyspeciestodemonstrateanincreaseinoccupancywithdistancetotheboundaryintheSouthernSectorwhiledecliningintheNorthernSectorHoweversimilartootherlargerspeciesoccupancywashigherintheSouthernSector(Figure6)
With regard to the remainingduiker speciesmodelled aRoylendashNicholsmodelwithdistancetotheprotectedareaboundarywasiden‐tifiedasthemostappropriateTheprobabilityofasitebeingoccupiedbyblueduikerandbayduikerincreasedwithdistancetotheboundarywith no discernible difference betweenmanagement sectors in themodel(Figure7)
White‐belliedpangolinhadasingle‐seasonoccupancymodelse‐lectedsuggestingdifferences inabundancebetweenthemanage‐mentsectorsdidnotaffectdetectionprobabilitiesTheprobabilityofasitebeingoccupiedbywhite‐belliedpangolin increasedintheNorthernSectoranddeclinedintheSouthernSectorwithincreasingdistancetotheboundary(Figure8)
Seven speciesweredetectedonly inone sectoror lacked suffi‐cientdetectionsinonesectortoreliablymodeloccupancyacrossbothmanagement sectors Therefore only the effect of distance to theboundarycouldbemodelledThesewereAfricangoldencatwesternlowlandgorillawhite‐belliedduikergiantpangolinAfricanpalmcivet(Nandinia binotata Gray 1830) Batesrsquos pygmy antelope and waterchevrotain (Hymeoschus aquaticusOgilby 1841)African palm civetwastheonlyspeciestohavedistancetotheboundaryselectedastheoptimummodel to explain occupancy as occupancy increasedwithdistance from the boundary of the protected area (Table 2)All theremainingspecieshadthenullmodelselectedastheoptimummodelaccordingtoAICcriteria (Table2)Howeverdistancetothebound‐arywaswithinlt2AICforthesespeciessuggestingthatasignificantSp
ecie
sN
orth
ern
sect
or (ψ
)N
orth
ern
sect
or (p
)So
uthe
rn s
ecto
r (ψ
)So
uthe
rn s
ecto
r (p
)M
odel
Beta
mdashPa
ram
eter
ch
osen
Low
er 9
5
beta
Upp
er 9
5
beta
C‐ha
t val
ueCh
i‐squ
arep
va
lue
Africangolden
cat
ndashndash
041(013)
013(004)
Null
ndashndash
ndashndash
ndash
Africanpalm
civet
[047]
ndash073(017)
012(003)
DOccu
psi(DistanceSTD)
minus8177158
Inf
197
008
Black‐legged
mongoose
047(01)a
025(004)
082(008)
a031(003)
SRN
lam(sectorSouthern)
028
0266
31
4627
420
011
058
Cameroon
cusimanse
075(009)
027(004)
056(015)
012(004)
SRN
lam(sectorSouthern)
minus1808131
minus05098939
005
073
Long‐nosed
mongoose
055(012)
a02(004)
015(006)
a027(007)
Null
ndashndash
ndashndash
ndash
Servalinegenet
092(006)
035(003)
08(009)
02(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus09202819
003
5821
570
50
26
Not
esNaiumlveoccupancyvaluesarepresentedinsquarebracketsforspecieswithadetectionprobabilitylt01TheoptimummodelchosenbyAkaikersquosinformationcriteriaforeachspeciesgeneratingsuf‐
ficientoccupancyvaluesinbothsectorswiththeBetaparameteranditisrespectivelowerandupper95confidencelimitsisshownandtheassociatedc‐hatandchi‐squaredp
val
ue
DdistancetoboundarySmanagementsectorRNRoylendashNicholsmodelOccuMckenziesingle‐seasonoccupancymodesynergisticinteraction
a IndicatesasignificantdifferenceinoccupancybetweensectorsasmeasuredbytheWaldteststatistic
TAB
LE 2
emsp(Continued)
770emsp |emsp emspensp Bruce et al
relationshipwithdistancetotheboundarycouldbeinfluencingoccu‐pancyIntheSouthernSectortheoccupancyincreasedwithdistanceto theboundary forwestern lowlandgorillaandgiantpangolinbutdecreasedforAfricangoldencatwhite‐belliedduikerandwaterchev‐rotainIntheNorthernSectoroccupancyincreasedwithdistancetotheboundaryforBatesrsquospygmyantelope
4emsp |emspDISCUSSION
Thecomparisonofthetwosurveysconfirmsthatstandardcameratrap surveys and derived metrics of presenceabsence trappingrates andoccupancy candiscern confidentdifferences in ground‐dwellingmammalcommunitiesinCentralAfricanforests
41emsp|emspCamera trap surveys for documenting species
Thecomparativeefficacyofcamera traps for surveyingmediumto large ground‐dwelling mammals in the DFR is indicated byobservationratesandverifiabilityofrecordsespeciallyofelusivesmallerandnocturnalspeciesForexamplethedirectencounterraterecordedbyrangersonpatrolthroughouttheentirereserveover a nine‐month period is much lower than the combinednumberofindependentphotographiceventsinbothmanagementsectors (ZSL amp MINFOF 2017b) even for relatively largeconspicuous species such as forest elephant (96 photographiceventscomparedto29directencounters)andcentralchimpanzee(204 independent photographic events compared to 23 directencounters)Methodologiessuchascameratrapping therefore
provideimportantbaselinedatathatwhenrepeatedthroughtimeusingastandardisedprotocolcanallowatleasttrendsinrelativeabundanceindicestobemonitored
42emsp|emspCamera trap surveys for comparing assemblages among sites
Despitebeingseparatedbyonlyc32kmthemammalcommunitiesbetween the twocamera trapgridsdisplayedmarkeddifferencesThiswasthecaseeventhoughbothgridshadlowShannonndashWeinerandSimpsonsdiversityindicesduetothedominanceofthreeorfourspeciesineachcameratrapgridSignificantdifferencesamongthesiteswere observed for the trapping rates of species of differentsizesbetweensectorsSmaller‐bodiedspecieswithintheherbivoreand omnivore guilds were more prevalent within the NorthernSector (Figure 2) Trapping rates and occupancy values for smallcarnivoresarealsolowerintheSouthernSectorThiscouldbeduetothedifficultyofidentifyingmorphologicallysimilarspeciessuchasmarshmongooseandlong‐nosedmongoose(Bahaa‐el‐dinetal2013 Ray 1997) in infrared imagery with single cameras Thereweremoreunidentifiablemongooseeventsthatwereclassifiedtoafamilylevel―66224intheSouthernSectorcomparedto29156intheNorthernSectorofallcombinedmongooseevents
43emsp|emspThe potential impact of seasonality on estimates derived from camera traps
Due to logistical and financial constraints the surveys could notberuninthesameseasonThishasthepotentialtoaffecttrapping
F I G U R E 5 emspChangeintheprobabilityofoccupancyforblack‐leggedmongoosecentralchimpanzeeandCamerooncusimansewithmanagementsectoraccordingtoaRoylendashNicholsmodel
emspensp emsp | emsp771Bruce et al
rates and occupancy for specieswith larger home ranges becausewhenspeciesarewide‐rangingoccupancycanproveineffectiveformeasuring relative abundance Forest elephants (Blake 2002) andgreatapesareknowntodisplayseasonalshiftsintheirhabitatusageover great distances in response to increased fruit availability andprecipitation(HeadRobbinsMundryMakagaampBoesch2012)Thiscouldalsoinfluenceothergregariousspeciessuchasredriverhogthatarealsothoughttooccasionallydisplaysimilaraggregationsandmovementsinresponsetomastingevents(LeslieampHuffman2015)However as both red river hog and chimpanzee had significantlyhigherRAIandhigheroccupancywithvariabledetectionprobabilityaccording to the number of individuals incorporated this supports
thepossibilitythatthesespeciesarefavouringtheSouthernSectorIfmanagersareable toestablishwhetherwide‐rangingspeciesarepredictably moving to known areas within the reserve they canrespondinamannerthatprovidesenhancedprotectiontovulnerablewildlifepopulations in concentration areasAsmost species in thissurveylikelyhaveasmallerhomerangethantheinter‐trapdistanceand display fixed territories it can be regarded as appropriate tocompare occupancy values as the extent of overlap of territorieswithin the two surveys are unlikely to change in such away as toaffecttheresultsFuturestudieswouldbenefitfromtryingtomatchcameratrapsurveysseasonallytotryandclarifytheissueofseasonalshiftsinhabitatusagewithintheDFR
F I G U R E 6 emspChangeintheprobabilityofoccupancyforAfricanbrush‐tailedporcupineEminspouchedratredriverhogservalinegenetPetersrsquoduikerandyellow‐backedduikerwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
772emsp |emsp emspensp Bruce et al
F I G U R E 7 emspChangeintheprobabilityofoccupancyforblueduikerandbayduikerwithdistancetotheboundaryinkilometresacrossbothmanagementsectorsaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
F I G U R E 8 emspChangeintheprobabilityofoccupancyforwhite‐belliedpangolinwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaMackenzieoccupancymodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
emspensp emsp | emsp773Bruce et al
44emsp|emspCamera trap surveys for measuring the impacts of hunting on mammal communities
The spatial scale at which mammal communities are affected byandhowpopulationsrespondtoanthropogenicpressuressuchasbushmeat hunting is difficult to empiricallymeasure (Laurance etal2006)Thisisespeciallytrueformammalsresidingwithintropi‐cal forestswheregatheringconsistentandmeaningfulpopulation‐andcommunity‐levelmetrics ischallenging(Ahumadaetal2013)Population density of tropical mammals can vary greatly due toheterogeneity present within the environment For example for‐est elephants havedifferent distributions and aggregations inwetanddryseasonsinNouabaleacute‐Ndoki NationalParkwhichispartiallydependentonspatio‐temporalpatternsoffruitingtreesacrossthelandscape(Blake2002)
Whether the differences observed among the two sites sur‐veyedhereareattributabletodifferent levelsofhuntingpressureremains to be confirmed There are however indications thathuntingpressureanditsimpactsonmammalfaunasaregreaterintheNorthern Sector than in the Southern Sector The effects ofhuntingpressureonmammaliandeclinesinCentralAfricanforestsarewell documented The pattern in general is the largest‐bod‐ied species frugivores and thosewith high hunter or blackmar‐ketvalue(Abernethyetal2013Cardilloetal2005FaOliveroFarfaacutenMaacuterquezDuarteetal2014aFaOliveroFarfaacutenMaacuterquezVargasetal2014bPeresampPalacios2007)arethefirstspeciestoshownoticeabledeclineInthisstudythesignificantdeclineintherelativeabundance for frugivores suchasPetersʼduikerandspe‐cieswithhighhuntervalueliketheredriverhogunderincreasedhuntingpressure in theNorthernSector is reported inother sur‐veys(Abernethyetal2013)Thisisalsoreflectedinthedifferencesobserved in this study in biomass in the different guilds of eachmammalcommunityThemammalcommunitywithintheNorthernSector shows indications of a community that is disturbed and isexperiencingelevatedhuntingpressureThesearehigher(camera)trapping rates for smaller‐bodiedspecies suchasEminrsquospouchedrat and significantly fewer encounters of larger‐bodiedmammalsthataretargetsofthebushmeattradesuchasPetersʼduikerandredriverhog(FaRyanampBell2005JerozolimskiampPeres2003)Additionalindicatorsaretheabsenceinthesurveysoflargercarni‐voresintheNorthernSectorsuchasgoldencatandleopardwhicharesensitivetosnaring(Bahaa‐el‐dinetal2015)andsignificantlyreducedabundancemetricsfordisturbance‐sensitivespeciessuchasblack‐leggedmongooseandwaterchevrotain(Hart2013a)Theabsence of white‐bellied duiker in the Northern Sector also sug‐gestselevatedhumandisturbanceasthisspecieshasbeenreportedasverysensitivetoevenminorperturbationwithintheenvironment(Hart2013b)IncomparisontheSouthernSectorcontainedindica‐torfaunasuchasthewhite‐belliedduikerandhadhighertrappingratesforlarger‐bodiedspecies
WesuspectthedifferencesobservedaremostlikelyduetolowerhumandisturbanceintheSouthernSectorTheteamsdeployingand
recoveringthecamerasintheSouthernSectorcovered238kmandencountered few signs of humanperturbation (T Brucepers obs)whereashumansignwascommonlyencounteredbytheteamsintheNorthernSectorThisperceiveddifference is reflected in the2017and 2018 density of hunting signwithin each camera trap grid asdetected throughMINFOF ranger patrols (ZSL ampMINFOF 2017a2017b) and through the2018DistanceSampling inventory for theDFR (Bruce et al 2018) Higher numbers of hunting sign in theNorthernSectorwouldbeconsistentwithanelevatedhuntingpres‐sureinthatarea
45emsp|emspProtection of refugia from hunting
Though inferences made for wide‐ranging species such as forestelephantsandgreatapesusingcameratrapsaredifficultthefactthattrappingrateswerehigherinmorechallengingterrainwithassumedlower hunting pressure could be indicative of complex habitatprovidingsomelevelofprotectionfromhuntingElephantisknownto retreatwhen they aredisturbed to terrain that ismoredifficulttoaccessbyhumans (Hedges2012)Thuswithin largerprotectedareas certain zones may act as refugia for wildlife populations(Campbelletal2011)Thiscanbeduetoarangeof factorssuchas remoteanddifficult terrain forpoachers (Attum2007Hedges2012) or the regular presence of field researchers and rangers(Campbell et al 2011) The significanceof these refugia for largerprotected areas is that the populations of wildlife residing withinthem if adequately protected may provide source populations toallowrecolonisationofotherareasofthereserve(NaranjoampBodmer2007)Thereforeifadequateprotectioncanbeprovidedtorelativelysmallbutimportantareasoflargereservesthismayprovidetropicalforestswithabetterchanceofbeingecologicallyresilienttoongoingand increasing human perturbation Well‐designed camera trapsurveys may provide data on the status of wildlife populations atrelativelyfinespatialresolutionssoastoidentifyfunctionalrefugiawithgreaterconfidence
ACKNOWLEDG EMENTS
WeappreciatetheongoingsupportofCameroonrsquosMinistryofForestsandWildlife(MINFOF)andtheopportunitytocontributetobiodiver‐sityconservationthroughoutthecountryInparticularwewouldliketothanktheChefdrsquoAntenneSergeJacobMeyeforhisongoingsup‐portofconservationresearchwithintheprotectedareaWeappreci‐atethestalwarteffortsofMINFOFecoguardsandlocalporterswhoaccompaniedthesurveyteamsinthefieldWewouldalsoliketothanktheUnitedStatesFishandWildlifeService(USFWS)mdashAfricanElephantConservationandIUCNSOSmdashFondationSegreacutePangolinConservationInitiativeforsupportingthiswork
ORCID
Tom Bruce httporcidorg0000‐0001‐6958‐1657
774emsp |emsp emspensp Bruce et al
R E FE R E N C E S
AbernethyKACoad L TaylorG LeeMEampMaisels F (2013)Extent and ecological consequences of hunting in Central Africanrainforests in thetwenty‐firstcenturyPhilosophical Transactions of the Royal Society of London Biological Sciences368(1625)20120303httpsdoiorg101098rstb20120303
AbrahamsM I Peres C A amp Costa H C (2017)Measuring localdepletion of terrestrial game vertebrates by central‐place hunt‐ers in rural Amazonia PLoS ONE 12(10) e0186653 httpsdoiorg101371journalpone0186653
AhumadaJAHurtadoJampLizcanoD(2013)MonitoringthestatusandtrendsoftropicalforestterrestrialvertebratecommunitiesfromcameratrapdataAtool forconservationPLoS ONE8(9)e73707httpsdoiorg101371journalpone0073707
Ahumada J A Silva C E Gajapersad K Hallam C Hurtado JMartin E hellip Sheil D (2011) Community structure and diver‐sity of tropical forest mammals Data from a global camera trapnetwork Philosophical Transactions of the Royal Society of London Biological Sciences366(1578)2703ndash2711httpsdoiorg101098rstb20110115
AminRAndanjeSAOgwonkaBAliAHBowkettAEOmarMampWacherT(2015)ThenortherncoastalforestsofKenyaarenationally and globally important for the conservation of AdersrsquoduikerCephalophusadersiandotherantelopespeciesBiodiversity and Conservation 24(3) 641ndash658 httpsdoiorg101007s10531‐014‐0842‐z
Attum O (2007) Can landscape use be among the factors that po‐tentiallymake some ungulates speciesmore difficult to conserveJournal of Arid Environments69(3)410ndash419
Bahaa‐el‐dinLHenschelPAbaaRAbernethyKBohmTBoutNhellipLeeM (2013)NotesonthedistributionandstatusofsmallcarnivoresinGabonSmall Carnivore Conservation4819ndash29
Bahaa‐el‐dinLHenschelPButynskiTMMacdonaldDWMillsDSlotowRampHunterL (2015)TheAfricangoldencatCaracalaurataAfricasleast‐knownfelidMammal Review45(1)63ndash77
Bennett E L Blencowe E Brandon K Brown D Burn R WCowlishaw G hellip Robinson J G (2007) Hunting for consensusReconcilingbushmeatharvestconservationanddevelopmentpol‐icyinWestandCentralAfricaConservation Biology21(3)884ndash887httpsdoiorg101111j1523‐1739200600595x
BlakeSDeemSLMossimboEMaiselsFampWalshP(2009)Forestelephants Tree planters of the CongoBiotropica41(4) 459ndash468httpsdoiorg101111j1744‐7429200900512x
Blake S (2002) The ecology of forest elephant distribution and itsimplications for conservation Doctoral dissertation University ofEdinburgh
BruceTNdjassiCFowlerANdimbeMFankemOTabueRhellipOlsonD(2018)Faunal inventory of the Dja Faunal Reserve Cameroon Yaoundeacute Cameroon Ministry of Forests and Wildlife (MINFOF)Zoological Society of London ndash Cameroon Country ProgrammeAfricanWildlifeFoundation
BruceTWacherTNdingaHBidjokaVMeyongFNgoBataMampOlsonD(2017)camera trap survey for larger terrestrial wildlife in the Dja Biosphere Reserve CameroonYaoundeacuteCameroonZoologicalSocietyofLondon(ZSL)ampCameroonMinistryofForestsandWildlife(MINFOF)
BurnhamKPampAndersonDR(2002)Model selection and multimodel inferenceNewYorkNYSpringer
Campbell G Kuehl H Diarrassouba A NGoran P K amp BoeschC (2011) Long‐term research sites as refugia for threatened andover‐harvested species Biology Letters 7(5) 723ndash726 httpsdoiorg101098rsbl20110155
CardilloMMaceGMJonesKEBielbyJBininda‐EmondsORSechrestWhellipPurvisA(2005)Multiplecausesofhighextinction
riskinlargemammalspeciesScience309(5738)1239ndash1241httpsdoiorg101126science1116030
Craigie IDBaillieJEBalmfordACarboneCCollenBGreenREampHuttonJM (2010)Largemammalpopulationdeclines inAfricarsquosprotectedareasBiological Conservation143(9)2221ndash2228httpsdoiorg101016jbiocon201006007
DaveyKWacherTampAminR(2017)Analysis tool for camera-trap sur-vey data [Computer software]ZoologicalSocietyofLondonRetrievedfromhttpswwwzslorgzsl‐camera‐trap‐data‐management‐ and‐analysis‐package
Djuikouo M N K Doucet J L Nguembou C K Lewis S L ampSonkeacute B (2010) Diversity and aboveground biomass in threetropical forest types in the Dja Biosphere Reserve Cameroon African Journal of Ecology 48(4) 1053ndash1063 httpsdoiorg101111j1365‐2028201001212x
DupainJBombomeKampVanElsackerL(2003)LeschimpanzeacutesetlesgorillesdelareacuteservedefauneduDjaCanopeacutee2414ndash15
EffordMGampDawsonDK(2012)OccupancyincontinuoushabitatEcosphere3(4)1ndash15httpsdoiorg101890ES11‐003081
Efron B amp Tibshirani R J (1994) An introduction to the bootstrap WashingtonDCCRCPress
FaJEOliveroJFarfaacutenMAacuteMaacuterquezALDuarteJNackoneyJhellipMacdonaldDW(2014a)CorrelatesofbushmeatinmarketsanddepletionofwildlifeConservation Biology29(3)805ndash815
Fa J EOlivero J FarfaacutenMAacuteMaacuterquezA LVargas JMRealRampNasiR(2014b)IntegratingsustainablehuntinginbiodiversityprotectioninCentralAfricaHotspotsweakspotsandstrongspotsPLoS ONE9(11)e112367
FaJERyanSFampBellDJ (2005)Huntingvulnerabilityecolog‐ical characteristics and harvest rates of bushmeat species in afro‐tropicalforestsBiological Conservation121(2)167ndash176httpsdoiorg101016jbiocon200404016
Fa J E Seymour S Dupain J E F Amin R Albrechtsen L ampMacdonaldD (2006) Getting to gripswith themagnitude of ex‐ploitationBushmeat in theCross‐SanagariversregionNigeria and Cameroon Biological Conservation 129(4) 497ndash510 httpsdoiorg101016jbiocon200511031
Farris Z J Boone H M Karpanty S Murphy A Ratelolahy FAndrianjakariveloVampKellyMJ(2015)FeralcatsandthefitoatyFirstpopulationassessmentoftheblackforestcatinMadagascarrsquosrainforestsJournal of Mammalogy97(2)518ndash525
Fiske IampChandlerR (2011)UnmarkedAnRpackageforfittinghi‐erarchicalmodelsofwildlifeoccurrenceandabundanceJournal of Statistical Software43(10)1ndash23
HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences107(19)8650ndash8655httpsdoiorg101073pnas0912668107
HartJ(2013a)WaterchevrotainHymemoschusaquaticusInJKingdonampMHoffmann (Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp88ndash92)LondonUKBloomsbury
Hart J (2013b) White‐bellied duiker Cephalophus leucogaster In JKingdonampMHoffmann(Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp255ndash258)LondonUKBloomsbury
HeadJSRobbinsMMMundryRMakagaLampBoeschC(2012)Remotevideo‐cameratrapsmeasurehabitatuseandcompetitiveex‐clusionamongsympatricchimpanzeegorillaandelephantinLoangoNational ParkGabon Journal of Tropical Ecology28(06) 571ndash583httpsdoiorg101017S0266467412000612
HedgesS(2012)Monitoring elephant populations and assessing threats HimayatnagarTelanganaUniversitiesPress
HedwigDKienastIBonnetMCurranBKCourageABoeschChellipKingT(2018)Acameratrapassessmentoftheforestmam‐mal community within the transitional savannah‐forest mosaic oftheBateacutekeacutePlateauNationalParkGabonAfrican Journal of Ecology56(4)777ndash790httpsdoiorg101111aje12497
emspensp emsp | emsp775Bruce et al
HijmansRJCameronSEParraJLJonesPGampJarvisA(2005)Very high resolution interpolated climate surfaces for global landareasInternational Journal of Climatology25(15)1965ndash1978httpsdoiorg101002joc1276
HuggelA(2012)Exiv2softwaretool[Computersoftware]Retrievedfromhttpswwwexiv2orgindexhtml
Jerozolimski A amp Peres C A (2003) Bringing home the biggestbacon A cross‐site analysis of the structure of hunter‐kill profilesin Neotropical forests Biological Conservation 111(3) 415ndash425httpsdoiorg101016S0006‐3207(02)00310‐5
KingdonJ (2015)The Kingdon field guide to African mammalsLondonUKBloomsburyPublishing
KuumlhlHFMaiselsMAncrenazampEAWilliamson(Eds)(2008)Best practice guidelines for surveys and monitoring of great ape populations GlandSwitzerlandIUCN
LauranceWFCroesBMTchignoumbaLLahmSAAlonsoALeeMEhellipOndzeanoC(2006)ImpactsofroadsandhuntingoncentralAfrican rainforestmammalsConservation Biology20(4)1251ndash1261httpsdoiorg101111j1523‐1739200600420x
LauranceWFUsecheDCRendeiroJKalkaMBradshawCJSloan S P hellip Arroyo‐Rodriguez V (2012) Averting biodiversitycollapse in tropical forestprotectedareasNature489(7415)290httpsdoiorg101038nature11318
LeslieDMampHuffmanBA(2015)Potamochoerus porcus(ArtiodactylaSuidae)Mammalian Species4715ndash31
MacKenzieD IampBailey L L (2004)Assessing the fit of site‐occu‐pancy models Journal of Agricultural Biological and Environmental Statistics9300ndash318httpsdoiorg101198108571104X3361
MacKenzieDINicholsJDRoyleJAPollockKHBaileyLLampHinesJE (2006)Occupancy estimation and modellingBurlingtonMAAcademicPress
Magurran A E (2005) Species abundance distributions Patternor process Functional Ecology 19(1) 177ndash181 httpsdoiorg101111j0269‐8463200500930x
MaiselsFStrindbergSBlakeSWittemyerGHartJWilliamsonEAhellipWarrenY (2013)DevastatingdeclineofforestelephantsinCentralAfricaPLoS ONE8(3)e59469httpsdoiorg101371journalpone0059469
MalhiYAdu‐BreduSAsareRA LewisS LampMayauxP (2013)AfricanrainforestsPastpresentandfuturePhilosophical Transactions of the Royal Society of London Biological Sciences 368(1625)20120312
MallonDPHoffmannMGraingerMJHibertFVanVlietNampMcGowanP JK (2015)An IUCNsituationanalysisof terrestrialandfreshwaterfaunainWestandCentralAfricaOccasionalpaperoftheIUCNspeciessurvivalcommission(54)
MambeyaMMBakerFMombouaBRKoumbaPamboAFHegaMOkouyiOkouyiVJhellipAbernethyK(2018)TheemergenceofacommercialtradeinpangolinsfromGabonAfrican Journal of Ecology56(3)601ndash609httpsdoiorg101111aje12507
MINFOFampIUCN(2015)CaracteacuterisationdelapopulationdegrandsetmoyensmammifegraveresdanslaReservedeFauneduDjaPotentieletmenacesYaoundeacuteCameroun
Muchaal P K amp Ngandjui G (1999) Impact of village hunt‐ing on wildlife populations in the western Dja ReserveCameroon Conservation Biology 13(2) 385ndash396 httpsdoiorg101046j1523‐17391999013002385x
NaranjoEJampBodmerRE (2007) Sourcendashsink systemsandconser‐vationofhuntedungulatesintheLacandonForestMexico Biological Conservation 138(3ndash4) 412ndash420 httpsdoiorg101016jbiocon 200705010
NielsenMR(2006)ImportancecauseandeffectofbushmeathuntingintheUdzungwaMountainsTanzania ImplicationsforcommunitybasedwildlifemanagementBiological Conservation128(4)509ndash516httpsdoiorg101016jbiocon200510017
OBrienTGKinnairdMFampWibisonoHT (2003)Crouching ti‐gers hiddenprey Sumatran tiger andprey populations in a tropi‐calforestlandscapeAnimal Conservation6(2)131ndash139httpsdoiorg101017S1367943003003172
OksanenJ(2015)VegananintroductiontoordinationVol8(p19)Retrieved from httpscranr‐projectorgwebpackagesveganvi‐gnettesintroveganpdf
PeresCAampPalaciosE(2007)Basin‐wideeffectsofgameharvestonvertebrate populationdensities inAmazonian forests Implicationsfor animal‐mediated seed dispersal Biotropica 39(3) 304ndash315httpsdoiorg101111j1744‐7429200700272x
PotapovPVTurubanovaSAHansenMCAduseiBBroichMAltstattAhellipJusticeCO(2012)QuantifyingforestcoverlossinDemocraticRepublicoftheCongo2000ndash2010withLandsatETM+data Remote Sensing of Environment 122 106ndash116 httpsdoiorg101016jrse201108027
PoulsenJRKoernerSEMooreSMedjibeVPBlakeSClarkC JhellipRosinC (2017) Poaching empties criticalCentralAfricanwilderness of forest elephants Current Biology 27(4) 134ndashR135httpsdoiorg101016jcub201701023
PurvisAGittlemanJlCowlishawGampMaceGM(2000)PredictingextinctionriskindecliningspeciesProceedings of the Royal Society B Biological Sciences267(1456) 1947ndash1952 httpsdoiorg101098rspb20001234
RayJ(1997)ComparativeecologyoftwoAfricanforestmongoosesHerpestesnasoandAtilaxpaludinosusAfrican Journal of Ecology35(3)237ndash253httpsdoiorg101111j1365‐20281997086‐ 89086x
Redford K H (1992) The empty forest BioScience 42(6) 412ndash422httpsdoiorg1023071311860
RepublicofCameroon(1994)Lawno9401du20janvier1994portantreacutegimedesforecirctsdelafauneetdelapecirccheRepublicofCameroon
RoveroFampMarshallAR(2009)CameratrappingphotographicrateasanindexofdensityinforestungulatesJournal of Applied Ecology46(5)1011ndash1017httpsdoiorg101111j1365‐2664200901705x
Royle J A amp Nichols J D (2003) Estimating abundance from re‐peated presence‐absence data or point counts Ecology 84(3)777ndash790 httpsdoiorg1018900012‐9658(2003)084[0777EAFRPA]20CO2
Seddon P J Griffiths C J Soorae P S ampArmstrongD P (2014)ReversingdefaunationRestoringspeciesinachangingworldScience345(6195)406ndash412httpsdoiorg101126science1251818
Silveira L Jacomo A T amp Diniz‐Filho J A F (2003) Camera trapline transect census and track surveys A comparative evaluationBiological Conservation 114(3) 351ndash355 httpsdoiorg101016S0006‐3207(03)00063‐6
Sonkeacute B (1998) Etudes floristiques et structurales des forecircts de laReacuteserve de Faune du Dja (Cameroun) Laboratoire de BotaniqueSysteacutematique et de Phytosociologie Universiteacute Libre de Bruxelles(ULB)
Srbek‐AraujoACampChiarelloAG(2005)Iscameratrappinganeffi‐cientmethodforsurveyingmammalsinNeotropicalforestsAcasestudyinsouth‐easternBrazilJournal of Tropical Ecology21(1)121ndash125httpsdoiorg101017S0266467404001956
Stiles D (2011) Elephant meat and ivory trade in Central AfricaPachyderm5026ndash36
TEAMNetwork(2008)Terrestrialvertebrateprotocol implementationmanualv30(p56)WashingtonDCTropicalEcologyAssessmentandMonitoringNetworkCenter forAppliedBiodiversity ScienceConservationInternational
Tobler M W Carrillo‐Percastegui S E Leite Pitman R MaresR amp Powell G (2008) An evaluation of camera traps for in‐ventorying large‐and medium‐sized terrestrial rainforestmammals Animal Conservation 11(3) 169ndash178 httpsdoiorg101111j1469‐1795200800169x
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
766emsp |emsp emspensp Bruce et al
F I G U R E 2 emspRarefiedspeciesaccumulationcurvesformedium‐to‐largeterrestrialmammalsintheNorthernandSouthernsectorsofDjaFaunalReserveCameroon
F I G U R E 3 emspDistributionofmedium‐to‐largeterrestrialmammalspeciesintheNorthernSectoroftheDjaFaunalReserveCameroononthebasisofbodysizeandtrophiccategoryEachcirclerepresentsaspeciesinfunctionalspaceSizeofthecircleproportionaltothetrappingrateforthatspecies
emspensp emsp | emsp767Bruce et al
trappingrateintheNorthernSector(Table1)butlackedsufficientdetectionstoreliablycalculateoccupancyAbundanceofCamerooncusimanse(Crossarchus platycephalusGoldman1984)didnotdiffersignificantlybetweenthetwosectors(NorthernSectorRAI=183[LCL=124 UCL=247 ψ=075] Southern Sector RAI=083[LCL=046UCL=127]ψ=056p=028)
36emsp|emspElephants great apes and giant pangolin (illegal wildlife trade targets)
Amongtheterrestrialmammalstargetedbytheillegalwildlifetradespecifically central chimpanzee (Pan troglodytes Blumenbachsubsp troglodytes 1799) western lowland gorilla (Gorilla gorillaSavagesubsp gorilla1847)forestelephantgiantpangolin(Smutsia gigantea Illiger 1815) and white‐bellied pangolin (Phataginus tri-cuspis Rafinesque 1821) only central chimpanzee displayed asignificant difference in RAI between the management sectors(Northern Sector RAI=161 [LCL=077 UCL=29] SouthernSector RAI=457 [LCL=314 UCL=617]) However there wasnosignificantdifferenceinmeanoccupancybetweenthetwosec‐tors (p=074) Giant pangolin displayed the greatest differencewithathreefoldincreaseinRAIfrom027[LCL=008UCL=052]in the Northern Sector to 068 [LCL=038 UCL=101] in theSouthernSectorbutthiswasnotsignificantduetotheoverlapping
confidencelimitsTheRAIsandwhereappropriateoccupancyofforestelephantwesternlowlandgorillaandwhite‐belliedpangolinwerenotsignificantlyhigher intheSouthernSectorcomparedtotheNorthernSector(Tables12and12)
37emsp|emspOther bushmeat‐targeted species
Eminrsquospouchedrat(Cricetomys eminiWroughton1910)wasmoreabundantasmeasuredbybothoccupancy(pge001)andtrapratesintheNorthernSectorcomparedtotheSouthernSector(Table1)Africanbrush‐tailedporcupine(Atherurus africanusGray1842)didnothavesignificantdifferencesinRAIbetweenthemanagementsectors but occupancywas significantly higher in theNorthernSector (pge004) In comparison the larger‐bodied red river hog(Potamochoerus porcus Linneaus1758)wasmore frequentlyen‐countered as measured by both species abundance metrics intheSouthernSector(RAI=7[LCL=336UCL=1304]ψ=091)compared to the Northern Sector (RAI=161 [LCL=102UCL=228]ψ=065(p=004)
38emsp|emspSpecies occupancy with covariates
Therewasatotalof15speciesthathadsufficientdetectionstomodeloccupancywithinteractingsitecovariates(distancetoparkboundary
F I G U R E 4 emspDistributionofmedium‐to‐largeterrestrialmammalspeciesintheSouthernSectoroftheDjaFaunalReserveCameroononthebasisofbodysizeandtrophiccategoryEachcirclerepresentsaspeciesinfunctionalspaceSizeofthecircleproportionaltothetrappingrateforthatspecies
768emsp |emsp emspensp Bruce et al
TAB
LE 2
emspNullmeanoccupancy(ψ)anddetection(p)probabilitieswithstandarderrorpresentedinbracketsfortheNorthernSectorandSouthernSector
Spec
ies
Nor
ther
n se
ctor
(ψ)
Nor
ther
n se
ctor
(p)
Sout
hern
sec
tor
(ψ)
Sout
hern
sec
tor
(p)
Mod
elBe
tamdash
Para
met
er
chos
enLo
wer
95
be
taU
pper
95
be
taC‐
hat v
alue
Chi‐s
quar
ep
valu
e
Certiodactyla
Batesrsquospygmy
antelope
022(01)
015(006)
[026]
ndashNull
ndashndash
ndashndash
ndash
Bayduiker
091(006)
04(003)
087(006)
04(003)
DRN
lam(DistanceSTD)
000
6356
808
043
3356
50
930
25
Black‐fronted
duiker
01(006)
036(01)
015(006)
025(008)
Null
ndashndash
ndashndash
ndash
Blueduiker
097(003)
082(002)
1(0)
1(0)
DRN
lam(DistanceSTD)
002
0135
490
3637
492
021
024
Petersrsquoduiker
083(007)
a056(003)
1(0)a
1(0)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus07435528
003
6592
430
004
03
Waterchevrotain
[007]
ndash04(008)
045(005)
ndashndash
ndashndash
ndashndash
White‐bellied
duiker
ndashndash
072(008)
031(003)
Null
ndashndash
ndashndash
ndash
Yellow‐backed
duiker
084(008)
027(003)
086(007)
039(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
010
8837
21
0251
104
069
021
Redriverhog
065(011)
a021(003)
091(006)
a033(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus12560347
minus01352547
027
044
Proboscidae
Forestelephant
067(015)
014(004)
063(013)
014(004)
Null
ndashndash
ndashndash
ndash
Primates
Central
chimpanzee
077(014)
015(004)
082(007)
035(003)
SRN
lam(sectorSouthern)
037
3686
91
4429
314
03
039
Westernlowland
goril
la[007]
ndash045(017)
01(004)
Null
ndashndash
ndashndash
ndash
Philodota
Giantpangolin
[02]
ndash061(016)
011(004)
Null
ndashndash
ndashndash
ndash
White‐bellied
pangolin
045(016)
012(005)
063(017)
011(003)
DSoccu
psi(DistanceSTDsec
torSouthern)
minus48425115
minus1910401
022
06
Rodentia
African
brush‐tailed
porcupine
098(003)
a057(003)
084(006)
a042(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus10008123
minus01586108
042
071
Eminrsquospouched
rat
1(0)a
1(0)
079(007)
a038(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus095574568
minus01390762
021
075
Carnivora
(Con
tinue
s)
emspensp emsp | emsp769Bruce et al
and management sector Table 2) Forest elephant black‐frontedduikerand long‐nosedmongoose (Herpestes nasodeWinton1901)lackedamodel thathadanAICdifferenceofgt2 therefore theco‐variatemodelswerenotsignificantlydifferent to thenullmodel forthese species Elevenof 15 species had aRoylendashNicholsmodel se‐lectedasthelowestAICvaluesuggestingadifferenceinthenumberofindividualswassignificantlyinfluencingdetectionprobabilitiesandthereforeoccupancy
RoylendashNichols models accounted for occupancy being signifi‐cantlyhigherindifferingmanagementsectorswithnointeractionofdistancetotheprotectedareaboundaryforthreespeciesCamerooncusimanse had higher occupancy in the Northern Sector In con‐trast central chimpanzee and black‐legged mongoose had signifi‐cantlyloweroccupancywithintheNorthernSectorcomparedtotheSouthernSector(Figure5)
African brush‐tailed porcupine Eminrsquos pouched rat and servalinegenet(Genetta servalinaPucheran1855)hadasynergisticRoylendashNicholsmodelselectedasthemostsupportedTheprobabilityofsiteoccupancyslightlyincreasedwithdistancetotheboundaryandwasoverallhigherin theNorthernSector butdeclinedwithdistance to theboundary intheSouthernSector(Figure6)BothPetersrsquoduikerandredriverhogalsodisplayedthispatternofoccupancybuthadamuchgreaterincreaseinoccupancyintheNorthernSectorandhadhigheroccupancyoverallintheSouthernSector(Figure6)Incontrastyellow‐backedduiker(Cephalophus silvicultorAfezilus1815)wastheonlyspeciestodemonstrateanincreaseinoccupancywithdistancetotheboundaryintheSouthernSectorwhiledecliningintheNorthernSectorHoweversimilartootherlargerspeciesoccupancywashigherintheSouthernSector(Figure6)
With regard to the remainingduiker speciesmodelled aRoylendashNicholsmodelwithdistancetotheprotectedareaboundarywasiden‐tifiedasthemostappropriateTheprobabilityofasitebeingoccupiedbyblueduikerandbayduikerincreasedwithdistancetotheboundarywith no discernible difference betweenmanagement sectors in themodel(Figure7)
White‐belliedpangolinhadasingle‐seasonoccupancymodelse‐lectedsuggestingdifferences inabundancebetweenthemanage‐mentsectorsdidnotaffectdetectionprobabilitiesTheprobabilityofasitebeingoccupiedbywhite‐belliedpangolin increasedintheNorthernSectoranddeclinedintheSouthernSectorwithincreasingdistancetotheboundary(Figure8)
Seven speciesweredetectedonly inone sectoror lacked suffi‐cientdetectionsinonesectortoreliablymodeloccupancyacrossbothmanagement sectors Therefore only the effect of distance to theboundarycouldbemodelledThesewereAfricangoldencatwesternlowlandgorillawhite‐belliedduikergiantpangolinAfricanpalmcivet(Nandinia binotata Gray 1830) Batesrsquos pygmy antelope and waterchevrotain (Hymeoschus aquaticusOgilby 1841)African palm civetwastheonlyspeciestohavedistancetotheboundaryselectedastheoptimummodel to explain occupancy as occupancy increasedwithdistance from the boundary of the protected area (Table 2)All theremainingspecieshadthenullmodelselectedastheoptimummodelaccordingtoAICcriteria (Table2)Howeverdistancetothebound‐arywaswithinlt2AICforthesespeciessuggestingthatasignificantSp
ecie
sN
orth
ern
sect
or (ψ
)N
orth
ern
sect
or (p
)So
uthe
rn s
ecto
r (ψ
)So
uthe
rn s
ecto
r (p
)M
odel
Beta
mdashPa
ram
eter
ch
osen
Low
er 9
5
beta
Upp
er 9
5
beta
C‐ha
t val
ueCh
i‐squ
arep
va
lue
Africangolden
cat
ndashndash
041(013)
013(004)
Null
ndashndash
ndashndash
ndash
Africanpalm
civet
[047]
ndash073(017)
012(003)
DOccu
psi(DistanceSTD)
minus8177158
Inf
197
008
Black‐legged
mongoose
047(01)a
025(004)
082(008)
a031(003)
SRN
lam(sectorSouthern)
028
0266
31
4627
420
011
058
Cameroon
cusimanse
075(009)
027(004)
056(015)
012(004)
SRN
lam(sectorSouthern)
minus1808131
minus05098939
005
073
Long‐nosed
mongoose
055(012)
a02(004)
015(006)
a027(007)
Null
ndashndash
ndashndash
ndash
Servalinegenet
092(006)
035(003)
08(009)
02(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus09202819
003
5821
570
50
26
Not
esNaiumlveoccupancyvaluesarepresentedinsquarebracketsforspecieswithadetectionprobabilitylt01TheoptimummodelchosenbyAkaikersquosinformationcriteriaforeachspeciesgeneratingsuf‐
ficientoccupancyvaluesinbothsectorswiththeBetaparameteranditisrespectivelowerandupper95confidencelimitsisshownandtheassociatedc‐hatandchi‐squaredp
val
ue
DdistancetoboundarySmanagementsectorRNRoylendashNicholsmodelOccuMckenziesingle‐seasonoccupancymodesynergisticinteraction
a IndicatesasignificantdifferenceinoccupancybetweensectorsasmeasuredbytheWaldteststatistic
TAB
LE 2
emsp(Continued)
770emsp |emsp emspensp Bruce et al
relationshipwithdistancetotheboundarycouldbeinfluencingoccu‐pancyIntheSouthernSectortheoccupancyincreasedwithdistanceto theboundary forwestern lowlandgorillaandgiantpangolinbutdecreasedforAfricangoldencatwhite‐belliedduikerandwaterchev‐rotainIntheNorthernSectoroccupancyincreasedwithdistancetotheboundaryforBatesrsquospygmyantelope
4emsp |emspDISCUSSION
Thecomparisonofthetwosurveysconfirmsthatstandardcameratrap surveys and derived metrics of presenceabsence trappingrates andoccupancy candiscern confidentdifferences in ground‐dwellingmammalcommunitiesinCentralAfricanforests
41emsp|emspCamera trap surveys for documenting species
Thecomparativeefficacyofcamera traps for surveyingmediumto large ground‐dwelling mammals in the DFR is indicated byobservationratesandverifiabilityofrecordsespeciallyofelusivesmallerandnocturnalspeciesForexamplethedirectencounterraterecordedbyrangersonpatrolthroughouttheentirereserveover a nine‐month period is much lower than the combinednumberofindependentphotographiceventsinbothmanagementsectors (ZSL amp MINFOF 2017b) even for relatively largeconspicuous species such as forest elephant (96 photographiceventscomparedto29directencounters)andcentralchimpanzee(204 independent photographic events compared to 23 directencounters)Methodologiessuchascameratrapping therefore
provideimportantbaselinedatathatwhenrepeatedthroughtimeusingastandardisedprotocolcanallowatleasttrendsinrelativeabundanceindicestobemonitored
42emsp|emspCamera trap surveys for comparing assemblages among sites
Despitebeingseparatedbyonlyc32kmthemammalcommunitiesbetween the twocamera trapgridsdisplayedmarkeddifferencesThiswasthecaseeventhoughbothgridshadlowShannonndashWeinerandSimpsonsdiversityindicesduetothedominanceofthreeorfourspeciesineachcameratrapgridSignificantdifferencesamongthesiteswere observed for the trapping rates of species of differentsizesbetweensectorsSmaller‐bodiedspecieswithintheherbivoreand omnivore guilds were more prevalent within the NorthernSector (Figure 2) Trapping rates and occupancy values for smallcarnivoresarealsolowerintheSouthernSectorThiscouldbeduetothedifficultyofidentifyingmorphologicallysimilarspeciessuchasmarshmongooseandlong‐nosedmongoose(Bahaa‐el‐dinetal2013 Ray 1997) in infrared imagery with single cameras Thereweremoreunidentifiablemongooseeventsthatwereclassifiedtoafamilylevel―66224intheSouthernSectorcomparedto29156intheNorthernSectorofallcombinedmongooseevents
43emsp|emspThe potential impact of seasonality on estimates derived from camera traps
Due to logistical and financial constraints the surveys could notberuninthesameseasonThishasthepotentialtoaffecttrapping
F I G U R E 5 emspChangeintheprobabilityofoccupancyforblack‐leggedmongoosecentralchimpanzeeandCamerooncusimansewithmanagementsectoraccordingtoaRoylendashNicholsmodel
emspensp emsp | emsp771Bruce et al
rates and occupancy for specieswith larger home ranges becausewhenspeciesarewide‐rangingoccupancycanproveineffectiveformeasuring relative abundance Forest elephants (Blake 2002) andgreatapesareknowntodisplayseasonalshiftsintheirhabitatusageover great distances in response to increased fruit availability andprecipitation(HeadRobbinsMundryMakagaampBoesch2012)Thiscouldalsoinfluenceothergregariousspeciessuchasredriverhogthatarealsothoughttooccasionallydisplaysimilaraggregationsandmovementsinresponsetomastingevents(LeslieampHuffman2015)However as both red river hog and chimpanzee had significantlyhigherRAIandhigheroccupancywithvariabledetectionprobabilityaccording to the number of individuals incorporated this supports
thepossibilitythatthesespeciesarefavouringtheSouthernSectorIfmanagersareable toestablishwhetherwide‐rangingspeciesarepredictably moving to known areas within the reserve they canrespondinamannerthatprovidesenhancedprotectiontovulnerablewildlifepopulations in concentration areasAsmost species in thissurveylikelyhaveasmallerhomerangethantheinter‐trapdistanceand display fixed territories it can be regarded as appropriate tocompare occupancy values as the extent of overlap of territorieswithin the two surveys are unlikely to change in such away as toaffecttheresultsFuturestudieswouldbenefitfromtryingtomatchcameratrapsurveysseasonallytotryandclarifytheissueofseasonalshiftsinhabitatusagewithintheDFR
F I G U R E 6 emspChangeintheprobabilityofoccupancyforAfricanbrush‐tailedporcupineEminspouchedratredriverhogservalinegenetPetersrsquoduikerandyellow‐backedduikerwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
772emsp |emsp emspensp Bruce et al
F I G U R E 7 emspChangeintheprobabilityofoccupancyforblueduikerandbayduikerwithdistancetotheboundaryinkilometresacrossbothmanagementsectorsaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
F I G U R E 8 emspChangeintheprobabilityofoccupancyforwhite‐belliedpangolinwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaMackenzieoccupancymodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
emspensp emsp | emsp773Bruce et al
44emsp|emspCamera trap surveys for measuring the impacts of hunting on mammal communities
The spatial scale at which mammal communities are affected byandhowpopulationsrespondtoanthropogenicpressuressuchasbushmeat hunting is difficult to empiricallymeasure (Laurance etal2006)Thisisespeciallytrueformammalsresidingwithintropi‐cal forestswheregatheringconsistentandmeaningfulpopulation‐andcommunity‐levelmetrics ischallenging(Ahumadaetal2013)Population density of tropical mammals can vary greatly due toheterogeneity present within the environment For example for‐est elephants havedifferent distributions and aggregations inwetanddryseasonsinNouabaleacute‐Ndoki NationalParkwhichispartiallydependentonspatio‐temporalpatternsoffruitingtreesacrossthelandscape(Blake2002)
Whether the differences observed among the two sites sur‐veyedhereareattributabletodifferent levelsofhuntingpressureremains to be confirmed There are however indications thathuntingpressureanditsimpactsonmammalfaunasaregreaterintheNorthern Sector than in the Southern Sector The effects ofhuntingpressureonmammaliandeclinesinCentralAfricanforestsarewell documented The pattern in general is the largest‐bod‐ied species frugivores and thosewith high hunter or blackmar‐ketvalue(Abernethyetal2013Cardilloetal2005FaOliveroFarfaacutenMaacuterquezDuarteetal2014aFaOliveroFarfaacutenMaacuterquezVargasetal2014bPeresampPalacios2007)arethefirstspeciestoshownoticeabledeclineInthisstudythesignificantdeclineintherelativeabundance for frugivores suchasPetersʼduikerandspe‐cieswithhighhuntervalueliketheredriverhogunderincreasedhuntingpressure in theNorthernSector is reported inother sur‐veys(Abernethyetal2013)Thisisalsoreflectedinthedifferencesobserved in this study in biomass in the different guilds of eachmammalcommunityThemammalcommunitywithintheNorthernSector shows indications of a community that is disturbed and isexperiencingelevatedhuntingpressureThesearehigher(camera)trapping rates for smaller‐bodiedspecies suchasEminrsquospouchedrat and significantly fewer encounters of larger‐bodiedmammalsthataretargetsofthebushmeattradesuchasPetersʼduikerandredriverhog(FaRyanampBell2005JerozolimskiampPeres2003)Additionalindicatorsaretheabsenceinthesurveysoflargercarni‐voresintheNorthernSectorsuchasgoldencatandleopardwhicharesensitivetosnaring(Bahaa‐el‐dinetal2015)andsignificantlyreducedabundancemetricsfordisturbance‐sensitivespeciessuchasblack‐leggedmongooseandwaterchevrotain(Hart2013a)Theabsence of white‐bellied duiker in the Northern Sector also sug‐gestselevatedhumandisturbanceasthisspecieshasbeenreportedasverysensitivetoevenminorperturbationwithintheenvironment(Hart2013b)IncomparisontheSouthernSectorcontainedindica‐torfaunasuchasthewhite‐belliedduikerandhadhighertrappingratesforlarger‐bodiedspecies
WesuspectthedifferencesobservedaremostlikelyduetolowerhumandisturbanceintheSouthernSectorTheteamsdeployingand
recoveringthecamerasintheSouthernSectorcovered238kmandencountered few signs of humanperturbation (T Brucepers obs)whereashumansignwascommonlyencounteredbytheteamsintheNorthernSectorThisperceiveddifference is reflected in the2017and 2018 density of hunting signwithin each camera trap grid asdetected throughMINFOF ranger patrols (ZSL ampMINFOF 2017a2017b) and through the2018DistanceSampling inventory for theDFR (Bruce et al 2018) Higher numbers of hunting sign in theNorthernSectorwouldbeconsistentwithanelevatedhuntingpres‐sureinthatarea
45emsp|emspProtection of refugia from hunting
Though inferences made for wide‐ranging species such as forestelephantsandgreatapesusingcameratrapsaredifficultthefactthattrappingrateswerehigherinmorechallengingterrainwithassumedlower hunting pressure could be indicative of complex habitatprovidingsomelevelofprotectionfromhuntingElephantisknownto retreatwhen they aredisturbed to terrain that ismoredifficulttoaccessbyhumans (Hedges2012)Thuswithin largerprotectedareas certain zones may act as refugia for wildlife populations(Campbelletal2011)Thiscanbeduetoarangeof factorssuchas remoteanddifficult terrain forpoachers (Attum2007Hedges2012) or the regular presence of field researchers and rangers(Campbell et al 2011) The significanceof these refugia for largerprotected areas is that the populations of wildlife residing withinthem if adequately protected may provide source populations toallowrecolonisationofotherareasofthereserve(NaranjoampBodmer2007)Thereforeifadequateprotectioncanbeprovidedtorelativelysmallbutimportantareasoflargereservesthismayprovidetropicalforestswithabetterchanceofbeingecologicallyresilienttoongoingand increasing human perturbation Well‐designed camera trapsurveys may provide data on the status of wildlife populations atrelativelyfinespatialresolutionssoastoidentifyfunctionalrefugiawithgreaterconfidence
ACKNOWLEDG EMENTS
WeappreciatetheongoingsupportofCameroonrsquosMinistryofForestsandWildlife(MINFOF)andtheopportunitytocontributetobiodiver‐sityconservationthroughoutthecountryInparticularwewouldliketothanktheChefdrsquoAntenneSergeJacobMeyeforhisongoingsup‐portofconservationresearchwithintheprotectedareaWeappreci‐atethestalwarteffortsofMINFOFecoguardsandlocalporterswhoaccompaniedthesurveyteamsinthefieldWewouldalsoliketothanktheUnitedStatesFishandWildlifeService(USFWS)mdashAfricanElephantConservationandIUCNSOSmdashFondationSegreacutePangolinConservationInitiativeforsupportingthiswork
ORCID
Tom Bruce httporcidorg0000‐0001‐6958‐1657
774emsp |emsp emspensp Bruce et al
R E FE R E N C E S
AbernethyKACoad L TaylorG LeeMEampMaisels F (2013)Extent and ecological consequences of hunting in Central Africanrainforests in thetwenty‐firstcenturyPhilosophical Transactions of the Royal Society of London Biological Sciences368(1625)20120303httpsdoiorg101098rstb20120303
AbrahamsM I Peres C A amp Costa H C (2017)Measuring localdepletion of terrestrial game vertebrates by central‐place hunt‐ers in rural Amazonia PLoS ONE 12(10) e0186653 httpsdoiorg101371journalpone0186653
AhumadaJAHurtadoJampLizcanoD(2013)MonitoringthestatusandtrendsoftropicalforestterrestrialvertebratecommunitiesfromcameratrapdataAtool forconservationPLoS ONE8(9)e73707httpsdoiorg101371journalpone0073707
Ahumada J A Silva C E Gajapersad K Hallam C Hurtado JMartin E hellip Sheil D (2011) Community structure and diver‐sity of tropical forest mammals Data from a global camera trapnetwork Philosophical Transactions of the Royal Society of London Biological Sciences366(1578)2703ndash2711httpsdoiorg101098rstb20110115
AminRAndanjeSAOgwonkaBAliAHBowkettAEOmarMampWacherT(2015)ThenortherncoastalforestsofKenyaarenationally and globally important for the conservation of AdersrsquoduikerCephalophusadersiandotherantelopespeciesBiodiversity and Conservation 24(3) 641ndash658 httpsdoiorg101007s10531‐014‐0842‐z
Attum O (2007) Can landscape use be among the factors that po‐tentiallymake some ungulates speciesmore difficult to conserveJournal of Arid Environments69(3)410ndash419
Bahaa‐el‐dinLHenschelPAbaaRAbernethyKBohmTBoutNhellipLeeM (2013)NotesonthedistributionandstatusofsmallcarnivoresinGabonSmall Carnivore Conservation4819ndash29
Bahaa‐el‐dinLHenschelPButynskiTMMacdonaldDWMillsDSlotowRampHunterL (2015)TheAfricangoldencatCaracalaurataAfricasleast‐knownfelidMammal Review45(1)63ndash77
Bennett E L Blencowe E Brandon K Brown D Burn R WCowlishaw G hellip Robinson J G (2007) Hunting for consensusReconcilingbushmeatharvestconservationanddevelopmentpol‐icyinWestandCentralAfricaConservation Biology21(3)884ndash887httpsdoiorg101111j1523‐1739200600595x
BlakeSDeemSLMossimboEMaiselsFampWalshP(2009)Forestelephants Tree planters of the CongoBiotropica41(4) 459ndash468httpsdoiorg101111j1744‐7429200900512x
Blake S (2002) The ecology of forest elephant distribution and itsimplications for conservation Doctoral dissertation University ofEdinburgh
BruceTNdjassiCFowlerANdimbeMFankemOTabueRhellipOlsonD(2018)Faunal inventory of the Dja Faunal Reserve Cameroon Yaoundeacute Cameroon Ministry of Forests and Wildlife (MINFOF)Zoological Society of London ndash Cameroon Country ProgrammeAfricanWildlifeFoundation
BruceTWacherTNdingaHBidjokaVMeyongFNgoBataMampOlsonD(2017)camera trap survey for larger terrestrial wildlife in the Dja Biosphere Reserve CameroonYaoundeacuteCameroonZoologicalSocietyofLondon(ZSL)ampCameroonMinistryofForestsandWildlife(MINFOF)
BurnhamKPampAndersonDR(2002)Model selection and multimodel inferenceNewYorkNYSpringer
Campbell G Kuehl H Diarrassouba A NGoran P K amp BoeschC (2011) Long‐term research sites as refugia for threatened andover‐harvested species Biology Letters 7(5) 723ndash726 httpsdoiorg101098rsbl20110155
CardilloMMaceGMJonesKEBielbyJBininda‐EmondsORSechrestWhellipPurvisA(2005)Multiplecausesofhighextinction
riskinlargemammalspeciesScience309(5738)1239ndash1241httpsdoiorg101126science1116030
Craigie IDBaillieJEBalmfordACarboneCCollenBGreenREampHuttonJM (2010)Largemammalpopulationdeclines inAfricarsquosprotectedareasBiological Conservation143(9)2221ndash2228httpsdoiorg101016jbiocon201006007
DaveyKWacherTampAminR(2017)Analysis tool for camera-trap sur-vey data [Computer software]ZoologicalSocietyofLondonRetrievedfromhttpswwwzslorgzsl‐camera‐trap‐data‐management‐ and‐analysis‐package
Djuikouo M N K Doucet J L Nguembou C K Lewis S L ampSonkeacute B (2010) Diversity and aboveground biomass in threetropical forest types in the Dja Biosphere Reserve Cameroon African Journal of Ecology 48(4) 1053ndash1063 httpsdoiorg101111j1365‐2028201001212x
DupainJBombomeKampVanElsackerL(2003)LeschimpanzeacutesetlesgorillesdelareacuteservedefauneduDjaCanopeacutee2414ndash15
EffordMGampDawsonDK(2012)OccupancyincontinuoushabitatEcosphere3(4)1ndash15httpsdoiorg101890ES11‐003081
Efron B amp Tibshirani R J (1994) An introduction to the bootstrap WashingtonDCCRCPress
FaJEOliveroJFarfaacutenMAacuteMaacuterquezALDuarteJNackoneyJhellipMacdonaldDW(2014a)CorrelatesofbushmeatinmarketsanddepletionofwildlifeConservation Biology29(3)805ndash815
Fa J EOlivero J FarfaacutenMAacuteMaacuterquezA LVargas JMRealRampNasiR(2014b)IntegratingsustainablehuntinginbiodiversityprotectioninCentralAfricaHotspotsweakspotsandstrongspotsPLoS ONE9(11)e112367
FaJERyanSFampBellDJ (2005)Huntingvulnerabilityecolog‐ical characteristics and harvest rates of bushmeat species in afro‐tropicalforestsBiological Conservation121(2)167ndash176httpsdoiorg101016jbiocon200404016
Fa J E Seymour S Dupain J E F Amin R Albrechtsen L ampMacdonaldD (2006) Getting to gripswith themagnitude of ex‐ploitationBushmeat in theCross‐SanagariversregionNigeria and Cameroon Biological Conservation 129(4) 497ndash510 httpsdoiorg101016jbiocon200511031
Farris Z J Boone H M Karpanty S Murphy A Ratelolahy FAndrianjakariveloVampKellyMJ(2015)FeralcatsandthefitoatyFirstpopulationassessmentoftheblackforestcatinMadagascarrsquosrainforestsJournal of Mammalogy97(2)518ndash525
Fiske IampChandlerR (2011)UnmarkedAnRpackageforfittinghi‐erarchicalmodelsofwildlifeoccurrenceandabundanceJournal of Statistical Software43(10)1ndash23
HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences107(19)8650ndash8655httpsdoiorg101073pnas0912668107
HartJ(2013a)WaterchevrotainHymemoschusaquaticusInJKingdonampMHoffmann (Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp88ndash92)LondonUKBloomsbury
Hart J (2013b) White‐bellied duiker Cephalophus leucogaster In JKingdonampMHoffmann(Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp255ndash258)LondonUKBloomsbury
HeadJSRobbinsMMMundryRMakagaLampBoeschC(2012)Remotevideo‐cameratrapsmeasurehabitatuseandcompetitiveex‐clusionamongsympatricchimpanzeegorillaandelephantinLoangoNational ParkGabon Journal of Tropical Ecology28(06) 571ndash583httpsdoiorg101017S0266467412000612
HedgesS(2012)Monitoring elephant populations and assessing threats HimayatnagarTelanganaUniversitiesPress
HedwigDKienastIBonnetMCurranBKCourageABoeschChellipKingT(2018)Acameratrapassessmentoftheforestmam‐mal community within the transitional savannah‐forest mosaic oftheBateacutekeacutePlateauNationalParkGabonAfrican Journal of Ecology56(4)777ndash790httpsdoiorg101111aje12497
emspensp emsp | emsp775Bruce et al
HijmansRJCameronSEParraJLJonesPGampJarvisA(2005)Very high resolution interpolated climate surfaces for global landareasInternational Journal of Climatology25(15)1965ndash1978httpsdoiorg101002joc1276
HuggelA(2012)Exiv2softwaretool[Computersoftware]Retrievedfromhttpswwwexiv2orgindexhtml
Jerozolimski A amp Peres C A (2003) Bringing home the biggestbacon A cross‐site analysis of the structure of hunter‐kill profilesin Neotropical forests Biological Conservation 111(3) 415ndash425httpsdoiorg101016S0006‐3207(02)00310‐5
KingdonJ (2015)The Kingdon field guide to African mammalsLondonUKBloomsburyPublishing
KuumlhlHFMaiselsMAncrenazampEAWilliamson(Eds)(2008)Best practice guidelines for surveys and monitoring of great ape populations GlandSwitzerlandIUCN
LauranceWFCroesBMTchignoumbaLLahmSAAlonsoALeeMEhellipOndzeanoC(2006)ImpactsofroadsandhuntingoncentralAfrican rainforestmammalsConservation Biology20(4)1251ndash1261httpsdoiorg101111j1523‐1739200600420x
LauranceWFUsecheDCRendeiroJKalkaMBradshawCJSloan S P hellip Arroyo‐Rodriguez V (2012) Averting biodiversitycollapse in tropical forestprotectedareasNature489(7415)290httpsdoiorg101038nature11318
LeslieDMampHuffmanBA(2015)Potamochoerus porcus(ArtiodactylaSuidae)Mammalian Species4715ndash31
MacKenzieD IampBailey L L (2004)Assessing the fit of site‐occu‐pancy models Journal of Agricultural Biological and Environmental Statistics9300ndash318httpsdoiorg101198108571104X3361
MacKenzieDINicholsJDRoyleJAPollockKHBaileyLLampHinesJE (2006)Occupancy estimation and modellingBurlingtonMAAcademicPress
Magurran A E (2005) Species abundance distributions Patternor process Functional Ecology 19(1) 177ndash181 httpsdoiorg101111j0269‐8463200500930x
MaiselsFStrindbergSBlakeSWittemyerGHartJWilliamsonEAhellipWarrenY (2013)DevastatingdeclineofforestelephantsinCentralAfricaPLoS ONE8(3)e59469httpsdoiorg101371journalpone0059469
MalhiYAdu‐BreduSAsareRA LewisS LampMayauxP (2013)AfricanrainforestsPastpresentandfuturePhilosophical Transactions of the Royal Society of London Biological Sciences 368(1625)20120312
MallonDPHoffmannMGraingerMJHibertFVanVlietNampMcGowanP JK (2015)An IUCNsituationanalysisof terrestrialandfreshwaterfaunainWestandCentralAfricaOccasionalpaperoftheIUCNspeciessurvivalcommission(54)
MambeyaMMBakerFMombouaBRKoumbaPamboAFHegaMOkouyiOkouyiVJhellipAbernethyK(2018)TheemergenceofacommercialtradeinpangolinsfromGabonAfrican Journal of Ecology56(3)601ndash609httpsdoiorg101111aje12507
MINFOFampIUCN(2015)CaracteacuterisationdelapopulationdegrandsetmoyensmammifegraveresdanslaReservedeFauneduDjaPotentieletmenacesYaoundeacuteCameroun
Muchaal P K amp Ngandjui G (1999) Impact of village hunt‐ing on wildlife populations in the western Dja ReserveCameroon Conservation Biology 13(2) 385ndash396 httpsdoiorg101046j1523‐17391999013002385x
NaranjoEJampBodmerRE (2007) Sourcendashsink systemsandconser‐vationofhuntedungulatesintheLacandonForestMexico Biological Conservation 138(3ndash4) 412ndash420 httpsdoiorg101016jbiocon 200705010
NielsenMR(2006)ImportancecauseandeffectofbushmeathuntingintheUdzungwaMountainsTanzania ImplicationsforcommunitybasedwildlifemanagementBiological Conservation128(4)509ndash516httpsdoiorg101016jbiocon200510017
OBrienTGKinnairdMFampWibisonoHT (2003)Crouching ti‐gers hiddenprey Sumatran tiger andprey populations in a tropi‐calforestlandscapeAnimal Conservation6(2)131ndash139httpsdoiorg101017S1367943003003172
OksanenJ(2015)VegananintroductiontoordinationVol8(p19)Retrieved from httpscranr‐projectorgwebpackagesveganvi‐gnettesintroveganpdf
PeresCAampPalaciosE(2007)Basin‐wideeffectsofgameharvestonvertebrate populationdensities inAmazonian forests Implicationsfor animal‐mediated seed dispersal Biotropica 39(3) 304ndash315httpsdoiorg101111j1744‐7429200700272x
PotapovPVTurubanovaSAHansenMCAduseiBBroichMAltstattAhellipJusticeCO(2012)QuantifyingforestcoverlossinDemocraticRepublicoftheCongo2000ndash2010withLandsatETM+data Remote Sensing of Environment 122 106ndash116 httpsdoiorg101016jrse201108027
PoulsenJRKoernerSEMooreSMedjibeVPBlakeSClarkC JhellipRosinC (2017) Poaching empties criticalCentralAfricanwilderness of forest elephants Current Biology 27(4) 134ndashR135httpsdoiorg101016jcub201701023
PurvisAGittlemanJlCowlishawGampMaceGM(2000)PredictingextinctionriskindecliningspeciesProceedings of the Royal Society B Biological Sciences267(1456) 1947ndash1952 httpsdoiorg101098rspb20001234
RayJ(1997)ComparativeecologyoftwoAfricanforestmongoosesHerpestesnasoandAtilaxpaludinosusAfrican Journal of Ecology35(3)237ndash253httpsdoiorg101111j1365‐20281997086‐ 89086x
Redford K H (1992) The empty forest BioScience 42(6) 412ndash422httpsdoiorg1023071311860
RepublicofCameroon(1994)Lawno9401du20janvier1994portantreacutegimedesforecirctsdelafauneetdelapecirccheRepublicofCameroon
RoveroFampMarshallAR(2009)CameratrappingphotographicrateasanindexofdensityinforestungulatesJournal of Applied Ecology46(5)1011ndash1017httpsdoiorg101111j1365‐2664200901705x
Royle J A amp Nichols J D (2003) Estimating abundance from re‐peated presence‐absence data or point counts Ecology 84(3)777ndash790 httpsdoiorg1018900012‐9658(2003)084[0777EAFRPA]20CO2
Seddon P J Griffiths C J Soorae P S ampArmstrongD P (2014)ReversingdefaunationRestoringspeciesinachangingworldScience345(6195)406ndash412httpsdoiorg101126science1251818
Silveira L Jacomo A T amp Diniz‐Filho J A F (2003) Camera trapline transect census and track surveys A comparative evaluationBiological Conservation 114(3) 351ndash355 httpsdoiorg101016S0006‐3207(03)00063‐6
Sonkeacute B (1998) Etudes floristiques et structurales des forecircts de laReacuteserve de Faune du Dja (Cameroun) Laboratoire de BotaniqueSysteacutematique et de Phytosociologie Universiteacute Libre de Bruxelles(ULB)
Srbek‐AraujoACampChiarelloAG(2005)Iscameratrappinganeffi‐cientmethodforsurveyingmammalsinNeotropicalforestsAcasestudyinsouth‐easternBrazilJournal of Tropical Ecology21(1)121ndash125httpsdoiorg101017S0266467404001956
Stiles D (2011) Elephant meat and ivory trade in Central AfricaPachyderm5026ndash36
TEAMNetwork(2008)Terrestrialvertebrateprotocol implementationmanualv30(p56)WashingtonDCTropicalEcologyAssessmentandMonitoringNetworkCenter forAppliedBiodiversity ScienceConservationInternational
Tobler M W Carrillo‐Percastegui S E Leite Pitman R MaresR amp Powell G (2008) An evaluation of camera traps for in‐ventorying large‐and medium‐sized terrestrial rainforestmammals Animal Conservation 11(3) 169ndash178 httpsdoiorg101111j1469‐1795200800169x
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
emspensp emsp | emsp767Bruce et al
trappingrateintheNorthernSector(Table1)butlackedsufficientdetectionstoreliablycalculateoccupancyAbundanceofCamerooncusimanse(Crossarchus platycephalusGoldman1984)didnotdiffersignificantlybetweenthetwosectors(NorthernSectorRAI=183[LCL=124 UCL=247 ψ=075] Southern Sector RAI=083[LCL=046UCL=127]ψ=056p=028)
36emsp|emspElephants great apes and giant pangolin (illegal wildlife trade targets)
Amongtheterrestrialmammalstargetedbytheillegalwildlifetradespecifically central chimpanzee (Pan troglodytes Blumenbachsubsp troglodytes 1799) western lowland gorilla (Gorilla gorillaSavagesubsp gorilla1847)forestelephantgiantpangolin(Smutsia gigantea Illiger 1815) and white‐bellied pangolin (Phataginus tri-cuspis Rafinesque 1821) only central chimpanzee displayed asignificant difference in RAI between the management sectors(Northern Sector RAI=161 [LCL=077 UCL=29] SouthernSector RAI=457 [LCL=314 UCL=617]) However there wasnosignificantdifferenceinmeanoccupancybetweenthetwosec‐tors (p=074) Giant pangolin displayed the greatest differencewithathreefoldincreaseinRAIfrom027[LCL=008UCL=052]in the Northern Sector to 068 [LCL=038 UCL=101] in theSouthernSectorbutthiswasnotsignificantduetotheoverlapping
confidencelimitsTheRAIsandwhereappropriateoccupancyofforestelephantwesternlowlandgorillaandwhite‐belliedpangolinwerenotsignificantlyhigher intheSouthernSectorcomparedtotheNorthernSector(Tables12and12)
37emsp|emspOther bushmeat‐targeted species
Eminrsquospouchedrat(Cricetomys eminiWroughton1910)wasmoreabundantasmeasuredbybothoccupancy(pge001)andtrapratesintheNorthernSectorcomparedtotheSouthernSector(Table1)Africanbrush‐tailedporcupine(Atherurus africanusGray1842)didnothavesignificantdifferencesinRAIbetweenthemanagementsectors but occupancywas significantly higher in theNorthernSector (pge004) In comparison the larger‐bodied red river hog(Potamochoerus porcus Linneaus1758)wasmore frequentlyen‐countered as measured by both species abundance metrics intheSouthernSector(RAI=7[LCL=336UCL=1304]ψ=091)compared to the Northern Sector (RAI=161 [LCL=102UCL=228]ψ=065(p=004)
38emsp|emspSpecies occupancy with covariates
Therewasatotalof15speciesthathadsufficientdetectionstomodeloccupancywithinteractingsitecovariates(distancetoparkboundary
F I G U R E 4 emspDistributionofmedium‐to‐largeterrestrialmammalspeciesintheSouthernSectoroftheDjaFaunalReserveCameroononthebasisofbodysizeandtrophiccategoryEachcirclerepresentsaspeciesinfunctionalspaceSizeofthecircleproportionaltothetrappingrateforthatspecies
768emsp |emsp emspensp Bruce et al
TAB
LE 2
emspNullmeanoccupancy(ψ)anddetection(p)probabilitieswithstandarderrorpresentedinbracketsfortheNorthernSectorandSouthernSector
Spec
ies
Nor
ther
n se
ctor
(ψ)
Nor
ther
n se
ctor
(p)
Sout
hern
sec
tor
(ψ)
Sout
hern
sec
tor
(p)
Mod
elBe
tamdash
Para
met
er
chos
enLo
wer
95
be
taU
pper
95
be
taC‐
hat v
alue
Chi‐s
quar
ep
valu
e
Certiodactyla
Batesrsquospygmy
antelope
022(01)
015(006)
[026]
ndashNull
ndashndash
ndashndash
ndash
Bayduiker
091(006)
04(003)
087(006)
04(003)
DRN
lam(DistanceSTD)
000
6356
808
043
3356
50
930
25
Black‐fronted
duiker
01(006)
036(01)
015(006)
025(008)
Null
ndashndash
ndashndash
ndash
Blueduiker
097(003)
082(002)
1(0)
1(0)
DRN
lam(DistanceSTD)
002
0135
490
3637
492
021
024
Petersrsquoduiker
083(007)
a056(003)
1(0)a
1(0)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus07435528
003
6592
430
004
03
Waterchevrotain
[007]
ndash04(008)
045(005)
ndashndash
ndashndash
ndashndash
White‐bellied
duiker
ndashndash
072(008)
031(003)
Null
ndashndash
ndashndash
ndash
Yellow‐backed
duiker
084(008)
027(003)
086(007)
039(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
010
8837
21
0251
104
069
021
Redriverhog
065(011)
a021(003)
091(006)
a033(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus12560347
minus01352547
027
044
Proboscidae
Forestelephant
067(015)
014(004)
063(013)
014(004)
Null
ndashndash
ndashndash
ndash
Primates
Central
chimpanzee
077(014)
015(004)
082(007)
035(003)
SRN
lam(sectorSouthern)
037
3686
91
4429
314
03
039
Westernlowland
goril
la[007]
ndash045(017)
01(004)
Null
ndashndash
ndashndash
ndash
Philodota
Giantpangolin
[02]
ndash061(016)
011(004)
Null
ndashndash
ndashndash
ndash
White‐bellied
pangolin
045(016)
012(005)
063(017)
011(003)
DSoccu
psi(DistanceSTDsec
torSouthern)
minus48425115
minus1910401
022
06
Rodentia
African
brush‐tailed
porcupine
098(003)
a057(003)
084(006)
a042(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus10008123
minus01586108
042
071
Eminrsquospouched
rat
1(0)a
1(0)
079(007)
a038(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus095574568
minus01390762
021
075
Carnivora
(Con
tinue
s)
emspensp emsp | emsp769Bruce et al
and management sector Table 2) Forest elephant black‐frontedduikerand long‐nosedmongoose (Herpestes nasodeWinton1901)lackedamodel thathadanAICdifferenceofgt2 therefore theco‐variatemodelswerenotsignificantlydifferent to thenullmodel forthese species Elevenof 15 species had aRoylendashNicholsmodel se‐lectedasthelowestAICvaluesuggestingadifferenceinthenumberofindividualswassignificantlyinfluencingdetectionprobabilitiesandthereforeoccupancy
RoylendashNichols models accounted for occupancy being signifi‐cantlyhigherindifferingmanagementsectorswithnointeractionofdistancetotheprotectedareaboundaryforthreespeciesCamerooncusimanse had higher occupancy in the Northern Sector In con‐trast central chimpanzee and black‐legged mongoose had signifi‐cantlyloweroccupancywithintheNorthernSectorcomparedtotheSouthernSector(Figure5)
African brush‐tailed porcupine Eminrsquos pouched rat and servalinegenet(Genetta servalinaPucheran1855)hadasynergisticRoylendashNicholsmodelselectedasthemostsupportedTheprobabilityofsiteoccupancyslightlyincreasedwithdistancetotheboundaryandwasoverallhigherin theNorthernSector butdeclinedwithdistance to theboundary intheSouthernSector(Figure6)BothPetersrsquoduikerandredriverhogalsodisplayedthispatternofoccupancybuthadamuchgreaterincreaseinoccupancyintheNorthernSectorandhadhigheroccupancyoverallintheSouthernSector(Figure6)Incontrastyellow‐backedduiker(Cephalophus silvicultorAfezilus1815)wastheonlyspeciestodemonstrateanincreaseinoccupancywithdistancetotheboundaryintheSouthernSectorwhiledecliningintheNorthernSectorHoweversimilartootherlargerspeciesoccupancywashigherintheSouthernSector(Figure6)
With regard to the remainingduiker speciesmodelled aRoylendashNicholsmodelwithdistancetotheprotectedareaboundarywasiden‐tifiedasthemostappropriateTheprobabilityofasitebeingoccupiedbyblueduikerandbayduikerincreasedwithdistancetotheboundarywith no discernible difference betweenmanagement sectors in themodel(Figure7)
White‐belliedpangolinhadasingle‐seasonoccupancymodelse‐lectedsuggestingdifferences inabundancebetweenthemanage‐mentsectorsdidnotaffectdetectionprobabilitiesTheprobabilityofasitebeingoccupiedbywhite‐belliedpangolin increasedintheNorthernSectoranddeclinedintheSouthernSectorwithincreasingdistancetotheboundary(Figure8)
Seven speciesweredetectedonly inone sectoror lacked suffi‐cientdetectionsinonesectortoreliablymodeloccupancyacrossbothmanagement sectors Therefore only the effect of distance to theboundarycouldbemodelledThesewereAfricangoldencatwesternlowlandgorillawhite‐belliedduikergiantpangolinAfricanpalmcivet(Nandinia binotata Gray 1830) Batesrsquos pygmy antelope and waterchevrotain (Hymeoschus aquaticusOgilby 1841)African palm civetwastheonlyspeciestohavedistancetotheboundaryselectedastheoptimummodel to explain occupancy as occupancy increasedwithdistance from the boundary of the protected area (Table 2)All theremainingspecieshadthenullmodelselectedastheoptimummodelaccordingtoAICcriteria (Table2)Howeverdistancetothebound‐arywaswithinlt2AICforthesespeciessuggestingthatasignificantSp
ecie
sN
orth
ern
sect
or (ψ
)N
orth
ern
sect
or (p
)So
uthe
rn s
ecto
r (ψ
)So
uthe
rn s
ecto
r (p
)M
odel
Beta
mdashPa
ram
eter
ch
osen
Low
er 9
5
beta
Upp
er 9
5
beta
C‐ha
t val
ueCh
i‐squ
arep
va
lue
Africangolden
cat
ndashndash
041(013)
013(004)
Null
ndashndash
ndashndash
ndash
Africanpalm
civet
[047]
ndash073(017)
012(003)
DOccu
psi(DistanceSTD)
minus8177158
Inf
197
008
Black‐legged
mongoose
047(01)a
025(004)
082(008)
a031(003)
SRN
lam(sectorSouthern)
028
0266
31
4627
420
011
058
Cameroon
cusimanse
075(009)
027(004)
056(015)
012(004)
SRN
lam(sectorSouthern)
minus1808131
minus05098939
005
073
Long‐nosed
mongoose
055(012)
a02(004)
015(006)
a027(007)
Null
ndashndash
ndashndash
ndash
Servalinegenet
092(006)
035(003)
08(009)
02(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus09202819
003
5821
570
50
26
Not
esNaiumlveoccupancyvaluesarepresentedinsquarebracketsforspecieswithadetectionprobabilitylt01TheoptimummodelchosenbyAkaikersquosinformationcriteriaforeachspeciesgeneratingsuf‐
ficientoccupancyvaluesinbothsectorswiththeBetaparameteranditisrespectivelowerandupper95confidencelimitsisshownandtheassociatedc‐hatandchi‐squaredp
val
ue
DdistancetoboundarySmanagementsectorRNRoylendashNicholsmodelOccuMckenziesingle‐seasonoccupancymodesynergisticinteraction
a IndicatesasignificantdifferenceinoccupancybetweensectorsasmeasuredbytheWaldteststatistic
TAB
LE 2
emsp(Continued)
770emsp |emsp emspensp Bruce et al
relationshipwithdistancetotheboundarycouldbeinfluencingoccu‐pancyIntheSouthernSectortheoccupancyincreasedwithdistanceto theboundary forwestern lowlandgorillaandgiantpangolinbutdecreasedforAfricangoldencatwhite‐belliedduikerandwaterchev‐rotainIntheNorthernSectoroccupancyincreasedwithdistancetotheboundaryforBatesrsquospygmyantelope
4emsp |emspDISCUSSION
Thecomparisonofthetwosurveysconfirmsthatstandardcameratrap surveys and derived metrics of presenceabsence trappingrates andoccupancy candiscern confidentdifferences in ground‐dwellingmammalcommunitiesinCentralAfricanforests
41emsp|emspCamera trap surveys for documenting species
Thecomparativeefficacyofcamera traps for surveyingmediumto large ground‐dwelling mammals in the DFR is indicated byobservationratesandverifiabilityofrecordsespeciallyofelusivesmallerandnocturnalspeciesForexamplethedirectencounterraterecordedbyrangersonpatrolthroughouttheentirereserveover a nine‐month period is much lower than the combinednumberofindependentphotographiceventsinbothmanagementsectors (ZSL amp MINFOF 2017b) even for relatively largeconspicuous species such as forest elephant (96 photographiceventscomparedto29directencounters)andcentralchimpanzee(204 independent photographic events compared to 23 directencounters)Methodologiessuchascameratrapping therefore
provideimportantbaselinedatathatwhenrepeatedthroughtimeusingastandardisedprotocolcanallowatleasttrendsinrelativeabundanceindicestobemonitored
42emsp|emspCamera trap surveys for comparing assemblages among sites
Despitebeingseparatedbyonlyc32kmthemammalcommunitiesbetween the twocamera trapgridsdisplayedmarkeddifferencesThiswasthecaseeventhoughbothgridshadlowShannonndashWeinerandSimpsonsdiversityindicesduetothedominanceofthreeorfourspeciesineachcameratrapgridSignificantdifferencesamongthesiteswere observed for the trapping rates of species of differentsizesbetweensectorsSmaller‐bodiedspecieswithintheherbivoreand omnivore guilds were more prevalent within the NorthernSector (Figure 2) Trapping rates and occupancy values for smallcarnivoresarealsolowerintheSouthernSectorThiscouldbeduetothedifficultyofidentifyingmorphologicallysimilarspeciessuchasmarshmongooseandlong‐nosedmongoose(Bahaa‐el‐dinetal2013 Ray 1997) in infrared imagery with single cameras Thereweremoreunidentifiablemongooseeventsthatwereclassifiedtoafamilylevel―66224intheSouthernSectorcomparedto29156intheNorthernSectorofallcombinedmongooseevents
43emsp|emspThe potential impact of seasonality on estimates derived from camera traps
Due to logistical and financial constraints the surveys could notberuninthesameseasonThishasthepotentialtoaffecttrapping
F I G U R E 5 emspChangeintheprobabilityofoccupancyforblack‐leggedmongoosecentralchimpanzeeandCamerooncusimansewithmanagementsectoraccordingtoaRoylendashNicholsmodel
emspensp emsp | emsp771Bruce et al
rates and occupancy for specieswith larger home ranges becausewhenspeciesarewide‐rangingoccupancycanproveineffectiveformeasuring relative abundance Forest elephants (Blake 2002) andgreatapesareknowntodisplayseasonalshiftsintheirhabitatusageover great distances in response to increased fruit availability andprecipitation(HeadRobbinsMundryMakagaampBoesch2012)Thiscouldalsoinfluenceothergregariousspeciessuchasredriverhogthatarealsothoughttooccasionallydisplaysimilaraggregationsandmovementsinresponsetomastingevents(LeslieampHuffman2015)However as both red river hog and chimpanzee had significantlyhigherRAIandhigheroccupancywithvariabledetectionprobabilityaccording to the number of individuals incorporated this supports
thepossibilitythatthesespeciesarefavouringtheSouthernSectorIfmanagersareable toestablishwhetherwide‐rangingspeciesarepredictably moving to known areas within the reserve they canrespondinamannerthatprovidesenhancedprotectiontovulnerablewildlifepopulations in concentration areasAsmost species in thissurveylikelyhaveasmallerhomerangethantheinter‐trapdistanceand display fixed territories it can be regarded as appropriate tocompare occupancy values as the extent of overlap of territorieswithin the two surveys are unlikely to change in such away as toaffecttheresultsFuturestudieswouldbenefitfromtryingtomatchcameratrapsurveysseasonallytotryandclarifytheissueofseasonalshiftsinhabitatusagewithintheDFR
F I G U R E 6 emspChangeintheprobabilityofoccupancyforAfricanbrush‐tailedporcupineEminspouchedratredriverhogservalinegenetPetersrsquoduikerandyellow‐backedduikerwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
772emsp |emsp emspensp Bruce et al
F I G U R E 7 emspChangeintheprobabilityofoccupancyforblueduikerandbayduikerwithdistancetotheboundaryinkilometresacrossbothmanagementsectorsaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
F I G U R E 8 emspChangeintheprobabilityofoccupancyforwhite‐belliedpangolinwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaMackenzieoccupancymodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
emspensp emsp | emsp773Bruce et al
44emsp|emspCamera trap surveys for measuring the impacts of hunting on mammal communities
The spatial scale at which mammal communities are affected byandhowpopulationsrespondtoanthropogenicpressuressuchasbushmeat hunting is difficult to empiricallymeasure (Laurance etal2006)Thisisespeciallytrueformammalsresidingwithintropi‐cal forestswheregatheringconsistentandmeaningfulpopulation‐andcommunity‐levelmetrics ischallenging(Ahumadaetal2013)Population density of tropical mammals can vary greatly due toheterogeneity present within the environment For example for‐est elephants havedifferent distributions and aggregations inwetanddryseasonsinNouabaleacute‐Ndoki NationalParkwhichispartiallydependentonspatio‐temporalpatternsoffruitingtreesacrossthelandscape(Blake2002)
Whether the differences observed among the two sites sur‐veyedhereareattributabletodifferent levelsofhuntingpressureremains to be confirmed There are however indications thathuntingpressureanditsimpactsonmammalfaunasaregreaterintheNorthern Sector than in the Southern Sector The effects ofhuntingpressureonmammaliandeclinesinCentralAfricanforestsarewell documented The pattern in general is the largest‐bod‐ied species frugivores and thosewith high hunter or blackmar‐ketvalue(Abernethyetal2013Cardilloetal2005FaOliveroFarfaacutenMaacuterquezDuarteetal2014aFaOliveroFarfaacutenMaacuterquezVargasetal2014bPeresampPalacios2007)arethefirstspeciestoshownoticeabledeclineInthisstudythesignificantdeclineintherelativeabundance for frugivores suchasPetersʼduikerandspe‐cieswithhighhuntervalueliketheredriverhogunderincreasedhuntingpressure in theNorthernSector is reported inother sur‐veys(Abernethyetal2013)Thisisalsoreflectedinthedifferencesobserved in this study in biomass in the different guilds of eachmammalcommunityThemammalcommunitywithintheNorthernSector shows indications of a community that is disturbed and isexperiencingelevatedhuntingpressureThesearehigher(camera)trapping rates for smaller‐bodiedspecies suchasEminrsquospouchedrat and significantly fewer encounters of larger‐bodiedmammalsthataretargetsofthebushmeattradesuchasPetersʼduikerandredriverhog(FaRyanampBell2005JerozolimskiampPeres2003)Additionalindicatorsaretheabsenceinthesurveysoflargercarni‐voresintheNorthernSectorsuchasgoldencatandleopardwhicharesensitivetosnaring(Bahaa‐el‐dinetal2015)andsignificantlyreducedabundancemetricsfordisturbance‐sensitivespeciessuchasblack‐leggedmongooseandwaterchevrotain(Hart2013a)Theabsence of white‐bellied duiker in the Northern Sector also sug‐gestselevatedhumandisturbanceasthisspecieshasbeenreportedasverysensitivetoevenminorperturbationwithintheenvironment(Hart2013b)IncomparisontheSouthernSectorcontainedindica‐torfaunasuchasthewhite‐belliedduikerandhadhighertrappingratesforlarger‐bodiedspecies
WesuspectthedifferencesobservedaremostlikelyduetolowerhumandisturbanceintheSouthernSectorTheteamsdeployingand
recoveringthecamerasintheSouthernSectorcovered238kmandencountered few signs of humanperturbation (T Brucepers obs)whereashumansignwascommonlyencounteredbytheteamsintheNorthernSectorThisperceiveddifference is reflected in the2017and 2018 density of hunting signwithin each camera trap grid asdetected throughMINFOF ranger patrols (ZSL ampMINFOF 2017a2017b) and through the2018DistanceSampling inventory for theDFR (Bruce et al 2018) Higher numbers of hunting sign in theNorthernSectorwouldbeconsistentwithanelevatedhuntingpres‐sureinthatarea
45emsp|emspProtection of refugia from hunting
Though inferences made for wide‐ranging species such as forestelephantsandgreatapesusingcameratrapsaredifficultthefactthattrappingrateswerehigherinmorechallengingterrainwithassumedlower hunting pressure could be indicative of complex habitatprovidingsomelevelofprotectionfromhuntingElephantisknownto retreatwhen they aredisturbed to terrain that ismoredifficulttoaccessbyhumans (Hedges2012)Thuswithin largerprotectedareas certain zones may act as refugia for wildlife populations(Campbelletal2011)Thiscanbeduetoarangeof factorssuchas remoteanddifficult terrain forpoachers (Attum2007Hedges2012) or the regular presence of field researchers and rangers(Campbell et al 2011) The significanceof these refugia for largerprotected areas is that the populations of wildlife residing withinthem if adequately protected may provide source populations toallowrecolonisationofotherareasofthereserve(NaranjoampBodmer2007)Thereforeifadequateprotectioncanbeprovidedtorelativelysmallbutimportantareasoflargereservesthismayprovidetropicalforestswithabetterchanceofbeingecologicallyresilienttoongoingand increasing human perturbation Well‐designed camera trapsurveys may provide data on the status of wildlife populations atrelativelyfinespatialresolutionssoastoidentifyfunctionalrefugiawithgreaterconfidence
ACKNOWLEDG EMENTS
WeappreciatetheongoingsupportofCameroonrsquosMinistryofForestsandWildlife(MINFOF)andtheopportunitytocontributetobiodiver‐sityconservationthroughoutthecountryInparticularwewouldliketothanktheChefdrsquoAntenneSergeJacobMeyeforhisongoingsup‐portofconservationresearchwithintheprotectedareaWeappreci‐atethestalwarteffortsofMINFOFecoguardsandlocalporterswhoaccompaniedthesurveyteamsinthefieldWewouldalsoliketothanktheUnitedStatesFishandWildlifeService(USFWS)mdashAfricanElephantConservationandIUCNSOSmdashFondationSegreacutePangolinConservationInitiativeforsupportingthiswork
ORCID
Tom Bruce httporcidorg0000‐0001‐6958‐1657
774emsp |emsp emspensp Bruce et al
R E FE R E N C E S
AbernethyKACoad L TaylorG LeeMEampMaisels F (2013)Extent and ecological consequences of hunting in Central Africanrainforests in thetwenty‐firstcenturyPhilosophical Transactions of the Royal Society of London Biological Sciences368(1625)20120303httpsdoiorg101098rstb20120303
AbrahamsM I Peres C A amp Costa H C (2017)Measuring localdepletion of terrestrial game vertebrates by central‐place hunt‐ers in rural Amazonia PLoS ONE 12(10) e0186653 httpsdoiorg101371journalpone0186653
AhumadaJAHurtadoJampLizcanoD(2013)MonitoringthestatusandtrendsoftropicalforestterrestrialvertebratecommunitiesfromcameratrapdataAtool forconservationPLoS ONE8(9)e73707httpsdoiorg101371journalpone0073707
Ahumada J A Silva C E Gajapersad K Hallam C Hurtado JMartin E hellip Sheil D (2011) Community structure and diver‐sity of tropical forest mammals Data from a global camera trapnetwork Philosophical Transactions of the Royal Society of London Biological Sciences366(1578)2703ndash2711httpsdoiorg101098rstb20110115
AminRAndanjeSAOgwonkaBAliAHBowkettAEOmarMampWacherT(2015)ThenortherncoastalforestsofKenyaarenationally and globally important for the conservation of AdersrsquoduikerCephalophusadersiandotherantelopespeciesBiodiversity and Conservation 24(3) 641ndash658 httpsdoiorg101007s10531‐014‐0842‐z
Attum O (2007) Can landscape use be among the factors that po‐tentiallymake some ungulates speciesmore difficult to conserveJournal of Arid Environments69(3)410ndash419
Bahaa‐el‐dinLHenschelPAbaaRAbernethyKBohmTBoutNhellipLeeM (2013)NotesonthedistributionandstatusofsmallcarnivoresinGabonSmall Carnivore Conservation4819ndash29
Bahaa‐el‐dinLHenschelPButynskiTMMacdonaldDWMillsDSlotowRampHunterL (2015)TheAfricangoldencatCaracalaurataAfricasleast‐knownfelidMammal Review45(1)63ndash77
Bennett E L Blencowe E Brandon K Brown D Burn R WCowlishaw G hellip Robinson J G (2007) Hunting for consensusReconcilingbushmeatharvestconservationanddevelopmentpol‐icyinWestandCentralAfricaConservation Biology21(3)884ndash887httpsdoiorg101111j1523‐1739200600595x
BlakeSDeemSLMossimboEMaiselsFampWalshP(2009)Forestelephants Tree planters of the CongoBiotropica41(4) 459ndash468httpsdoiorg101111j1744‐7429200900512x
Blake S (2002) The ecology of forest elephant distribution and itsimplications for conservation Doctoral dissertation University ofEdinburgh
BruceTNdjassiCFowlerANdimbeMFankemOTabueRhellipOlsonD(2018)Faunal inventory of the Dja Faunal Reserve Cameroon Yaoundeacute Cameroon Ministry of Forests and Wildlife (MINFOF)Zoological Society of London ndash Cameroon Country ProgrammeAfricanWildlifeFoundation
BruceTWacherTNdingaHBidjokaVMeyongFNgoBataMampOlsonD(2017)camera trap survey for larger terrestrial wildlife in the Dja Biosphere Reserve CameroonYaoundeacuteCameroonZoologicalSocietyofLondon(ZSL)ampCameroonMinistryofForestsandWildlife(MINFOF)
BurnhamKPampAndersonDR(2002)Model selection and multimodel inferenceNewYorkNYSpringer
Campbell G Kuehl H Diarrassouba A NGoran P K amp BoeschC (2011) Long‐term research sites as refugia for threatened andover‐harvested species Biology Letters 7(5) 723ndash726 httpsdoiorg101098rsbl20110155
CardilloMMaceGMJonesKEBielbyJBininda‐EmondsORSechrestWhellipPurvisA(2005)Multiplecausesofhighextinction
riskinlargemammalspeciesScience309(5738)1239ndash1241httpsdoiorg101126science1116030
Craigie IDBaillieJEBalmfordACarboneCCollenBGreenREampHuttonJM (2010)Largemammalpopulationdeclines inAfricarsquosprotectedareasBiological Conservation143(9)2221ndash2228httpsdoiorg101016jbiocon201006007
DaveyKWacherTampAminR(2017)Analysis tool for camera-trap sur-vey data [Computer software]ZoologicalSocietyofLondonRetrievedfromhttpswwwzslorgzsl‐camera‐trap‐data‐management‐ and‐analysis‐package
Djuikouo M N K Doucet J L Nguembou C K Lewis S L ampSonkeacute B (2010) Diversity and aboveground biomass in threetropical forest types in the Dja Biosphere Reserve Cameroon African Journal of Ecology 48(4) 1053ndash1063 httpsdoiorg101111j1365‐2028201001212x
DupainJBombomeKampVanElsackerL(2003)LeschimpanzeacutesetlesgorillesdelareacuteservedefauneduDjaCanopeacutee2414ndash15
EffordMGampDawsonDK(2012)OccupancyincontinuoushabitatEcosphere3(4)1ndash15httpsdoiorg101890ES11‐003081
Efron B amp Tibshirani R J (1994) An introduction to the bootstrap WashingtonDCCRCPress
FaJEOliveroJFarfaacutenMAacuteMaacuterquezALDuarteJNackoneyJhellipMacdonaldDW(2014a)CorrelatesofbushmeatinmarketsanddepletionofwildlifeConservation Biology29(3)805ndash815
Fa J EOlivero J FarfaacutenMAacuteMaacuterquezA LVargas JMRealRampNasiR(2014b)IntegratingsustainablehuntinginbiodiversityprotectioninCentralAfricaHotspotsweakspotsandstrongspotsPLoS ONE9(11)e112367
FaJERyanSFampBellDJ (2005)Huntingvulnerabilityecolog‐ical characteristics and harvest rates of bushmeat species in afro‐tropicalforestsBiological Conservation121(2)167ndash176httpsdoiorg101016jbiocon200404016
Fa J E Seymour S Dupain J E F Amin R Albrechtsen L ampMacdonaldD (2006) Getting to gripswith themagnitude of ex‐ploitationBushmeat in theCross‐SanagariversregionNigeria and Cameroon Biological Conservation 129(4) 497ndash510 httpsdoiorg101016jbiocon200511031
Farris Z J Boone H M Karpanty S Murphy A Ratelolahy FAndrianjakariveloVampKellyMJ(2015)FeralcatsandthefitoatyFirstpopulationassessmentoftheblackforestcatinMadagascarrsquosrainforestsJournal of Mammalogy97(2)518ndash525
Fiske IampChandlerR (2011)UnmarkedAnRpackageforfittinghi‐erarchicalmodelsofwildlifeoccurrenceandabundanceJournal of Statistical Software43(10)1ndash23
HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences107(19)8650ndash8655httpsdoiorg101073pnas0912668107
HartJ(2013a)WaterchevrotainHymemoschusaquaticusInJKingdonampMHoffmann (Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp88ndash92)LondonUKBloomsbury
Hart J (2013b) White‐bellied duiker Cephalophus leucogaster In JKingdonampMHoffmann(Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp255ndash258)LondonUKBloomsbury
HeadJSRobbinsMMMundryRMakagaLampBoeschC(2012)Remotevideo‐cameratrapsmeasurehabitatuseandcompetitiveex‐clusionamongsympatricchimpanzeegorillaandelephantinLoangoNational ParkGabon Journal of Tropical Ecology28(06) 571ndash583httpsdoiorg101017S0266467412000612
HedgesS(2012)Monitoring elephant populations and assessing threats HimayatnagarTelanganaUniversitiesPress
HedwigDKienastIBonnetMCurranBKCourageABoeschChellipKingT(2018)Acameratrapassessmentoftheforestmam‐mal community within the transitional savannah‐forest mosaic oftheBateacutekeacutePlateauNationalParkGabonAfrican Journal of Ecology56(4)777ndash790httpsdoiorg101111aje12497
emspensp emsp | emsp775Bruce et al
HijmansRJCameronSEParraJLJonesPGampJarvisA(2005)Very high resolution interpolated climate surfaces for global landareasInternational Journal of Climatology25(15)1965ndash1978httpsdoiorg101002joc1276
HuggelA(2012)Exiv2softwaretool[Computersoftware]Retrievedfromhttpswwwexiv2orgindexhtml
Jerozolimski A amp Peres C A (2003) Bringing home the biggestbacon A cross‐site analysis of the structure of hunter‐kill profilesin Neotropical forests Biological Conservation 111(3) 415ndash425httpsdoiorg101016S0006‐3207(02)00310‐5
KingdonJ (2015)The Kingdon field guide to African mammalsLondonUKBloomsburyPublishing
KuumlhlHFMaiselsMAncrenazampEAWilliamson(Eds)(2008)Best practice guidelines for surveys and monitoring of great ape populations GlandSwitzerlandIUCN
LauranceWFCroesBMTchignoumbaLLahmSAAlonsoALeeMEhellipOndzeanoC(2006)ImpactsofroadsandhuntingoncentralAfrican rainforestmammalsConservation Biology20(4)1251ndash1261httpsdoiorg101111j1523‐1739200600420x
LauranceWFUsecheDCRendeiroJKalkaMBradshawCJSloan S P hellip Arroyo‐Rodriguez V (2012) Averting biodiversitycollapse in tropical forestprotectedareasNature489(7415)290httpsdoiorg101038nature11318
LeslieDMampHuffmanBA(2015)Potamochoerus porcus(ArtiodactylaSuidae)Mammalian Species4715ndash31
MacKenzieD IampBailey L L (2004)Assessing the fit of site‐occu‐pancy models Journal of Agricultural Biological and Environmental Statistics9300ndash318httpsdoiorg101198108571104X3361
MacKenzieDINicholsJDRoyleJAPollockKHBaileyLLampHinesJE (2006)Occupancy estimation and modellingBurlingtonMAAcademicPress
Magurran A E (2005) Species abundance distributions Patternor process Functional Ecology 19(1) 177ndash181 httpsdoiorg101111j0269‐8463200500930x
MaiselsFStrindbergSBlakeSWittemyerGHartJWilliamsonEAhellipWarrenY (2013)DevastatingdeclineofforestelephantsinCentralAfricaPLoS ONE8(3)e59469httpsdoiorg101371journalpone0059469
MalhiYAdu‐BreduSAsareRA LewisS LampMayauxP (2013)AfricanrainforestsPastpresentandfuturePhilosophical Transactions of the Royal Society of London Biological Sciences 368(1625)20120312
MallonDPHoffmannMGraingerMJHibertFVanVlietNampMcGowanP JK (2015)An IUCNsituationanalysisof terrestrialandfreshwaterfaunainWestandCentralAfricaOccasionalpaperoftheIUCNspeciessurvivalcommission(54)
MambeyaMMBakerFMombouaBRKoumbaPamboAFHegaMOkouyiOkouyiVJhellipAbernethyK(2018)TheemergenceofacommercialtradeinpangolinsfromGabonAfrican Journal of Ecology56(3)601ndash609httpsdoiorg101111aje12507
MINFOFampIUCN(2015)CaracteacuterisationdelapopulationdegrandsetmoyensmammifegraveresdanslaReservedeFauneduDjaPotentieletmenacesYaoundeacuteCameroun
Muchaal P K amp Ngandjui G (1999) Impact of village hunt‐ing on wildlife populations in the western Dja ReserveCameroon Conservation Biology 13(2) 385ndash396 httpsdoiorg101046j1523‐17391999013002385x
NaranjoEJampBodmerRE (2007) Sourcendashsink systemsandconser‐vationofhuntedungulatesintheLacandonForestMexico Biological Conservation 138(3ndash4) 412ndash420 httpsdoiorg101016jbiocon 200705010
NielsenMR(2006)ImportancecauseandeffectofbushmeathuntingintheUdzungwaMountainsTanzania ImplicationsforcommunitybasedwildlifemanagementBiological Conservation128(4)509ndash516httpsdoiorg101016jbiocon200510017
OBrienTGKinnairdMFampWibisonoHT (2003)Crouching ti‐gers hiddenprey Sumatran tiger andprey populations in a tropi‐calforestlandscapeAnimal Conservation6(2)131ndash139httpsdoiorg101017S1367943003003172
OksanenJ(2015)VegananintroductiontoordinationVol8(p19)Retrieved from httpscranr‐projectorgwebpackagesveganvi‐gnettesintroveganpdf
PeresCAampPalaciosE(2007)Basin‐wideeffectsofgameharvestonvertebrate populationdensities inAmazonian forests Implicationsfor animal‐mediated seed dispersal Biotropica 39(3) 304ndash315httpsdoiorg101111j1744‐7429200700272x
PotapovPVTurubanovaSAHansenMCAduseiBBroichMAltstattAhellipJusticeCO(2012)QuantifyingforestcoverlossinDemocraticRepublicoftheCongo2000ndash2010withLandsatETM+data Remote Sensing of Environment 122 106ndash116 httpsdoiorg101016jrse201108027
PoulsenJRKoernerSEMooreSMedjibeVPBlakeSClarkC JhellipRosinC (2017) Poaching empties criticalCentralAfricanwilderness of forest elephants Current Biology 27(4) 134ndashR135httpsdoiorg101016jcub201701023
PurvisAGittlemanJlCowlishawGampMaceGM(2000)PredictingextinctionriskindecliningspeciesProceedings of the Royal Society B Biological Sciences267(1456) 1947ndash1952 httpsdoiorg101098rspb20001234
RayJ(1997)ComparativeecologyoftwoAfricanforestmongoosesHerpestesnasoandAtilaxpaludinosusAfrican Journal of Ecology35(3)237ndash253httpsdoiorg101111j1365‐20281997086‐ 89086x
Redford K H (1992) The empty forest BioScience 42(6) 412ndash422httpsdoiorg1023071311860
RepublicofCameroon(1994)Lawno9401du20janvier1994portantreacutegimedesforecirctsdelafauneetdelapecirccheRepublicofCameroon
RoveroFampMarshallAR(2009)CameratrappingphotographicrateasanindexofdensityinforestungulatesJournal of Applied Ecology46(5)1011ndash1017httpsdoiorg101111j1365‐2664200901705x
Royle J A amp Nichols J D (2003) Estimating abundance from re‐peated presence‐absence data or point counts Ecology 84(3)777ndash790 httpsdoiorg1018900012‐9658(2003)084[0777EAFRPA]20CO2
Seddon P J Griffiths C J Soorae P S ampArmstrongD P (2014)ReversingdefaunationRestoringspeciesinachangingworldScience345(6195)406ndash412httpsdoiorg101126science1251818
Silveira L Jacomo A T amp Diniz‐Filho J A F (2003) Camera trapline transect census and track surveys A comparative evaluationBiological Conservation 114(3) 351ndash355 httpsdoiorg101016S0006‐3207(03)00063‐6
Sonkeacute B (1998) Etudes floristiques et structurales des forecircts de laReacuteserve de Faune du Dja (Cameroun) Laboratoire de BotaniqueSysteacutematique et de Phytosociologie Universiteacute Libre de Bruxelles(ULB)
Srbek‐AraujoACampChiarelloAG(2005)Iscameratrappinganeffi‐cientmethodforsurveyingmammalsinNeotropicalforestsAcasestudyinsouth‐easternBrazilJournal of Tropical Ecology21(1)121ndash125httpsdoiorg101017S0266467404001956
Stiles D (2011) Elephant meat and ivory trade in Central AfricaPachyderm5026ndash36
TEAMNetwork(2008)Terrestrialvertebrateprotocol implementationmanualv30(p56)WashingtonDCTropicalEcologyAssessmentandMonitoringNetworkCenter forAppliedBiodiversity ScienceConservationInternational
Tobler M W Carrillo‐Percastegui S E Leite Pitman R MaresR amp Powell G (2008) An evaluation of camera traps for in‐ventorying large‐and medium‐sized terrestrial rainforestmammals Animal Conservation 11(3) 169ndash178 httpsdoiorg101111j1469‐1795200800169x
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
768emsp |emsp emspensp Bruce et al
TAB
LE 2
emspNullmeanoccupancy(ψ)anddetection(p)probabilitieswithstandarderrorpresentedinbracketsfortheNorthernSectorandSouthernSector
Spec
ies
Nor
ther
n se
ctor
(ψ)
Nor
ther
n se
ctor
(p)
Sout
hern
sec
tor
(ψ)
Sout
hern
sec
tor
(p)
Mod
elBe
tamdash
Para
met
er
chos
enLo
wer
95
be
taU
pper
95
be
taC‐
hat v
alue
Chi‐s
quar
ep
valu
e
Certiodactyla
Batesrsquospygmy
antelope
022(01)
015(006)
[026]
ndashNull
ndashndash
ndashndash
ndash
Bayduiker
091(006)
04(003)
087(006)
04(003)
DRN
lam(DistanceSTD)
000
6356
808
043
3356
50
930
25
Black‐fronted
duiker
01(006)
036(01)
015(006)
025(008)
Null
ndashndash
ndashndash
ndash
Blueduiker
097(003)
082(002)
1(0)
1(0)
DRN
lam(DistanceSTD)
002
0135
490
3637
492
021
024
Petersrsquoduiker
083(007)
a056(003)
1(0)a
1(0)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus07435528
003
6592
430
004
03
Waterchevrotain
[007]
ndash04(008)
045(005)
ndashndash
ndashndash
ndashndash
White‐bellied
duiker
ndashndash
072(008)
031(003)
Null
ndashndash
ndashndash
ndash
Yellow‐backed
duiker
084(008)
027(003)
086(007)
039(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
010
8837
21
0251
104
069
021
Redriverhog
065(011)
a021(003)
091(006)
a033(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus12560347
minus01352547
027
044
Proboscidae
Forestelephant
067(015)
014(004)
063(013)
014(004)
Null
ndashndash
ndashndash
ndash
Primates
Central
chimpanzee
077(014)
015(004)
082(007)
035(003)
SRN
lam(sectorSouthern)
037
3686
91
4429
314
03
039
Westernlowland
goril
la[007]
ndash045(017)
01(004)
Null
ndashndash
ndashndash
ndash
Philodota
Giantpangolin
[02]
ndash061(016)
011(004)
Null
ndashndash
ndashndash
ndash
White‐bellied
pangolin
045(016)
012(005)
063(017)
011(003)
DSoccu
psi(DistanceSTDsec
torSouthern)
minus48425115
minus1910401
022
06
Rodentia
African
brush‐tailed
porcupine
098(003)
a057(003)
084(006)
a042(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus10008123
minus01586108
042
071
Eminrsquospouched
rat
1(0)a
1(0)
079(007)
a038(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus095574568
minus01390762
021
075
Carnivora
(Con
tinue
s)
emspensp emsp | emsp769Bruce et al
and management sector Table 2) Forest elephant black‐frontedduikerand long‐nosedmongoose (Herpestes nasodeWinton1901)lackedamodel thathadanAICdifferenceofgt2 therefore theco‐variatemodelswerenotsignificantlydifferent to thenullmodel forthese species Elevenof 15 species had aRoylendashNicholsmodel se‐lectedasthelowestAICvaluesuggestingadifferenceinthenumberofindividualswassignificantlyinfluencingdetectionprobabilitiesandthereforeoccupancy
RoylendashNichols models accounted for occupancy being signifi‐cantlyhigherindifferingmanagementsectorswithnointeractionofdistancetotheprotectedareaboundaryforthreespeciesCamerooncusimanse had higher occupancy in the Northern Sector In con‐trast central chimpanzee and black‐legged mongoose had signifi‐cantlyloweroccupancywithintheNorthernSectorcomparedtotheSouthernSector(Figure5)
African brush‐tailed porcupine Eminrsquos pouched rat and servalinegenet(Genetta servalinaPucheran1855)hadasynergisticRoylendashNicholsmodelselectedasthemostsupportedTheprobabilityofsiteoccupancyslightlyincreasedwithdistancetotheboundaryandwasoverallhigherin theNorthernSector butdeclinedwithdistance to theboundary intheSouthernSector(Figure6)BothPetersrsquoduikerandredriverhogalsodisplayedthispatternofoccupancybuthadamuchgreaterincreaseinoccupancyintheNorthernSectorandhadhigheroccupancyoverallintheSouthernSector(Figure6)Incontrastyellow‐backedduiker(Cephalophus silvicultorAfezilus1815)wastheonlyspeciestodemonstrateanincreaseinoccupancywithdistancetotheboundaryintheSouthernSectorwhiledecliningintheNorthernSectorHoweversimilartootherlargerspeciesoccupancywashigherintheSouthernSector(Figure6)
With regard to the remainingduiker speciesmodelled aRoylendashNicholsmodelwithdistancetotheprotectedareaboundarywasiden‐tifiedasthemostappropriateTheprobabilityofasitebeingoccupiedbyblueduikerandbayduikerincreasedwithdistancetotheboundarywith no discernible difference betweenmanagement sectors in themodel(Figure7)
White‐belliedpangolinhadasingle‐seasonoccupancymodelse‐lectedsuggestingdifferences inabundancebetweenthemanage‐mentsectorsdidnotaffectdetectionprobabilitiesTheprobabilityofasitebeingoccupiedbywhite‐belliedpangolin increasedintheNorthernSectoranddeclinedintheSouthernSectorwithincreasingdistancetotheboundary(Figure8)
Seven speciesweredetectedonly inone sectoror lacked suffi‐cientdetectionsinonesectortoreliablymodeloccupancyacrossbothmanagement sectors Therefore only the effect of distance to theboundarycouldbemodelledThesewereAfricangoldencatwesternlowlandgorillawhite‐belliedduikergiantpangolinAfricanpalmcivet(Nandinia binotata Gray 1830) Batesrsquos pygmy antelope and waterchevrotain (Hymeoschus aquaticusOgilby 1841)African palm civetwastheonlyspeciestohavedistancetotheboundaryselectedastheoptimummodel to explain occupancy as occupancy increasedwithdistance from the boundary of the protected area (Table 2)All theremainingspecieshadthenullmodelselectedastheoptimummodelaccordingtoAICcriteria (Table2)Howeverdistancetothebound‐arywaswithinlt2AICforthesespeciessuggestingthatasignificantSp
ecie
sN
orth
ern
sect
or (ψ
)N
orth
ern
sect
or (p
)So
uthe
rn s
ecto
r (ψ
)So
uthe
rn s
ecto
r (p
)M
odel
Beta
mdashPa
ram
eter
ch
osen
Low
er 9
5
beta
Upp
er 9
5
beta
C‐ha
t val
ueCh
i‐squ
arep
va
lue
Africangolden
cat
ndashndash
041(013)
013(004)
Null
ndashndash
ndashndash
ndash
Africanpalm
civet
[047]
ndash073(017)
012(003)
DOccu
psi(DistanceSTD)
minus8177158
Inf
197
008
Black‐legged
mongoose
047(01)a
025(004)
082(008)
a031(003)
SRN
lam(sectorSouthern)
028
0266
31
4627
420
011
058
Cameroon
cusimanse
075(009)
027(004)
056(015)
012(004)
SRN
lam(sectorSouthern)
minus1808131
minus05098939
005
073
Long‐nosed
mongoose
055(012)
a02(004)
015(006)
a027(007)
Null
ndashndash
ndashndash
ndash
Servalinegenet
092(006)
035(003)
08(009)
02(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus09202819
003
5821
570
50
26
Not
esNaiumlveoccupancyvaluesarepresentedinsquarebracketsforspecieswithadetectionprobabilitylt01TheoptimummodelchosenbyAkaikersquosinformationcriteriaforeachspeciesgeneratingsuf‐
ficientoccupancyvaluesinbothsectorswiththeBetaparameteranditisrespectivelowerandupper95confidencelimitsisshownandtheassociatedc‐hatandchi‐squaredp
val
ue
DdistancetoboundarySmanagementsectorRNRoylendashNicholsmodelOccuMckenziesingle‐seasonoccupancymodesynergisticinteraction
a IndicatesasignificantdifferenceinoccupancybetweensectorsasmeasuredbytheWaldteststatistic
TAB
LE 2
emsp(Continued)
770emsp |emsp emspensp Bruce et al
relationshipwithdistancetotheboundarycouldbeinfluencingoccu‐pancyIntheSouthernSectortheoccupancyincreasedwithdistanceto theboundary forwestern lowlandgorillaandgiantpangolinbutdecreasedforAfricangoldencatwhite‐belliedduikerandwaterchev‐rotainIntheNorthernSectoroccupancyincreasedwithdistancetotheboundaryforBatesrsquospygmyantelope
4emsp |emspDISCUSSION
Thecomparisonofthetwosurveysconfirmsthatstandardcameratrap surveys and derived metrics of presenceabsence trappingrates andoccupancy candiscern confidentdifferences in ground‐dwellingmammalcommunitiesinCentralAfricanforests
41emsp|emspCamera trap surveys for documenting species
Thecomparativeefficacyofcamera traps for surveyingmediumto large ground‐dwelling mammals in the DFR is indicated byobservationratesandverifiabilityofrecordsespeciallyofelusivesmallerandnocturnalspeciesForexamplethedirectencounterraterecordedbyrangersonpatrolthroughouttheentirereserveover a nine‐month period is much lower than the combinednumberofindependentphotographiceventsinbothmanagementsectors (ZSL amp MINFOF 2017b) even for relatively largeconspicuous species such as forest elephant (96 photographiceventscomparedto29directencounters)andcentralchimpanzee(204 independent photographic events compared to 23 directencounters)Methodologiessuchascameratrapping therefore
provideimportantbaselinedatathatwhenrepeatedthroughtimeusingastandardisedprotocolcanallowatleasttrendsinrelativeabundanceindicestobemonitored
42emsp|emspCamera trap surveys for comparing assemblages among sites
Despitebeingseparatedbyonlyc32kmthemammalcommunitiesbetween the twocamera trapgridsdisplayedmarkeddifferencesThiswasthecaseeventhoughbothgridshadlowShannonndashWeinerandSimpsonsdiversityindicesduetothedominanceofthreeorfourspeciesineachcameratrapgridSignificantdifferencesamongthesiteswere observed for the trapping rates of species of differentsizesbetweensectorsSmaller‐bodiedspecieswithintheherbivoreand omnivore guilds were more prevalent within the NorthernSector (Figure 2) Trapping rates and occupancy values for smallcarnivoresarealsolowerintheSouthernSectorThiscouldbeduetothedifficultyofidentifyingmorphologicallysimilarspeciessuchasmarshmongooseandlong‐nosedmongoose(Bahaa‐el‐dinetal2013 Ray 1997) in infrared imagery with single cameras Thereweremoreunidentifiablemongooseeventsthatwereclassifiedtoafamilylevel―66224intheSouthernSectorcomparedto29156intheNorthernSectorofallcombinedmongooseevents
43emsp|emspThe potential impact of seasonality on estimates derived from camera traps
Due to logistical and financial constraints the surveys could notberuninthesameseasonThishasthepotentialtoaffecttrapping
F I G U R E 5 emspChangeintheprobabilityofoccupancyforblack‐leggedmongoosecentralchimpanzeeandCamerooncusimansewithmanagementsectoraccordingtoaRoylendashNicholsmodel
emspensp emsp | emsp771Bruce et al
rates and occupancy for specieswith larger home ranges becausewhenspeciesarewide‐rangingoccupancycanproveineffectiveformeasuring relative abundance Forest elephants (Blake 2002) andgreatapesareknowntodisplayseasonalshiftsintheirhabitatusageover great distances in response to increased fruit availability andprecipitation(HeadRobbinsMundryMakagaampBoesch2012)Thiscouldalsoinfluenceothergregariousspeciessuchasredriverhogthatarealsothoughttooccasionallydisplaysimilaraggregationsandmovementsinresponsetomastingevents(LeslieampHuffman2015)However as both red river hog and chimpanzee had significantlyhigherRAIandhigheroccupancywithvariabledetectionprobabilityaccording to the number of individuals incorporated this supports
thepossibilitythatthesespeciesarefavouringtheSouthernSectorIfmanagersareable toestablishwhetherwide‐rangingspeciesarepredictably moving to known areas within the reserve they canrespondinamannerthatprovidesenhancedprotectiontovulnerablewildlifepopulations in concentration areasAsmost species in thissurveylikelyhaveasmallerhomerangethantheinter‐trapdistanceand display fixed territories it can be regarded as appropriate tocompare occupancy values as the extent of overlap of territorieswithin the two surveys are unlikely to change in such away as toaffecttheresultsFuturestudieswouldbenefitfromtryingtomatchcameratrapsurveysseasonallytotryandclarifytheissueofseasonalshiftsinhabitatusagewithintheDFR
F I G U R E 6 emspChangeintheprobabilityofoccupancyforAfricanbrush‐tailedporcupineEminspouchedratredriverhogservalinegenetPetersrsquoduikerandyellow‐backedduikerwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
772emsp |emsp emspensp Bruce et al
F I G U R E 7 emspChangeintheprobabilityofoccupancyforblueduikerandbayduikerwithdistancetotheboundaryinkilometresacrossbothmanagementsectorsaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
F I G U R E 8 emspChangeintheprobabilityofoccupancyforwhite‐belliedpangolinwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaMackenzieoccupancymodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
emspensp emsp | emsp773Bruce et al
44emsp|emspCamera trap surveys for measuring the impacts of hunting on mammal communities
The spatial scale at which mammal communities are affected byandhowpopulationsrespondtoanthropogenicpressuressuchasbushmeat hunting is difficult to empiricallymeasure (Laurance etal2006)Thisisespeciallytrueformammalsresidingwithintropi‐cal forestswheregatheringconsistentandmeaningfulpopulation‐andcommunity‐levelmetrics ischallenging(Ahumadaetal2013)Population density of tropical mammals can vary greatly due toheterogeneity present within the environment For example for‐est elephants havedifferent distributions and aggregations inwetanddryseasonsinNouabaleacute‐Ndoki NationalParkwhichispartiallydependentonspatio‐temporalpatternsoffruitingtreesacrossthelandscape(Blake2002)
Whether the differences observed among the two sites sur‐veyedhereareattributabletodifferent levelsofhuntingpressureremains to be confirmed There are however indications thathuntingpressureanditsimpactsonmammalfaunasaregreaterintheNorthern Sector than in the Southern Sector The effects ofhuntingpressureonmammaliandeclinesinCentralAfricanforestsarewell documented The pattern in general is the largest‐bod‐ied species frugivores and thosewith high hunter or blackmar‐ketvalue(Abernethyetal2013Cardilloetal2005FaOliveroFarfaacutenMaacuterquezDuarteetal2014aFaOliveroFarfaacutenMaacuterquezVargasetal2014bPeresampPalacios2007)arethefirstspeciestoshownoticeabledeclineInthisstudythesignificantdeclineintherelativeabundance for frugivores suchasPetersʼduikerandspe‐cieswithhighhuntervalueliketheredriverhogunderincreasedhuntingpressure in theNorthernSector is reported inother sur‐veys(Abernethyetal2013)Thisisalsoreflectedinthedifferencesobserved in this study in biomass in the different guilds of eachmammalcommunityThemammalcommunitywithintheNorthernSector shows indications of a community that is disturbed and isexperiencingelevatedhuntingpressureThesearehigher(camera)trapping rates for smaller‐bodiedspecies suchasEminrsquospouchedrat and significantly fewer encounters of larger‐bodiedmammalsthataretargetsofthebushmeattradesuchasPetersʼduikerandredriverhog(FaRyanampBell2005JerozolimskiampPeres2003)Additionalindicatorsaretheabsenceinthesurveysoflargercarni‐voresintheNorthernSectorsuchasgoldencatandleopardwhicharesensitivetosnaring(Bahaa‐el‐dinetal2015)andsignificantlyreducedabundancemetricsfordisturbance‐sensitivespeciessuchasblack‐leggedmongooseandwaterchevrotain(Hart2013a)Theabsence of white‐bellied duiker in the Northern Sector also sug‐gestselevatedhumandisturbanceasthisspecieshasbeenreportedasverysensitivetoevenminorperturbationwithintheenvironment(Hart2013b)IncomparisontheSouthernSectorcontainedindica‐torfaunasuchasthewhite‐belliedduikerandhadhighertrappingratesforlarger‐bodiedspecies
WesuspectthedifferencesobservedaremostlikelyduetolowerhumandisturbanceintheSouthernSectorTheteamsdeployingand
recoveringthecamerasintheSouthernSectorcovered238kmandencountered few signs of humanperturbation (T Brucepers obs)whereashumansignwascommonlyencounteredbytheteamsintheNorthernSectorThisperceiveddifference is reflected in the2017and 2018 density of hunting signwithin each camera trap grid asdetected throughMINFOF ranger patrols (ZSL ampMINFOF 2017a2017b) and through the2018DistanceSampling inventory for theDFR (Bruce et al 2018) Higher numbers of hunting sign in theNorthernSectorwouldbeconsistentwithanelevatedhuntingpres‐sureinthatarea
45emsp|emspProtection of refugia from hunting
Though inferences made for wide‐ranging species such as forestelephantsandgreatapesusingcameratrapsaredifficultthefactthattrappingrateswerehigherinmorechallengingterrainwithassumedlower hunting pressure could be indicative of complex habitatprovidingsomelevelofprotectionfromhuntingElephantisknownto retreatwhen they aredisturbed to terrain that ismoredifficulttoaccessbyhumans (Hedges2012)Thuswithin largerprotectedareas certain zones may act as refugia for wildlife populations(Campbelletal2011)Thiscanbeduetoarangeof factorssuchas remoteanddifficult terrain forpoachers (Attum2007Hedges2012) or the regular presence of field researchers and rangers(Campbell et al 2011) The significanceof these refugia for largerprotected areas is that the populations of wildlife residing withinthem if adequately protected may provide source populations toallowrecolonisationofotherareasofthereserve(NaranjoampBodmer2007)Thereforeifadequateprotectioncanbeprovidedtorelativelysmallbutimportantareasoflargereservesthismayprovidetropicalforestswithabetterchanceofbeingecologicallyresilienttoongoingand increasing human perturbation Well‐designed camera trapsurveys may provide data on the status of wildlife populations atrelativelyfinespatialresolutionssoastoidentifyfunctionalrefugiawithgreaterconfidence
ACKNOWLEDG EMENTS
WeappreciatetheongoingsupportofCameroonrsquosMinistryofForestsandWildlife(MINFOF)andtheopportunitytocontributetobiodiver‐sityconservationthroughoutthecountryInparticularwewouldliketothanktheChefdrsquoAntenneSergeJacobMeyeforhisongoingsup‐portofconservationresearchwithintheprotectedareaWeappreci‐atethestalwarteffortsofMINFOFecoguardsandlocalporterswhoaccompaniedthesurveyteamsinthefieldWewouldalsoliketothanktheUnitedStatesFishandWildlifeService(USFWS)mdashAfricanElephantConservationandIUCNSOSmdashFondationSegreacutePangolinConservationInitiativeforsupportingthiswork
ORCID
Tom Bruce httporcidorg0000‐0001‐6958‐1657
774emsp |emsp emspensp Bruce et al
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AbrahamsM I Peres C A amp Costa H C (2017)Measuring localdepletion of terrestrial game vertebrates by central‐place hunt‐ers in rural Amazonia PLoS ONE 12(10) e0186653 httpsdoiorg101371journalpone0186653
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Ahumada J A Silva C E Gajapersad K Hallam C Hurtado JMartin E hellip Sheil D (2011) Community structure and diver‐sity of tropical forest mammals Data from a global camera trapnetwork Philosophical Transactions of the Royal Society of London Biological Sciences366(1578)2703ndash2711httpsdoiorg101098rstb20110115
AminRAndanjeSAOgwonkaBAliAHBowkettAEOmarMampWacherT(2015)ThenortherncoastalforestsofKenyaarenationally and globally important for the conservation of AdersrsquoduikerCephalophusadersiandotherantelopespeciesBiodiversity and Conservation 24(3) 641ndash658 httpsdoiorg101007s10531‐014‐0842‐z
Attum O (2007) Can landscape use be among the factors that po‐tentiallymake some ungulates speciesmore difficult to conserveJournal of Arid Environments69(3)410ndash419
Bahaa‐el‐dinLHenschelPAbaaRAbernethyKBohmTBoutNhellipLeeM (2013)NotesonthedistributionandstatusofsmallcarnivoresinGabonSmall Carnivore Conservation4819ndash29
Bahaa‐el‐dinLHenschelPButynskiTMMacdonaldDWMillsDSlotowRampHunterL (2015)TheAfricangoldencatCaracalaurataAfricasleast‐knownfelidMammal Review45(1)63ndash77
Bennett E L Blencowe E Brandon K Brown D Burn R WCowlishaw G hellip Robinson J G (2007) Hunting for consensusReconcilingbushmeatharvestconservationanddevelopmentpol‐icyinWestandCentralAfricaConservation Biology21(3)884ndash887httpsdoiorg101111j1523‐1739200600595x
BlakeSDeemSLMossimboEMaiselsFampWalshP(2009)Forestelephants Tree planters of the CongoBiotropica41(4) 459ndash468httpsdoiorg101111j1744‐7429200900512x
Blake S (2002) The ecology of forest elephant distribution and itsimplications for conservation Doctoral dissertation University ofEdinburgh
BruceTNdjassiCFowlerANdimbeMFankemOTabueRhellipOlsonD(2018)Faunal inventory of the Dja Faunal Reserve Cameroon Yaoundeacute Cameroon Ministry of Forests and Wildlife (MINFOF)Zoological Society of London ndash Cameroon Country ProgrammeAfricanWildlifeFoundation
BruceTWacherTNdingaHBidjokaVMeyongFNgoBataMampOlsonD(2017)camera trap survey for larger terrestrial wildlife in the Dja Biosphere Reserve CameroonYaoundeacuteCameroonZoologicalSocietyofLondon(ZSL)ampCameroonMinistryofForestsandWildlife(MINFOF)
BurnhamKPampAndersonDR(2002)Model selection and multimodel inferenceNewYorkNYSpringer
Campbell G Kuehl H Diarrassouba A NGoran P K amp BoeschC (2011) Long‐term research sites as refugia for threatened andover‐harvested species Biology Letters 7(5) 723ndash726 httpsdoiorg101098rsbl20110155
CardilloMMaceGMJonesKEBielbyJBininda‐EmondsORSechrestWhellipPurvisA(2005)Multiplecausesofhighextinction
riskinlargemammalspeciesScience309(5738)1239ndash1241httpsdoiorg101126science1116030
Craigie IDBaillieJEBalmfordACarboneCCollenBGreenREampHuttonJM (2010)Largemammalpopulationdeclines inAfricarsquosprotectedareasBiological Conservation143(9)2221ndash2228httpsdoiorg101016jbiocon201006007
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Djuikouo M N K Doucet J L Nguembou C K Lewis S L ampSonkeacute B (2010) Diversity and aboveground biomass in threetropical forest types in the Dja Biosphere Reserve Cameroon African Journal of Ecology 48(4) 1053ndash1063 httpsdoiorg101111j1365‐2028201001212x
DupainJBombomeKampVanElsackerL(2003)LeschimpanzeacutesetlesgorillesdelareacuteservedefauneduDjaCanopeacutee2414ndash15
EffordMGampDawsonDK(2012)OccupancyincontinuoushabitatEcosphere3(4)1ndash15httpsdoiorg101890ES11‐003081
Efron B amp Tibshirani R J (1994) An introduction to the bootstrap WashingtonDCCRCPress
FaJEOliveroJFarfaacutenMAacuteMaacuterquezALDuarteJNackoneyJhellipMacdonaldDW(2014a)CorrelatesofbushmeatinmarketsanddepletionofwildlifeConservation Biology29(3)805ndash815
Fa J EOlivero J FarfaacutenMAacuteMaacuterquezA LVargas JMRealRampNasiR(2014b)IntegratingsustainablehuntinginbiodiversityprotectioninCentralAfricaHotspotsweakspotsandstrongspotsPLoS ONE9(11)e112367
FaJERyanSFampBellDJ (2005)Huntingvulnerabilityecolog‐ical characteristics and harvest rates of bushmeat species in afro‐tropicalforestsBiological Conservation121(2)167ndash176httpsdoiorg101016jbiocon200404016
Fa J E Seymour S Dupain J E F Amin R Albrechtsen L ampMacdonaldD (2006) Getting to gripswith themagnitude of ex‐ploitationBushmeat in theCross‐SanagariversregionNigeria and Cameroon Biological Conservation 129(4) 497ndash510 httpsdoiorg101016jbiocon200511031
Farris Z J Boone H M Karpanty S Murphy A Ratelolahy FAndrianjakariveloVampKellyMJ(2015)FeralcatsandthefitoatyFirstpopulationassessmentoftheblackforestcatinMadagascarrsquosrainforestsJournal of Mammalogy97(2)518ndash525
Fiske IampChandlerR (2011)UnmarkedAnRpackageforfittinghi‐erarchicalmodelsofwildlifeoccurrenceandabundanceJournal of Statistical Software43(10)1ndash23
HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences107(19)8650ndash8655httpsdoiorg101073pnas0912668107
HartJ(2013a)WaterchevrotainHymemoschusaquaticusInJKingdonampMHoffmann (Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp88ndash92)LondonUKBloomsbury
Hart J (2013b) White‐bellied duiker Cephalophus leucogaster In JKingdonampMHoffmann(Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp255ndash258)LondonUKBloomsbury
HeadJSRobbinsMMMundryRMakagaLampBoeschC(2012)Remotevideo‐cameratrapsmeasurehabitatuseandcompetitiveex‐clusionamongsympatricchimpanzeegorillaandelephantinLoangoNational ParkGabon Journal of Tropical Ecology28(06) 571ndash583httpsdoiorg101017S0266467412000612
HedgesS(2012)Monitoring elephant populations and assessing threats HimayatnagarTelanganaUniversitiesPress
HedwigDKienastIBonnetMCurranBKCourageABoeschChellipKingT(2018)Acameratrapassessmentoftheforestmam‐mal community within the transitional savannah‐forest mosaic oftheBateacutekeacutePlateauNationalParkGabonAfrican Journal of Ecology56(4)777ndash790httpsdoiorg101111aje12497
emspensp emsp | emsp775Bruce et al
HijmansRJCameronSEParraJLJonesPGampJarvisA(2005)Very high resolution interpolated climate surfaces for global landareasInternational Journal of Climatology25(15)1965ndash1978httpsdoiorg101002joc1276
HuggelA(2012)Exiv2softwaretool[Computersoftware]Retrievedfromhttpswwwexiv2orgindexhtml
Jerozolimski A amp Peres C A (2003) Bringing home the biggestbacon A cross‐site analysis of the structure of hunter‐kill profilesin Neotropical forests Biological Conservation 111(3) 415ndash425httpsdoiorg101016S0006‐3207(02)00310‐5
KingdonJ (2015)The Kingdon field guide to African mammalsLondonUKBloomsburyPublishing
KuumlhlHFMaiselsMAncrenazampEAWilliamson(Eds)(2008)Best practice guidelines for surveys and monitoring of great ape populations GlandSwitzerlandIUCN
LauranceWFCroesBMTchignoumbaLLahmSAAlonsoALeeMEhellipOndzeanoC(2006)ImpactsofroadsandhuntingoncentralAfrican rainforestmammalsConservation Biology20(4)1251ndash1261httpsdoiorg101111j1523‐1739200600420x
LauranceWFUsecheDCRendeiroJKalkaMBradshawCJSloan S P hellip Arroyo‐Rodriguez V (2012) Averting biodiversitycollapse in tropical forestprotectedareasNature489(7415)290httpsdoiorg101038nature11318
LeslieDMampHuffmanBA(2015)Potamochoerus porcus(ArtiodactylaSuidae)Mammalian Species4715ndash31
MacKenzieD IampBailey L L (2004)Assessing the fit of site‐occu‐pancy models Journal of Agricultural Biological and Environmental Statistics9300ndash318httpsdoiorg101198108571104X3361
MacKenzieDINicholsJDRoyleJAPollockKHBaileyLLampHinesJE (2006)Occupancy estimation and modellingBurlingtonMAAcademicPress
Magurran A E (2005) Species abundance distributions Patternor process Functional Ecology 19(1) 177ndash181 httpsdoiorg101111j0269‐8463200500930x
MaiselsFStrindbergSBlakeSWittemyerGHartJWilliamsonEAhellipWarrenY (2013)DevastatingdeclineofforestelephantsinCentralAfricaPLoS ONE8(3)e59469httpsdoiorg101371journalpone0059469
MalhiYAdu‐BreduSAsareRA LewisS LampMayauxP (2013)AfricanrainforestsPastpresentandfuturePhilosophical Transactions of the Royal Society of London Biological Sciences 368(1625)20120312
MallonDPHoffmannMGraingerMJHibertFVanVlietNampMcGowanP JK (2015)An IUCNsituationanalysisof terrestrialandfreshwaterfaunainWestandCentralAfricaOccasionalpaperoftheIUCNspeciessurvivalcommission(54)
MambeyaMMBakerFMombouaBRKoumbaPamboAFHegaMOkouyiOkouyiVJhellipAbernethyK(2018)TheemergenceofacommercialtradeinpangolinsfromGabonAfrican Journal of Ecology56(3)601ndash609httpsdoiorg101111aje12507
MINFOFampIUCN(2015)CaracteacuterisationdelapopulationdegrandsetmoyensmammifegraveresdanslaReservedeFauneduDjaPotentieletmenacesYaoundeacuteCameroun
Muchaal P K amp Ngandjui G (1999) Impact of village hunt‐ing on wildlife populations in the western Dja ReserveCameroon Conservation Biology 13(2) 385ndash396 httpsdoiorg101046j1523‐17391999013002385x
NaranjoEJampBodmerRE (2007) Sourcendashsink systemsandconser‐vationofhuntedungulatesintheLacandonForestMexico Biological Conservation 138(3ndash4) 412ndash420 httpsdoiorg101016jbiocon 200705010
NielsenMR(2006)ImportancecauseandeffectofbushmeathuntingintheUdzungwaMountainsTanzania ImplicationsforcommunitybasedwildlifemanagementBiological Conservation128(4)509ndash516httpsdoiorg101016jbiocon200510017
OBrienTGKinnairdMFampWibisonoHT (2003)Crouching ti‐gers hiddenprey Sumatran tiger andprey populations in a tropi‐calforestlandscapeAnimal Conservation6(2)131ndash139httpsdoiorg101017S1367943003003172
OksanenJ(2015)VegananintroductiontoordinationVol8(p19)Retrieved from httpscranr‐projectorgwebpackagesveganvi‐gnettesintroveganpdf
PeresCAampPalaciosE(2007)Basin‐wideeffectsofgameharvestonvertebrate populationdensities inAmazonian forests Implicationsfor animal‐mediated seed dispersal Biotropica 39(3) 304ndash315httpsdoiorg101111j1744‐7429200700272x
PotapovPVTurubanovaSAHansenMCAduseiBBroichMAltstattAhellipJusticeCO(2012)QuantifyingforestcoverlossinDemocraticRepublicoftheCongo2000ndash2010withLandsatETM+data Remote Sensing of Environment 122 106ndash116 httpsdoiorg101016jrse201108027
PoulsenJRKoernerSEMooreSMedjibeVPBlakeSClarkC JhellipRosinC (2017) Poaching empties criticalCentralAfricanwilderness of forest elephants Current Biology 27(4) 134ndashR135httpsdoiorg101016jcub201701023
PurvisAGittlemanJlCowlishawGampMaceGM(2000)PredictingextinctionriskindecliningspeciesProceedings of the Royal Society B Biological Sciences267(1456) 1947ndash1952 httpsdoiorg101098rspb20001234
RayJ(1997)ComparativeecologyoftwoAfricanforestmongoosesHerpestesnasoandAtilaxpaludinosusAfrican Journal of Ecology35(3)237ndash253httpsdoiorg101111j1365‐20281997086‐ 89086x
Redford K H (1992) The empty forest BioScience 42(6) 412ndash422httpsdoiorg1023071311860
RepublicofCameroon(1994)Lawno9401du20janvier1994portantreacutegimedesforecirctsdelafauneetdelapecirccheRepublicofCameroon
RoveroFampMarshallAR(2009)CameratrappingphotographicrateasanindexofdensityinforestungulatesJournal of Applied Ecology46(5)1011ndash1017httpsdoiorg101111j1365‐2664200901705x
Royle J A amp Nichols J D (2003) Estimating abundance from re‐peated presence‐absence data or point counts Ecology 84(3)777ndash790 httpsdoiorg1018900012‐9658(2003)084[0777EAFRPA]20CO2
Seddon P J Griffiths C J Soorae P S ampArmstrongD P (2014)ReversingdefaunationRestoringspeciesinachangingworldScience345(6195)406ndash412httpsdoiorg101126science1251818
Silveira L Jacomo A T amp Diniz‐Filho J A F (2003) Camera trapline transect census and track surveys A comparative evaluationBiological Conservation 114(3) 351ndash355 httpsdoiorg101016S0006‐3207(03)00063‐6
Sonkeacute B (1998) Etudes floristiques et structurales des forecircts de laReacuteserve de Faune du Dja (Cameroun) Laboratoire de BotaniqueSysteacutematique et de Phytosociologie Universiteacute Libre de Bruxelles(ULB)
Srbek‐AraujoACampChiarelloAG(2005)Iscameratrappinganeffi‐cientmethodforsurveyingmammalsinNeotropicalforestsAcasestudyinsouth‐easternBrazilJournal of Tropical Ecology21(1)121ndash125httpsdoiorg101017S0266467404001956
Stiles D (2011) Elephant meat and ivory trade in Central AfricaPachyderm5026ndash36
TEAMNetwork(2008)Terrestrialvertebrateprotocol implementationmanualv30(p56)WashingtonDCTropicalEcologyAssessmentandMonitoringNetworkCenter forAppliedBiodiversity ScienceConservationInternational
Tobler M W Carrillo‐Percastegui S E Leite Pitman R MaresR amp Powell G (2008) An evaluation of camera traps for in‐ventorying large‐and medium‐sized terrestrial rainforestmammals Animal Conservation 11(3) 169ndash178 httpsdoiorg101111j1469‐1795200800169x
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
emspensp emsp | emsp769Bruce et al
and management sector Table 2) Forest elephant black‐frontedduikerand long‐nosedmongoose (Herpestes nasodeWinton1901)lackedamodel thathadanAICdifferenceofgt2 therefore theco‐variatemodelswerenotsignificantlydifferent to thenullmodel forthese species Elevenof 15 species had aRoylendashNicholsmodel se‐lectedasthelowestAICvaluesuggestingadifferenceinthenumberofindividualswassignificantlyinfluencingdetectionprobabilitiesandthereforeoccupancy
RoylendashNichols models accounted for occupancy being signifi‐cantlyhigherindifferingmanagementsectorswithnointeractionofdistancetotheprotectedareaboundaryforthreespeciesCamerooncusimanse had higher occupancy in the Northern Sector In con‐trast central chimpanzee and black‐legged mongoose had signifi‐cantlyloweroccupancywithintheNorthernSectorcomparedtotheSouthernSector(Figure5)
African brush‐tailed porcupine Eminrsquos pouched rat and servalinegenet(Genetta servalinaPucheran1855)hadasynergisticRoylendashNicholsmodelselectedasthemostsupportedTheprobabilityofsiteoccupancyslightlyincreasedwithdistancetotheboundaryandwasoverallhigherin theNorthernSector butdeclinedwithdistance to theboundary intheSouthernSector(Figure6)BothPetersrsquoduikerandredriverhogalsodisplayedthispatternofoccupancybuthadamuchgreaterincreaseinoccupancyintheNorthernSectorandhadhigheroccupancyoverallintheSouthernSector(Figure6)Incontrastyellow‐backedduiker(Cephalophus silvicultorAfezilus1815)wastheonlyspeciestodemonstrateanincreaseinoccupancywithdistancetotheboundaryintheSouthernSectorwhiledecliningintheNorthernSectorHoweversimilartootherlargerspeciesoccupancywashigherintheSouthernSector(Figure6)
With regard to the remainingduiker speciesmodelled aRoylendashNicholsmodelwithdistancetotheprotectedareaboundarywasiden‐tifiedasthemostappropriateTheprobabilityofasitebeingoccupiedbyblueduikerandbayduikerincreasedwithdistancetotheboundarywith no discernible difference betweenmanagement sectors in themodel(Figure7)
White‐belliedpangolinhadasingle‐seasonoccupancymodelse‐lectedsuggestingdifferences inabundancebetweenthemanage‐mentsectorsdidnotaffectdetectionprobabilitiesTheprobabilityofasitebeingoccupiedbywhite‐belliedpangolin increasedintheNorthernSectoranddeclinedintheSouthernSectorwithincreasingdistancetotheboundary(Figure8)
Seven speciesweredetectedonly inone sectoror lacked suffi‐cientdetectionsinonesectortoreliablymodeloccupancyacrossbothmanagement sectors Therefore only the effect of distance to theboundarycouldbemodelledThesewereAfricangoldencatwesternlowlandgorillawhite‐belliedduikergiantpangolinAfricanpalmcivet(Nandinia binotata Gray 1830) Batesrsquos pygmy antelope and waterchevrotain (Hymeoschus aquaticusOgilby 1841)African palm civetwastheonlyspeciestohavedistancetotheboundaryselectedastheoptimummodel to explain occupancy as occupancy increasedwithdistance from the boundary of the protected area (Table 2)All theremainingspecieshadthenullmodelselectedastheoptimummodelaccordingtoAICcriteria (Table2)Howeverdistancetothebound‐arywaswithinlt2AICforthesespeciessuggestingthatasignificantSp
ecie
sN
orth
ern
sect
or (ψ
)N
orth
ern
sect
or (p
)So
uthe
rn s
ecto
r (ψ
)So
uthe
rn s
ecto
r (p
)M
odel
Beta
mdashPa
ram
eter
ch
osen
Low
er 9
5
beta
Upp
er 9
5
beta
C‐ha
t val
ueCh
i‐squ
arep
va
lue
Africangolden
cat
ndashndash
041(013)
013(004)
Null
ndashndash
ndashndash
ndash
Africanpalm
civet
[047]
ndash073(017)
012(003)
DOccu
psi(DistanceSTD)
minus8177158
Inf
197
008
Black‐legged
mongoose
047(01)a
025(004)
082(008)
a031(003)
SRN
lam(sectorSouthern)
028
0266
31
4627
420
011
058
Cameroon
cusimanse
075(009)
027(004)
056(015)
012(004)
SRN
lam(sectorSouthern)
minus1808131
minus05098939
005
073
Long‐nosed
mongoose
055(012)
a02(004)
015(006)
a027(007)
Null
ndashndash
ndashndash
ndash
Servalinegenet
092(006)
035(003)
08(009)
02(003)
DSRN
lam(DistanceSTDse
ctorSouthern)
minus09202819
003
5821
570
50
26
Not
esNaiumlveoccupancyvaluesarepresentedinsquarebracketsforspecieswithadetectionprobabilitylt01TheoptimummodelchosenbyAkaikersquosinformationcriteriaforeachspeciesgeneratingsuf‐
ficientoccupancyvaluesinbothsectorswiththeBetaparameteranditisrespectivelowerandupper95confidencelimitsisshownandtheassociatedc‐hatandchi‐squaredp
val
ue
DdistancetoboundarySmanagementsectorRNRoylendashNicholsmodelOccuMckenziesingle‐seasonoccupancymodesynergisticinteraction
a IndicatesasignificantdifferenceinoccupancybetweensectorsasmeasuredbytheWaldteststatistic
TAB
LE 2
emsp(Continued)
770emsp |emsp emspensp Bruce et al
relationshipwithdistancetotheboundarycouldbeinfluencingoccu‐pancyIntheSouthernSectortheoccupancyincreasedwithdistanceto theboundary forwestern lowlandgorillaandgiantpangolinbutdecreasedforAfricangoldencatwhite‐belliedduikerandwaterchev‐rotainIntheNorthernSectoroccupancyincreasedwithdistancetotheboundaryforBatesrsquospygmyantelope
4emsp |emspDISCUSSION
Thecomparisonofthetwosurveysconfirmsthatstandardcameratrap surveys and derived metrics of presenceabsence trappingrates andoccupancy candiscern confidentdifferences in ground‐dwellingmammalcommunitiesinCentralAfricanforests
41emsp|emspCamera trap surveys for documenting species
Thecomparativeefficacyofcamera traps for surveyingmediumto large ground‐dwelling mammals in the DFR is indicated byobservationratesandverifiabilityofrecordsespeciallyofelusivesmallerandnocturnalspeciesForexamplethedirectencounterraterecordedbyrangersonpatrolthroughouttheentirereserveover a nine‐month period is much lower than the combinednumberofindependentphotographiceventsinbothmanagementsectors (ZSL amp MINFOF 2017b) even for relatively largeconspicuous species such as forest elephant (96 photographiceventscomparedto29directencounters)andcentralchimpanzee(204 independent photographic events compared to 23 directencounters)Methodologiessuchascameratrapping therefore
provideimportantbaselinedatathatwhenrepeatedthroughtimeusingastandardisedprotocolcanallowatleasttrendsinrelativeabundanceindicestobemonitored
42emsp|emspCamera trap surveys for comparing assemblages among sites
Despitebeingseparatedbyonlyc32kmthemammalcommunitiesbetween the twocamera trapgridsdisplayedmarkeddifferencesThiswasthecaseeventhoughbothgridshadlowShannonndashWeinerandSimpsonsdiversityindicesduetothedominanceofthreeorfourspeciesineachcameratrapgridSignificantdifferencesamongthesiteswere observed for the trapping rates of species of differentsizesbetweensectorsSmaller‐bodiedspecieswithintheherbivoreand omnivore guilds were more prevalent within the NorthernSector (Figure 2) Trapping rates and occupancy values for smallcarnivoresarealsolowerintheSouthernSectorThiscouldbeduetothedifficultyofidentifyingmorphologicallysimilarspeciessuchasmarshmongooseandlong‐nosedmongoose(Bahaa‐el‐dinetal2013 Ray 1997) in infrared imagery with single cameras Thereweremoreunidentifiablemongooseeventsthatwereclassifiedtoafamilylevel―66224intheSouthernSectorcomparedto29156intheNorthernSectorofallcombinedmongooseevents
43emsp|emspThe potential impact of seasonality on estimates derived from camera traps
Due to logistical and financial constraints the surveys could notberuninthesameseasonThishasthepotentialtoaffecttrapping
F I G U R E 5 emspChangeintheprobabilityofoccupancyforblack‐leggedmongoosecentralchimpanzeeandCamerooncusimansewithmanagementsectoraccordingtoaRoylendashNicholsmodel
emspensp emsp | emsp771Bruce et al
rates and occupancy for specieswith larger home ranges becausewhenspeciesarewide‐rangingoccupancycanproveineffectiveformeasuring relative abundance Forest elephants (Blake 2002) andgreatapesareknowntodisplayseasonalshiftsintheirhabitatusageover great distances in response to increased fruit availability andprecipitation(HeadRobbinsMundryMakagaampBoesch2012)Thiscouldalsoinfluenceothergregariousspeciessuchasredriverhogthatarealsothoughttooccasionallydisplaysimilaraggregationsandmovementsinresponsetomastingevents(LeslieampHuffman2015)However as both red river hog and chimpanzee had significantlyhigherRAIandhigheroccupancywithvariabledetectionprobabilityaccording to the number of individuals incorporated this supports
thepossibilitythatthesespeciesarefavouringtheSouthernSectorIfmanagersareable toestablishwhetherwide‐rangingspeciesarepredictably moving to known areas within the reserve they canrespondinamannerthatprovidesenhancedprotectiontovulnerablewildlifepopulations in concentration areasAsmost species in thissurveylikelyhaveasmallerhomerangethantheinter‐trapdistanceand display fixed territories it can be regarded as appropriate tocompare occupancy values as the extent of overlap of territorieswithin the two surveys are unlikely to change in such away as toaffecttheresultsFuturestudieswouldbenefitfromtryingtomatchcameratrapsurveysseasonallytotryandclarifytheissueofseasonalshiftsinhabitatusagewithintheDFR
F I G U R E 6 emspChangeintheprobabilityofoccupancyforAfricanbrush‐tailedporcupineEminspouchedratredriverhogservalinegenetPetersrsquoduikerandyellow‐backedduikerwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
772emsp |emsp emspensp Bruce et al
F I G U R E 7 emspChangeintheprobabilityofoccupancyforblueduikerandbayduikerwithdistancetotheboundaryinkilometresacrossbothmanagementsectorsaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
F I G U R E 8 emspChangeintheprobabilityofoccupancyforwhite‐belliedpangolinwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaMackenzieoccupancymodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
emspensp emsp | emsp773Bruce et al
44emsp|emspCamera trap surveys for measuring the impacts of hunting on mammal communities
The spatial scale at which mammal communities are affected byandhowpopulationsrespondtoanthropogenicpressuressuchasbushmeat hunting is difficult to empiricallymeasure (Laurance etal2006)Thisisespeciallytrueformammalsresidingwithintropi‐cal forestswheregatheringconsistentandmeaningfulpopulation‐andcommunity‐levelmetrics ischallenging(Ahumadaetal2013)Population density of tropical mammals can vary greatly due toheterogeneity present within the environment For example for‐est elephants havedifferent distributions and aggregations inwetanddryseasonsinNouabaleacute‐Ndoki NationalParkwhichispartiallydependentonspatio‐temporalpatternsoffruitingtreesacrossthelandscape(Blake2002)
Whether the differences observed among the two sites sur‐veyedhereareattributabletodifferent levelsofhuntingpressureremains to be confirmed There are however indications thathuntingpressureanditsimpactsonmammalfaunasaregreaterintheNorthern Sector than in the Southern Sector The effects ofhuntingpressureonmammaliandeclinesinCentralAfricanforestsarewell documented The pattern in general is the largest‐bod‐ied species frugivores and thosewith high hunter or blackmar‐ketvalue(Abernethyetal2013Cardilloetal2005FaOliveroFarfaacutenMaacuterquezDuarteetal2014aFaOliveroFarfaacutenMaacuterquezVargasetal2014bPeresampPalacios2007)arethefirstspeciestoshownoticeabledeclineInthisstudythesignificantdeclineintherelativeabundance for frugivores suchasPetersʼduikerandspe‐cieswithhighhuntervalueliketheredriverhogunderincreasedhuntingpressure in theNorthernSector is reported inother sur‐veys(Abernethyetal2013)Thisisalsoreflectedinthedifferencesobserved in this study in biomass in the different guilds of eachmammalcommunityThemammalcommunitywithintheNorthernSector shows indications of a community that is disturbed and isexperiencingelevatedhuntingpressureThesearehigher(camera)trapping rates for smaller‐bodiedspecies suchasEminrsquospouchedrat and significantly fewer encounters of larger‐bodiedmammalsthataretargetsofthebushmeattradesuchasPetersʼduikerandredriverhog(FaRyanampBell2005JerozolimskiampPeres2003)Additionalindicatorsaretheabsenceinthesurveysoflargercarni‐voresintheNorthernSectorsuchasgoldencatandleopardwhicharesensitivetosnaring(Bahaa‐el‐dinetal2015)andsignificantlyreducedabundancemetricsfordisturbance‐sensitivespeciessuchasblack‐leggedmongooseandwaterchevrotain(Hart2013a)Theabsence of white‐bellied duiker in the Northern Sector also sug‐gestselevatedhumandisturbanceasthisspecieshasbeenreportedasverysensitivetoevenminorperturbationwithintheenvironment(Hart2013b)IncomparisontheSouthernSectorcontainedindica‐torfaunasuchasthewhite‐belliedduikerandhadhighertrappingratesforlarger‐bodiedspecies
WesuspectthedifferencesobservedaremostlikelyduetolowerhumandisturbanceintheSouthernSectorTheteamsdeployingand
recoveringthecamerasintheSouthernSectorcovered238kmandencountered few signs of humanperturbation (T Brucepers obs)whereashumansignwascommonlyencounteredbytheteamsintheNorthernSectorThisperceiveddifference is reflected in the2017and 2018 density of hunting signwithin each camera trap grid asdetected throughMINFOF ranger patrols (ZSL ampMINFOF 2017a2017b) and through the2018DistanceSampling inventory for theDFR (Bruce et al 2018) Higher numbers of hunting sign in theNorthernSectorwouldbeconsistentwithanelevatedhuntingpres‐sureinthatarea
45emsp|emspProtection of refugia from hunting
Though inferences made for wide‐ranging species such as forestelephantsandgreatapesusingcameratrapsaredifficultthefactthattrappingrateswerehigherinmorechallengingterrainwithassumedlower hunting pressure could be indicative of complex habitatprovidingsomelevelofprotectionfromhuntingElephantisknownto retreatwhen they aredisturbed to terrain that ismoredifficulttoaccessbyhumans (Hedges2012)Thuswithin largerprotectedareas certain zones may act as refugia for wildlife populations(Campbelletal2011)Thiscanbeduetoarangeof factorssuchas remoteanddifficult terrain forpoachers (Attum2007Hedges2012) or the regular presence of field researchers and rangers(Campbell et al 2011) The significanceof these refugia for largerprotected areas is that the populations of wildlife residing withinthem if adequately protected may provide source populations toallowrecolonisationofotherareasofthereserve(NaranjoampBodmer2007)Thereforeifadequateprotectioncanbeprovidedtorelativelysmallbutimportantareasoflargereservesthismayprovidetropicalforestswithabetterchanceofbeingecologicallyresilienttoongoingand increasing human perturbation Well‐designed camera trapsurveys may provide data on the status of wildlife populations atrelativelyfinespatialresolutionssoastoidentifyfunctionalrefugiawithgreaterconfidence
ACKNOWLEDG EMENTS
WeappreciatetheongoingsupportofCameroonrsquosMinistryofForestsandWildlife(MINFOF)andtheopportunitytocontributetobiodiver‐sityconservationthroughoutthecountryInparticularwewouldliketothanktheChefdrsquoAntenneSergeJacobMeyeforhisongoingsup‐portofconservationresearchwithintheprotectedareaWeappreci‐atethestalwarteffortsofMINFOFecoguardsandlocalporterswhoaccompaniedthesurveyteamsinthefieldWewouldalsoliketothanktheUnitedStatesFishandWildlifeService(USFWS)mdashAfricanElephantConservationandIUCNSOSmdashFondationSegreacutePangolinConservationInitiativeforsupportingthiswork
ORCID
Tom Bruce httporcidorg0000‐0001‐6958‐1657
774emsp |emsp emspensp Bruce et al
R E FE R E N C E S
AbernethyKACoad L TaylorG LeeMEampMaisels F (2013)Extent and ecological consequences of hunting in Central Africanrainforests in thetwenty‐firstcenturyPhilosophical Transactions of the Royal Society of London Biological Sciences368(1625)20120303httpsdoiorg101098rstb20120303
AbrahamsM I Peres C A amp Costa H C (2017)Measuring localdepletion of terrestrial game vertebrates by central‐place hunt‐ers in rural Amazonia PLoS ONE 12(10) e0186653 httpsdoiorg101371journalpone0186653
AhumadaJAHurtadoJampLizcanoD(2013)MonitoringthestatusandtrendsoftropicalforestterrestrialvertebratecommunitiesfromcameratrapdataAtool forconservationPLoS ONE8(9)e73707httpsdoiorg101371journalpone0073707
Ahumada J A Silva C E Gajapersad K Hallam C Hurtado JMartin E hellip Sheil D (2011) Community structure and diver‐sity of tropical forest mammals Data from a global camera trapnetwork Philosophical Transactions of the Royal Society of London Biological Sciences366(1578)2703ndash2711httpsdoiorg101098rstb20110115
AminRAndanjeSAOgwonkaBAliAHBowkettAEOmarMampWacherT(2015)ThenortherncoastalforestsofKenyaarenationally and globally important for the conservation of AdersrsquoduikerCephalophusadersiandotherantelopespeciesBiodiversity and Conservation 24(3) 641ndash658 httpsdoiorg101007s10531‐014‐0842‐z
Attum O (2007) Can landscape use be among the factors that po‐tentiallymake some ungulates speciesmore difficult to conserveJournal of Arid Environments69(3)410ndash419
Bahaa‐el‐dinLHenschelPAbaaRAbernethyKBohmTBoutNhellipLeeM (2013)NotesonthedistributionandstatusofsmallcarnivoresinGabonSmall Carnivore Conservation4819ndash29
Bahaa‐el‐dinLHenschelPButynskiTMMacdonaldDWMillsDSlotowRampHunterL (2015)TheAfricangoldencatCaracalaurataAfricasleast‐knownfelidMammal Review45(1)63ndash77
Bennett E L Blencowe E Brandon K Brown D Burn R WCowlishaw G hellip Robinson J G (2007) Hunting for consensusReconcilingbushmeatharvestconservationanddevelopmentpol‐icyinWestandCentralAfricaConservation Biology21(3)884ndash887httpsdoiorg101111j1523‐1739200600595x
BlakeSDeemSLMossimboEMaiselsFampWalshP(2009)Forestelephants Tree planters of the CongoBiotropica41(4) 459ndash468httpsdoiorg101111j1744‐7429200900512x
Blake S (2002) The ecology of forest elephant distribution and itsimplications for conservation Doctoral dissertation University ofEdinburgh
BruceTNdjassiCFowlerANdimbeMFankemOTabueRhellipOlsonD(2018)Faunal inventory of the Dja Faunal Reserve Cameroon Yaoundeacute Cameroon Ministry of Forests and Wildlife (MINFOF)Zoological Society of London ndash Cameroon Country ProgrammeAfricanWildlifeFoundation
BruceTWacherTNdingaHBidjokaVMeyongFNgoBataMampOlsonD(2017)camera trap survey for larger terrestrial wildlife in the Dja Biosphere Reserve CameroonYaoundeacuteCameroonZoologicalSocietyofLondon(ZSL)ampCameroonMinistryofForestsandWildlife(MINFOF)
BurnhamKPampAndersonDR(2002)Model selection and multimodel inferenceNewYorkNYSpringer
Campbell G Kuehl H Diarrassouba A NGoran P K amp BoeschC (2011) Long‐term research sites as refugia for threatened andover‐harvested species Biology Letters 7(5) 723ndash726 httpsdoiorg101098rsbl20110155
CardilloMMaceGMJonesKEBielbyJBininda‐EmondsORSechrestWhellipPurvisA(2005)Multiplecausesofhighextinction
riskinlargemammalspeciesScience309(5738)1239ndash1241httpsdoiorg101126science1116030
Craigie IDBaillieJEBalmfordACarboneCCollenBGreenREampHuttonJM (2010)Largemammalpopulationdeclines inAfricarsquosprotectedareasBiological Conservation143(9)2221ndash2228httpsdoiorg101016jbiocon201006007
DaveyKWacherTampAminR(2017)Analysis tool for camera-trap sur-vey data [Computer software]ZoologicalSocietyofLondonRetrievedfromhttpswwwzslorgzsl‐camera‐trap‐data‐management‐ and‐analysis‐package
Djuikouo M N K Doucet J L Nguembou C K Lewis S L ampSonkeacute B (2010) Diversity and aboveground biomass in threetropical forest types in the Dja Biosphere Reserve Cameroon African Journal of Ecology 48(4) 1053ndash1063 httpsdoiorg101111j1365‐2028201001212x
DupainJBombomeKampVanElsackerL(2003)LeschimpanzeacutesetlesgorillesdelareacuteservedefauneduDjaCanopeacutee2414ndash15
EffordMGampDawsonDK(2012)OccupancyincontinuoushabitatEcosphere3(4)1ndash15httpsdoiorg101890ES11‐003081
Efron B amp Tibshirani R J (1994) An introduction to the bootstrap WashingtonDCCRCPress
FaJEOliveroJFarfaacutenMAacuteMaacuterquezALDuarteJNackoneyJhellipMacdonaldDW(2014a)CorrelatesofbushmeatinmarketsanddepletionofwildlifeConservation Biology29(3)805ndash815
Fa J EOlivero J FarfaacutenMAacuteMaacuterquezA LVargas JMRealRampNasiR(2014b)IntegratingsustainablehuntinginbiodiversityprotectioninCentralAfricaHotspotsweakspotsandstrongspotsPLoS ONE9(11)e112367
FaJERyanSFampBellDJ (2005)Huntingvulnerabilityecolog‐ical characteristics and harvest rates of bushmeat species in afro‐tropicalforestsBiological Conservation121(2)167ndash176httpsdoiorg101016jbiocon200404016
Fa J E Seymour S Dupain J E F Amin R Albrechtsen L ampMacdonaldD (2006) Getting to gripswith themagnitude of ex‐ploitationBushmeat in theCross‐SanagariversregionNigeria and Cameroon Biological Conservation 129(4) 497ndash510 httpsdoiorg101016jbiocon200511031
Farris Z J Boone H M Karpanty S Murphy A Ratelolahy FAndrianjakariveloVampKellyMJ(2015)FeralcatsandthefitoatyFirstpopulationassessmentoftheblackforestcatinMadagascarrsquosrainforestsJournal of Mammalogy97(2)518ndash525
Fiske IampChandlerR (2011)UnmarkedAnRpackageforfittinghi‐erarchicalmodelsofwildlifeoccurrenceandabundanceJournal of Statistical Software43(10)1ndash23
HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences107(19)8650ndash8655httpsdoiorg101073pnas0912668107
HartJ(2013a)WaterchevrotainHymemoschusaquaticusInJKingdonampMHoffmann (Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp88ndash92)LondonUKBloomsbury
Hart J (2013b) White‐bellied duiker Cephalophus leucogaster In JKingdonampMHoffmann(Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp255ndash258)LondonUKBloomsbury
HeadJSRobbinsMMMundryRMakagaLampBoeschC(2012)Remotevideo‐cameratrapsmeasurehabitatuseandcompetitiveex‐clusionamongsympatricchimpanzeegorillaandelephantinLoangoNational ParkGabon Journal of Tropical Ecology28(06) 571ndash583httpsdoiorg101017S0266467412000612
HedgesS(2012)Monitoring elephant populations and assessing threats HimayatnagarTelanganaUniversitiesPress
HedwigDKienastIBonnetMCurranBKCourageABoeschChellipKingT(2018)Acameratrapassessmentoftheforestmam‐mal community within the transitional savannah‐forest mosaic oftheBateacutekeacutePlateauNationalParkGabonAfrican Journal of Ecology56(4)777ndash790httpsdoiorg101111aje12497
emspensp emsp | emsp775Bruce et al
HijmansRJCameronSEParraJLJonesPGampJarvisA(2005)Very high resolution interpolated climate surfaces for global landareasInternational Journal of Climatology25(15)1965ndash1978httpsdoiorg101002joc1276
HuggelA(2012)Exiv2softwaretool[Computersoftware]Retrievedfromhttpswwwexiv2orgindexhtml
Jerozolimski A amp Peres C A (2003) Bringing home the biggestbacon A cross‐site analysis of the structure of hunter‐kill profilesin Neotropical forests Biological Conservation 111(3) 415ndash425httpsdoiorg101016S0006‐3207(02)00310‐5
KingdonJ (2015)The Kingdon field guide to African mammalsLondonUKBloomsburyPublishing
KuumlhlHFMaiselsMAncrenazampEAWilliamson(Eds)(2008)Best practice guidelines for surveys and monitoring of great ape populations GlandSwitzerlandIUCN
LauranceWFCroesBMTchignoumbaLLahmSAAlonsoALeeMEhellipOndzeanoC(2006)ImpactsofroadsandhuntingoncentralAfrican rainforestmammalsConservation Biology20(4)1251ndash1261httpsdoiorg101111j1523‐1739200600420x
LauranceWFUsecheDCRendeiroJKalkaMBradshawCJSloan S P hellip Arroyo‐Rodriguez V (2012) Averting biodiversitycollapse in tropical forestprotectedareasNature489(7415)290httpsdoiorg101038nature11318
LeslieDMampHuffmanBA(2015)Potamochoerus porcus(ArtiodactylaSuidae)Mammalian Species4715ndash31
MacKenzieD IampBailey L L (2004)Assessing the fit of site‐occu‐pancy models Journal of Agricultural Biological and Environmental Statistics9300ndash318httpsdoiorg101198108571104X3361
MacKenzieDINicholsJDRoyleJAPollockKHBaileyLLampHinesJE (2006)Occupancy estimation and modellingBurlingtonMAAcademicPress
Magurran A E (2005) Species abundance distributions Patternor process Functional Ecology 19(1) 177ndash181 httpsdoiorg101111j0269‐8463200500930x
MaiselsFStrindbergSBlakeSWittemyerGHartJWilliamsonEAhellipWarrenY (2013)DevastatingdeclineofforestelephantsinCentralAfricaPLoS ONE8(3)e59469httpsdoiorg101371journalpone0059469
MalhiYAdu‐BreduSAsareRA LewisS LampMayauxP (2013)AfricanrainforestsPastpresentandfuturePhilosophical Transactions of the Royal Society of London Biological Sciences 368(1625)20120312
MallonDPHoffmannMGraingerMJHibertFVanVlietNampMcGowanP JK (2015)An IUCNsituationanalysisof terrestrialandfreshwaterfaunainWestandCentralAfricaOccasionalpaperoftheIUCNspeciessurvivalcommission(54)
MambeyaMMBakerFMombouaBRKoumbaPamboAFHegaMOkouyiOkouyiVJhellipAbernethyK(2018)TheemergenceofacommercialtradeinpangolinsfromGabonAfrican Journal of Ecology56(3)601ndash609httpsdoiorg101111aje12507
MINFOFampIUCN(2015)CaracteacuterisationdelapopulationdegrandsetmoyensmammifegraveresdanslaReservedeFauneduDjaPotentieletmenacesYaoundeacuteCameroun
Muchaal P K amp Ngandjui G (1999) Impact of village hunt‐ing on wildlife populations in the western Dja ReserveCameroon Conservation Biology 13(2) 385ndash396 httpsdoiorg101046j1523‐17391999013002385x
NaranjoEJampBodmerRE (2007) Sourcendashsink systemsandconser‐vationofhuntedungulatesintheLacandonForestMexico Biological Conservation 138(3ndash4) 412ndash420 httpsdoiorg101016jbiocon 200705010
NielsenMR(2006)ImportancecauseandeffectofbushmeathuntingintheUdzungwaMountainsTanzania ImplicationsforcommunitybasedwildlifemanagementBiological Conservation128(4)509ndash516httpsdoiorg101016jbiocon200510017
OBrienTGKinnairdMFampWibisonoHT (2003)Crouching ti‐gers hiddenprey Sumatran tiger andprey populations in a tropi‐calforestlandscapeAnimal Conservation6(2)131ndash139httpsdoiorg101017S1367943003003172
OksanenJ(2015)VegananintroductiontoordinationVol8(p19)Retrieved from httpscranr‐projectorgwebpackagesveganvi‐gnettesintroveganpdf
PeresCAampPalaciosE(2007)Basin‐wideeffectsofgameharvestonvertebrate populationdensities inAmazonian forests Implicationsfor animal‐mediated seed dispersal Biotropica 39(3) 304ndash315httpsdoiorg101111j1744‐7429200700272x
PotapovPVTurubanovaSAHansenMCAduseiBBroichMAltstattAhellipJusticeCO(2012)QuantifyingforestcoverlossinDemocraticRepublicoftheCongo2000ndash2010withLandsatETM+data Remote Sensing of Environment 122 106ndash116 httpsdoiorg101016jrse201108027
PoulsenJRKoernerSEMooreSMedjibeVPBlakeSClarkC JhellipRosinC (2017) Poaching empties criticalCentralAfricanwilderness of forest elephants Current Biology 27(4) 134ndashR135httpsdoiorg101016jcub201701023
PurvisAGittlemanJlCowlishawGampMaceGM(2000)PredictingextinctionriskindecliningspeciesProceedings of the Royal Society B Biological Sciences267(1456) 1947ndash1952 httpsdoiorg101098rspb20001234
RayJ(1997)ComparativeecologyoftwoAfricanforestmongoosesHerpestesnasoandAtilaxpaludinosusAfrican Journal of Ecology35(3)237ndash253httpsdoiorg101111j1365‐20281997086‐ 89086x
Redford K H (1992) The empty forest BioScience 42(6) 412ndash422httpsdoiorg1023071311860
RepublicofCameroon(1994)Lawno9401du20janvier1994portantreacutegimedesforecirctsdelafauneetdelapecirccheRepublicofCameroon
RoveroFampMarshallAR(2009)CameratrappingphotographicrateasanindexofdensityinforestungulatesJournal of Applied Ecology46(5)1011ndash1017httpsdoiorg101111j1365‐2664200901705x
Royle J A amp Nichols J D (2003) Estimating abundance from re‐peated presence‐absence data or point counts Ecology 84(3)777ndash790 httpsdoiorg1018900012‐9658(2003)084[0777EAFRPA]20CO2
Seddon P J Griffiths C J Soorae P S ampArmstrongD P (2014)ReversingdefaunationRestoringspeciesinachangingworldScience345(6195)406ndash412httpsdoiorg101126science1251818
Silveira L Jacomo A T amp Diniz‐Filho J A F (2003) Camera trapline transect census and track surveys A comparative evaluationBiological Conservation 114(3) 351ndash355 httpsdoiorg101016S0006‐3207(03)00063‐6
Sonkeacute B (1998) Etudes floristiques et structurales des forecircts de laReacuteserve de Faune du Dja (Cameroun) Laboratoire de BotaniqueSysteacutematique et de Phytosociologie Universiteacute Libre de Bruxelles(ULB)
Srbek‐AraujoACampChiarelloAG(2005)Iscameratrappinganeffi‐cientmethodforsurveyingmammalsinNeotropicalforestsAcasestudyinsouth‐easternBrazilJournal of Tropical Ecology21(1)121ndash125httpsdoiorg101017S0266467404001956
Stiles D (2011) Elephant meat and ivory trade in Central AfricaPachyderm5026ndash36
TEAMNetwork(2008)Terrestrialvertebrateprotocol implementationmanualv30(p56)WashingtonDCTropicalEcologyAssessmentandMonitoringNetworkCenter forAppliedBiodiversity ScienceConservationInternational
Tobler M W Carrillo‐Percastegui S E Leite Pitman R MaresR amp Powell G (2008) An evaluation of camera traps for in‐ventorying large‐and medium‐sized terrestrial rainforestmammals Animal Conservation 11(3) 169ndash178 httpsdoiorg101111j1469‐1795200800169x
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
770emsp |emsp emspensp Bruce et al
relationshipwithdistancetotheboundarycouldbeinfluencingoccu‐pancyIntheSouthernSectortheoccupancyincreasedwithdistanceto theboundary forwestern lowlandgorillaandgiantpangolinbutdecreasedforAfricangoldencatwhite‐belliedduikerandwaterchev‐rotainIntheNorthernSectoroccupancyincreasedwithdistancetotheboundaryforBatesrsquospygmyantelope
4emsp |emspDISCUSSION
Thecomparisonofthetwosurveysconfirmsthatstandardcameratrap surveys and derived metrics of presenceabsence trappingrates andoccupancy candiscern confidentdifferences in ground‐dwellingmammalcommunitiesinCentralAfricanforests
41emsp|emspCamera trap surveys for documenting species
Thecomparativeefficacyofcamera traps for surveyingmediumto large ground‐dwelling mammals in the DFR is indicated byobservationratesandverifiabilityofrecordsespeciallyofelusivesmallerandnocturnalspeciesForexamplethedirectencounterraterecordedbyrangersonpatrolthroughouttheentirereserveover a nine‐month period is much lower than the combinednumberofindependentphotographiceventsinbothmanagementsectors (ZSL amp MINFOF 2017b) even for relatively largeconspicuous species such as forest elephant (96 photographiceventscomparedto29directencounters)andcentralchimpanzee(204 independent photographic events compared to 23 directencounters)Methodologiessuchascameratrapping therefore
provideimportantbaselinedatathatwhenrepeatedthroughtimeusingastandardisedprotocolcanallowatleasttrendsinrelativeabundanceindicestobemonitored
42emsp|emspCamera trap surveys for comparing assemblages among sites
Despitebeingseparatedbyonlyc32kmthemammalcommunitiesbetween the twocamera trapgridsdisplayedmarkeddifferencesThiswasthecaseeventhoughbothgridshadlowShannonndashWeinerandSimpsonsdiversityindicesduetothedominanceofthreeorfourspeciesineachcameratrapgridSignificantdifferencesamongthesiteswere observed for the trapping rates of species of differentsizesbetweensectorsSmaller‐bodiedspecieswithintheherbivoreand omnivore guilds were more prevalent within the NorthernSector (Figure 2) Trapping rates and occupancy values for smallcarnivoresarealsolowerintheSouthernSectorThiscouldbeduetothedifficultyofidentifyingmorphologicallysimilarspeciessuchasmarshmongooseandlong‐nosedmongoose(Bahaa‐el‐dinetal2013 Ray 1997) in infrared imagery with single cameras Thereweremoreunidentifiablemongooseeventsthatwereclassifiedtoafamilylevel―66224intheSouthernSectorcomparedto29156intheNorthernSectorofallcombinedmongooseevents
43emsp|emspThe potential impact of seasonality on estimates derived from camera traps
Due to logistical and financial constraints the surveys could notberuninthesameseasonThishasthepotentialtoaffecttrapping
F I G U R E 5 emspChangeintheprobabilityofoccupancyforblack‐leggedmongoosecentralchimpanzeeandCamerooncusimansewithmanagementsectoraccordingtoaRoylendashNicholsmodel
emspensp emsp | emsp771Bruce et al
rates and occupancy for specieswith larger home ranges becausewhenspeciesarewide‐rangingoccupancycanproveineffectiveformeasuring relative abundance Forest elephants (Blake 2002) andgreatapesareknowntodisplayseasonalshiftsintheirhabitatusageover great distances in response to increased fruit availability andprecipitation(HeadRobbinsMundryMakagaampBoesch2012)Thiscouldalsoinfluenceothergregariousspeciessuchasredriverhogthatarealsothoughttooccasionallydisplaysimilaraggregationsandmovementsinresponsetomastingevents(LeslieampHuffman2015)However as both red river hog and chimpanzee had significantlyhigherRAIandhigheroccupancywithvariabledetectionprobabilityaccording to the number of individuals incorporated this supports
thepossibilitythatthesespeciesarefavouringtheSouthernSectorIfmanagersareable toestablishwhetherwide‐rangingspeciesarepredictably moving to known areas within the reserve they canrespondinamannerthatprovidesenhancedprotectiontovulnerablewildlifepopulations in concentration areasAsmost species in thissurveylikelyhaveasmallerhomerangethantheinter‐trapdistanceand display fixed territories it can be regarded as appropriate tocompare occupancy values as the extent of overlap of territorieswithin the two surveys are unlikely to change in such away as toaffecttheresultsFuturestudieswouldbenefitfromtryingtomatchcameratrapsurveysseasonallytotryandclarifytheissueofseasonalshiftsinhabitatusagewithintheDFR
F I G U R E 6 emspChangeintheprobabilityofoccupancyforAfricanbrush‐tailedporcupineEminspouchedratredriverhogservalinegenetPetersrsquoduikerandyellow‐backedduikerwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
772emsp |emsp emspensp Bruce et al
F I G U R E 7 emspChangeintheprobabilityofoccupancyforblueduikerandbayduikerwithdistancetotheboundaryinkilometresacrossbothmanagementsectorsaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
F I G U R E 8 emspChangeintheprobabilityofoccupancyforwhite‐belliedpangolinwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaMackenzieoccupancymodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
emspensp emsp | emsp773Bruce et al
44emsp|emspCamera trap surveys for measuring the impacts of hunting on mammal communities
The spatial scale at which mammal communities are affected byandhowpopulationsrespondtoanthropogenicpressuressuchasbushmeat hunting is difficult to empiricallymeasure (Laurance etal2006)Thisisespeciallytrueformammalsresidingwithintropi‐cal forestswheregatheringconsistentandmeaningfulpopulation‐andcommunity‐levelmetrics ischallenging(Ahumadaetal2013)Population density of tropical mammals can vary greatly due toheterogeneity present within the environment For example for‐est elephants havedifferent distributions and aggregations inwetanddryseasonsinNouabaleacute‐Ndoki NationalParkwhichispartiallydependentonspatio‐temporalpatternsoffruitingtreesacrossthelandscape(Blake2002)
Whether the differences observed among the two sites sur‐veyedhereareattributabletodifferent levelsofhuntingpressureremains to be confirmed There are however indications thathuntingpressureanditsimpactsonmammalfaunasaregreaterintheNorthern Sector than in the Southern Sector The effects ofhuntingpressureonmammaliandeclinesinCentralAfricanforestsarewell documented The pattern in general is the largest‐bod‐ied species frugivores and thosewith high hunter or blackmar‐ketvalue(Abernethyetal2013Cardilloetal2005FaOliveroFarfaacutenMaacuterquezDuarteetal2014aFaOliveroFarfaacutenMaacuterquezVargasetal2014bPeresampPalacios2007)arethefirstspeciestoshownoticeabledeclineInthisstudythesignificantdeclineintherelativeabundance for frugivores suchasPetersʼduikerandspe‐cieswithhighhuntervalueliketheredriverhogunderincreasedhuntingpressure in theNorthernSector is reported inother sur‐veys(Abernethyetal2013)Thisisalsoreflectedinthedifferencesobserved in this study in biomass in the different guilds of eachmammalcommunityThemammalcommunitywithintheNorthernSector shows indications of a community that is disturbed and isexperiencingelevatedhuntingpressureThesearehigher(camera)trapping rates for smaller‐bodiedspecies suchasEminrsquospouchedrat and significantly fewer encounters of larger‐bodiedmammalsthataretargetsofthebushmeattradesuchasPetersʼduikerandredriverhog(FaRyanampBell2005JerozolimskiampPeres2003)Additionalindicatorsaretheabsenceinthesurveysoflargercarni‐voresintheNorthernSectorsuchasgoldencatandleopardwhicharesensitivetosnaring(Bahaa‐el‐dinetal2015)andsignificantlyreducedabundancemetricsfordisturbance‐sensitivespeciessuchasblack‐leggedmongooseandwaterchevrotain(Hart2013a)Theabsence of white‐bellied duiker in the Northern Sector also sug‐gestselevatedhumandisturbanceasthisspecieshasbeenreportedasverysensitivetoevenminorperturbationwithintheenvironment(Hart2013b)IncomparisontheSouthernSectorcontainedindica‐torfaunasuchasthewhite‐belliedduikerandhadhighertrappingratesforlarger‐bodiedspecies
WesuspectthedifferencesobservedaremostlikelyduetolowerhumandisturbanceintheSouthernSectorTheteamsdeployingand
recoveringthecamerasintheSouthernSectorcovered238kmandencountered few signs of humanperturbation (T Brucepers obs)whereashumansignwascommonlyencounteredbytheteamsintheNorthernSectorThisperceiveddifference is reflected in the2017and 2018 density of hunting signwithin each camera trap grid asdetected throughMINFOF ranger patrols (ZSL ampMINFOF 2017a2017b) and through the2018DistanceSampling inventory for theDFR (Bruce et al 2018) Higher numbers of hunting sign in theNorthernSectorwouldbeconsistentwithanelevatedhuntingpres‐sureinthatarea
45emsp|emspProtection of refugia from hunting
Though inferences made for wide‐ranging species such as forestelephantsandgreatapesusingcameratrapsaredifficultthefactthattrappingrateswerehigherinmorechallengingterrainwithassumedlower hunting pressure could be indicative of complex habitatprovidingsomelevelofprotectionfromhuntingElephantisknownto retreatwhen they aredisturbed to terrain that ismoredifficulttoaccessbyhumans (Hedges2012)Thuswithin largerprotectedareas certain zones may act as refugia for wildlife populations(Campbelletal2011)Thiscanbeduetoarangeof factorssuchas remoteanddifficult terrain forpoachers (Attum2007Hedges2012) or the regular presence of field researchers and rangers(Campbell et al 2011) The significanceof these refugia for largerprotected areas is that the populations of wildlife residing withinthem if adequately protected may provide source populations toallowrecolonisationofotherareasofthereserve(NaranjoampBodmer2007)Thereforeifadequateprotectioncanbeprovidedtorelativelysmallbutimportantareasoflargereservesthismayprovidetropicalforestswithabetterchanceofbeingecologicallyresilienttoongoingand increasing human perturbation Well‐designed camera trapsurveys may provide data on the status of wildlife populations atrelativelyfinespatialresolutionssoastoidentifyfunctionalrefugiawithgreaterconfidence
ACKNOWLEDG EMENTS
WeappreciatetheongoingsupportofCameroonrsquosMinistryofForestsandWildlife(MINFOF)andtheopportunitytocontributetobiodiver‐sityconservationthroughoutthecountryInparticularwewouldliketothanktheChefdrsquoAntenneSergeJacobMeyeforhisongoingsup‐portofconservationresearchwithintheprotectedareaWeappreci‐atethestalwarteffortsofMINFOFecoguardsandlocalporterswhoaccompaniedthesurveyteamsinthefieldWewouldalsoliketothanktheUnitedStatesFishandWildlifeService(USFWS)mdashAfricanElephantConservationandIUCNSOSmdashFondationSegreacutePangolinConservationInitiativeforsupportingthiswork
ORCID
Tom Bruce httporcidorg0000‐0001‐6958‐1657
774emsp |emsp emspensp Bruce et al
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AbrahamsM I Peres C A amp Costa H C (2017)Measuring localdepletion of terrestrial game vertebrates by central‐place hunt‐ers in rural Amazonia PLoS ONE 12(10) e0186653 httpsdoiorg101371journalpone0186653
AhumadaJAHurtadoJampLizcanoD(2013)MonitoringthestatusandtrendsoftropicalforestterrestrialvertebratecommunitiesfromcameratrapdataAtool forconservationPLoS ONE8(9)e73707httpsdoiorg101371journalpone0073707
Ahumada J A Silva C E Gajapersad K Hallam C Hurtado JMartin E hellip Sheil D (2011) Community structure and diver‐sity of tropical forest mammals Data from a global camera trapnetwork Philosophical Transactions of the Royal Society of London Biological Sciences366(1578)2703ndash2711httpsdoiorg101098rstb20110115
AminRAndanjeSAOgwonkaBAliAHBowkettAEOmarMampWacherT(2015)ThenortherncoastalforestsofKenyaarenationally and globally important for the conservation of AdersrsquoduikerCephalophusadersiandotherantelopespeciesBiodiversity and Conservation 24(3) 641ndash658 httpsdoiorg101007s10531‐014‐0842‐z
Attum O (2007) Can landscape use be among the factors that po‐tentiallymake some ungulates speciesmore difficult to conserveJournal of Arid Environments69(3)410ndash419
Bahaa‐el‐dinLHenschelPAbaaRAbernethyKBohmTBoutNhellipLeeM (2013)NotesonthedistributionandstatusofsmallcarnivoresinGabonSmall Carnivore Conservation4819ndash29
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Bennett E L Blencowe E Brandon K Brown D Burn R WCowlishaw G hellip Robinson J G (2007) Hunting for consensusReconcilingbushmeatharvestconservationanddevelopmentpol‐icyinWestandCentralAfricaConservation Biology21(3)884ndash887httpsdoiorg101111j1523‐1739200600595x
BlakeSDeemSLMossimboEMaiselsFampWalshP(2009)Forestelephants Tree planters of the CongoBiotropica41(4) 459ndash468httpsdoiorg101111j1744‐7429200900512x
Blake S (2002) The ecology of forest elephant distribution and itsimplications for conservation Doctoral dissertation University ofEdinburgh
BruceTNdjassiCFowlerANdimbeMFankemOTabueRhellipOlsonD(2018)Faunal inventory of the Dja Faunal Reserve Cameroon Yaoundeacute Cameroon Ministry of Forests and Wildlife (MINFOF)Zoological Society of London ndash Cameroon Country ProgrammeAfricanWildlifeFoundation
BruceTWacherTNdingaHBidjokaVMeyongFNgoBataMampOlsonD(2017)camera trap survey for larger terrestrial wildlife in the Dja Biosphere Reserve CameroonYaoundeacuteCameroonZoologicalSocietyofLondon(ZSL)ampCameroonMinistryofForestsandWildlife(MINFOF)
BurnhamKPampAndersonDR(2002)Model selection and multimodel inferenceNewYorkNYSpringer
Campbell G Kuehl H Diarrassouba A NGoran P K amp BoeschC (2011) Long‐term research sites as refugia for threatened andover‐harvested species Biology Letters 7(5) 723ndash726 httpsdoiorg101098rsbl20110155
CardilloMMaceGMJonesKEBielbyJBininda‐EmondsORSechrestWhellipPurvisA(2005)Multiplecausesofhighextinction
riskinlargemammalspeciesScience309(5738)1239ndash1241httpsdoiorg101126science1116030
Craigie IDBaillieJEBalmfordACarboneCCollenBGreenREampHuttonJM (2010)Largemammalpopulationdeclines inAfricarsquosprotectedareasBiological Conservation143(9)2221ndash2228httpsdoiorg101016jbiocon201006007
DaveyKWacherTampAminR(2017)Analysis tool for camera-trap sur-vey data [Computer software]ZoologicalSocietyofLondonRetrievedfromhttpswwwzslorgzsl‐camera‐trap‐data‐management‐ and‐analysis‐package
Djuikouo M N K Doucet J L Nguembou C K Lewis S L ampSonkeacute B (2010) Diversity and aboveground biomass in threetropical forest types in the Dja Biosphere Reserve Cameroon African Journal of Ecology 48(4) 1053ndash1063 httpsdoiorg101111j1365‐2028201001212x
DupainJBombomeKampVanElsackerL(2003)LeschimpanzeacutesetlesgorillesdelareacuteservedefauneduDjaCanopeacutee2414ndash15
EffordMGampDawsonDK(2012)OccupancyincontinuoushabitatEcosphere3(4)1ndash15httpsdoiorg101890ES11‐003081
Efron B amp Tibshirani R J (1994) An introduction to the bootstrap WashingtonDCCRCPress
FaJEOliveroJFarfaacutenMAacuteMaacuterquezALDuarteJNackoneyJhellipMacdonaldDW(2014a)CorrelatesofbushmeatinmarketsanddepletionofwildlifeConservation Biology29(3)805ndash815
Fa J EOlivero J FarfaacutenMAacuteMaacuterquezA LVargas JMRealRampNasiR(2014b)IntegratingsustainablehuntinginbiodiversityprotectioninCentralAfricaHotspotsweakspotsandstrongspotsPLoS ONE9(11)e112367
FaJERyanSFampBellDJ (2005)Huntingvulnerabilityecolog‐ical characteristics and harvest rates of bushmeat species in afro‐tropicalforestsBiological Conservation121(2)167ndash176httpsdoiorg101016jbiocon200404016
Fa J E Seymour S Dupain J E F Amin R Albrechtsen L ampMacdonaldD (2006) Getting to gripswith themagnitude of ex‐ploitationBushmeat in theCross‐SanagariversregionNigeria and Cameroon Biological Conservation 129(4) 497ndash510 httpsdoiorg101016jbiocon200511031
Farris Z J Boone H M Karpanty S Murphy A Ratelolahy FAndrianjakariveloVampKellyMJ(2015)FeralcatsandthefitoatyFirstpopulationassessmentoftheblackforestcatinMadagascarrsquosrainforestsJournal of Mammalogy97(2)518ndash525
Fiske IampChandlerR (2011)UnmarkedAnRpackageforfittinghi‐erarchicalmodelsofwildlifeoccurrenceandabundanceJournal of Statistical Software43(10)1ndash23
HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences107(19)8650ndash8655httpsdoiorg101073pnas0912668107
HartJ(2013a)WaterchevrotainHymemoschusaquaticusInJKingdonampMHoffmann (Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp88ndash92)LondonUKBloomsbury
Hart J (2013b) White‐bellied duiker Cephalophus leucogaster In JKingdonampMHoffmann(Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp255ndash258)LondonUKBloomsbury
HeadJSRobbinsMMMundryRMakagaLampBoeschC(2012)Remotevideo‐cameratrapsmeasurehabitatuseandcompetitiveex‐clusionamongsympatricchimpanzeegorillaandelephantinLoangoNational ParkGabon Journal of Tropical Ecology28(06) 571ndash583httpsdoiorg101017S0266467412000612
HedgesS(2012)Monitoring elephant populations and assessing threats HimayatnagarTelanganaUniversitiesPress
HedwigDKienastIBonnetMCurranBKCourageABoeschChellipKingT(2018)Acameratrapassessmentoftheforestmam‐mal community within the transitional savannah‐forest mosaic oftheBateacutekeacutePlateauNationalParkGabonAfrican Journal of Ecology56(4)777ndash790httpsdoiorg101111aje12497
emspensp emsp | emsp775Bruce et al
HijmansRJCameronSEParraJLJonesPGampJarvisA(2005)Very high resolution interpolated climate surfaces for global landareasInternational Journal of Climatology25(15)1965ndash1978httpsdoiorg101002joc1276
HuggelA(2012)Exiv2softwaretool[Computersoftware]Retrievedfromhttpswwwexiv2orgindexhtml
Jerozolimski A amp Peres C A (2003) Bringing home the biggestbacon A cross‐site analysis of the structure of hunter‐kill profilesin Neotropical forests Biological Conservation 111(3) 415ndash425httpsdoiorg101016S0006‐3207(02)00310‐5
KingdonJ (2015)The Kingdon field guide to African mammalsLondonUKBloomsburyPublishing
KuumlhlHFMaiselsMAncrenazampEAWilliamson(Eds)(2008)Best practice guidelines for surveys and monitoring of great ape populations GlandSwitzerlandIUCN
LauranceWFCroesBMTchignoumbaLLahmSAAlonsoALeeMEhellipOndzeanoC(2006)ImpactsofroadsandhuntingoncentralAfrican rainforestmammalsConservation Biology20(4)1251ndash1261httpsdoiorg101111j1523‐1739200600420x
LauranceWFUsecheDCRendeiroJKalkaMBradshawCJSloan S P hellip Arroyo‐Rodriguez V (2012) Averting biodiversitycollapse in tropical forestprotectedareasNature489(7415)290httpsdoiorg101038nature11318
LeslieDMampHuffmanBA(2015)Potamochoerus porcus(ArtiodactylaSuidae)Mammalian Species4715ndash31
MacKenzieD IampBailey L L (2004)Assessing the fit of site‐occu‐pancy models Journal of Agricultural Biological and Environmental Statistics9300ndash318httpsdoiorg101198108571104X3361
MacKenzieDINicholsJDRoyleJAPollockKHBaileyLLampHinesJE (2006)Occupancy estimation and modellingBurlingtonMAAcademicPress
Magurran A E (2005) Species abundance distributions Patternor process Functional Ecology 19(1) 177ndash181 httpsdoiorg101111j0269‐8463200500930x
MaiselsFStrindbergSBlakeSWittemyerGHartJWilliamsonEAhellipWarrenY (2013)DevastatingdeclineofforestelephantsinCentralAfricaPLoS ONE8(3)e59469httpsdoiorg101371journalpone0059469
MalhiYAdu‐BreduSAsareRA LewisS LampMayauxP (2013)AfricanrainforestsPastpresentandfuturePhilosophical Transactions of the Royal Society of London Biological Sciences 368(1625)20120312
MallonDPHoffmannMGraingerMJHibertFVanVlietNampMcGowanP JK (2015)An IUCNsituationanalysisof terrestrialandfreshwaterfaunainWestandCentralAfricaOccasionalpaperoftheIUCNspeciessurvivalcommission(54)
MambeyaMMBakerFMombouaBRKoumbaPamboAFHegaMOkouyiOkouyiVJhellipAbernethyK(2018)TheemergenceofacommercialtradeinpangolinsfromGabonAfrican Journal of Ecology56(3)601ndash609httpsdoiorg101111aje12507
MINFOFampIUCN(2015)CaracteacuterisationdelapopulationdegrandsetmoyensmammifegraveresdanslaReservedeFauneduDjaPotentieletmenacesYaoundeacuteCameroun
Muchaal P K amp Ngandjui G (1999) Impact of village hunt‐ing on wildlife populations in the western Dja ReserveCameroon Conservation Biology 13(2) 385ndash396 httpsdoiorg101046j1523‐17391999013002385x
NaranjoEJampBodmerRE (2007) Sourcendashsink systemsandconser‐vationofhuntedungulatesintheLacandonForestMexico Biological Conservation 138(3ndash4) 412ndash420 httpsdoiorg101016jbiocon 200705010
NielsenMR(2006)ImportancecauseandeffectofbushmeathuntingintheUdzungwaMountainsTanzania ImplicationsforcommunitybasedwildlifemanagementBiological Conservation128(4)509ndash516httpsdoiorg101016jbiocon200510017
OBrienTGKinnairdMFampWibisonoHT (2003)Crouching ti‐gers hiddenprey Sumatran tiger andprey populations in a tropi‐calforestlandscapeAnimal Conservation6(2)131ndash139httpsdoiorg101017S1367943003003172
OksanenJ(2015)VegananintroductiontoordinationVol8(p19)Retrieved from httpscranr‐projectorgwebpackagesveganvi‐gnettesintroveganpdf
PeresCAampPalaciosE(2007)Basin‐wideeffectsofgameharvestonvertebrate populationdensities inAmazonian forests Implicationsfor animal‐mediated seed dispersal Biotropica 39(3) 304ndash315httpsdoiorg101111j1744‐7429200700272x
PotapovPVTurubanovaSAHansenMCAduseiBBroichMAltstattAhellipJusticeCO(2012)QuantifyingforestcoverlossinDemocraticRepublicoftheCongo2000ndash2010withLandsatETM+data Remote Sensing of Environment 122 106ndash116 httpsdoiorg101016jrse201108027
PoulsenJRKoernerSEMooreSMedjibeVPBlakeSClarkC JhellipRosinC (2017) Poaching empties criticalCentralAfricanwilderness of forest elephants Current Biology 27(4) 134ndashR135httpsdoiorg101016jcub201701023
PurvisAGittlemanJlCowlishawGampMaceGM(2000)PredictingextinctionriskindecliningspeciesProceedings of the Royal Society B Biological Sciences267(1456) 1947ndash1952 httpsdoiorg101098rspb20001234
RayJ(1997)ComparativeecologyoftwoAfricanforestmongoosesHerpestesnasoandAtilaxpaludinosusAfrican Journal of Ecology35(3)237ndash253httpsdoiorg101111j1365‐20281997086‐ 89086x
Redford K H (1992) The empty forest BioScience 42(6) 412ndash422httpsdoiorg1023071311860
RepublicofCameroon(1994)Lawno9401du20janvier1994portantreacutegimedesforecirctsdelafauneetdelapecirccheRepublicofCameroon
RoveroFampMarshallAR(2009)CameratrappingphotographicrateasanindexofdensityinforestungulatesJournal of Applied Ecology46(5)1011ndash1017httpsdoiorg101111j1365‐2664200901705x
Royle J A amp Nichols J D (2003) Estimating abundance from re‐peated presence‐absence data or point counts Ecology 84(3)777ndash790 httpsdoiorg1018900012‐9658(2003)084[0777EAFRPA]20CO2
Seddon P J Griffiths C J Soorae P S ampArmstrongD P (2014)ReversingdefaunationRestoringspeciesinachangingworldScience345(6195)406ndash412httpsdoiorg101126science1251818
Silveira L Jacomo A T amp Diniz‐Filho J A F (2003) Camera trapline transect census and track surveys A comparative evaluationBiological Conservation 114(3) 351ndash355 httpsdoiorg101016S0006‐3207(03)00063‐6
Sonkeacute B (1998) Etudes floristiques et structurales des forecircts de laReacuteserve de Faune du Dja (Cameroun) Laboratoire de BotaniqueSysteacutematique et de Phytosociologie Universiteacute Libre de Bruxelles(ULB)
Srbek‐AraujoACampChiarelloAG(2005)Iscameratrappinganeffi‐cientmethodforsurveyingmammalsinNeotropicalforestsAcasestudyinsouth‐easternBrazilJournal of Tropical Ecology21(1)121ndash125httpsdoiorg101017S0266467404001956
Stiles D (2011) Elephant meat and ivory trade in Central AfricaPachyderm5026ndash36
TEAMNetwork(2008)Terrestrialvertebrateprotocol implementationmanualv30(p56)WashingtonDCTropicalEcologyAssessmentandMonitoringNetworkCenter forAppliedBiodiversity ScienceConservationInternational
Tobler M W Carrillo‐Percastegui S E Leite Pitman R MaresR amp Powell G (2008) An evaluation of camera traps for in‐ventorying large‐and medium‐sized terrestrial rainforestmammals Animal Conservation 11(3) 169ndash178 httpsdoiorg101111j1469‐1795200800169x
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
emspensp emsp | emsp771Bruce et al
rates and occupancy for specieswith larger home ranges becausewhenspeciesarewide‐rangingoccupancycanproveineffectiveformeasuring relative abundance Forest elephants (Blake 2002) andgreatapesareknowntodisplayseasonalshiftsintheirhabitatusageover great distances in response to increased fruit availability andprecipitation(HeadRobbinsMundryMakagaampBoesch2012)Thiscouldalsoinfluenceothergregariousspeciessuchasredriverhogthatarealsothoughttooccasionallydisplaysimilaraggregationsandmovementsinresponsetomastingevents(LeslieampHuffman2015)However as both red river hog and chimpanzee had significantlyhigherRAIandhigheroccupancywithvariabledetectionprobabilityaccording to the number of individuals incorporated this supports
thepossibilitythatthesespeciesarefavouringtheSouthernSectorIfmanagersareable toestablishwhetherwide‐rangingspeciesarepredictably moving to known areas within the reserve they canrespondinamannerthatprovidesenhancedprotectiontovulnerablewildlifepopulations in concentration areasAsmost species in thissurveylikelyhaveasmallerhomerangethantheinter‐trapdistanceand display fixed territories it can be regarded as appropriate tocompare occupancy values as the extent of overlap of territorieswithin the two surveys are unlikely to change in such away as toaffecttheresultsFuturestudieswouldbenefitfromtryingtomatchcameratrapsurveysseasonallytotryandclarifytheissueofseasonalshiftsinhabitatusagewithintheDFR
F I G U R E 6 emspChangeintheprobabilityofoccupancyforAfricanbrush‐tailedporcupineEminspouchedratredriverhogservalinegenetPetersrsquoduikerandyellow‐backedduikerwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
772emsp |emsp emspensp Bruce et al
F I G U R E 7 emspChangeintheprobabilityofoccupancyforblueduikerandbayduikerwithdistancetotheboundaryinkilometresacrossbothmanagementsectorsaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
F I G U R E 8 emspChangeintheprobabilityofoccupancyforwhite‐belliedpangolinwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaMackenzieoccupancymodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
emspensp emsp | emsp773Bruce et al
44emsp|emspCamera trap surveys for measuring the impacts of hunting on mammal communities
The spatial scale at which mammal communities are affected byandhowpopulationsrespondtoanthropogenicpressuressuchasbushmeat hunting is difficult to empiricallymeasure (Laurance etal2006)Thisisespeciallytrueformammalsresidingwithintropi‐cal forestswheregatheringconsistentandmeaningfulpopulation‐andcommunity‐levelmetrics ischallenging(Ahumadaetal2013)Population density of tropical mammals can vary greatly due toheterogeneity present within the environment For example for‐est elephants havedifferent distributions and aggregations inwetanddryseasonsinNouabaleacute‐Ndoki NationalParkwhichispartiallydependentonspatio‐temporalpatternsoffruitingtreesacrossthelandscape(Blake2002)
Whether the differences observed among the two sites sur‐veyedhereareattributabletodifferent levelsofhuntingpressureremains to be confirmed There are however indications thathuntingpressureanditsimpactsonmammalfaunasaregreaterintheNorthern Sector than in the Southern Sector The effects ofhuntingpressureonmammaliandeclinesinCentralAfricanforestsarewell documented The pattern in general is the largest‐bod‐ied species frugivores and thosewith high hunter or blackmar‐ketvalue(Abernethyetal2013Cardilloetal2005FaOliveroFarfaacutenMaacuterquezDuarteetal2014aFaOliveroFarfaacutenMaacuterquezVargasetal2014bPeresampPalacios2007)arethefirstspeciestoshownoticeabledeclineInthisstudythesignificantdeclineintherelativeabundance for frugivores suchasPetersʼduikerandspe‐cieswithhighhuntervalueliketheredriverhogunderincreasedhuntingpressure in theNorthernSector is reported inother sur‐veys(Abernethyetal2013)Thisisalsoreflectedinthedifferencesobserved in this study in biomass in the different guilds of eachmammalcommunityThemammalcommunitywithintheNorthernSector shows indications of a community that is disturbed and isexperiencingelevatedhuntingpressureThesearehigher(camera)trapping rates for smaller‐bodiedspecies suchasEminrsquospouchedrat and significantly fewer encounters of larger‐bodiedmammalsthataretargetsofthebushmeattradesuchasPetersʼduikerandredriverhog(FaRyanampBell2005JerozolimskiampPeres2003)Additionalindicatorsaretheabsenceinthesurveysoflargercarni‐voresintheNorthernSectorsuchasgoldencatandleopardwhicharesensitivetosnaring(Bahaa‐el‐dinetal2015)andsignificantlyreducedabundancemetricsfordisturbance‐sensitivespeciessuchasblack‐leggedmongooseandwaterchevrotain(Hart2013a)Theabsence of white‐bellied duiker in the Northern Sector also sug‐gestselevatedhumandisturbanceasthisspecieshasbeenreportedasverysensitivetoevenminorperturbationwithintheenvironment(Hart2013b)IncomparisontheSouthernSectorcontainedindica‐torfaunasuchasthewhite‐belliedduikerandhadhighertrappingratesforlarger‐bodiedspecies
WesuspectthedifferencesobservedaremostlikelyduetolowerhumandisturbanceintheSouthernSectorTheteamsdeployingand
recoveringthecamerasintheSouthernSectorcovered238kmandencountered few signs of humanperturbation (T Brucepers obs)whereashumansignwascommonlyencounteredbytheteamsintheNorthernSectorThisperceiveddifference is reflected in the2017and 2018 density of hunting signwithin each camera trap grid asdetected throughMINFOF ranger patrols (ZSL ampMINFOF 2017a2017b) and through the2018DistanceSampling inventory for theDFR (Bruce et al 2018) Higher numbers of hunting sign in theNorthernSectorwouldbeconsistentwithanelevatedhuntingpres‐sureinthatarea
45emsp|emspProtection of refugia from hunting
Though inferences made for wide‐ranging species such as forestelephantsandgreatapesusingcameratrapsaredifficultthefactthattrappingrateswerehigherinmorechallengingterrainwithassumedlower hunting pressure could be indicative of complex habitatprovidingsomelevelofprotectionfromhuntingElephantisknownto retreatwhen they aredisturbed to terrain that ismoredifficulttoaccessbyhumans (Hedges2012)Thuswithin largerprotectedareas certain zones may act as refugia for wildlife populations(Campbelletal2011)Thiscanbeduetoarangeof factorssuchas remoteanddifficult terrain forpoachers (Attum2007Hedges2012) or the regular presence of field researchers and rangers(Campbell et al 2011) The significanceof these refugia for largerprotected areas is that the populations of wildlife residing withinthem if adequately protected may provide source populations toallowrecolonisationofotherareasofthereserve(NaranjoampBodmer2007)Thereforeifadequateprotectioncanbeprovidedtorelativelysmallbutimportantareasoflargereservesthismayprovidetropicalforestswithabetterchanceofbeingecologicallyresilienttoongoingand increasing human perturbation Well‐designed camera trapsurveys may provide data on the status of wildlife populations atrelativelyfinespatialresolutionssoastoidentifyfunctionalrefugiawithgreaterconfidence
ACKNOWLEDG EMENTS
WeappreciatetheongoingsupportofCameroonrsquosMinistryofForestsandWildlife(MINFOF)andtheopportunitytocontributetobiodiver‐sityconservationthroughoutthecountryInparticularwewouldliketothanktheChefdrsquoAntenneSergeJacobMeyeforhisongoingsup‐portofconservationresearchwithintheprotectedareaWeappreci‐atethestalwarteffortsofMINFOFecoguardsandlocalporterswhoaccompaniedthesurveyteamsinthefieldWewouldalsoliketothanktheUnitedStatesFishandWildlifeService(USFWS)mdashAfricanElephantConservationandIUCNSOSmdashFondationSegreacutePangolinConservationInitiativeforsupportingthiswork
ORCID
Tom Bruce httporcidorg0000‐0001‐6958‐1657
774emsp |emsp emspensp Bruce et al
R E FE R E N C E S
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AbrahamsM I Peres C A amp Costa H C (2017)Measuring localdepletion of terrestrial game vertebrates by central‐place hunt‐ers in rural Amazonia PLoS ONE 12(10) e0186653 httpsdoiorg101371journalpone0186653
AhumadaJAHurtadoJampLizcanoD(2013)MonitoringthestatusandtrendsoftropicalforestterrestrialvertebratecommunitiesfromcameratrapdataAtool forconservationPLoS ONE8(9)e73707httpsdoiorg101371journalpone0073707
Ahumada J A Silva C E Gajapersad K Hallam C Hurtado JMartin E hellip Sheil D (2011) Community structure and diver‐sity of tropical forest mammals Data from a global camera trapnetwork Philosophical Transactions of the Royal Society of London Biological Sciences366(1578)2703ndash2711httpsdoiorg101098rstb20110115
AminRAndanjeSAOgwonkaBAliAHBowkettAEOmarMampWacherT(2015)ThenortherncoastalforestsofKenyaarenationally and globally important for the conservation of AdersrsquoduikerCephalophusadersiandotherantelopespeciesBiodiversity and Conservation 24(3) 641ndash658 httpsdoiorg101007s10531‐014‐0842‐z
Attum O (2007) Can landscape use be among the factors that po‐tentiallymake some ungulates speciesmore difficult to conserveJournal of Arid Environments69(3)410ndash419
Bahaa‐el‐dinLHenschelPAbaaRAbernethyKBohmTBoutNhellipLeeM (2013)NotesonthedistributionandstatusofsmallcarnivoresinGabonSmall Carnivore Conservation4819ndash29
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Bennett E L Blencowe E Brandon K Brown D Burn R WCowlishaw G hellip Robinson J G (2007) Hunting for consensusReconcilingbushmeatharvestconservationanddevelopmentpol‐icyinWestandCentralAfricaConservation Biology21(3)884ndash887httpsdoiorg101111j1523‐1739200600595x
BlakeSDeemSLMossimboEMaiselsFampWalshP(2009)Forestelephants Tree planters of the CongoBiotropica41(4) 459ndash468httpsdoiorg101111j1744‐7429200900512x
Blake S (2002) The ecology of forest elephant distribution and itsimplications for conservation Doctoral dissertation University ofEdinburgh
BruceTNdjassiCFowlerANdimbeMFankemOTabueRhellipOlsonD(2018)Faunal inventory of the Dja Faunal Reserve Cameroon Yaoundeacute Cameroon Ministry of Forests and Wildlife (MINFOF)Zoological Society of London ndash Cameroon Country ProgrammeAfricanWildlifeFoundation
BruceTWacherTNdingaHBidjokaVMeyongFNgoBataMampOlsonD(2017)camera trap survey for larger terrestrial wildlife in the Dja Biosphere Reserve CameroonYaoundeacuteCameroonZoologicalSocietyofLondon(ZSL)ampCameroonMinistryofForestsandWildlife(MINFOF)
BurnhamKPampAndersonDR(2002)Model selection and multimodel inferenceNewYorkNYSpringer
Campbell G Kuehl H Diarrassouba A NGoran P K amp BoeschC (2011) Long‐term research sites as refugia for threatened andover‐harvested species Biology Letters 7(5) 723ndash726 httpsdoiorg101098rsbl20110155
CardilloMMaceGMJonesKEBielbyJBininda‐EmondsORSechrestWhellipPurvisA(2005)Multiplecausesofhighextinction
riskinlargemammalspeciesScience309(5738)1239ndash1241httpsdoiorg101126science1116030
Craigie IDBaillieJEBalmfordACarboneCCollenBGreenREampHuttonJM (2010)Largemammalpopulationdeclines inAfricarsquosprotectedareasBiological Conservation143(9)2221ndash2228httpsdoiorg101016jbiocon201006007
DaveyKWacherTampAminR(2017)Analysis tool for camera-trap sur-vey data [Computer software]ZoologicalSocietyofLondonRetrievedfromhttpswwwzslorgzsl‐camera‐trap‐data‐management‐ and‐analysis‐package
Djuikouo M N K Doucet J L Nguembou C K Lewis S L ampSonkeacute B (2010) Diversity and aboveground biomass in threetropical forest types in the Dja Biosphere Reserve Cameroon African Journal of Ecology 48(4) 1053ndash1063 httpsdoiorg101111j1365‐2028201001212x
DupainJBombomeKampVanElsackerL(2003)LeschimpanzeacutesetlesgorillesdelareacuteservedefauneduDjaCanopeacutee2414ndash15
EffordMGampDawsonDK(2012)OccupancyincontinuoushabitatEcosphere3(4)1ndash15httpsdoiorg101890ES11‐003081
Efron B amp Tibshirani R J (1994) An introduction to the bootstrap WashingtonDCCRCPress
FaJEOliveroJFarfaacutenMAacuteMaacuterquezALDuarteJNackoneyJhellipMacdonaldDW(2014a)CorrelatesofbushmeatinmarketsanddepletionofwildlifeConservation Biology29(3)805ndash815
Fa J EOlivero J FarfaacutenMAacuteMaacuterquezA LVargas JMRealRampNasiR(2014b)IntegratingsustainablehuntinginbiodiversityprotectioninCentralAfricaHotspotsweakspotsandstrongspotsPLoS ONE9(11)e112367
FaJERyanSFampBellDJ (2005)Huntingvulnerabilityecolog‐ical characteristics and harvest rates of bushmeat species in afro‐tropicalforestsBiological Conservation121(2)167ndash176httpsdoiorg101016jbiocon200404016
Fa J E Seymour S Dupain J E F Amin R Albrechtsen L ampMacdonaldD (2006) Getting to gripswith themagnitude of ex‐ploitationBushmeat in theCross‐SanagariversregionNigeria and Cameroon Biological Conservation 129(4) 497ndash510 httpsdoiorg101016jbiocon200511031
Farris Z J Boone H M Karpanty S Murphy A Ratelolahy FAndrianjakariveloVampKellyMJ(2015)FeralcatsandthefitoatyFirstpopulationassessmentoftheblackforestcatinMadagascarrsquosrainforestsJournal of Mammalogy97(2)518ndash525
Fiske IampChandlerR (2011)UnmarkedAnRpackageforfittinghi‐erarchicalmodelsofwildlifeoccurrenceandabundanceJournal of Statistical Software43(10)1ndash23
HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences107(19)8650ndash8655httpsdoiorg101073pnas0912668107
HartJ(2013a)WaterchevrotainHymemoschusaquaticusInJKingdonampMHoffmann (Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp88ndash92)LondonUKBloomsbury
Hart J (2013b) White‐bellied duiker Cephalophus leucogaster In JKingdonampMHoffmann(Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp255ndash258)LondonUKBloomsbury
HeadJSRobbinsMMMundryRMakagaLampBoeschC(2012)Remotevideo‐cameratrapsmeasurehabitatuseandcompetitiveex‐clusionamongsympatricchimpanzeegorillaandelephantinLoangoNational ParkGabon Journal of Tropical Ecology28(06) 571ndash583httpsdoiorg101017S0266467412000612
HedgesS(2012)Monitoring elephant populations and assessing threats HimayatnagarTelanganaUniversitiesPress
HedwigDKienastIBonnetMCurranBKCourageABoeschChellipKingT(2018)Acameratrapassessmentoftheforestmam‐mal community within the transitional savannah‐forest mosaic oftheBateacutekeacutePlateauNationalParkGabonAfrican Journal of Ecology56(4)777ndash790httpsdoiorg101111aje12497
emspensp emsp | emsp775Bruce et al
HijmansRJCameronSEParraJLJonesPGampJarvisA(2005)Very high resolution interpolated climate surfaces for global landareasInternational Journal of Climatology25(15)1965ndash1978httpsdoiorg101002joc1276
HuggelA(2012)Exiv2softwaretool[Computersoftware]Retrievedfromhttpswwwexiv2orgindexhtml
Jerozolimski A amp Peres C A (2003) Bringing home the biggestbacon A cross‐site analysis of the structure of hunter‐kill profilesin Neotropical forests Biological Conservation 111(3) 415ndash425httpsdoiorg101016S0006‐3207(02)00310‐5
KingdonJ (2015)The Kingdon field guide to African mammalsLondonUKBloomsburyPublishing
KuumlhlHFMaiselsMAncrenazampEAWilliamson(Eds)(2008)Best practice guidelines for surveys and monitoring of great ape populations GlandSwitzerlandIUCN
LauranceWFCroesBMTchignoumbaLLahmSAAlonsoALeeMEhellipOndzeanoC(2006)ImpactsofroadsandhuntingoncentralAfrican rainforestmammalsConservation Biology20(4)1251ndash1261httpsdoiorg101111j1523‐1739200600420x
LauranceWFUsecheDCRendeiroJKalkaMBradshawCJSloan S P hellip Arroyo‐Rodriguez V (2012) Averting biodiversitycollapse in tropical forestprotectedareasNature489(7415)290httpsdoiorg101038nature11318
LeslieDMampHuffmanBA(2015)Potamochoerus porcus(ArtiodactylaSuidae)Mammalian Species4715ndash31
MacKenzieD IampBailey L L (2004)Assessing the fit of site‐occu‐pancy models Journal of Agricultural Biological and Environmental Statistics9300ndash318httpsdoiorg101198108571104X3361
MacKenzieDINicholsJDRoyleJAPollockKHBaileyLLampHinesJE (2006)Occupancy estimation and modellingBurlingtonMAAcademicPress
Magurran A E (2005) Species abundance distributions Patternor process Functional Ecology 19(1) 177ndash181 httpsdoiorg101111j0269‐8463200500930x
MaiselsFStrindbergSBlakeSWittemyerGHartJWilliamsonEAhellipWarrenY (2013)DevastatingdeclineofforestelephantsinCentralAfricaPLoS ONE8(3)e59469httpsdoiorg101371journalpone0059469
MalhiYAdu‐BreduSAsareRA LewisS LampMayauxP (2013)AfricanrainforestsPastpresentandfuturePhilosophical Transactions of the Royal Society of London Biological Sciences 368(1625)20120312
MallonDPHoffmannMGraingerMJHibertFVanVlietNampMcGowanP JK (2015)An IUCNsituationanalysisof terrestrialandfreshwaterfaunainWestandCentralAfricaOccasionalpaperoftheIUCNspeciessurvivalcommission(54)
MambeyaMMBakerFMombouaBRKoumbaPamboAFHegaMOkouyiOkouyiVJhellipAbernethyK(2018)TheemergenceofacommercialtradeinpangolinsfromGabonAfrican Journal of Ecology56(3)601ndash609httpsdoiorg101111aje12507
MINFOFampIUCN(2015)CaracteacuterisationdelapopulationdegrandsetmoyensmammifegraveresdanslaReservedeFauneduDjaPotentieletmenacesYaoundeacuteCameroun
Muchaal P K amp Ngandjui G (1999) Impact of village hunt‐ing on wildlife populations in the western Dja ReserveCameroon Conservation Biology 13(2) 385ndash396 httpsdoiorg101046j1523‐17391999013002385x
NaranjoEJampBodmerRE (2007) Sourcendashsink systemsandconser‐vationofhuntedungulatesintheLacandonForestMexico Biological Conservation 138(3ndash4) 412ndash420 httpsdoiorg101016jbiocon 200705010
NielsenMR(2006)ImportancecauseandeffectofbushmeathuntingintheUdzungwaMountainsTanzania ImplicationsforcommunitybasedwildlifemanagementBiological Conservation128(4)509ndash516httpsdoiorg101016jbiocon200510017
OBrienTGKinnairdMFampWibisonoHT (2003)Crouching ti‐gers hiddenprey Sumatran tiger andprey populations in a tropi‐calforestlandscapeAnimal Conservation6(2)131ndash139httpsdoiorg101017S1367943003003172
OksanenJ(2015)VegananintroductiontoordinationVol8(p19)Retrieved from httpscranr‐projectorgwebpackagesveganvi‐gnettesintroveganpdf
PeresCAampPalaciosE(2007)Basin‐wideeffectsofgameharvestonvertebrate populationdensities inAmazonian forests Implicationsfor animal‐mediated seed dispersal Biotropica 39(3) 304ndash315httpsdoiorg101111j1744‐7429200700272x
PotapovPVTurubanovaSAHansenMCAduseiBBroichMAltstattAhellipJusticeCO(2012)QuantifyingforestcoverlossinDemocraticRepublicoftheCongo2000ndash2010withLandsatETM+data Remote Sensing of Environment 122 106ndash116 httpsdoiorg101016jrse201108027
PoulsenJRKoernerSEMooreSMedjibeVPBlakeSClarkC JhellipRosinC (2017) Poaching empties criticalCentralAfricanwilderness of forest elephants Current Biology 27(4) 134ndashR135httpsdoiorg101016jcub201701023
PurvisAGittlemanJlCowlishawGampMaceGM(2000)PredictingextinctionriskindecliningspeciesProceedings of the Royal Society B Biological Sciences267(1456) 1947ndash1952 httpsdoiorg101098rspb20001234
RayJ(1997)ComparativeecologyoftwoAfricanforestmongoosesHerpestesnasoandAtilaxpaludinosusAfrican Journal of Ecology35(3)237ndash253httpsdoiorg101111j1365‐20281997086‐ 89086x
Redford K H (1992) The empty forest BioScience 42(6) 412ndash422httpsdoiorg1023071311860
RepublicofCameroon(1994)Lawno9401du20janvier1994portantreacutegimedesforecirctsdelafauneetdelapecirccheRepublicofCameroon
RoveroFampMarshallAR(2009)CameratrappingphotographicrateasanindexofdensityinforestungulatesJournal of Applied Ecology46(5)1011ndash1017httpsdoiorg101111j1365‐2664200901705x
Royle J A amp Nichols J D (2003) Estimating abundance from re‐peated presence‐absence data or point counts Ecology 84(3)777ndash790 httpsdoiorg1018900012‐9658(2003)084[0777EAFRPA]20CO2
Seddon P J Griffiths C J Soorae P S ampArmstrongD P (2014)ReversingdefaunationRestoringspeciesinachangingworldScience345(6195)406ndash412httpsdoiorg101126science1251818
Silveira L Jacomo A T amp Diniz‐Filho J A F (2003) Camera trapline transect census and track surveys A comparative evaluationBiological Conservation 114(3) 351ndash355 httpsdoiorg101016S0006‐3207(03)00063‐6
Sonkeacute B (1998) Etudes floristiques et structurales des forecircts de laReacuteserve de Faune du Dja (Cameroun) Laboratoire de BotaniqueSysteacutematique et de Phytosociologie Universiteacute Libre de Bruxelles(ULB)
Srbek‐AraujoACampChiarelloAG(2005)Iscameratrappinganeffi‐cientmethodforsurveyingmammalsinNeotropicalforestsAcasestudyinsouth‐easternBrazilJournal of Tropical Ecology21(1)121ndash125httpsdoiorg101017S0266467404001956
Stiles D (2011) Elephant meat and ivory trade in Central AfricaPachyderm5026ndash36
TEAMNetwork(2008)Terrestrialvertebrateprotocol implementationmanualv30(p56)WashingtonDCTropicalEcologyAssessmentandMonitoringNetworkCenter forAppliedBiodiversity ScienceConservationInternational
Tobler M W Carrillo‐Percastegui S E Leite Pitman R MaresR amp Powell G (2008) An evaluation of camera traps for in‐ventorying large‐and medium‐sized terrestrial rainforestmammals Animal Conservation 11(3) 169ndash178 httpsdoiorg101111j1469‐1795200800169x
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
772emsp |emsp emspensp Bruce et al
F I G U R E 7 emspChangeintheprobabilityofoccupancyforblueduikerandbayduikerwithdistancetotheboundaryinkilometresacrossbothmanagementsectorsaccordingtoaRoylendashNicholsmodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
F I G U R E 8 emspChangeintheprobabilityofoccupancyforwhite‐belliedpangolinwithmanagementsectoranddistancetotheboundaryinkilometresaccordingtoaMackenzieoccupancymodelGreycirclesrepresenttheSouthernSectorandblackcirclestheNorthernSector
emspensp emsp | emsp773Bruce et al
44emsp|emspCamera trap surveys for measuring the impacts of hunting on mammal communities
The spatial scale at which mammal communities are affected byandhowpopulationsrespondtoanthropogenicpressuressuchasbushmeat hunting is difficult to empiricallymeasure (Laurance etal2006)Thisisespeciallytrueformammalsresidingwithintropi‐cal forestswheregatheringconsistentandmeaningfulpopulation‐andcommunity‐levelmetrics ischallenging(Ahumadaetal2013)Population density of tropical mammals can vary greatly due toheterogeneity present within the environment For example for‐est elephants havedifferent distributions and aggregations inwetanddryseasonsinNouabaleacute‐Ndoki NationalParkwhichispartiallydependentonspatio‐temporalpatternsoffruitingtreesacrossthelandscape(Blake2002)
Whether the differences observed among the two sites sur‐veyedhereareattributabletodifferent levelsofhuntingpressureremains to be confirmed There are however indications thathuntingpressureanditsimpactsonmammalfaunasaregreaterintheNorthern Sector than in the Southern Sector The effects ofhuntingpressureonmammaliandeclinesinCentralAfricanforestsarewell documented The pattern in general is the largest‐bod‐ied species frugivores and thosewith high hunter or blackmar‐ketvalue(Abernethyetal2013Cardilloetal2005FaOliveroFarfaacutenMaacuterquezDuarteetal2014aFaOliveroFarfaacutenMaacuterquezVargasetal2014bPeresampPalacios2007)arethefirstspeciestoshownoticeabledeclineInthisstudythesignificantdeclineintherelativeabundance for frugivores suchasPetersʼduikerandspe‐cieswithhighhuntervalueliketheredriverhogunderincreasedhuntingpressure in theNorthernSector is reported inother sur‐veys(Abernethyetal2013)Thisisalsoreflectedinthedifferencesobserved in this study in biomass in the different guilds of eachmammalcommunityThemammalcommunitywithintheNorthernSector shows indications of a community that is disturbed and isexperiencingelevatedhuntingpressureThesearehigher(camera)trapping rates for smaller‐bodiedspecies suchasEminrsquospouchedrat and significantly fewer encounters of larger‐bodiedmammalsthataretargetsofthebushmeattradesuchasPetersʼduikerandredriverhog(FaRyanampBell2005JerozolimskiampPeres2003)Additionalindicatorsaretheabsenceinthesurveysoflargercarni‐voresintheNorthernSectorsuchasgoldencatandleopardwhicharesensitivetosnaring(Bahaa‐el‐dinetal2015)andsignificantlyreducedabundancemetricsfordisturbance‐sensitivespeciessuchasblack‐leggedmongooseandwaterchevrotain(Hart2013a)Theabsence of white‐bellied duiker in the Northern Sector also sug‐gestselevatedhumandisturbanceasthisspecieshasbeenreportedasverysensitivetoevenminorperturbationwithintheenvironment(Hart2013b)IncomparisontheSouthernSectorcontainedindica‐torfaunasuchasthewhite‐belliedduikerandhadhighertrappingratesforlarger‐bodiedspecies
WesuspectthedifferencesobservedaremostlikelyduetolowerhumandisturbanceintheSouthernSectorTheteamsdeployingand
recoveringthecamerasintheSouthernSectorcovered238kmandencountered few signs of humanperturbation (T Brucepers obs)whereashumansignwascommonlyencounteredbytheteamsintheNorthernSectorThisperceiveddifference is reflected in the2017and 2018 density of hunting signwithin each camera trap grid asdetected throughMINFOF ranger patrols (ZSL ampMINFOF 2017a2017b) and through the2018DistanceSampling inventory for theDFR (Bruce et al 2018) Higher numbers of hunting sign in theNorthernSectorwouldbeconsistentwithanelevatedhuntingpres‐sureinthatarea
45emsp|emspProtection of refugia from hunting
Though inferences made for wide‐ranging species such as forestelephantsandgreatapesusingcameratrapsaredifficultthefactthattrappingrateswerehigherinmorechallengingterrainwithassumedlower hunting pressure could be indicative of complex habitatprovidingsomelevelofprotectionfromhuntingElephantisknownto retreatwhen they aredisturbed to terrain that ismoredifficulttoaccessbyhumans (Hedges2012)Thuswithin largerprotectedareas certain zones may act as refugia for wildlife populations(Campbelletal2011)Thiscanbeduetoarangeof factorssuchas remoteanddifficult terrain forpoachers (Attum2007Hedges2012) or the regular presence of field researchers and rangers(Campbell et al 2011) The significanceof these refugia for largerprotected areas is that the populations of wildlife residing withinthem if adequately protected may provide source populations toallowrecolonisationofotherareasofthereserve(NaranjoampBodmer2007)Thereforeifadequateprotectioncanbeprovidedtorelativelysmallbutimportantareasoflargereservesthismayprovidetropicalforestswithabetterchanceofbeingecologicallyresilienttoongoingand increasing human perturbation Well‐designed camera trapsurveys may provide data on the status of wildlife populations atrelativelyfinespatialresolutionssoastoidentifyfunctionalrefugiawithgreaterconfidence
ACKNOWLEDG EMENTS
WeappreciatetheongoingsupportofCameroonrsquosMinistryofForestsandWildlife(MINFOF)andtheopportunitytocontributetobiodiver‐sityconservationthroughoutthecountryInparticularwewouldliketothanktheChefdrsquoAntenneSergeJacobMeyeforhisongoingsup‐portofconservationresearchwithintheprotectedareaWeappreci‐atethestalwarteffortsofMINFOFecoguardsandlocalporterswhoaccompaniedthesurveyteamsinthefieldWewouldalsoliketothanktheUnitedStatesFishandWildlifeService(USFWS)mdashAfricanElephantConservationandIUCNSOSmdashFondationSegreacutePangolinConservationInitiativeforsupportingthiswork
ORCID
Tom Bruce httporcidorg0000‐0001‐6958‐1657
774emsp |emsp emspensp Bruce et al
R E FE R E N C E S
AbernethyKACoad L TaylorG LeeMEampMaisels F (2013)Extent and ecological consequences of hunting in Central Africanrainforests in thetwenty‐firstcenturyPhilosophical Transactions of the Royal Society of London Biological Sciences368(1625)20120303httpsdoiorg101098rstb20120303
AbrahamsM I Peres C A amp Costa H C (2017)Measuring localdepletion of terrestrial game vertebrates by central‐place hunt‐ers in rural Amazonia PLoS ONE 12(10) e0186653 httpsdoiorg101371journalpone0186653
AhumadaJAHurtadoJampLizcanoD(2013)MonitoringthestatusandtrendsoftropicalforestterrestrialvertebratecommunitiesfromcameratrapdataAtool forconservationPLoS ONE8(9)e73707httpsdoiorg101371journalpone0073707
Ahumada J A Silva C E Gajapersad K Hallam C Hurtado JMartin E hellip Sheil D (2011) Community structure and diver‐sity of tropical forest mammals Data from a global camera trapnetwork Philosophical Transactions of the Royal Society of London Biological Sciences366(1578)2703ndash2711httpsdoiorg101098rstb20110115
AminRAndanjeSAOgwonkaBAliAHBowkettAEOmarMampWacherT(2015)ThenortherncoastalforestsofKenyaarenationally and globally important for the conservation of AdersrsquoduikerCephalophusadersiandotherantelopespeciesBiodiversity and Conservation 24(3) 641ndash658 httpsdoiorg101007s10531‐014‐0842‐z
Attum O (2007) Can landscape use be among the factors that po‐tentiallymake some ungulates speciesmore difficult to conserveJournal of Arid Environments69(3)410ndash419
Bahaa‐el‐dinLHenschelPAbaaRAbernethyKBohmTBoutNhellipLeeM (2013)NotesonthedistributionandstatusofsmallcarnivoresinGabonSmall Carnivore Conservation4819ndash29
Bahaa‐el‐dinLHenschelPButynskiTMMacdonaldDWMillsDSlotowRampHunterL (2015)TheAfricangoldencatCaracalaurataAfricasleast‐knownfelidMammal Review45(1)63ndash77
Bennett E L Blencowe E Brandon K Brown D Burn R WCowlishaw G hellip Robinson J G (2007) Hunting for consensusReconcilingbushmeatharvestconservationanddevelopmentpol‐icyinWestandCentralAfricaConservation Biology21(3)884ndash887httpsdoiorg101111j1523‐1739200600595x
BlakeSDeemSLMossimboEMaiselsFampWalshP(2009)Forestelephants Tree planters of the CongoBiotropica41(4) 459ndash468httpsdoiorg101111j1744‐7429200900512x
Blake S (2002) The ecology of forest elephant distribution and itsimplications for conservation Doctoral dissertation University ofEdinburgh
BruceTNdjassiCFowlerANdimbeMFankemOTabueRhellipOlsonD(2018)Faunal inventory of the Dja Faunal Reserve Cameroon Yaoundeacute Cameroon Ministry of Forests and Wildlife (MINFOF)Zoological Society of London ndash Cameroon Country ProgrammeAfricanWildlifeFoundation
BruceTWacherTNdingaHBidjokaVMeyongFNgoBataMampOlsonD(2017)camera trap survey for larger terrestrial wildlife in the Dja Biosphere Reserve CameroonYaoundeacuteCameroonZoologicalSocietyofLondon(ZSL)ampCameroonMinistryofForestsandWildlife(MINFOF)
BurnhamKPampAndersonDR(2002)Model selection and multimodel inferenceNewYorkNYSpringer
Campbell G Kuehl H Diarrassouba A NGoran P K amp BoeschC (2011) Long‐term research sites as refugia for threatened andover‐harvested species Biology Letters 7(5) 723ndash726 httpsdoiorg101098rsbl20110155
CardilloMMaceGMJonesKEBielbyJBininda‐EmondsORSechrestWhellipPurvisA(2005)Multiplecausesofhighextinction
riskinlargemammalspeciesScience309(5738)1239ndash1241httpsdoiorg101126science1116030
Craigie IDBaillieJEBalmfordACarboneCCollenBGreenREampHuttonJM (2010)Largemammalpopulationdeclines inAfricarsquosprotectedareasBiological Conservation143(9)2221ndash2228httpsdoiorg101016jbiocon201006007
DaveyKWacherTampAminR(2017)Analysis tool for camera-trap sur-vey data [Computer software]ZoologicalSocietyofLondonRetrievedfromhttpswwwzslorgzsl‐camera‐trap‐data‐management‐ and‐analysis‐package
Djuikouo M N K Doucet J L Nguembou C K Lewis S L ampSonkeacute B (2010) Diversity and aboveground biomass in threetropical forest types in the Dja Biosphere Reserve Cameroon African Journal of Ecology 48(4) 1053ndash1063 httpsdoiorg101111j1365‐2028201001212x
DupainJBombomeKampVanElsackerL(2003)LeschimpanzeacutesetlesgorillesdelareacuteservedefauneduDjaCanopeacutee2414ndash15
EffordMGampDawsonDK(2012)OccupancyincontinuoushabitatEcosphere3(4)1ndash15httpsdoiorg101890ES11‐003081
Efron B amp Tibshirani R J (1994) An introduction to the bootstrap WashingtonDCCRCPress
FaJEOliveroJFarfaacutenMAacuteMaacuterquezALDuarteJNackoneyJhellipMacdonaldDW(2014a)CorrelatesofbushmeatinmarketsanddepletionofwildlifeConservation Biology29(3)805ndash815
Fa J EOlivero J FarfaacutenMAacuteMaacuterquezA LVargas JMRealRampNasiR(2014b)IntegratingsustainablehuntinginbiodiversityprotectioninCentralAfricaHotspotsweakspotsandstrongspotsPLoS ONE9(11)e112367
FaJERyanSFampBellDJ (2005)Huntingvulnerabilityecolog‐ical characteristics and harvest rates of bushmeat species in afro‐tropicalforestsBiological Conservation121(2)167ndash176httpsdoiorg101016jbiocon200404016
Fa J E Seymour S Dupain J E F Amin R Albrechtsen L ampMacdonaldD (2006) Getting to gripswith themagnitude of ex‐ploitationBushmeat in theCross‐SanagariversregionNigeria and Cameroon Biological Conservation 129(4) 497ndash510 httpsdoiorg101016jbiocon200511031
Farris Z J Boone H M Karpanty S Murphy A Ratelolahy FAndrianjakariveloVampKellyMJ(2015)FeralcatsandthefitoatyFirstpopulationassessmentoftheblackforestcatinMadagascarrsquosrainforestsJournal of Mammalogy97(2)518ndash525
Fiske IampChandlerR (2011)UnmarkedAnRpackageforfittinghi‐erarchicalmodelsofwildlifeoccurrenceandabundanceJournal of Statistical Software43(10)1ndash23
HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences107(19)8650ndash8655httpsdoiorg101073pnas0912668107
HartJ(2013a)WaterchevrotainHymemoschusaquaticusInJKingdonampMHoffmann (Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp88ndash92)LondonUKBloomsbury
Hart J (2013b) White‐bellied duiker Cephalophus leucogaster In JKingdonampMHoffmann(Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp255ndash258)LondonUKBloomsbury
HeadJSRobbinsMMMundryRMakagaLampBoeschC(2012)Remotevideo‐cameratrapsmeasurehabitatuseandcompetitiveex‐clusionamongsympatricchimpanzeegorillaandelephantinLoangoNational ParkGabon Journal of Tropical Ecology28(06) 571ndash583httpsdoiorg101017S0266467412000612
HedgesS(2012)Monitoring elephant populations and assessing threats HimayatnagarTelanganaUniversitiesPress
HedwigDKienastIBonnetMCurranBKCourageABoeschChellipKingT(2018)Acameratrapassessmentoftheforestmam‐mal community within the transitional savannah‐forest mosaic oftheBateacutekeacutePlateauNationalParkGabonAfrican Journal of Ecology56(4)777ndash790httpsdoiorg101111aje12497
emspensp emsp | emsp775Bruce et al
HijmansRJCameronSEParraJLJonesPGampJarvisA(2005)Very high resolution interpolated climate surfaces for global landareasInternational Journal of Climatology25(15)1965ndash1978httpsdoiorg101002joc1276
HuggelA(2012)Exiv2softwaretool[Computersoftware]Retrievedfromhttpswwwexiv2orgindexhtml
Jerozolimski A amp Peres C A (2003) Bringing home the biggestbacon A cross‐site analysis of the structure of hunter‐kill profilesin Neotropical forests Biological Conservation 111(3) 415ndash425httpsdoiorg101016S0006‐3207(02)00310‐5
KingdonJ (2015)The Kingdon field guide to African mammalsLondonUKBloomsburyPublishing
KuumlhlHFMaiselsMAncrenazampEAWilliamson(Eds)(2008)Best practice guidelines for surveys and monitoring of great ape populations GlandSwitzerlandIUCN
LauranceWFCroesBMTchignoumbaLLahmSAAlonsoALeeMEhellipOndzeanoC(2006)ImpactsofroadsandhuntingoncentralAfrican rainforestmammalsConservation Biology20(4)1251ndash1261httpsdoiorg101111j1523‐1739200600420x
LauranceWFUsecheDCRendeiroJKalkaMBradshawCJSloan S P hellip Arroyo‐Rodriguez V (2012) Averting biodiversitycollapse in tropical forestprotectedareasNature489(7415)290httpsdoiorg101038nature11318
LeslieDMampHuffmanBA(2015)Potamochoerus porcus(ArtiodactylaSuidae)Mammalian Species4715ndash31
MacKenzieD IampBailey L L (2004)Assessing the fit of site‐occu‐pancy models Journal of Agricultural Biological and Environmental Statistics9300ndash318httpsdoiorg101198108571104X3361
MacKenzieDINicholsJDRoyleJAPollockKHBaileyLLampHinesJE (2006)Occupancy estimation and modellingBurlingtonMAAcademicPress
Magurran A E (2005) Species abundance distributions Patternor process Functional Ecology 19(1) 177ndash181 httpsdoiorg101111j0269‐8463200500930x
MaiselsFStrindbergSBlakeSWittemyerGHartJWilliamsonEAhellipWarrenY (2013)DevastatingdeclineofforestelephantsinCentralAfricaPLoS ONE8(3)e59469httpsdoiorg101371journalpone0059469
MalhiYAdu‐BreduSAsareRA LewisS LampMayauxP (2013)AfricanrainforestsPastpresentandfuturePhilosophical Transactions of the Royal Society of London Biological Sciences 368(1625)20120312
MallonDPHoffmannMGraingerMJHibertFVanVlietNampMcGowanP JK (2015)An IUCNsituationanalysisof terrestrialandfreshwaterfaunainWestandCentralAfricaOccasionalpaperoftheIUCNspeciessurvivalcommission(54)
MambeyaMMBakerFMombouaBRKoumbaPamboAFHegaMOkouyiOkouyiVJhellipAbernethyK(2018)TheemergenceofacommercialtradeinpangolinsfromGabonAfrican Journal of Ecology56(3)601ndash609httpsdoiorg101111aje12507
MINFOFampIUCN(2015)CaracteacuterisationdelapopulationdegrandsetmoyensmammifegraveresdanslaReservedeFauneduDjaPotentieletmenacesYaoundeacuteCameroun
Muchaal P K amp Ngandjui G (1999) Impact of village hunt‐ing on wildlife populations in the western Dja ReserveCameroon Conservation Biology 13(2) 385ndash396 httpsdoiorg101046j1523‐17391999013002385x
NaranjoEJampBodmerRE (2007) Sourcendashsink systemsandconser‐vationofhuntedungulatesintheLacandonForestMexico Biological Conservation 138(3ndash4) 412ndash420 httpsdoiorg101016jbiocon 200705010
NielsenMR(2006)ImportancecauseandeffectofbushmeathuntingintheUdzungwaMountainsTanzania ImplicationsforcommunitybasedwildlifemanagementBiological Conservation128(4)509ndash516httpsdoiorg101016jbiocon200510017
OBrienTGKinnairdMFampWibisonoHT (2003)Crouching ti‐gers hiddenprey Sumatran tiger andprey populations in a tropi‐calforestlandscapeAnimal Conservation6(2)131ndash139httpsdoiorg101017S1367943003003172
OksanenJ(2015)VegananintroductiontoordinationVol8(p19)Retrieved from httpscranr‐projectorgwebpackagesveganvi‐gnettesintroveganpdf
PeresCAampPalaciosE(2007)Basin‐wideeffectsofgameharvestonvertebrate populationdensities inAmazonian forests Implicationsfor animal‐mediated seed dispersal Biotropica 39(3) 304ndash315httpsdoiorg101111j1744‐7429200700272x
PotapovPVTurubanovaSAHansenMCAduseiBBroichMAltstattAhellipJusticeCO(2012)QuantifyingforestcoverlossinDemocraticRepublicoftheCongo2000ndash2010withLandsatETM+data Remote Sensing of Environment 122 106ndash116 httpsdoiorg101016jrse201108027
PoulsenJRKoernerSEMooreSMedjibeVPBlakeSClarkC JhellipRosinC (2017) Poaching empties criticalCentralAfricanwilderness of forest elephants Current Biology 27(4) 134ndashR135httpsdoiorg101016jcub201701023
PurvisAGittlemanJlCowlishawGampMaceGM(2000)PredictingextinctionriskindecliningspeciesProceedings of the Royal Society B Biological Sciences267(1456) 1947ndash1952 httpsdoiorg101098rspb20001234
RayJ(1997)ComparativeecologyoftwoAfricanforestmongoosesHerpestesnasoandAtilaxpaludinosusAfrican Journal of Ecology35(3)237ndash253httpsdoiorg101111j1365‐20281997086‐ 89086x
Redford K H (1992) The empty forest BioScience 42(6) 412ndash422httpsdoiorg1023071311860
RepublicofCameroon(1994)Lawno9401du20janvier1994portantreacutegimedesforecirctsdelafauneetdelapecirccheRepublicofCameroon
RoveroFampMarshallAR(2009)CameratrappingphotographicrateasanindexofdensityinforestungulatesJournal of Applied Ecology46(5)1011ndash1017httpsdoiorg101111j1365‐2664200901705x
Royle J A amp Nichols J D (2003) Estimating abundance from re‐peated presence‐absence data or point counts Ecology 84(3)777ndash790 httpsdoiorg1018900012‐9658(2003)084[0777EAFRPA]20CO2
Seddon P J Griffiths C J Soorae P S ampArmstrongD P (2014)ReversingdefaunationRestoringspeciesinachangingworldScience345(6195)406ndash412httpsdoiorg101126science1251818
Silveira L Jacomo A T amp Diniz‐Filho J A F (2003) Camera trapline transect census and track surveys A comparative evaluationBiological Conservation 114(3) 351ndash355 httpsdoiorg101016S0006‐3207(03)00063‐6
Sonkeacute B (1998) Etudes floristiques et structurales des forecircts de laReacuteserve de Faune du Dja (Cameroun) Laboratoire de BotaniqueSysteacutematique et de Phytosociologie Universiteacute Libre de Bruxelles(ULB)
Srbek‐AraujoACampChiarelloAG(2005)Iscameratrappinganeffi‐cientmethodforsurveyingmammalsinNeotropicalforestsAcasestudyinsouth‐easternBrazilJournal of Tropical Ecology21(1)121ndash125httpsdoiorg101017S0266467404001956
Stiles D (2011) Elephant meat and ivory trade in Central AfricaPachyderm5026ndash36
TEAMNetwork(2008)Terrestrialvertebrateprotocol implementationmanualv30(p56)WashingtonDCTropicalEcologyAssessmentandMonitoringNetworkCenter forAppliedBiodiversity ScienceConservationInternational
Tobler M W Carrillo‐Percastegui S E Leite Pitman R MaresR amp Powell G (2008) An evaluation of camera traps for in‐ventorying large‐and medium‐sized terrestrial rainforestmammals Animal Conservation 11(3) 169ndash178 httpsdoiorg101111j1469‐1795200800169x
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
emspensp emsp | emsp773Bruce et al
44emsp|emspCamera trap surveys for measuring the impacts of hunting on mammal communities
The spatial scale at which mammal communities are affected byandhowpopulationsrespondtoanthropogenicpressuressuchasbushmeat hunting is difficult to empiricallymeasure (Laurance etal2006)Thisisespeciallytrueformammalsresidingwithintropi‐cal forestswheregatheringconsistentandmeaningfulpopulation‐andcommunity‐levelmetrics ischallenging(Ahumadaetal2013)Population density of tropical mammals can vary greatly due toheterogeneity present within the environment For example for‐est elephants havedifferent distributions and aggregations inwetanddryseasonsinNouabaleacute‐Ndoki NationalParkwhichispartiallydependentonspatio‐temporalpatternsoffruitingtreesacrossthelandscape(Blake2002)
Whether the differences observed among the two sites sur‐veyedhereareattributabletodifferent levelsofhuntingpressureremains to be confirmed There are however indications thathuntingpressureanditsimpactsonmammalfaunasaregreaterintheNorthern Sector than in the Southern Sector The effects ofhuntingpressureonmammaliandeclinesinCentralAfricanforestsarewell documented The pattern in general is the largest‐bod‐ied species frugivores and thosewith high hunter or blackmar‐ketvalue(Abernethyetal2013Cardilloetal2005FaOliveroFarfaacutenMaacuterquezDuarteetal2014aFaOliveroFarfaacutenMaacuterquezVargasetal2014bPeresampPalacios2007)arethefirstspeciestoshownoticeabledeclineInthisstudythesignificantdeclineintherelativeabundance for frugivores suchasPetersʼduikerandspe‐cieswithhighhuntervalueliketheredriverhogunderincreasedhuntingpressure in theNorthernSector is reported inother sur‐veys(Abernethyetal2013)Thisisalsoreflectedinthedifferencesobserved in this study in biomass in the different guilds of eachmammalcommunityThemammalcommunitywithintheNorthernSector shows indications of a community that is disturbed and isexperiencingelevatedhuntingpressureThesearehigher(camera)trapping rates for smaller‐bodiedspecies suchasEminrsquospouchedrat and significantly fewer encounters of larger‐bodiedmammalsthataretargetsofthebushmeattradesuchasPetersʼduikerandredriverhog(FaRyanampBell2005JerozolimskiampPeres2003)Additionalindicatorsaretheabsenceinthesurveysoflargercarni‐voresintheNorthernSectorsuchasgoldencatandleopardwhicharesensitivetosnaring(Bahaa‐el‐dinetal2015)andsignificantlyreducedabundancemetricsfordisturbance‐sensitivespeciessuchasblack‐leggedmongooseandwaterchevrotain(Hart2013a)Theabsence of white‐bellied duiker in the Northern Sector also sug‐gestselevatedhumandisturbanceasthisspecieshasbeenreportedasverysensitivetoevenminorperturbationwithintheenvironment(Hart2013b)IncomparisontheSouthernSectorcontainedindica‐torfaunasuchasthewhite‐belliedduikerandhadhighertrappingratesforlarger‐bodiedspecies
WesuspectthedifferencesobservedaremostlikelyduetolowerhumandisturbanceintheSouthernSectorTheteamsdeployingand
recoveringthecamerasintheSouthernSectorcovered238kmandencountered few signs of humanperturbation (T Brucepers obs)whereashumansignwascommonlyencounteredbytheteamsintheNorthernSectorThisperceiveddifference is reflected in the2017and 2018 density of hunting signwithin each camera trap grid asdetected throughMINFOF ranger patrols (ZSL ampMINFOF 2017a2017b) and through the2018DistanceSampling inventory for theDFR (Bruce et al 2018) Higher numbers of hunting sign in theNorthernSectorwouldbeconsistentwithanelevatedhuntingpres‐sureinthatarea
45emsp|emspProtection of refugia from hunting
Though inferences made for wide‐ranging species such as forestelephantsandgreatapesusingcameratrapsaredifficultthefactthattrappingrateswerehigherinmorechallengingterrainwithassumedlower hunting pressure could be indicative of complex habitatprovidingsomelevelofprotectionfromhuntingElephantisknownto retreatwhen they aredisturbed to terrain that ismoredifficulttoaccessbyhumans (Hedges2012)Thuswithin largerprotectedareas certain zones may act as refugia for wildlife populations(Campbelletal2011)Thiscanbeduetoarangeof factorssuchas remoteanddifficult terrain forpoachers (Attum2007Hedges2012) or the regular presence of field researchers and rangers(Campbell et al 2011) The significanceof these refugia for largerprotected areas is that the populations of wildlife residing withinthem if adequately protected may provide source populations toallowrecolonisationofotherareasofthereserve(NaranjoampBodmer2007)Thereforeifadequateprotectioncanbeprovidedtorelativelysmallbutimportantareasoflargereservesthismayprovidetropicalforestswithabetterchanceofbeingecologicallyresilienttoongoingand increasing human perturbation Well‐designed camera trapsurveys may provide data on the status of wildlife populations atrelativelyfinespatialresolutionssoastoidentifyfunctionalrefugiawithgreaterconfidence
ACKNOWLEDG EMENTS
WeappreciatetheongoingsupportofCameroonrsquosMinistryofForestsandWildlife(MINFOF)andtheopportunitytocontributetobiodiver‐sityconservationthroughoutthecountryInparticularwewouldliketothanktheChefdrsquoAntenneSergeJacobMeyeforhisongoingsup‐portofconservationresearchwithintheprotectedareaWeappreci‐atethestalwarteffortsofMINFOFecoguardsandlocalporterswhoaccompaniedthesurveyteamsinthefieldWewouldalsoliketothanktheUnitedStatesFishandWildlifeService(USFWS)mdashAfricanElephantConservationandIUCNSOSmdashFondationSegreacutePangolinConservationInitiativeforsupportingthiswork
ORCID
Tom Bruce httporcidorg0000‐0001‐6958‐1657
774emsp |emsp emspensp Bruce et al
R E FE R E N C E S
AbernethyKACoad L TaylorG LeeMEampMaisels F (2013)Extent and ecological consequences of hunting in Central Africanrainforests in thetwenty‐firstcenturyPhilosophical Transactions of the Royal Society of London Biological Sciences368(1625)20120303httpsdoiorg101098rstb20120303
AbrahamsM I Peres C A amp Costa H C (2017)Measuring localdepletion of terrestrial game vertebrates by central‐place hunt‐ers in rural Amazonia PLoS ONE 12(10) e0186653 httpsdoiorg101371journalpone0186653
AhumadaJAHurtadoJampLizcanoD(2013)MonitoringthestatusandtrendsoftropicalforestterrestrialvertebratecommunitiesfromcameratrapdataAtool forconservationPLoS ONE8(9)e73707httpsdoiorg101371journalpone0073707
Ahumada J A Silva C E Gajapersad K Hallam C Hurtado JMartin E hellip Sheil D (2011) Community structure and diver‐sity of tropical forest mammals Data from a global camera trapnetwork Philosophical Transactions of the Royal Society of London Biological Sciences366(1578)2703ndash2711httpsdoiorg101098rstb20110115
AminRAndanjeSAOgwonkaBAliAHBowkettAEOmarMampWacherT(2015)ThenortherncoastalforestsofKenyaarenationally and globally important for the conservation of AdersrsquoduikerCephalophusadersiandotherantelopespeciesBiodiversity and Conservation 24(3) 641ndash658 httpsdoiorg101007s10531‐014‐0842‐z
Attum O (2007) Can landscape use be among the factors that po‐tentiallymake some ungulates speciesmore difficult to conserveJournal of Arid Environments69(3)410ndash419
Bahaa‐el‐dinLHenschelPAbaaRAbernethyKBohmTBoutNhellipLeeM (2013)NotesonthedistributionandstatusofsmallcarnivoresinGabonSmall Carnivore Conservation4819ndash29
Bahaa‐el‐dinLHenschelPButynskiTMMacdonaldDWMillsDSlotowRampHunterL (2015)TheAfricangoldencatCaracalaurataAfricasleast‐knownfelidMammal Review45(1)63ndash77
Bennett E L Blencowe E Brandon K Brown D Burn R WCowlishaw G hellip Robinson J G (2007) Hunting for consensusReconcilingbushmeatharvestconservationanddevelopmentpol‐icyinWestandCentralAfricaConservation Biology21(3)884ndash887httpsdoiorg101111j1523‐1739200600595x
BlakeSDeemSLMossimboEMaiselsFampWalshP(2009)Forestelephants Tree planters of the CongoBiotropica41(4) 459ndash468httpsdoiorg101111j1744‐7429200900512x
Blake S (2002) The ecology of forest elephant distribution and itsimplications for conservation Doctoral dissertation University ofEdinburgh
BruceTNdjassiCFowlerANdimbeMFankemOTabueRhellipOlsonD(2018)Faunal inventory of the Dja Faunal Reserve Cameroon Yaoundeacute Cameroon Ministry of Forests and Wildlife (MINFOF)Zoological Society of London ndash Cameroon Country ProgrammeAfricanWildlifeFoundation
BruceTWacherTNdingaHBidjokaVMeyongFNgoBataMampOlsonD(2017)camera trap survey for larger terrestrial wildlife in the Dja Biosphere Reserve CameroonYaoundeacuteCameroonZoologicalSocietyofLondon(ZSL)ampCameroonMinistryofForestsandWildlife(MINFOF)
BurnhamKPampAndersonDR(2002)Model selection and multimodel inferenceNewYorkNYSpringer
Campbell G Kuehl H Diarrassouba A NGoran P K amp BoeschC (2011) Long‐term research sites as refugia for threatened andover‐harvested species Biology Letters 7(5) 723ndash726 httpsdoiorg101098rsbl20110155
CardilloMMaceGMJonesKEBielbyJBininda‐EmondsORSechrestWhellipPurvisA(2005)Multiplecausesofhighextinction
riskinlargemammalspeciesScience309(5738)1239ndash1241httpsdoiorg101126science1116030
Craigie IDBaillieJEBalmfordACarboneCCollenBGreenREampHuttonJM (2010)Largemammalpopulationdeclines inAfricarsquosprotectedareasBiological Conservation143(9)2221ndash2228httpsdoiorg101016jbiocon201006007
DaveyKWacherTampAminR(2017)Analysis tool for camera-trap sur-vey data [Computer software]ZoologicalSocietyofLondonRetrievedfromhttpswwwzslorgzsl‐camera‐trap‐data‐management‐ and‐analysis‐package
Djuikouo M N K Doucet J L Nguembou C K Lewis S L ampSonkeacute B (2010) Diversity and aboveground biomass in threetropical forest types in the Dja Biosphere Reserve Cameroon African Journal of Ecology 48(4) 1053ndash1063 httpsdoiorg101111j1365‐2028201001212x
DupainJBombomeKampVanElsackerL(2003)LeschimpanzeacutesetlesgorillesdelareacuteservedefauneduDjaCanopeacutee2414ndash15
EffordMGampDawsonDK(2012)OccupancyincontinuoushabitatEcosphere3(4)1ndash15httpsdoiorg101890ES11‐003081
Efron B amp Tibshirani R J (1994) An introduction to the bootstrap WashingtonDCCRCPress
FaJEOliveroJFarfaacutenMAacuteMaacuterquezALDuarteJNackoneyJhellipMacdonaldDW(2014a)CorrelatesofbushmeatinmarketsanddepletionofwildlifeConservation Biology29(3)805ndash815
Fa J EOlivero J FarfaacutenMAacuteMaacuterquezA LVargas JMRealRampNasiR(2014b)IntegratingsustainablehuntinginbiodiversityprotectioninCentralAfricaHotspotsweakspotsandstrongspotsPLoS ONE9(11)e112367
FaJERyanSFampBellDJ (2005)Huntingvulnerabilityecolog‐ical characteristics and harvest rates of bushmeat species in afro‐tropicalforestsBiological Conservation121(2)167ndash176httpsdoiorg101016jbiocon200404016
Fa J E Seymour S Dupain J E F Amin R Albrechtsen L ampMacdonaldD (2006) Getting to gripswith themagnitude of ex‐ploitationBushmeat in theCross‐SanagariversregionNigeria and Cameroon Biological Conservation 129(4) 497ndash510 httpsdoiorg101016jbiocon200511031
Farris Z J Boone H M Karpanty S Murphy A Ratelolahy FAndrianjakariveloVampKellyMJ(2015)FeralcatsandthefitoatyFirstpopulationassessmentoftheblackforestcatinMadagascarrsquosrainforestsJournal of Mammalogy97(2)518ndash525
Fiske IampChandlerR (2011)UnmarkedAnRpackageforfittinghi‐erarchicalmodelsofwildlifeoccurrenceandabundanceJournal of Statistical Software43(10)1ndash23
HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences107(19)8650ndash8655httpsdoiorg101073pnas0912668107
HartJ(2013a)WaterchevrotainHymemoschusaquaticusInJKingdonampMHoffmann (Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp88ndash92)LondonUKBloomsbury
Hart J (2013b) White‐bellied duiker Cephalophus leucogaster In JKingdonampMHoffmann(Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp255ndash258)LondonUKBloomsbury
HeadJSRobbinsMMMundryRMakagaLampBoeschC(2012)Remotevideo‐cameratrapsmeasurehabitatuseandcompetitiveex‐clusionamongsympatricchimpanzeegorillaandelephantinLoangoNational ParkGabon Journal of Tropical Ecology28(06) 571ndash583httpsdoiorg101017S0266467412000612
HedgesS(2012)Monitoring elephant populations and assessing threats HimayatnagarTelanganaUniversitiesPress
HedwigDKienastIBonnetMCurranBKCourageABoeschChellipKingT(2018)Acameratrapassessmentoftheforestmam‐mal community within the transitional savannah‐forest mosaic oftheBateacutekeacutePlateauNationalParkGabonAfrican Journal of Ecology56(4)777ndash790httpsdoiorg101111aje12497
emspensp emsp | emsp775Bruce et al
HijmansRJCameronSEParraJLJonesPGampJarvisA(2005)Very high resolution interpolated climate surfaces for global landareasInternational Journal of Climatology25(15)1965ndash1978httpsdoiorg101002joc1276
HuggelA(2012)Exiv2softwaretool[Computersoftware]Retrievedfromhttpswwwexiv2orgindexhtml
Jerozolimski A amp Peres C A (2003) Bringing home the biggestbacon A cross‐site analysis of the structure of hunter‐kill profilesin Neotropical forests Biological Conservation 111(3) 415ndash425httpsdoiorg101016S0006‐3207(02)00310‐5
KingdonJ (2015)The Kingdon field guide to African mammalsLondonUKBloomsburyPublishing
KuumlhlHFMaiselsMAncrenazampEAWilliamson(Eds)(2008)Best practice guidelines for surveys and monitoring of great ape populations GlandSwitzerlandIUCN
LauranceWFCroesBMTchignoumbaLLahmSAAlonsoALeeMEhellipOndzeanoC(2006)ImpactsofroadsandhuntingoncentralAfrican rainforestmammalsConservation Biology20(4)1251ndash1261httpsdoiorg101111j1523‐1739200600420x
LauranceWFUsecheDCRendeiroJKalkaMBradshawCJSloan S P hellip Arroyo‐Rodriguez V (2012) Averting biodiversitycollapse in tropical forestprotectedareasNature489(7415)290httpsdoiorg101038nature11318
LeslieDMampHuffmanBA(2015)Potamochoerus porcus(ArtiodactylaSuidae)Mammalian Species4715ndash31
MacKenzieD IampBailey L L (2004)Assessing the fit of site‐occu‐pancy models Journal of Agricultural Biological and Environmental Statistics9300ndash318httpsdoiorg101198108571104X3361
MacKenzieDINicholsJDRoyleJAPollockKHBaileyLLampHinesJE (2006)Occupancy estimation and modellingBurlingtonMAAcademicPress
Magurran A E (2005) Species abundance distributions Patternor process Functional Ecology 19(1) 177ndash181 httpsdoiorg101111j0269‐8463200500930x
MaiselsFStrindbergSBlakeSWittemyerGHartJWilliamsonEAhellipWarrenY (2013)DevastatingdeclineofforestelephantsinCentralAfricaPLoS ONE8(3)e59469httpsdoiorg101371journalpone0059469
MalhiYAdu‐BreduSAsareRA LewisS LampMayauxP (2013)AfricanrainforestsPastpresentandfuturePhilosophical Transactions of the Royal Society of London Biological Sciences 368(1625)20120312
MallonDPHoffmannMGraingerMJHibertFVanVlietNampMcGowanP JK (2015)An IUCNsituationanalysisof terrestrialandfreshwaterfaunainWestandCentralAfricaOccasionalpaperoftheIUCNspeciessurvivalcommission(54)
MambeyaMMBakerFMombouaBRKoumbaPamboAFHegaMOkouyiOkouyiVJhellipAbernethyK(2018)TheemergenceofacommercialtradeinpangolinsfromGabonAfrican Journal of Ecology56(3)601ndash609httpsdoiorg101111aje12507
MINFOFampIUCN(2015)CaracteacuterisationdelapopulationdegrandsetmoyensmammifegraveresdanslaReservedeFauneduDjaPotentieletmenacesYaoundeacuteCameroun
Muchaal P K amp Ngandjui G (1999) Impact of village hunt‐ing on wildlife populations in the western Dja ReserveCameroon Conservation Biology 13(2) 385ndash396 httpsdoiorg101046j1523‐17391999013002385x
NaranjoEJampBodmerRE (2007) Sourcendashsink systemsandconser‐vationofhuntedungulatesintheLacandonForestMexico Biological Conservation 138(3ndash4) 412ndash420 httpsdoiorg101016jbiocon 200705010
NielsenMR(2006)ImportancecauseandeffectofbushmeathuntingintheUdzungwaMountainsTanzania ImplicationsforcommunitybasedwildlifemanagementBiological Conservation128(4)509ndash516httpsdoiorg101016jbiocon200510017
OBrienTGKinnairdMFampWibisonoHT (2003)Crouching ti‐gers hiddenprey Sumatran tiger andprey populations in a tropi‐calforestlandscapeAnimal Conservation6(2)131ndash139httpsdoiorg101017S1367943003003172
OksanenJ(2015)VegananintroductiontoordinationVol8(p19)Retrieved from httpscranr‐projectorgwebpackagesveganvi‐gnettesintroveganpdf
PeresCAampPalaciosE(2007)Basin‐wideeffectsofgameharvestonvertebrate populationdensities inAmazonian forests Implicationsfor animal‐mediated seed dispersal Biotropica 39(3) 304ndash315httpsdoiorg101111j1744‐7429200700272x
PotapovPVTurubanovaSAHansenMCAduseiBBroichMAltstattAhellipJusticeCO(2012)QuantifyingforestcoverlossinDemocraticRepublicoftheCongo2000ndash2010withLandsatETM+data Remote Sensing of Environment 122 106ndash116 httpsdoiorg101016jrse201108027
PoulsenJRKoernerSEMooreSMedjibeVPBlakeSClarkC JhellipRosinC (2017) Poaching empties criticalCentralAfricanwilderness of forest elephants Current Biology 27(4) 134ndashR135httpsdoiorg101016jcub201701023
PurvisAGittlemanJlCowlishawGampMaceGM(2000)PredictingextinctionriskindecliningspeciesProceedings of the Royal Society B Biological Sciences267(1456) 1947ndash1952 httpsdoiorg101098rspb20001234
RayJ(1997)ComparativeecologyoftwoAfricanforestmongoosesHerpestesnasoandAtilaxpaludinosusAfrican Journal of Ecology35(3)237ndash253httpsdoiorg101111j1365‐20281997086‐ 89086x
Redford K H (1992) The empty forest BioScience 42(6) 412ndash422httpsdoiorg1023071311860
RepublicofCameroon(1994)Lawno9401du20janvier1994portantreacutegimedesforecirctsdelafauneetdelapecirccheRepublicofCameroon
RoveroFampMarshallAR(2009)CameratrappingphotographicrateasanindexofdensityinforestungulatesJournal of Applied Ecology46(5)1011ndash1017httpsdoiorg101111j1365‐2664200901705x
Royle J A amp Nichols J D (2003) Estimating abundance from re‐peated presence‐absence data or point counts Ecology 84(3)777ndash790 httpsdoiorg1018900012‐9658(2003)084[0777EAFRPA]20CO2
Seddon P J Griffiths C J Soorae P S ampArmstrongD P (2014)ReversingdefaunationRestoringspeciesinachangingworldScience345(6195)406ndash412httpsdoiorg101126science1251818
Silveira L Jacomo A T amp Diniz‐Filho J A F (2003) Camera trapline transect census and track surveys A comparative evaluationBiological Conservation 114(3) 351ndash355 httpsdoiorg101016S0006‐3207(03)00063‐6
Sonkeacute B (1998) Etudes floristiques et structurales des forecircts de laReacuteserve de Faune du Dja (Cameroun) Laboratoire de BotaniqueSysteacutematique et de Phytosociologie Universiteacute Libre de Bruxelles(ULB)
Srbek‐AraujoACampChiarelloAG(2005)Iscameratrappinganeffi‐cientmethodforsurveyingmammalsinNeotropicalforestsAcasestudyinsouth‐easternBrazilJournal of Tropical Ecology21(1)121ndash125httpsdoiorg101017S0266467404001956
Stiles D (2011) Elephant meat and ivory trade in Central AfricaPachyderm5026ndash36
TEAMNetwork(2008)Terrestrialvertebrateprotocol implementationmanualv30(p56)WashingtonDCTropicalEcologyAssessmentandMonitoringNetworkCenter forAppliedBiodiversity ScienceConservationInternational
Tobler M W Carrillo‐Percastegui S E Leite Pitman R MaresR amp Powell G (2008) An evaluation of camera traps for in‐ventorying large‐and medium‐sized terrestrial rainforestmammals Animal Conservation 11(3) 169ndash178 httpsdoiorg101111j1469‐1795200800169x
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
774emsp |emsp emspensp Bruce et al
R E FE R E N C E S
AbernethyKACoad L TaylorG LeeMEampMaisels F (2013)Extent and ecological consequences of hunting in Central Africanrainforests in thetwenty‐firstcenturyPhilosophical Transactions of the Royal Society of London Biological Sciences368(1625)20120303httpsdoiorg101098rstb20120303
AbrahamsM I Peres C A amp Costa H C (2017)Measuring localdepletion of terrestrial game vertebrates by central‐place hunt‐ers in rural Amazonia PLoS ONE 12(10) e0186653 httpsdoiorg101371journalpone0186653
AhumadaJAHurtadoJampLizcanoD(2013)MonitoringthestatusandtrendsoftropicalforestterrestrialvertebratecommunitiesfromcameratrapdataAtool forconservationPLoS ONE8(9)e73707httpsdoiorg101371journalpone0073707
Ahumada J A Silva C E Gajapersad K Hallam C Hurtado JMartin E hellip Sheil D (2011) Community structure and diver‐sity of tropical forest mammals Data from a global camera trapnetwork Philosophical Transactions of the Royal Society of London Biological Sciences366(1578)2703ndash2711httpsdoiorg101098rstb20110115
AminRAndanjeSAOgwonkaBAliAHBowkettAEOmarMampWacherT(2015)ThenortherncoastalforestsofKenyaarenationally and globally important for the conservation of AdersrsquoduikerCephalophusadersiandotherantelopespeciesBiodiversity and Conservation 24(3) 641ndash658 httpsdoiorg101007s10531‐014‐0842‐z
Attum O (2007) Can landscape use be among the factors that po‐tentiallymake some ungulates speciesmore difficult to conserveJournal of Arid Environments69(3)410ndash419
Bahaa‐el‐dinLHenschelPAbaaRAbernethyKBohmTBoutNhellipLeeM (2013)NotesonthedistributionandstatusofsmallcarnivoresinGabonSmall Carnivore Conservation4819ndash29
Bahaa‐el‐dinLHenschelPButynskiTMMacdonaldDWMillsDSlotowRampHunterL (2015)TheAfricangoldencatCaracalaurataAfricasleast‐knownfelidMammal Review45(1)63ndash77
Bennett E L Blencowe E Brandon K Brown D Burn R WCowlishaw G hellip Robinson J G (2007) Hunting for consensusReconcilingbushmeatharvestconservationanddevelopmentpol‐icyinWestandCentralAfricaConservation Biology21(3)884ndash887httpsdoiorg101111j1523‐1739200600595x
BlakeSDeemSLMossimboEMaiselsFampWalshP(2009)Forestelephants Tree planters of the CongoBiotropica41(4) 459ndash468httpsdoiorg101111j1744‐7429200900512x
Blake S (2002) The ecology of forest elephant distribution and itsimplications for conservation Doctoral dissertation University ofEdinburgh
BruceTNdjassiCFowlerANdimbeMFankemOTabueRhellipOlsonD(2018)Faunal inventory of the Dja Faunal Reserve Cameroon Yaoundeacute Cameroon Ministry of Forests and Wildlife (MINFOF)Zoological Society of London ndash Cameroon Country ProgrammeAfricanWildlifeFoundation
BruceTWacherTNdingaHBidjokaVMeyongFNgoBataMampOlsonD(2017)camera trap survey for larger terrestrial wildlife in the Dja Biosphere Reserve CameroonYaoundeacuteCameroonZoologicalSocietyofLondon(ZSL)ampCameroonMinistryofForestsandWildlife(MINFOF)
BurnhamKPampAndersonDR(2002)Model selection and multimodel inferenceNewYorkNYSpringer
Campbell G Kuehl H Diarrassouba A NGoran P K amp BoeschC (2011) Long‐term research sites as refugia for threatened andover‐harvested species Biology Letters 7(5) 723ndash726 httpsdoiorg101098rsbl20110155
CardilloMMaceGMJonesKEBielbyJBininda‐EmondsORSechrestWhellipPurvisA(2005)Multiplecausesofhighextinction
riskinlargemammalspeciesScience309(5738)1239ndash1241httpsdoiorg101126science1116030
Craigie IDBaillieJEBalmfordACarboneCCollenBGreenREampHuttonJM (2010)Largemammalpopulationdeclines inAfricarsquosprotectedareasBiological Conservation143(9)2221ndash2228httpsdoiorg101016jbiocon201006007
DaveyKWacherTampAminR(2017)Analysis tool for camera-trap sur-vey data [Computer software]ZoologicalSocietyofLondonRetrievedfromhttpswwwzslorgzsl‐camera‐trap‐data‐management‐ and‐analysis‐package
Djuikouo M N K Doucet J L Nguembou C K Lewis S L ampSonkeacute B (2010) Diversity and aboveground biomass in threetropical forest types in the Dja Biosphere Reserve Cameroon African Journal of Ecology 48(4) 1053ndash1063 httpsdoiorg101111j1365‐2028201001212x
DupainJBombomeKampVanElsackerL(2003)LeschimpanzeacutesetlesgorillesdelareacuteservedefauneduDjaCanopeacutee2414ndash15
EffordMGampDawsonDK(2012)OccupancyincontinuoushabitatEcosphere3(4)1ndash15httpsdoiorg101890ES11‐003081
Efron B amp Tibshirani R J (1994) An introduction to the bootstrap WashingtonDCCRCPress
FaJEOliveroJFarfaacutenMAacuteMaacuterquezALDuarteJNackoneyJhellipMacdonaldDW(2014a)CorrelatesofbushmeatinmarketsanddepletionofwildlifeConservation Biology29(3)805ndash815
Fa J EOlivero J FarfaacutenMAacuteMaacuterquezA LVargas JMRealRampNasiR(2014b)IntegratingsustainablehuntinginbiodiversityprotectioninCentralAfricaHotspotsweakspotsandstrongspotsPLoS ONE9(11)e112367
FaJERyanSFampBellDJ (2005)Huntingvulnerabilityecolog‐ical characteristics and harvest rates of bushmeat species in afro‐tropicalforestsBiological Conservation121(2)167ndash176httpsdoiorg101016jbiocon200404016
Fa J E Seymour S Dupain J E F Amin R Albrechtsen L ampMacdonaldD (2006) Getting to gripswith themagnitude of ex‐ploitationBushmeat in theCross‐SanagariversregionNigeria and Cameroon Biological Conservation 129(4) 497ndash510 httpsdoiorg101016jbiocon200511031
Farris Z J Boone H M Karpanty S Murphy A Ratelolahy FAndrianjakariveloVampKellyMJ(2015)FeralcatsandthefitoatyFirstpopulationassessmentoftheblackforestcatinMadagascarrsquosrainforestsJournal of Mammalogy97(2)518ndash525
Fiske IampChandlerR (2011)UnmarkedAnRpackageforfittinghi‐erarchicalmodelsofwildlifeoccurrenceandabundanceJournal of Statistical Software43(10)1ndash23
HansenMCStehmanSVampPotapovPV(2010)QuantificationofglobalgrossforestcoverlossProceedings of the National Academy of Sciences107(19)8650ndash8655httpsdoiorg101073pnas0912668107
HartJ(2013a)WaterchevrotainHymemoschusaquaticusInJKingdonampMHoffmann (Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp88ndash92)LondonUKBloomsbury
Hart J (2013b) White‐bellied duiker Cephalophus leucogaster In JKingdonampMHoffmann(Eds)Mammals of Africa VI Hippopotamuses pigs deer giraffe and bovids(pp255ndash258)LondonUKBloomsbury
HeadJSRobbinsMMMundryRMakagaLampBoeschC(2012)Remotevideo‐cameratrapsmeasurehabitatuseandcompetitiveex‐clusionamongsympatricchimpanzeegorillaandelephantinLoangoNational ParkGabon Journal of Tropical Ecology28(06) 571ndash583httpsdoiorg101017S0266467412000612
HedgesS(2012)Monitoring elephant populations and assessing threats HimayatnagarTelanganaUniversitiesPress
HedwigDKienastIBonnetMCurranBKCourageABoeschChellipKingT(2018)Acameratrapassessmentoftheforestmam‐mal community within the transitional savannah‐forest mosaic oftheBateacutekeacutePlateauNationalParkGabonAfrican Journal of Ecology56(4)777ndash790httpsdoiorg101111aje12497
emspensp emsp | emsp775Bruce et al
HijmansRJCameronSEParraJLJonesPGampJarvisA(2005)Very high resolution interpolated climate surfaces for global landareasInternational Journal of Climatology25(15)1965ndash1978httpsdoiorg101002joc1276
HuggelA(2012)Exiv2softwaretool[Computersoftware]Retrievedfromhttpswwwexiv2orgindexhtml
Jerozolimski A amp Peres C A (2003) Bringing home the biggestbacon A cross‐site analysis of the structure of hunter‐kill profilesin Neotropical forests Biological Conservation 111(3) 415ndash425httpsdoiorg101016S0006‐3207(02)00310‐5
KingdonJ (2015)The Kingdon field guide to African mammalsLondonUKBloomsburyPublishing
KuumlhlHFMaiselsMAncrenazampEAWilliamson(Eds)(2008)Best practice guidelines for surveys and monitoring of great ape populations GlandSwitzerlandIUCN
LauranceWFCroesBMTchignoumbaLLahmSAAlonsoALeeMEhellipOndzeanoC(2006)ImpactsofroadsandhuntingoncentralAfrican rainforestmammalsConservation Biology20(4)1251ndash1261httpsdoiorg101111j1523‐1739200600420x
LauranceWFUsecheDCRendeiroJKalkaMBradshawCJSloan S P hellip Arroyo‐Rodriguez V (2012) Averting biodiversitycollapse in tropical forestprotectedareasNature489(7415)290httpsdoiorg101038nature11318
LeslieDMampHuffmanBA(2015)Potamochoerus porcus(ArtiodactylaSuidae)Mammalian Species4715ndash31
MacKenzieD IampBailey L L (2004)Assessing the fit of site‐occu‐pancy models Journal of Agricultural Biological and Environmental Statistics9300ndash318httpsdoiorg101198108571104X3361
MacKenzieDINicholsJDRoyleJAPollockKHBaileyLLampHinesJE (2006)Occupancy estimation and modellingBurlingtonMAAcademicPress
Magurran A E (2005) Species abundance distributions Patternor process Functional Ecology 19(1) 177ndash181 httpsdoiorg101111j0269‐8463200500930x
MaiselsFStrindbergSBlakeSWittemyerGHartJWilliamsonEAhellipWarrenY (2013)DevastatingdeclineofforestelephantsinCentralAfricaPLoS ONE8(3)e59469httpsdoiorg101371journalpone0059469
MalhiYAdu‐BreduSAsareRA LewisS LampMayauxP (2013)AfricanrainforestsPastpresentandfuturePhilosophical Transactions of the Royal Society of London Biological Sciences 368(1625)20120312
MallonDPHoffmannMGraingerMJHibertFVanVlietNampMcGowanP JK (2015)An IUCNsituationanalysisof terrestrialandfreshwaterfaunainWestandCentralAfricaOccasionalpaperoftheIUCNspeciessurvivalcommission(54)
MambeyaMMBakerFMombouaBRKoumbaPamboAFHegaMOkouyiOkouyiVJhellipAbernethyK(2018)TheemergenceofacommercialtradeinpangolinsfromGabonAfrican Journal of Ecology56(3)601ndash609httpsdoiorg101111aje12507
MINFOFampIUCN(2015)CaracteacuterisationdelapopulationdegrandsetmoyensmammifegraveresdanslaReservedeFauneduDjaPotentieletmenacesYaoundeacuteCameroun
Muchaal P K amp Ngandjui G (1999) Impact of village hunt‐ing on wildlife populations in the western Dja ReserveCameroon Conservation Biology 13(2) 385ndash396 httpsdoiorg101046j1523‐17391999013002385x
NaranjoEJampBodmerRE (2007) Sourcendashsink systemsandconser‐vationofhuntedungulatesintheLacandonForestMexico Biological Conservation 138(3ndash4) 412ndash420 httpsdoiorg101016jbiocon 200705010
NielsenMR(2006)ImportancecauseandeffectofbushmeathuntingintheUdzungwaMountainsTanzania ImplicationsforcommunitybasedwildlifemanagementBiological Conservation128(4)509ndash516httpsdoiorg101016jbiocon200510017
OBrienTGKinnairdMFampWibisonoHT (2003)Crouching ti‐gers hiddenprey Sumatran tiger andprey populations in a tropi‐calforestlandscapeAnimal Conservation6(2)131ndash139httpsdoiorg101017S1367943003003172
OksanenJ(2015)VegananintroductiontoordinationVol8(p19)Retrieved from httpscranr‐projectorgwebpackagesveganvi‐gnettesintroveganpdf
PeresCAampPalaciosE(2007)Basin‐wideeffectsofgameharvestonvertebrate populationdensities inAmazonian forests Implicationsfor animal‐mediated seed dispersal Biotropica 39(3) 304ndash315httpsdoiorg101111j1744‐7429200700272x
PotapovPVTurubanovaSAHansenMCAduseiBBroichMAltstattAhellipJusticeCO(2012)QuantifyingforestcoverlossinDemocraticRepublicoftheCongo2000ndash2010withLandsatETM+data Remote Sensing of Environment 122 106ndash116 httpsdoiorg101016jrse201108027
PoulsenJRKoernerSEMooreSMedjibeVPBlakeSClarkC JhellipRosinC (2017) Poaching empties criticalCentralAfricanwilderness of forest elephants Current Biology 27(4) 134ndashR135httpsdoiorg101016jcub201701023
PurvisAGittlemanJlCowlishawGampMaceGM(2000)PredictingextinctionriskindecliningspeciesProceedings of the Royal Society B Biological Sciences267(1456) 1947ndash1952 httpsdoiorg101098rspb20001234
RayJ(1997)ComparativeecologyoftwoAfricanforestmongoosesHerpestesnasoandAtilaxpaludinosusAfrican Journal of Ecology35(3)237ndash253httpsdoiorg101111j1365‐20281997086‐ 89086x
Redford K H (1992) The empty forest BioScience 42(6) 412ndash422httpsdoiorg1023071311860
RepublicofCameroon(1994)Lawno9401du20janvier1994portantreacutegimedesforecirctsdelafauneetdelapecirccheRepublicofCameroon
RoveroFampMarshallAR(2009)CameratrappingphotographicrateasanindexofdensityinforestungulatesJournal of Applied Ecology46(5)1011ndash1017httpsdoiorg101111j1365‐2664200901705x
Royle J A amp Nichols J D (2003) Estimating abundance from re‐peated presence‐absence data or point counts Ecology 84(3)777ndash790 httpsdoiorg1018900012‐9658(2003)084[0777EAFRPA]20CO2
Seddon P J Griffiths C J Soorae P S ampArmstrongD P (2014)ReversingdefaunationRestoringspeciesinachangingworldScience345(6195)406ndash412httpsdoiorg101126science1251818
Silveira L Jacomo A T amp Diniz‐Filho J A F (2003) Camera trapline transect census and track surveys A comparative evaluationBiological Conservation 114(3) 351ndash355 httpsdoiorg101016S0006‐3207(03)00063‐6
Sonkeacute B (1998) Etudes floristiques et structurales des forecircts de laReacuteserve de Faune du Dja (Cameroun) Laboratoire de BotaniqueSysteacutematique et de Phytosociologie Universiteacute Libre de Bruxelles(ULB)
Srbek‐AraujoACampChiarelloAG(2005)Iscameratrappinganeffi‐cientmethodforsurveyingmammalsinNeotropicalforestsAcasestudyinsouth‐easternBrazilJournal of Tropical Ecology21(1)121ndash125httpsdoiorg101017S0266467404001956
Stiles D (2011) Elephant meat and ivory trade in Central AfricaPachyderm5026ndash36
TEAMNetwork(2008)Terrestrialvertebrateprotocol implementationmanualv30(p56)WashingtonDCTropicalEcologyAssessmentandMonitoringNetworkCenter forAppliedBiodiversity ScienceConservationInternational
Tobler M W Carrillo‐Percastegui S E Leite Pitman R MaresR amp Powell G (2008) An evaluation of camera traps for in‐ventorying large‐and medium‐sized terrestrial rainforestmammals Animal Conservation 11(3) 169ndash178 httpsdoiorg101111j1469‐1795200800169x
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
emspensp emsp | emsp775Bruce et al
HijmansRJCameronSEParraJLJonesPGampJarvisA(2005)Very high resolution interpolated climate surfaces for global landareasInternational Journal of Climatology25(15)1965ndash1978httpsdoiorg101002joc1276
HuggelA(2012)Exiv2softwaretool[Computersoftware]Retrievedfromhttpswwwexiv2orgindexhtml
Jerozolimski A amp Peres C A (2003) Bringing home the biggestbacon A cross‐site analysis of the structure of hunter‐kill profilesin Neotropical forests Biological Conservation 111(3) 415ndash425httpsdoiorg101016S0006‐3207(02)00310‐5
KingdonJ (2015)The Kingdon field guide to African mammalsLondonUKBloomsburyPublishing
KuumlhlHFMaiselsMAncrenazampEAWilliamson(Eds)(2008)Best practice guidelines for surveys and monitoring of great ape populations GlandSwitzerlandIUCN
LauranceWFCroesBMTchignoumbaLLahmSAAlonsoALeeMEhellipOndzeanoC(2006)ImpactsofroadsandhuntingoncentralAfrican rainforestmammalsConservation Biology20(4)1251ndash1261httpsdoiorg101111j1523‐1739200600420x
LauranceWFUsecheDCRendeiroJKalkaMBradshawCJSloan S P hellip Arroyo‐Rodriguez V (2012) Averting biodiversitycollapse in tropical forestprotectedareasNature489(7415)290httpsdoiorg101038nature11318
LeslieDMampHuffmanBA(2015)Potamochoerus porcus(ArtiodactylaSuidae)Mammalian Species4715ndash31
MacKenzieD IampBailey L L (2004)Assessing the fit of site‐occu‐pancy models Journal of Agricultural Biological and Environmental Statistics9300ndash318httpsdoiorg101198108571104X3361
MacKenzieDINicholsJDRoyleJAPollockKHBaileyLLampHinesJE (2006)Occupancy estimation and modellingBurlingtonMAAcademicPress
Magurran A E (2005) Species abundance distributions Patternor process Functional Ecology 19(1) 177ndash181 httpsdoiorg101111j0269‐8463200500930x
MaiselsFStrindbergSBlakeSWittemyerGHartJWilliamsonEAhellipWarrenY (2013)DevastatingdeclineofforestelephantsinCentralAfricaPLoS ONE8(3)e59469httpsdoiorg101371journalpone0059469
MalhiYAdu‐BreduSAsareRA LewisS LampMayauxP (2013)AfricanrainforestsPastpresentandfuturePhilosophical Transactions of the Royal Society of London Biological Sciences 368(1625)20120312
MallonDPHoffmannMGraingerMJHibertFVanVlietNampMcGowanP JK (2015)An IUCNsituationanalysisof terrestrialandfreshwaterfaunainWestandCentralAfricaOccasionalpaperoftheIUCNspeciessurvivalcommission(54)
MambeyaMMBakerFMombouaBRKoumbaPamboAFHegaMOkouyiOkouyiVJhellipAbernethyK(2018)TheemergenceofacommercialtradeinpangolinsfromGabonAfrican Journal of Ecology56(3)601ndash609httpsdoiorg101111aje12507
MINFOFampIUCN(2015)CaracteacuterisationdelapopulationdegrandsetmoyensmammifegraveresdanslaReservedeFauneduDjaPotentieletmenacesYaoundeacuteCameroun
Muchaal P K amp Ngandjui G (1999) Impact of village hunt‐ing on wildlife populations in the western Dja ReserveCameroon Conservation Biology 13(2) 385ndash396 httpsdoiorg101046j1523‐17391999013002385x
NaranjoEJampBodmerRE (2007) Sourcendashsink systemsandconser‐vationofhuntedungulatesintheLacandonForestMexico Biological Conservation 138(3ndash4) 412ndash420 httpsdoiorg101016jbiocon 200705010
NielsenMR(2006)ImportancecauseandeffectofbushmeathuntingintheUdzungwaMountainsTanzania ImplicationsforcommunitybasedwildlifemanagementBiological Conservation128(4)509ndash516httpsdoiorg101016jbiocon200510017
OBrienTGKinnairdMFampWibisonoHT (2003)Crouching ti‐gers hiddenprey Sumatran tiger andprey populations in a tropi‐calforestlandscapeAnimal Conservation6(2)131ndash139httpsdoiorg101017S1367943003003172
OksanenJ(2015)VegananintroductiontoordinationVol8(p19)Retrieved from httpscranr‐projectorgwebpackagesveganvi‐gnettesintroveganpdf
PeresCAampPalaciosE(2007)Basin‐wideeffectsofgameharvestonvertebrate populationdensities inAmazonian forests Implicationsfor animal‐mediated seed dispersal Biotropica 39(3) 304ndash315httpsdoiorg101111j1744‐7429200700272x
PotapovPVTurubanovaSAHansenMCAduseiBBroichMAltstattAhellipJusticeCO(2012)QuantifyingforestcoverlossinDemocraticRepublicoftheCongo2000ndash2010withLandsatETM+data Remote Sensing of Environment 122 106ndash116 httpsdoiorg101016jrse201108027
PoulsenJRKoernerSEMooreSMedjibeVPBlakeSClarkC JhellipRosinC (2017) Poaching empties criticalCentralAfricanwilderness of forest elephants Current Biology 27(4) 134ndashR135httpsdoiorg101016jcub201701023
PurvisAGittlemanJlCowlishawGampMaceGM(2000)PredictingextinctionriskindecliningspeciesProceedings of the Royal Society B Biological Sciences267(1456) 1947ndash1952 httpsdoiorg101098rspb20001234
RayJ(1997)ComparativeecologyoftwoAfricanforestmongoosesHerpestesnasoandAtilaxpaludinosusAfrican Journal of Ecology35(3)237ndash253httpsdoiorg101111j1365‐20281997086‐ 89086x
Redford K H (1992) The empty forest BioScience 42(6) 412ndash422httpsdoiorg1023071311860
RepublicofCameroon(1994)Lawno9401du20janvier1994portantreacutegimedesforecirctsdelafauneetdelapecirccheRepublicofCameroon
RoveroFampMarshallAR(2009)CameratrappingphotographicrateasanindexofdensityinforestungulatesJournal of Applied Ecology46(5)1011ndash1017httpsdoiorg101111j1365‐2664200901705x
Royle J A amp Nichols J D (2003) Estimating abundance from re‐peated presence‐absence data or point counts Ecology 84(3)777ndash790 httpsdoiorg1018900012‐9658(2003)084[0777EAFRPA]20CO2
Seddon P J Griffiths C J Soorae P S ampArmstrongD P (2014)ReversingdefaunationRestoringspeciesinachangingworldScience345(6195)406ndash412httpsdoiorg101126science1251818
Silveira L Jacomo A T amp Diniz‐Filho J A F (2003) Camera trapline transect census and track surveys A comparative evaluationBiological Conservation 114(3) 351ndash355 httpsdoiorg101016S0006‐3207(03)00063‐6
Sonkeacute B (1998) Etudes floristiques et structurales des forecircts de laReacuteserve de Faune du Dja (Cameroun) Laboratoire de BotaniqueSysteacutematique et de Phytosociologie Universiteacute Libre de Bruxelles(ULB)
Srbek‐AraujoACampChiarelloAG(2005)Iscameratrappinganeffi‐cientmethodforsurveyingmammalsinNeotropicalforestsAcasestudyinsouth‐easternBrazilJournal of Tropical Ecology21(1)121ndash125httpsdoiorg101017S0266467404001956
Stiles D (2011) Elephant meat and ivory trade in Central AfricaPachyderm5026ndash36
TEAMNetwork(2008)Terrestrialvertebrateprotocol implementationmanualv30(p56)WashingtonDCTropicalEcologyAssessmentandMonitoringNetworkCenter forAppliedBiodiversity ScienceConservationInternational
Tobler M W Carrillo‐Percastegui S E Leite Pitman R MaresR amp Powell G (2008) An evaluation of camera traps for in‐ventorying large‐and medium‐sized terrestrial rainforestmammals Animal Conservation 11(3) 169ndash178 httpsdoiorg101111j1469‐1795200800169x
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
776emsp |emsp emspensp Bruce et al
TuckerMAOrdTJampRogersTL(2014)EvolutionarypredictorsofmammalianhomerangesizeBodymassdietandtheenvironmentGlobal Ecology and Biogeography 23(10) 1105ndash1114 httpsdoiorg101111geb12194
Williamson L amp Usongo L (1995) Recensement des populationsde primates et inventaire des grands mammifegraveres Recensementdes eacuteleacutephants gorilles et chimpanzeacutes reacuteserve de faune du Dja‐CamerounProjetEcofac‐ComposanteCameroun
Ziegler S Fa J EWohlfartC StreitB Jacob SampWegmannM(2016) Mapping bushmeat hunting pressure in Central AfricaBiotropica48(3)405ndash412httpsdoiorg101111btp12286
ZSL amp MINFOF (2017a) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2016 au 31 deacutecembre 2016)UnpublishedreportZoologicalSocietyofLondon
ZSL amp MINFOF (2017b) Rapport de patrouilles SMART - Reacuteserve de Biosphegravere du Dja au Cameroun (Du 1 janvier 2017 au 30 septembre 2017)UnpublishedreportZoologicalSocietyofLondon
How to cite this articleBruceTAminRWacherTetalUsingcameratrapdatatocharacteriseterrestriallarger‐bodiedmammalcommunitiesindifferentmanagementsectorsoftheDjaFaunalReserveCameroonAfr J Ecol 201856759ndash776 httpsdoiorg101111aje12574
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