Alford & Richards, 1999

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Global Amphibian Declines: A Problem in Applied Ecology

Author(s): Ross A. Alford and Stephen J. RichardsReviewed work(s):Source: Annual Review of Ecology and Systematics, Vol. 30 (1999), pp. 133-165Published by: Annual ReviewsStable URL: http://www.jstor.org/stable/221682.

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Anniu.Rev. Ecol. Syst. 1999. 30:133-65Copyright? 1999 by AnnualReviews. All rightsreserved

GLOBAL MPHIBIAN ECLINES: PROBLEMIN APPLIEDECOLOGYRoss A. Alford andStephenJ.RichardsSchool of TropicalBiology and CooperativeResearch Centre or TropicalRainforestEcology andManagement,James CookUniversity,Townsville,Queensland4811, Australia;e-mail: [email protected] Words conservation, frog, salamander,null hypothesis, metapopulation* Abstract Declines and losses of amphibian populations are a global problemwith complex local causes. These may include ultraviolet radiation, predation, habi-tat modification, environmental acidity and toxicants, diseases, changes in climateor weather patterns, and interactions among these factors. Understanding the extentof the problem and its nature requires an understanding of how local factors affectthe dynamics of local populations. Hypotheses about population behavior must betested against appropriatenull hypotheses. We generated null hypotheses for the be-havior of amphibianpopulations using a model, and we used them to test hypothesesabout the behavior of 85 time series taken from the literature. Our results suggestthat most amphibianpopulations should decrease more often than they increase, dueto highly variable recruitment and less variable adult mortality. During the periodcovered by our data (1951-1997), more amphibian populations decreased than ourmodel predicted. However, there was no indication that the proportionof populationsdecreasing changed over time. In addition, our review of the literaturesuggests thatmany if not most amphibians exist in metapopulations. Understanding the dynamicsof amphibian populations will require an integration of studies on and within localpopulations and at the metapopulation level.

INTRODUCTIONThe currentwave of interest in amphibian population biology and in the possibilitythat there is a global pattern of decline and loss began in 1989 at the First WorldCongress of Herpetology (10). By 1993 more than 500 populations of frogs andsalamanders on five continents were listed as declining or of conservation concern(189). There is now a consensus that alarming declines of amphibians have oc-cuffed (30, 51, 725, 147, 192). Because most amphibians are exposed to terrestrialand aquatic habitats at different stages of their life cycles, and because they havehighly permeable skins, they may be more sensitive to environmental toxins or tochanges in patterns of temperature or rainfall than are other terrestrial vertebrate

0066-4162/99/1120-0133$08.00 133


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134 ALFORD . RICHARDS

TABLE 1 Techniquesused in 46 studies1 o quantifypopulationsof frogs salamanders.Manystudies used more than one techniqueor studied bothtaxa, so the total numberof techniques used doesnot equal the numberof studies cited.Technique Habitat2 Frogs SalamandersEgg mass counts B 4 1Countsof individuals B 12 1Driftfence/pit trapcounts B 7 8Mark-recapturestimates3 B 7 2Callingmale counts B 3 N/ADipnet samplesfor larvae B 2 2Countsof individuals N 1 6Mark-recapturestimates N 0 1Aquatictraps N 0 11Sourcesused in compilingtable: 15, 19, 20, 21, 41, 49, 53, 54, 63, 64, 73, 83, 84,86, 88, 90, 91, 92, 96, 102, 107, 111, 113, 117, 131, 136, 137, 142, 157, 158, 159,160, 161, 165, 169, 170, 171, 174, 177, 178, 179, 180, 181, 194, 196, 202.2B = Breeding,N = Non-breeding.3Includes, in descendingorderof frequencyused,Jolly-Seber,Petersen,Manly-Parr,Schnabel,andZippin techniques.

groups (29, 190). The best-documented declines have occurred in Europe andNorth America, are usually associated with habitat modification (87, 116), andare often attributed to interactions among causal factors (114, 125, 147). The fac-tors associated with population declines in relatively undisturbed habitats such asmontane tropical rainforests have been more difficult to elucidate (131, 163).

Although they have been the subject of many experimental and monitoringstudies, the autecology of amphibians in nature is poorly understood (87). Themajority of studies of ecology and population biology of amphibians (Table 1) havebeen conducted on aggregations at reproductive sites. Relatively little is knownof their movements or activities away from breeding sites, or of rates of exchangebetween populations.

Many authors have suggested that there is a need for long-term studies di-rected toward a combination of understanding ecological theory and increasingknowledge of the autecology of amphibians (17,39,79,80, 190). Simple long-term programs that monitor the fluctuations of single populations and associatedenvironmental factors, and then apply standard population models, are unlikely tobe useful for understanding the dynamics of amphibian populations as they havenot worked for that purpose when applied to other terrestrial vertebrates (164). Itappears likely that understanding the problem of amphibian declines will requiremuch more information on the ecology of the metapopulations in which manyspecies live (87).


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GLOBALAMPHIBIANDECLINES 135

Our goals in this review are to summarize and synthesize the literatureonpotential causes of amphibiandeclines, and to use the literatureon amphibianpopulation dynamics to develop a null hypothesis for the behavior of amphib-ian populations.We then use our null hypothesis and data from the literature odeterminewhetherthe incidence of declines has recently increased.Finally, weplace the dynamicsof amphibianpopulationsand their declines in the context ofmetapopulation ynamics.POTENTIALCAUSESOF AMPHIBIANDECLINESUltraviolet RadiationDepletion of stratosphericozone and resultantseasonal increases in ultravioletB (UV-B) radiationat the Earth's surface(119) have stimulated nterestin thepossible relationshipbetween resistanceof amphibianembryosto UV-B damageand population declines. Significant variationamong species in levels of pho-tolyase, a photoreactivatingDNA repair enzyme that repairs UV-B damage, iscorrelatedwith exposureof naturalegg depositionsites to sunlight(25,98). In asurveyof 10 Oregon amphibian pecies, photolyase activity,andhence abilitytorepairUV damage, was lowest in declining species andhighest in nondecliningspecies (25). Field experiments demonstrated that embryos of Hyla regilla, a non-declining species withhigh photolyaseactivity,had significantlyhigher hatchingsuccess thandidtwo declining species (Rana cascadae andBufo boreas) with lowphotolyase levels (25).A numberof otherstudieshave demonstrated hat ambient(6,24,28, 132) orenhanced 144) UV-Bradiation educes survivalorhatchingsuccessof amphibianembryos. Synergistic nteractionsbetween UV-B andotherenvironmental tressessuch as pathogens(120) andlow pH (133) may also significantly ncrease embry-onic mortality.Ranapipiens embryosthat are unaffectedwhen exposedto UV-Band low pH separatelyhave significantlyreducedsurvivalwhen exposedto thesefactorssimultaneously 133).Otherstudieshaveproducedmoreequivocalresults. Rana aurora s adecliningspecies withhigh levels of photolyase (98), andexperimentalhatchingsuccess isunaffectedby exposureto UV-B (26). The declining frog Litoria aurea fromeasternAustraliahas a lowerphotolyase activitythantwo sympatricnondecliningspecies, L. dentata and L.peroni,but thereis no significantdifferenceamongthethreespecies in hatchingsuccess underUV-B exposure (187). In many aquatichabitatsUV-Bradiations largely absorbednthe firstfew centimetersof the water

column (138), so increased UV-B may only affect species breedingin habitatswith a narrowrangeof chemicalandphysical parameters.Ecologically relevantlevels of UV-B had no effect on embryosof several Canadianamphibians,andexperimentalprotocolsused to test UV impactshave been questioned(85, 130).Moststudiesthathave examined herelationshipbetweenUV-B andpopulationdeclines havefocusedtheir attentionon species thatbreed n shallow,clearwater,


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136 ALFORD a RICHARDS

where exposureto UV-B is expectedto be greatest (6,25,28,132). Exposuretointense UV-B in shallow high-altitudeponds may exclude amphibians rom thesehabitats 138).Even when UV-B causes higher embryonicmortality n declining species, theecological significanceof this at the population evel is difficult to assess. Moreneeds to be understoodabout the basic naturalhistoryof amphibianspecies thatmight be at risk. For example, inforrnations needed on variation n ovipositionsite characteristics depth, vegetation) within local populations. Experimentsat"natural vipositionsites"using embryosof Ambystomamacrodactylumwere con-ducted n shallowwateralthough hisspecies lays eggs in avarietyof microhabitats(28). Loss of a large proportionof near-surface lutches to UV-B damage mayhave negligible impacts on populations f even a small numberof deeperclutchessurvive,as the survivorsare releasedfromdensity-dependent ffects (1).Even fewer data are availableto assess the indirecteffects of increasingUV-Bon amphibianpopulations. Potential indirect effects include changes in waterchemistryand food supplies,and shiftsin competitiveandpredator-preyelation-ships with other UV-B affectedspecies (143). Exposureto increasedUV-B mayreduce survivalrates of adult amphibians hroughdamage to eyes (77), increasedfrequencyof cancers or tumors(143), andimmunosuppression 143).Predation

Biotic interactionsamong amphibians,andbetween amphibiansand otherorgan-isms, can play a significantrole in determining heir distributionand populationdynamics (1). Larvalamphibiansare extremelyvulnerable o vertebrateandin-vertebratepredators 1), and the diversityof aquatic amphibianassemblages isfrequentlyreduced n habitatscontainingpredatory ish (1, 100).Larval amphibians hat coexist with aquatic predatorshave evolved a rangeof antipredatormechanisms(4,48,118). However, widespread ntroductionsofpredatoryfish have increasingly exposed native amphibiansto predatorswithwhichtheyhavenotpreviously nteracted.Inappropriateesponses onovelpreda-torsmay increasemortalityof nativeamphibians 82,121), leadingto significanteffects on populations.Colonization of normallyfish-free water bodies by predatory ish can resultin rapidextinctionof amphibianassemblages (76). The allotopicdistributionsofnative frogs and introduced ishes in many high-elevation (>2500 m asl) SierraNevada lakes indicate that introducedpredatory ishes have caused the extinc-tion of local frog populations here(31). Sixty percentof lakes thatfrogs couldforrnerlyoccupy now contain introduced ishes and no frogs. Fish introductionshave had a particularly evere impacton Rana muscosa, which breedsin the deeplakes inhabitedby fishes(31). A similarpatternof allotopicdistributions as beenrecorded or larvalnewts, Taricha orosa,and an introduced ish (Gambusiaaffi-nis) andcrayfish (Procambarusclarki) (both predatorsof newt eggs or larvae) nCalifornianmountainstreams 82).


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GLOBAL MPHIBIANECLINES 137Introducedpredatorsmay also have moresubtleeffects. Some Ranamuscosapopulationspersisting n fish-freeenvironmentshave become isolated from otherpopulationsby surrounding quatichabitats containingintroducedfishes. Thismay eventuallylead to regionalextinction by preventingmigrationamong localpopulations 35).North Americanbullfrogs (Rana catesbeiana) that have become establishedoutsidetheirnatural angehavebeenimplicated ndeclinesof native rogs (76, 102,127, but see 97). Adult bullfrogs consume native frogs and reach densities atwhich they are likely to have a severe impact on local amphibianpopulations(166). Experimental tudieshaveshown thatRana aurora arvaeexposed to adultorlarvalbullfrogshaveincreased arvalperiods, smallermass, and,whenexposedto both,lower survival 122).Humanshave devastated rog populations n several countriesfor the frog-legtrade.Before 1995, about wo hundredmillionfrogs wereexportedannually romAsia. By 1990 India was still illegally exportingapproximately eventymillionfrogs eachyear, resulting n seriouspopulationdeclines (145).

HabitatModificationHabitatmodification s the best documentedcause of amphibianpopulationde-clines. Habitat oss certainlyreducesamphibianabundanceand diversityin theareasdirectlyaffected (99, 101). Removalor modificationof vegetationduringforestryoperationshas a rapidand severeimpacton some amphibianpopulations(8). Clearcutting f mature orestsin the southernAppalachianshas reducedsala-manderpopulationsby almost9%, or more thana quarter f a billionsalamanders,below thenumbers hatcouldbe sustained n unloggedforests(149). Loggingex-poses terrestrial mphibians o drasticallyalteredmicroclimaticregimes (9), soilcompactionand desiccation, and reductionin habitatcomplexity (197). It ex-poses aquaticamphibianso streamenvironmentswith increasedsiltation 52) andreduced woody debris (43). Althoughpopulationsmay recoveras regeneratingforestsmature,recovery o predisturbanceevels cantakemany years(9) andmaynot occurat all if mixed forestsarereplacedwithnionocultures 108).Drainingwetlandsdirectlyaffectsfrog populationsby removingbreedingsites(116), and by fragmentingpopulations(74,168), which increases the regionalprobabilityof extinction(e.g. 53). Modificationof terrestrial ndaquatichabitatsfor urbandevelopmentcan reduce or eliminateamphibianpopulations. Popula-tions of some amphibians n urbanFloridadeclined afterdegradationof upland,dryseasonrefugesandmodificationof wetlandsusedforbreeding 62). Protectionof aquaticbreedingsites maybe of little value if adjacent errestrial abitatsusedby amphibians or feeding and shelteraredestroyed(167).Moresubtle alterations o habitat tructure an have severe mpactson amphib-ian populations. Bufo calamita populationsin Britain declined over a 40-yearperiod due to shifts in land use practicesthat alteredvegetationcharacteristics(13). Changing vegetationstructureand an associated increase in shadingwere


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138 ALFORD a RICHARDS

detrimental o B. calamita and providedconditionsunderwhich the common toadBufo bufo became a successful competitor.Althoughhabitatalterations an reduceamphibianpopulations, n some caseseven severe habitatmodificationscan have little effect. The response of a savannawoodland rog assemblageat Weipa,Queensland,Australia o stripminingappearsin Figure 1 (200). The structureand floristics of the plant assemblage at 60revegetated ites varywidely; none stronglyresemble he originalnativewoodland.

Percentof sites

U7nodynastesmatus -Bufomarinus o.Ylitoria aeruleaLitoriaicolor

Cycloranaovaehollandiae * >Litoria ubella- Ik

SphenophrtyneracilipesUimncxynastesonvexiusculus * -

litoriagracilenta $Litoriaothi

Cinia remotaUperoleieamimula- 0Litorianfrafrenata

Litoria asuta -Figure 1 Profiles of percent of sites of five habitat types at Weipa, Queensland,Australia at which frogs of 14 species occurred. Species sorted in order of frequencyof occurrencein native woodland. Dots andsolid lines indicate native woodland habitat(13 sites). Diamonds and dashed lines indicate sites revegetated following strip mining.Density of diamondsreflects age of revegetation;from least tomost dense this is: age 16 years. Therewere 15 revegetation sites in each age group in the survey.


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GLOBAL MPHIBIAN ECLINES 139The distance from revegetation ites to native woodlandvaries from a few metersto over 1 km. Despite this, within7 years, the majorityof frog species occur atrevegetationsites at frequenciesvery similarto the frequenciesat whichthey arefound at sites in native woodland.This indicates that the frogs in this assemblageareinsensitive to radicalalterations n the soil characteristics, lora, and structureof their terrestrial abitat,andthey can recolonize rapidlyfollowing disturbancesthat have eliminatedthem over a relatively wide area. It is possible that otheramphibian pecies assemblagesbehave similarly.

Acidity and ToxicantsThe acidity of aquatichabitatshas major mpacts on amphibiandistribution, e-production,and egg and larvalgrowth and mortality(78,79). Sensitivityto lowpH varies among (79) and within (150) species and is influenced by complexchemical interactionsamongpH and otherfactors,particularly luminumconcen-tration (71,110,151). Mortalityoccurs in both the embryonicand larval stagesvia severalmechanisms ncluding ncompleteabsorption f theyolk plug,arresteddevelopment,and deformationof larvae(11, 79, 109). Sublethaleffects of acidifi-cationincludedelayed (109) orearly (36) hatching,reduced arvalbody size (36),disturbed wimmingbehavior 5), and slower growthratesresulting rom reducedresponse to, and captureof, prey(155). Indirectsublethaleffects include changesto tadpole food sources through mpacts on algal communities 188), and shiftingpredator-prey elationshipsresulting fromdifferentialmortalityof predatory ishandinvertebratesn acidifiedhabitats 104).The population-leveleffects of acidity are less well understood. It is possi-ble that the effects of low pH, in combination with other abiotic factors, leadto decreased recruitment nto adultpopulations (12). Acidic breedingsites of-ten containless diverseamphibianassemblages,at lower densities, than do lessacidic sites (205). Long-termacidificationof pondsin Britainhas excludedBufocalamita frommanysites (16). ReducedpH andincreasedmetal concentrationsin an Appalachianstreameliminatedvirtuallyall salamanderarvae,causing se-vere long-termdeclines in populationsof Desmognathus quadramaculatusandEurycea wilderae (124). Low soil pH also influencesthedistribution, bundance,anddiversityof terrestrial mphibians 204, 205).Despite the well-documentedeffects of low pH on amphibians, here arefewdata to implicateacidification n recent, unexplainedcatastrophicpopulationde-clines. Aciddepositionwasproposedas a factor n thedeclineof tigersalamanders,Ambystoma igrinum, n the Rocky Mountains(96), but subsequent ield studiesdemonstrated hatmortalitydue to pond dryingwas equally likely to be the causeof this decline (201). Acid deposition s unlikelyto be involvedin populationde-clines of frogs and salamanders t high altitudes n the SierraNevadaMountains(33, 34,36) andRockyMountains 54,55, 188,201). Theremaybe no rigorouslydocumentedcases where acidificationof naturalhabitathas led to the extinctionof an amphibianpopulation (71). However,studies of acid tolerance have beenbiased towardspecies that arelikely to have evolved tolerance o low pH (195).


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Similarly,although here s anextensive literature n thetoxic effects on larvalamphibiansof metals and chemicals usedin insecticidesand herbicides(154), in-sufficientdataexist to determine heir ong-term mpactson amphibianpopulationdynamics (22). Environmental oxicants act directly to kill animals, or indirectlyby impairingreproduction, educinggrowthrates, disruptingnormaldevelopmentandreproduction endocrinedisruption),or increasingsusceptibility o disease byimmunosuppression r inhibitionof immune system development 22,46).Diseases

Little is known about the diseases of wild amphibians. Manydisease agents arepresent n healthyanimals,and disease occurs when immunesystems are compro-miised 56,57). Declines in populationsof Bufo boreas boreasbetween 1974 and1982 were associatedwith Aeromonashydrophila nfection, butCarey (47) sug-gested that environmental actor(s) caused sublethal stress in these populations,directly or indirectlysuppressingtheir immune systems. A pathogenic funguslargely responsiblefor egg mortality n one populationof Bufo boreasin Oregonmay have been more virulent o embryosunderenvironmental tress (27).Epidemicscan cause massmortalityof amphibians 123). In 1981 Aeromonashydrophilakilledall larvalRanasylvaticain a Rhode Islandpond,andthreeyearslater few adultfrogs were breedingat this site (141). The same bacteriumwasimplicatedin a well-documented decline to local extinction of a populationofRana muscosa in California(32). A chytridomycete ungus found on moribundanurans n Australiaand Panamaduringmass mortality s fatal to healthy frogsunderexperimentalconditions(18). This funguswas proposedas the proximatecause of declines in these two regions (18), but this hypothesis is untested atpresent.Viruses have been isolated from dead and dying frogs duringmass mortal-ity events (59,60) and may be the primarycause of mortality n animals whereother infections such as bacteriahave been identified(57). Lauranceet al (129)arguedthat the patternof populationdeclines amongAustralianrainforest rogswas indicative of a "wave"of epidemicdisease causedby an unidentifiedwater-borne virus. This interpretationwas challenged (3, 106) on statisticalgroundsandbecause numerousotherexplanations or the observedpatternswere equallyparsimonious.The involvementof a virusin these declineshas now been largelydiscounted,but thepossible involvementof a diseasehasnot. Thepatternof pop-ulationdeclines in CentralAmerica has also led to the suggestionthat a wave ofepidemicdiseasemightbe responsible(131).

Climate/WeatherImmediatelyprior o thedisappearance f golden toads, Bufoperiglenes, therain-forests of Monteverde,Costa Rica, had the lowest twelve-monthrainfall in 20years. Toadswere forcedto shift theirhabitatuse, andthedryconditionsmayhaveinteractedwith an unidentified actor such as disease or a pulse of contaminants


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GLOBAL MPHIBIANECLINES 141in cloud water to eliminate toadpopulations (152). Unusual weatherconditionswere dismissedas a cause of declines of Australianrainforest rogs (128). Thisresultrelieson seasonalrainfall otals calculated orfixed groupsof months,whilein northernAustralia he dateof onset of the wet seasonis highly variable,occur-ring betweenOctoberandFebruary 140). The analysisis therefore ikely to havemissed the extremes and underestimated he variancesof rainfall,and a reexam-ination of the data seems warranted.Severe, short-term limatic events such asviolent stormscan alterthedynamicsof amphibianpopulations.HurricaneHugocausedextensivedamageto the forests of PuertoRico in 1989. In the shortterm,populationsof the terrestrialrogEleutherodactylus richmondi decreasedby 83%,but increasedavailabilityof groundcover due to disturbanceed to a six-fold in-crease in the densities of E. coqui, followed by a long period of gradual populationdecrease(202,203).Alterations n local weatherconditions causedby global climate change willinfluence heecology of amphibiansn a numberof ways. The onset of spawning nRana temporaria in Finlandbetween 1846 and 1986 shifted earlierby 2-13 days,following shifts in air andwatertemperature nd dates of snow cover loss (182).At somesitesinBritain herehas been a statistically ignificant rend owardearlierfirstsightingandspawningof Bufo calamita, Rana esculenta, andR. temporariabetween 1978 and1994, correlatedwithchangingpatternsof spring emperatures(14).Amphibians n Canadaare affectedby decreasesin summerprecipitationandincreased emperatures ndwinterrainfall 105, 143). Inthe neotropics, ncreasedtemperatures, xtendeddry seasons, andincreasing nter-yearrainfallvariabilitymay affect litter species by reducing prey populationsand altering amphibiandistributions n increasinglydrysoil (67). Shiftingrainfallpatternswill affect thereproductive henologies of pond-breeding pecies. Pondswill filllaterandpersistfor shorterperiods, leadingto increasedcompetitionandpredationas amphibiansare concentrated t increasingly imitedaquaticsites (67). Frogs exposedto thesestressesmay also become morevulnerable o parasitesand disease (67).

Interactions Among Environmental FactorsMost studies invoke multiple causes or interactionsamong factors. IncreasedUV-B exposure may alter species interactionsor vulnerabilityto pathogens orchanges in pH. Predationmay eliminate local populationsandhave larger-scaleeffects by alteringratesof migrationbetweenpopulations. Outbreaksof diseasemay only occur when otherstressesreduceimmune function. Pesticides, pollu-tants, andenvironmentalacidity may interact o produceunforeseen effects. Alllocal effects may interactwith global climate change. Provingthe existence ofthese complex effects in naturalpopulationswill requirewell-plannedprogramsof observationandexperimentation.Toplan such studies,andto determinehowstresses affectpopulationbehavior,requiresanunderstanding f the natureof thepopulationsbeing studiedand the limitationsof study techniques.It also requires


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142 ALFORD RICHARDSthe developmentof null hypothesesregardinghow amphibianpopulationsbehavein the absence of externalpressures.

DEFININGAND STUDYINGAMPHIBIANPOPULATIONSMonitoringand CensusingTechniques

We have summarized he techniques used in 46 long-termpopulation studies offrogs and salamandersn Table 1. All but one of the studies of frogs were carriedout at breedingsites, while abouthalf of the studies of salamanders ncluded atleast some datacollected on densitiesof animals n nonbreedinghabitat.The mostcommonlyusedtechnique s directcounts,whereanimalsare locatedby intensivesearching, ocalization of calls, or by drift fences with pitfall traps. Manystudiesthat reporteddirectcounts also reported he results of mark-recapturestimates.Frequently,however, the standarderrors of mark-recapture stimates are verylarge, so that counts are regardedas being better estimates. The high standarderrors ypicallyobtained n mark-recapturestimates of animals atbreedingsitesprobablyreflectthe factthat he degreeof attraction f breedingsites varieswidelyovertime, as does the activityof individualanimals nearthem.

ProblemswithStudyingBreedingAggregationsasPopulationsMost estimatesof frog populationsare expressedin units such as total numbersof frogs attendinga pond, numbersof frogs per m2of pond area,andmaximumnumbersof frogs ata pondon a single night during hebreedingseason (70). Thefrog groups orwhichdataareavailableondensities nnonreproductive abitat endto be species that do not aggregateatbreedingsites (70, 115, 203). A few studieshave examined aquatic-breeding pecies in nonreproductive abitats (156,206).Theuse of breedingaggregations npopulationstudiescancauseproblems n datainterpretation.A simple illustrationof why censusing amphibiansatbreedingsites can causeproblemsin the interpretation f population dynamicsappears n Figure 2. Thenumberof frogs perunit of nonreproductive abitat theentirerectangle)remainsconstantat 50. InFigure2a, neitherof thetemporarypools in thehabitatcontainswater.If censuses arecarriedoutby visiting pool 1, a census atthe timeof Figure2a would detectonly 7-10 frogs in the habitat.A census carriedout afterpool 1filled (Figure 2b) would detect 43 frogs, while one carried out after both poolsfilled (Figure 2c) would detect only 23 frogs at pool 1. Similar variations inmeasureddensity could occur over time even if the pools remainfilled, becauseof changes in the reproductivebehaviorof frogs. Changesin habitatavailabilityand in the attractiveness f bodies of water are both likely to affect the numbersof amphibiansdetected(191), complicating he use of dataof this type as an indi-cationof the size or densityof thepopulationoccupyingthe surrounding abitat.Because behaviorand site attributes ary seasonallyand temporallywith weather


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GLOBAL MPHIBIAN ECLINES 143

S. bC

Ce

Figure 2 An illustration f the difficultiesor data nterpretationreatedby samplinganimalsnbreeding ggregations.Anareaof habitat ontains fixednumber f animalsand wopotential reedingites. Surveys recarried utat site 1. In(a),animals renotattractedobreeding ites,so a censusatsite 1wouldencounter nly9-10 individuals.In (b), animalsare attracted o site 1, and a censuswouldfind43 animals. In (c),animalsareattractedo bothsites,anda censusatsite 1wouldencounter 2 animals.All of thesesituationsmay occurwithina few daysin manyhabitats,makingcountsatbreeding iteshighlyvariable.

and nternal hythmsof theanimals,the besthopeforobtainingaccurateestimatesusing censuses atbreedingsites is to performcensuses frequently.Effectsof SamplingIntensityon PopulationSize Estimates

We used datacollectedby one of us (SJRichards,unpublisheddata)onthe numberof adultmalesof thestream-breeding ylidLitoriagenimaculata o investigate heeffects of sampling intensityon the accuracyof count data taken at a breedingaggregation.A 60-mtransectalonga rainforest treamsite was visitedanaverageof 19 times each year over seven years. All frogs on the transectwere counted,marked,andreleased. We usedaresampling echnique o explorehow less intensesamplingmighthaveaffectedtheresults. We set theprobability hata visit wouldoccur to 0.75, 0.5, and 0.25, and resampledthe dataset 5000 times using eachof these probabilities. It is apparent Figure 3) that decreasingthe intensity ofsamplingbelow about0.75 timesthenumberof visits actuallymade wouldgreatlydecreasethe accuracyof the annualmeans obtained. At intensitiesof 0.5, 0.25,


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144 ALFORD * RICHARDS

--- Actual ean35- - 75% amplingS 0 - - - 50% ampling

co \- - - 25%ampling25 " 1visitperyear20-

a0 = 00-

C _1989 1990 1991 1992 1993 1994 199516 25 21 10 17 22 23Year,Number f visits

Figure 3 Results of resampling analysis on numbersof adultmale Litoria genimac-ulata present on a 60-m transecton Birthday Creek, Mt. Spec, Queensland, Australia.Points indicate the mean number of individuals present taken over all visits in eachyear. The lines connecting the points are for illustration only. The dashed lines atincreasing distances from the mean are the upperand lower 95% confidence limits forthe location of the mean for each year at the given sampling intensity, as determinedfrom 5000 resamplings of the data. Upperand lower solid lines are the 95% confidencelimits for numbersobtainedif the site was visited once annually;they are the minimumand maximum numbersencountered each year.


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GLOBAL MPHIBIANECLINES 145or one visit per year,the observedpatternof changethrough ime would probablyhave differedfrom thepattern hat appears n the full data set, and the coefficientof variationof the annualmean would have increasedsubstantially.Problemscreatedby the changingattractiveness f breedingsites can also occurwhen animals are censusedin nonreproductive abitat,because the attractivenessof patches changes. A population of Rana arvalis in a 2000-m2 sampling areaincreasedmore thantenfoldover the period 1984-1988 (89); this might have beendue to a decrease n the local availabilityof water,causinganimalsto concentratewhere t was available 89). Densitiesof the neotropical itter rogs Bufo typhoniusand Colostethusnubicola nnonreproductive abitatvariedmore than enfold overthe course of a one-year study (183). This variationwas probably caused bydifferencesin the activitylevel and catchabilityof frogs, rather han by changesin populationsize (183).Once areasonable etof populationestimatesat a site is available, he nextstepin an analysisof thebehaviorof thepopulation s to examine how it changes overtime. It is unrealistic o expect perfect stabilityfromanynaturalpopulation;evenif the population s trulyconstant, sampling errorwill introducesome variation.Giventhatwe expectpopulations o fluctuate,we shouldtryto determinehowtheywill behave over time in the absenceof directionalpressures owardexpansionordecline.

A NullHypothesisforthe Behaviorof AmphibianPopulationsover TimeTherehasbeen substantial ebate n recentyears (23, 146, 148, 169) regardinghow"normal" mphibianpopulations houldchangethrough ime,but little theoreticalwork on thisquestion.Theproblemhas been definedclearly: Fluctuatingpopula-tions of amphibianswill be either ncreasingordecreasingat anytime (146, 148).There s a very largeopportunityorbias if populationsare declared o be "declin-ing"on the basis of shorttime series indicating hatnumbersaredecreasing.Amphibian PopulationsFluctuate It is almostuniversallyagreedthatmost lo-cal populationsof amphibiansare likely to fluctuateconsiderably n size. Thisoccursbecause recruitments highlyvariable 7, 15,20,44,65, 81, 185, 186, 194).Survivalratesof terrestrial tagesoftenappear o be relativelyconstant,with somedegreeof fluctuation 7,44,73, 185, 186). The survivalrates of eggs, hatchlings,and larvae often vary over severalordersof magnitude(1, 20,199). Pechmann& Wilbur(148) provideda useful review of approaches hat have been used toexaminepopulationbehavior.Examining Changesof Numberswith Time Oneapproachhathas been usedtoexamine rendswithinpopulationsof amphibianss simplecorrelations f numberswithtime. Fifteen-to-twenty-yearime series for six speciesof salamandersn theAppalachianmountainsof the United States showed no evidence for consistent


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trends in numbersover time (91). A lack of significantcorrelationsof numberswith yearsover a long-termstudy may indicatethat variationamong years repre-sents fluctuationsn numbersrather han declines (146, 169). Significantnegativecorrelationsbetweenpopulationsize and time have beeninterpreted s indicatingthatpopulationsare n decline (115, 117). Of 16 studiesthatmonitoredamphibianpopulations or fouror more years, five reported hat populationswere declining,one that six populationshad become extinct, seven that populationswere fluctu-ating,and three thatthey were stable(30). Most of the evaluationsof populationchangewere based on correlationsof populationsize with time, and some state-mentsthatpopulationswere not in decline were basedonfailure o finda significantcorrelation.Failure o find a significantcorrelationdoes notnecessarily mply thatnoneexists (162); it can also resultfroma lackof statisticalpower. Ineight studiesof amphibianpopulations hatreportedno trend n populationsize overtime, thepower of a product-moment orrelationwas insufficient to allow acceptanceofthe null hypothesis(162). Reed & Blaustein(162) suggestedthatstudiesshouldnot conclude thatpopulationsarenot in decline unless that conclusioncanbe sup-portedstatistically.Unfortunately,hepower analysisthey used, relyingon simplePearsoncorrelations,s not statisticallyvalid,as theadjacentannualvalues in timeseries on a singlepopulationare not independent andomsamples.Wedevelopanalternativeapproachbelow.A Simple Model of PopulationBehavior In orderto suggesthow more appro-priatetests might be carriedout, we exploredhow time series dataon amphibianpopulationsshould be analyzedandinterpreted,and what the "normal"patternsin such datamightbe. We constructeda simple verbal model of frog populationdynamicsandcompared ts predictionswiththebehaviorof 57 time seriesof frogabundancesand 28 salamander ime series (all studies cited in Table 1; detailsare availableon the WorldWide Web in the SupplementalMaterials section ofthe main AnnualReviews site [www.AnnualReviews.org]). inallywe comparedthe behaviorof those 85 timeseries with thatof a simulatedpopulation.Thesimpleverbalmodel is:

Assumptions:1. amphibianpopulationsoftenpersistfor many generations,neitherdecreasing o extinctionnorexplodingto infinity;2. survivalrates ofterrestrial tages may vary,but that variation s typicallyover less than asingle orderof magnitude;3. survivalratesof aquaticstagesoften varyoverseveralordersof magnitude.Deductions:(A) Assumption1 implies thatrecruitmentmuston averagebe sufficientforreplacement o occur. (B)Assumptions1 and2 together mply that most variation n the size ofterrestrial opulationsmustbe due to fluctuations n recruitmentrom theaquaticstages. (C) Assumptions 1, 2, and 3 together mply that whenaquaticsurvival s high, populationsmustrapidly ncrease,butthataquaticsurvivalmustfrequentlybe below replacement evel, so thatthe increasesdonot tend to lead to sustainedexplosions. Deductions(A-C) takentogether


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GLOBAL MPHIBIANECLINES 147suggestthatpopulationsshould decreasemoreoften thanthey increase,becauseincreasescan be veryrapidand mustbe counterbalanced y slowerdecreases.

This modelsuggeststhatpopulationsof species withhighly variable ecruitmentfrom the aquatic o the terrestrial tage might be expectedto decreaseduringmorethan 50%of time intervals. This is a potentially mportantpoint in the context oftheproblemof amphibiandeclines: If populationsnaturallydecreasein numbersmoreoften than they increase,relatively short-termpopulationstudiesmay oftenfind thatthepopulationor populationsstudiedappear o be in decline.Comparingthe Predictions of the Model withData To examine this problemin moredetail,we extracteddatafrom a databaseof informationon time series ofpopulation izes of frogs and salamanders ollatedfrom the literature ndavailablefrom the UnitedStates Geological Survey (USGS) (72). Most of thepopulationsstudiedwere notregardedas being in decline. Wemodified the database rom itsrawform in severalways. Thedatabase ncludes anumberof timeseriescollectedusing differenttechniques on the same species at the same sites and times. Weincluded only one time seriesof data on any species for any site and set of dates.We did not use dataon larvaeor juveniles in our analysis because they reflectreproductivenputmodifiedby highly variableaquaticmortalityratesand so areleast likely to reflectthedynamicsof adultpopulations.When datawere availablefor both male andfemale adults,we combined them. Whencount data and otherestimatessuchasmark-recapturealues wereavailable,we included he countdataif they had been collected in a mannerthatwas likely to be comparableamongyears; otherwisewe used the estimatednumbers.When only dataon numbersofegg masses were available,we includedthem in our analyses,as they shouldbehighly correlatedwith numbersof adult females. We includedonly time seriestaken over fouror moreyears. We also included datafromCohen(50) that werenotpresent n the USGS database.A summaryof the originalsourcesof the datawe used appears n Table1, anddetailsof the datafor each time series appearonthe WorldWide Webin the SupplementalMaterialssection of the main AnnualReviews site (www.AnnualReviews.org).We classified each yearly populationestimateas either the initialnumber n aseries,an increase,a decrease,or no change. Three familiesof frogs (Bufonidae,Hylidae, and Ranidae)and two families of salamanders AmbystomatidaeandPlethodontidae)containedsufficientnumbersof time series. We used nonpara-metricstatistics Table2) to determinewhether hepercentageof thetime in whichpopulationsdecreasedfromone year to the next variedamongfamilies. In bothorders,families differed in the percentageof the time thatpopulationsdeclinedbetweenyears. In theCaudata,populationsof speciesin thefamilyAmbystomati-dae,which arepool-breedingspecies withrelatively argeclutchsizes, decreasedbetween years an averageof 59.2% of the time. Species in the Plethodontidae,primarily errestrial gg layers and stream-breederswith smaller averageclutch


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TABLE 2 Means, standarddeviations,and numbersof time series analyzedforthe percentageof year-to-year hangesin populationsize that aredecreases,for amphibiansof five families,and tests for significantdifferences n the meanamongfamilies within orders.

Percent of population changes that are decreasesFamily Mean Standard Deviation N

Salamanders.Wilcoxon2-sample test, Z _ 2.43, P = 0.015Ambystomatidae 59.2 18.1 12Plethodontidae 42.0 16.1 14

Frogs. Kruskal-Wallisest, X2 = 8.82, 2 d.f., P = 0.012Bufonidae 55.5 19.8 19Hylidae 47.3 6.7 15Ranidae 60.6 13.0 23

sizes (see references in Table 1), declined between years only 42% of the time. Inthe Anura, species in the families Ranidae and Bufonidae decreased in more than50% of intervals, while species in the family Hylidae decreased in slightly lessthan 50% of intervals. (Table 2). The ranids and bufonids included in the databasegenerally produce larger clutches of eggs and often have highly variable offspringsurvival, while hylids produce smaller clutches and may have less variable ratesof offspring survival (references in Table 1).

The results of this analysis suggest strongly that the expected behavior of pop-ulations over time varies among families of frogs and salamanders, and that theadult populations of species that have more variable survival of premetamorphicoffspring tend to decrease between years more often than they increase. This resulthas implications for the ability to draw conclusions about population trends fromsimple time series of numbers over years. A species in the family Plethodontidae,in which the mean population behavior is to decrease between 40% of years, has aprobability of four successive decreases of only 0.031, and finding four successivedecreases between years in a censused population might be cause for alarm. How-ever, a ranid species would need to decrease in numbers six times in successionbefore the probability of that sequence of decreases was less than 0.05.

Our data set included populations from many times and places, some of whichmight have been undergoing declines caused by external pressures. This wouldbias the results of our analysis. To erect a null hypothesis independent of the datafrom natural populations, we examined the behavior of a simulated populationwith known characteristics.A Numerical Model of Population Behavior For comparisonwith our verbalmodel and the results of our data analysis, we used a simulation model based on a


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GLOBAL MPHIBIAN ECLINES 149long-termstudy of the populationdynamicsof Bufo marinus in northernAustralia(2). Our model incorporated imple density-dependence n the adult stage andlognormalvariation n recruitment uccess. Mean recruitment ates were adjustedso thatpopulationstendedto fluctuateabout a mean size rather han explode ordecline rapidly to extinction. The population arbitrarily tartedwith 100 adultfemale toads. Year-to-year urvivalof adult females was set at the lower of 50%or 50 total. Each female produced9000 eggs, which survived o reach maturityasfemales in one year at variablerates equal to 0.00047ea+l, wherea is a normallydistributed andom variable with mean 0, standarddeviation 1. The number ofadults was truncated o an integer following survival and recruitment n eachyear.We ran the simulation5000 times, for 1000 "years"each time. On average,the populationpersisted for 423 years before extinction and contained 296 adultfemales while extant. Withinarun,recruitment ifferedon averageapproximately300-fold between the lowest andhighest years, while adultsurvivaldiffered 15-fold as a consequence of density-dependence. While the population persisted,it decreasedin 56.32% of intervalsbetween years, a result that is in very closeagreementwith the observation(Table 2) thatpopulationsof bufonidsdeclinedbetween 55.5% of years. This suggests that our initial verbal model was correct:Whenpopulation luctuations redrivenby highlyvariablerecruitment,t is likelythatpopulationdynamicswill be characterized yoccasionaloutbreakswith longerinterveningperiodsof decrease,so thattheyare"indecline"more than50% of thetime. This result is similarto the "storage" ffect in open populations 45, 193).It is clear thatapopulationdecreasing n moreyearsthan t increases s not nec-essarilyin decline. However, f there has recentlybeen an increasein the generaltendencyof amphibianpopulationsto decline, there shouldbe a correlationbe-tween theyearin which a studyended andthefrequencyof decreases n thatstudy.We tested this hypothesis using the 85 time series in our database.We correlatedthefinalyearof eachstudywiththepercentageof intervalsacrosswhichthestudiedpopulationdeclined. We analyzedthe data for eachfamily of frogs and salaman-dersseparately, scombining hemmighthave confounded ealeffectsof time withthe effects of changesin the proportionsof studies that were carriedout on eachtaxon. We calculatedSpearman ankcorrelationsbecausethesestraightennonlin-earrelationshipsand decreasethe effects of outliersand datathatarenotnormallydistributed. We found no evidence for any significantcorrelationof proportiondecreaseswith time in any family (maximumrs = 0.327, minimum P = 0.234),an outcomesupportedby examinationof thedata(Figure4), which do not suggestany strongtrendfor eitherfrogs or salamanders.Theproportion f years n which apopulationdeclinesmaybe a weak indicatorof trendsandis potentiallysubject o difficulties n decidinghow largea changeinpopulation izerepresents realdecreaseratherhannoiseinthe data.Correlationsbetweenpopulationsize andtime mightbe a better ndicatorof populationstatus(30,148).


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w-b 100-

o 80n

0 60-en 800 0 DO0 ?0I*0~~~~~40- ? K ? L?

O~~~~~~~~K LbL20-0-tt 0 Li2 1980 1985 1990 1995 20000. Year(frogs)

1945 1955 1965 1975 1985 1995Year(salamanders)Figure4 Proportionf the ntervals romone year o the nextoverwhichpopulationsdecreased uring ong-termtudies 4ormoreyears)of 85localamphibian opulations(28 of salamanders,hownas squares, 7 of frogs, shownas diamonds).The abscissais thefinalyearof eachstudy.

CORRELATIONSOF POPULATION SIZE WITH TIMEIf there is a general global phenomenonacting on all amphibiansand increasingtheirtendencyto decreasein numbers,we would expect that recently completedstudies would show more or strongernegative relationshipsbetween populationsize andtime thanwould older ones. Foreach of the 85 time series in our database,we regressed oglo(N+ 1) onyear of the series. We usedloglo(N+ 1) because this


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GLOBAL MPHIBIAN ECLINES 151stabilizesvariancesandbecause a populationncreasingor decreasingat a constantproportional ate will show a linearrelationshipof logl0(N + 1) with time. Yearswere adjustedwithineach time series so thatthe firstyear was yearzero, to reducepossibleinfluencesof roundingerrorson theregressions. Weused the correlationsandslopes of these regressions n furtheranalysesto determinewhether herewasany evidence for an overall trendtowardan increasein the incidenceor intensityof negativerelationshipsbetween populationsize and time. In these analyses weexaminedthe data for frogs and salamanders eparatelybecause trends might bepresent none butnotin the other. We first ookedfor correlations f either he slopeor thecorrelation oefficient with the yearin which each time series ended, usingSpearman ankcorrelationsbecause of the unknownsamplingpropertiesof thesetwo measures. None of the correlationsof the correlationcoefficient or the slopewith finalyearwere significant salamanders: , =-0.021, P = 0.917 andr, =-0.024, P = 0.905; frogs: r, = 0.175, P = 0.174 and r, = 0.161, P = 0.232;respectively).Although herewas no trend n eitherorder or changesovertimeinthe relation-ship of populationsize to year of study, t is still possible that a generaldecliningtrendwas presentthroughout he period. To examinethis possibility,we plottedthe correlationsof populationsize with year and the slopes of the regressionsofpopulationsize on year againstfinalyearof the study (Figure5a and5b). Initialexaminationof these figurescould be a sourceof alarmbecause there aremanymore negative thanpositive correlationsandbecause most of the apparently ig-nificantcorrelationsandslopes are negative. Furtheranalysis shows that both ofthese effects areprobablyartifactsof thepopulationdynamicsof amphibiansandthe fact that standardassessmentsof significanceshouldnot be applied to timeseries data.Inorder o morerigorouslyassess the significanceof these correlationsandslopes,we returnedo the resultsof ourpopulationsimulation.Oneach of the5000 iterationsof the timeseries,we calculatedcorrelationsandslopes forregres-sions of log10(N + 1) on year for time series containing4 through9, 11, 12, 14,15, 16, 23, and 28 years, startingarbitrarily t year 20 of the simulated ime seriesto allowthe effects of initial conditionsto disappear.This resulted n at least4904coefficientsfor each combinationof parameterand series length (less than 5000because a few populationswent extinct before the final year of each simulatedseries). We sorted the vector of coefficients for each combinationof parameterand series lengthinto ascendingorder,and we took the coefficients at 0.025 fromthe bottom andtop of the series as theupperand lower 95%confidence imits forthe correlation ndslopeof regressionsof anamphibianpopulationonyear. Theseconfidencelimits appear n Figure 5, c andd, with plots of the correlationsandslopes obtained romthetime seriesin our database.Using thecriterion hatto besignificanta parametermust fall outside these empirical95% confidencelimits,only a single correlationandfour slopes are significant,well within the numberthatwould be expecteddue to TypeI errorwhen 85 comparisonsare made.Althoughwe mustconcludethat here s noevidencein the85 time series we an-alyzedto suggestthatcorrelationsorslopes of regressionsof logl0(N + 1) against


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1.0 04 b? 0.50 @?- Q0.2-Z ??0 ?? 8? *ot? D ?? j t? l?80e X ,0 .

E -1.0 * _ _ __ _ _ _ _ _i' ' I ' I ' I1-'-I ' 1'I I ' I1980 1985 1990 1995 2000 1980 1985 1990 1995 2000Year frogs) Year frogs)1945 1955 1965 199 1985 1995 1945 1955 199 1975 1985 1995Year (salamanders) Year (salamanders)

E-. Q0Q8 0.30 drC> Q 02>

0-0 -0.-08413~~~~~~~~~~~~~~~.

8 I. , ,- I I,0 10 20 30 0 10 20 3Yearsn imeenes Yearsn ime eriesFigure 5 (a) Product-moment correlationof 1og10(N + 1) with year of study for 85 timeseries of four or more years of data on local populations of amphibians,plotted against finalyear of the study. Data for salamandersshown as squares, frogs as diamonds. Correlationsthat would be significant at ae = 0.05 using standardparametric criteria are indicated byfilled shapes. (b) Slopes of regressions of 1og10(N + 1) on year of study, other details thesame as in (a). (c) The same correlation coefficients as in (a), plotted against number ofyears in the time series from which the correlation was derived. Lines indicate upper andlower 95%tconfidence limits derived from correlations calculated on 5000 simulated timeseries of each length. Only the single correlation outside these confidence limits should beconsidered significant (indicated by the filled shape). (d) The same slopes as in (b), plottedagainst number of years in the time series from which they were derived. Lines indicate95%tconfidence limits, derived as in (c). Only four of the 85 slopes should be regarded assignificant at the 0.05 level (filled shapes).


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GLOBAL MPHIBIANECLINES 153time have changedin recentyears, we might stillbe concernedoverthe apparentexcess of negative relationshipsof populationsize with time (Figure5, a and b).Fifty-sevenof the 85 relationships f population ize with time (67%)arenegative.The proportionof negativecorrelations rom our simulation ncreasedwith lengthof the time series from 54.8% negative with a series length of 4 years to 57.5%with a series length of 28 years. We used these expectedproportions,weightedby the numberof eachof the real time series that were of each length,to calculatetheexpectednumbersof correlations hat shouldhave beengreaterand less than0(37.6 and47.4, respectively),andcompared hese with the observednumbers 28and57) usingachi-squared oodness-of-fit est (chi-squared= 4.42, P _ 0.037).This significantresult indicatesthat the amphibianpopulationswe examinedhada greaternumberof negative correlationswith time than would be expected, ascomparedwith our simulatedpopulations. This could reflect a generaltendencytowarddecline, but it could also reflect the fact that our simulationmodel, whileit probablyprovides a more realistic null hypothesis than the simple assumptionthateffects in bothdirectionsshouldbe equal,does not perfectlyreflect the pop-ulation behaviorof all amphibians.Using a greatervarietyof models to generatenull hypothesesmore appropriateor each family, genus, or even species wouldobviouslybe preferable.It would also be useful to examine the sensitivityof ourconclusionsto variations n modelparameters nd form.The use of appropriate ull hypotheses will allow morerigorous examinationof the behaviorof individualpopulations. However,many amphibiansappear olive in local populations hatinteractstronglywith otherpopulations,so thatun-derstandinghe implicationsof local populationdynamicsfor species persistencerequiresa knowledgeof theirmetapopulation iology.

AMPHIBIANMETAPOPULATIONIOLOGYA metapopulationconsists of a group of local populationsinhabitingmore orless discrete patchesof habitat(94). A metapopulationdiffers from a collectionof independentpopulationsin that there is substantialmigrationbetween localpopulations,so that no local population s likely to remainextinctfor any lengthof time. Migrationratesmay be high enoughto affect rates of local populationincreaseanddecrease 95, 139). A metapopulation iffers roma singlesubdividedpopulationby having sufficiently ow ratesof migrationbetweenlocal populationsthatthey exhibit some degree of independence n theirdynamics,includingthepossibilityof decliningto extinction(93).

MetapopulationStudieson AmphibiansAlthoughit has been suggestedthatamphibiansaregenerallyhighly philopatric(30, 61, 172), many species departfrom this pattern. One of the problemsthatplagues mark-recapturetudiesof amphibianpopulationsatsingle sitesis thehigh


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rates at which animalsdisappear rom local populations 2, 31,40, 111, 134, 156).Substantialrates of dispersal among local populationshave been documentedin many species (2,21,37,38,42,58,66,81,112,161,173,198)). Additionalevi-dence thatmanyamphibians ive inmetapopulationsomes fromexplicit metapop-ulationstudies(175). Breedingpopulationsof the newtNotophthalmus iridescensact as cells in a regional metapopulation 83). The European pool frog Ranalessonae lives in spatiallycomplex metapopulations;he qualityof potentialbreed-ing sites and their degree of isolation from other sites determines their proba-bility of occupancy and the probability of local extinction (176). Increases inthe isolation of habitatpatches due to naturalsuccession or habitat destructiondecrease the persistenceof local populations (176). Surveys of Rana clamitansoccupancy at 160 ponds in three distinct regions (103) demonstrated he ex-istence of regional metapopulations.Colonization rates varied from 0 to 0.25ponds* (pond occupied. year)-1, while local extinctionrates were between 0 and0.5 ponds* (pond occupied. year)-. Smallpopulationswere moreproneto localextinctionthanwerelarge ones, and therewas no overalltrend n occupancyrateswhen allthreemetapopulationswereconsidered 103).Tenotherspeciesexaminedat 97 ponds in the same regions (101) also exhibitedmetapopulationdynamics,with rates of turnover rom 0.07 to 0.30 species. (pond. year)-. Pool size andisolation both affected species richness in 77 pools in the southernNetherlands(126) and 332 habitats n Bavaria 68).ModelsofAmphibianMetapopulationsand TheirImplications

Because amphibiansoften live in metapopulations,declines and extinctions oflocal populationsmay be common events. Detailed studies of local populationsmay give useful insights into the autecology of species, but they are of limiteduse in evaluating he statusof regional metapopulations.One approach o exam-ining the behaviorof metapopulationss to examinesimple probabilisticmodelsfor the frequencywith which local populationsmight change in status(184). Aprobabilisticnull model for populationdeclines anddisappearanceswas used toexamine whether the declines and disappearancesof frogs that occurred n the1980s at Monteverde, Costa Rica, might be due to chance (153). Pounds et al(153) used long-term studies to estimate probabilitiesof disappearance.Theythen comparedthe numbers of species disappearancesat their study sites tothe numbers of disappearancespredicted by the cumulativebinomial distribu-tion, andthey foundthat far morespecies haddisappeared han would have beenpredicted.Theprobabilisticapproach 153) seems to be a useful way to quantify he ideathat,when certainregionsor taxa areconsidered,species aredisappearing t a rate"toogreatto be coincidental." Several studies haveproduceddata that could beexaminedusing this technique. It seems likely that the disappearances f sevenspecies from all sites at elevations above 400 m throughout he AustralianWetTropics (135,163) would be shown to be extremely improbable,as would the


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GLOBAL MPHIBIANECLINES 155disappearances f three species and large declinesin site occupancyof fourothersin the Yosemiteareaof California 69), the disappearance f Rana cascadae fromthe southernend of its range (75), and the disappearances f many species at LasTablas,Costa Rica (131).A more complex analytical model was used to predict the rates of extinctionof local populationsof the common toad Bufo bufo and the crested newt Trituruscristatus nEurope,andto examinehow those ratesshouldrespond o the size of thelocal habitatpatchand ts distance rom a sourceof migrants 92). The persistenceof populationsof both species should increase with the carryingcapacityof thelocal habitatand should decreasewith increasingdistanceto a source of migrants.Overa wide rangeof carryingcapacities,the critical distances areapproximately10times as great(-5 km)for toads as they arefor newts(-500 m) (92). Thisstudysuggestedthat bothpatchsize andspatial distributionmustbe taken into accountwhen managing amphibianmetapopulations. Informationon patch occupancyfrom a geographicallyreferenced database(168) indicates that small, relativelyisolated wetlandsareimportantn themetapopulation ynamicsof amphibiansnSouthCarolina,USA. Loss of these habitatsmight ead to disproportionatelyargerates of extinction n regionalmetapopulations hat dependupon them as steppingstonesin colonization andas refuges from local extinctions (168).Delineating and monitoringthe status of metapopulations equiresextensivesampling,but because metapopulationdynamicsare concernedmostly with thepresence or absence of species in local populations,samplingof local populationsdoes not need to be intense(87). Fully understandinghe dynamicsof amphibianmetapopulationswill requiremuch more informationon movementsanddispersalamong local populations han is presentlyavailable.

CONCLUSIONSIt is clear that local populationsof many amphibian species have declined inrecentyears, andthereare severalwell-documented ases of declines atandabovethe level of regional metapopulations.Although manyenvironmentalactors canadverselyaffect thegrowth,survival,andreproduction f amphibians, ew studieshave convincinglydemonstratedhatthese effects alter heirpopulationdynamics.Studies linking factorsthatnegatively affect amphibians n the laboratoryor inartificial ield trialswith effects on populationdynamicsin more naturalsettingsareurgentlyneeded.Local populationsof amphibians end to fluctuate,and our results show it islikely that many normallydecrease more often thanthey increase. It is thereforeimportant o develop realisticnull hypothesesfor their behavior. If we had notbased ournullhypothesison a simulationof frog populationdynamics,we wouldhave reachedvery different conclusions in our analysis of populationbehavior.Additional dataon an ecologically diverserangeof species will allow the devel-opmentof more sophisticatedandspecific null hypothesesfor a greaterrangeof


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populations. This is necessary to make rigorous tests of the responses of localpopulations o environmentalactorspossible.Many amphibianspecies occur as metapopulations, o the dynamicsof localpopulationsmay be poor indicatorsof their status. Declines and extinctions ofmetapopulations re likely to result frominteractionsbetween changesin the dy-namics of local populations and habitatmodification or loss (93,94, 168). Formany species, understanding he factors affecting the status and dynamics ofmetapopulationshouldthereforebe the ultimategoal of studies aimingto preventor reversedeclines. Monitoringmetapopulationsequiresdifferentdatacollectiontechniques han monitoring solated populations,so the firststepin designing anymonitoringprogram hould be to determinewhether he species of interestformsa metapopulation.Studies integratingresearchwithin local populationswith in-vestigationsat the metapopulationevel aremost likely to discoverthe causes ofamphibiandeclines andprovidea basis for theconservation f amphibiandiversity.ACKNOWLEDGMENTS

The originaldata ncluded nthis review werecollected with the supportof fundingfrom the AustralianResearch Council and the CooperativeResearchCentre forTropicalRainforestEcology andManagement.We thankJ Winterand the Com-monwealthAluminiumCorporationorpermission o include data romReference200, and S Droege for permission o use dataextracted romtheUSGS amphibiancount database(72). The manuscriptwas improvedwith the help of MJ Caley,CN Johnson,andL Schwarzkopf.

Visit the Annual Reviews homepage at http://www.AnnualReviews.orgLITERATURE CITED1. Alford RA. 1999. Ecology: resourceuse,competition, and predation. In Tadpoles:TheBiology of AnuranLarvae, ed.RW Mc-Diarmid,R Altig. Chicago: Univ. ChicagoPress. In press2. Alford RA, Cohen MP, Crossland MR,HearndenMN, SchwarzkopfL. 1995. Pop-ulationbiology of Bufomarinus n northernAustralia.In WetlandResearch in the Wet-Dry Tropicsof Australia,ed. CMFinlayson,pp. 173-181. Canberra:CommonwealthofAustralia3. Alford RA, RichardsSJ. 1997. Lack of ev-idence for epidemic disease as an agent inthe catastrophicdecline of Australianrainforestfrogs. Conserv.Biol. 11:1026-29

4. Altig R, Channing A. 1993. Hypothesis:functionalsignificanceof colour andpatternof anuran adpoles.Herpetol.J. 3:73-755. Andren C, Henrikson L, Olsson M, Nil-son G. 1988. Effects of pH and aluminiumon embryonic and early larval stages ofSwedish brownfrogs Rana arvalis, R. tem-poraria and R. dalmatina.Holarctic Ecol.11:127-356. AnzaloneCR, KatsLB, GordonMS. 1998.Effects of solar UV-B radiationon embry-onic development nHyla cadaverina,Hylaregilla, and Tarichatorosa. Conserv.Biol.12:646-537. Arntzen JW, Teunis SFM. 1993. A six-year studyonthepopulationdynamicsof the


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crestednewt (Triturus ristatus)followingthe colonization of a newly createdpond.Herpetol.J. 3:99-1 108. AshAN. 1988. Disappearance f salaman-dersfrom clearcutplots. J. ElishaMitchellSci. Soc. 104:116-229. Ash AN. 1997. Disappearanceand returnof Plethodontid salamanders to clearcutplots in the southern Blue Ridge Moun-tains. Conserv.Biol. 11:983-8910. BarinagaM. 1990. Wherehaveallthe frog-gies gone? Science 247:1033-3411. Beattie RC, Tyler-JonesR. 1992. The ef-fects of low pH and aluminumon breed-ing success in thefrog Rana temporaria. .Herpetol. 26:353-6012. Beattie RC, Tyler-Jones R, Baxter MJ.1992. The effects of pH, aluminiumcon-centration and temperatureon the em-bryonic development of the Europeancommon frog, Rana temporaria.J. Zool.,London 228:557-7013. BeebeeTJ.1977. Environmentalhange asa cause of NatterjackToadBufo calamitadeclines in Britain. Biol. Cons. 11:87-10214. Beebee TJC. 1995. Amphibianbreedingand climate. Nature 374:219-2015. Beebee TJC,DentonJS, BuckleyJ. 1996.Factors affecting populationdensities ofadult natterjacktoads Bufo calamita inBritain.J. Appl.Ecol. 33:263-6816. Beebee TJC, Flower RJ, Stevenson AC,PatrickST, Appleby PG, et al. 1990. De-cline of theNatterjackToadBufocalamitain Britain:paleoecological, documentary,and experimentalevidence for breedingsite acidification.Biol. Conserv.53:1-2017. Beiswenger RE. 1986. An endangeredspecies, the Wyoming toad Bufo hemio-phrys baxteri-the importanceof an earlywarningsystem.Biol. Cons. 37:59-7118. Berger L, Speare R, DaszakP, GreenDE,Cunningham AA, et al. 1998. Chytrid-iomycosis causes amphibianmortalityas-sociated with populationdeclines in therainforests of AustraliaandCentralAmer-

ica. Proc. Natl. Acad. Sci., USA 95:9031-3619. BertramS, Berrill M. 1997. Fluctuationsin a northernpopulationof gray treefrogs,Hyla versicolor. See Ref. 87, pp. 57-6320. Berven KA. 1990. Factorsaffecting popu-lationfluctuationsnlarvaland adultstagesof the wood frog (Ranasylvatica).Ecology71:1599-160821. Berven KA, Grudzien TA. 1990. Disper-sal in the wood frog (Rana sylvatica): im-plications for genetic populationstructure.Evolution44:2047-5622. Bishop CA. 1992. The effects of pesticideson amphibians ndtheimplications or de-terminingcauses of declines in amphib-ian populations.In Declines in CanadianAmphibianPopulations: Designing a Na-tionalMonitoringStrategy, d. CABishop,KE Pettit, pp. 67-70. Occas. Pap.No. 76,Can.WildlifeServ.

23. Blaustein AR. 1994. Chicken Little orNero's fiddle? A perspectiveon decliningamphibianpopulations.Herpetologica50:85-9724. Blaustein AR, EdmundB, Kiesecker JM,Beatty JJ, Hokit DG. 1995. Ambient ul-travioletradiation ausesmortality n sala-mandereggs. Ecol. Appl. 5:740-4325. Blaustein AR, Hoffman PD, Hokit DG,Kiesecker JM, Walls SD, Hays JB. 1994.UV repairand resistanceto solarUV-B inamphibianeggs: a link to populationde-clines? Proc. Natl. Acad. Sci., USA 91:1791-9526. BlausteinAR,HoffmanPD, KieseckerJM,Hays JB. 1996. DNA repair activity andresistanceto solar UV-B radiation n eggsof the red-legged frog. Conserv.Biol. 10:1398-140227. BlausteinAR,HokitDG, O'HaraRK,HoltRA. 1994. Pathogenic fungus contributesto amphibian osses in the Pacific North-west. Biol. Conserv.67:251-5428. BlausteinAR, KieseckerJM, ChiversDP,Anthony RG. 1997. Ambient UV-B ra-diation causes deformities in amphibian


27/34


embryos.Proc. Natl. Acad. Sci., USA94:13735-3729. Blaustein AR, Wake DB. 1990. Declin-ing amphibianpopulations: a global phe-nomenon? TrendsEcol. Evol. 5:203-430. BlausteinAR, WakeDB, SousaWP.1994.Amphibiandeclines:judgingstability,per-sistence, and susceptibilityof populationsto local and global extinctions. Conserv.Biol. 8:60-7131. BradfordDF. 1989.Allotopicdistributionsof native rogsand ntroducedishes nhighSierraNevada lakes of California: impli-cationsof the negativeeffect of fish intro-ductions.Copeia 1989:775-7832. BradfordDF. 1991. Massmortalityandex-tinction in a high-elevationpopulationofRanamuscosa.J. Herpetol.25:174-7733. BradfordDF, Gordon MS, Johnson DF,AndrewsRD, JenningsWB. 1994. Acidicdeposition as an unlikely cause for am-phibianpopulationdeclines in the SierraNevada,California.Biol. Conserv.69:155-6134. Bradford DF, Swanson C, Gordon MS.1994. Effects of low pH and aluminumonamphibiansat high elevationin the SierraNevada,California.Can.J.Zool.72:1272-7935. Bradford DF, TabatabaiF, GraberDM.1993. Isolation of remaining populationsof the nativefrog,Rana muscosa, by intro-ducedfishesinSequoiaandKing'sCanyonNationalParks,California.Conserv.Biol.7:882-8836. BradfordDF, Swanson C, Gordon MS.1992. Effects of low pH and aluminumon two declining species of amphibians nthe SierraNevada,California.J. Herpetol.26:369-7737. Breckenridge WJ, Tester JR. 1961.Growth, ocal movementsandhibernationof the Manitobatoad, Bufo hemiophrys.Ecology 42:637-4638. Breden F. 1987. The effect of post-metamorphicdispersal on the populationgenetic structureof Fowler's toad, Bufo

woodhouseifowleri. Copeia 1987:386-9539. Brooks RJ. 1992.Monitoringwildlifepop-ulationsin long-termstudies.See Ref. 22,

pp. 94-9740. Brown WC, Alcala AC. 1970. Popula-tion ecology of the frog Rana erythraeain southern Negros, Philippines. Copeia1970:611-2241. Bruce RC. 1995. The use of temporaryremoval sampling in a study of popula-tion dynamicsof the salamanderDesmog-nathusmonticola.Aust.J. Ecol. 20:403-1242. Buckley D, Arano B, HerreroP, LlorenteG. 1996. Populationstructureof Moroc-can water rogs: geneticcohesiondespiteafragmenteddistribution. .Zool.Syst.Evol.Res. 34:173-7943. Bury RB, Corn PS. 1988. Responses ofaquaticand streamsideamphibians o tim-berharvest:A review.InStreamsideMan-agement: Riparian Wildlifeand ForestryInteractions,ed. KJ Raedeke,pp. 165-8 1.Seattle:Univ.Was.Press44. Caldwell JP. 1987. Demographyand lifehistory of two species of chorus frogs(Anura:Hylidae)n SouthCarolina.Copeia1987:114-2745. Caley MJ, CarrMH, Hixon MA, HughesTP,Jones GP,Menge BA. 1996. Recruit-ment andthe local dynamicsof open ma-rine populations.Annu. Rev. Ecol. Syst.27:477-50046. Carey C, BryantCJ. 1995. Possible inter-relationshipsamong environmentaltoxi-cants, amphibiandevelopment,anddeclineof amphibianpopulations.Environ.HealthPerspec. 103(Suppl.4):13-1747. Carey CL. 1993. Hypothesis concerningthe causes of the disappearanceof bo-real toadsfrom the mountainsof Colorado.Conserv.Biol. 7:355-62

48. ChovanecA. 1992. The influence of tad-pole swimmingbehaviouron predationbydragonflynymphs.Amphibia-Reptilia13:341-4949. Clay D. 1997. The effects of temperatureand acidity on spawning of the spotted


28/34


salamander, Ambystoma maculatum, inFundyNationalPark.See Ref. 87, pp. 226-3250. Cohen MP. 1995. Ecology of two popu-lations of Bufo marinus in north-easternAustralia. PhD thesis, James Cook Univ.,Townsville, Australia.203 pp.51. CornPS. 1994. What we know anddon'tknow aboutamphibian eclines n the west.InSustainableEcological Systems: Imple-menting an Ecological Approachto LandManagement,ed. LF DeBano, WW Cov-ington,pp. 59-67. FortCollins, CO:USDAFor. Serv., Rocky Mountain For. RangeExp. Station52. CornPS, BuryRB. 1989. Logging in west-ernOregon: responsesof headwaterhabi-tats and stream amphibians. For. Ecol.Manage. 29:39-5753. CornPS, FoglemanJC. 1984. Extinctionof montane populations of the NorthernLeopardFrog (Ranapipiens) in Colorado.J. Herpetol. 18:147-5254. CornPS, StolzenburgW, BuryRB. 1989.Acid PrecipitationStudies n ColoradoandWyoming: InterimReport of Surveys ofMontane Amphibians and Water Chem-istry. Biol. Rep. 80, US Fish & WildlifeServ.pp. 1-5655. Corn PS, VertucciFA. 1992. Descriptiveriskassessmentof the effects of acidic de-position on Rocky Mountainamphibians.J. Herpetol. 26:361-6956. CrawshawGJ. 1992.Therole of diseaseinamphibiandecline. See Ref. 22, pp. 60-6257. CrawshawGJ. 1997. Disease in Canadianamphibianpopulations.See Ref. 87, pp.258-7058. CrumpML. 1986.Homingandsitefidelityin a neotropical rog, Atelopus varius (Bu-fonidae). Copeia 1986:438-44

59. CunninghamAA, Langton TES, BennettPM,LewinJF,DrurySEN,et al. 1993. Un-usual mortalityassociated with poxvirus-like particlesin frogs (Rana temporaria).Vet.Rec. 133:141-4260. CunninghamAA, Langton TES, Bennett

PM, Lewin JF, Drury SEN, et al. 1996.Pathological and microbiological findingsfrom incidents of unusualmortalityof thecommon frog (Rana temporaria).Philos.Trans.R. Soc. Lond. Ser B. 351:1539-5761. Daugherty CH, Sheldon AL. 1982. Age-specific movementpatternsof the frog As-caphus truei. Herpetologica 38:468-7462. Delis PR, Mushinsky HR, McCoy ED.1996. Declineof some west-centralFloridaanuranpopulations in response to habitatdegradation.Biodiv. Conserv.5:1579-9563. Dodd CK Jr. 1991. Drift fence-associatedsampling bias of amphibiansat a Floridasandhillstemporarypond. J. Herpetol. 25:296-30164. Dodd CK Jr. 1992. Biological diversityofa temporarypond herpetofauna n northFlorida sandhills.Biodiv. Conserv. 1:125-14265. Dodd CK Jr. 1994. The effects of droughtonpopulation tructure, ctivity,andorien-tation of toads (Bufo quercicusandB ter-restris) at a temporarypond. Ecol. Ethol.Evol. 6:331-4966. Dole WJ. 1965. Summer movements ofadult eopard rogs, Ranapipiens Schreber,in northernMichigan.Ecology 46:236-5567. Donnelly MA, Crump ML. 1998. Po-tential effects of climate change on twoneotropical amphibian assemblages. Cli-mate Change 39:541-6168. DornWMP,BrandlR. 1991. Local distri-bution of amphibians: the importanceofhabitatfragmentation.Global Ecol. Bio-geogr Lett. 1:36-4169. DrostCA,Fellers GM. 1996.Collapseof aregionalfrogfauna n the Yosemiteareaofthe CaliforniaSierraNevada, USA. Con-serv. Biol. 10:414-2570. Duellman WE, Trueb L. 1986. Biologyof Amphibians.New York: McGraw-Hill.670 pp.71. Dunson WA, Wyman RL, Corbett ES.1992.A symposiumonamphibiandeclinesandacidification.J. Herpetol.26:349-5272. EagleP.1999. AmphibianCountDatabase.


29/34


United States Geological Survey, http:IIwww.mp2-pwrc.usgs.gov/ampCV/ampdb.cfm73. Elmberg J. 1990. Long-term survival,length of breedingseason,and operationalsex ratio n a borealpopulationof commonfrogs, Rana temporariaL. Can.J. Zool. 68:121-2774. Elmberg J. 1993. Threatsto boreal frogs.Ambio 22:254-25575. Fellers GM, Drost CA. 1993. Disappear-ance of the cascades frog Rana cascadaeat the southern nd of its range, California,USA. Biol. Conserv.65:177-8176. FisherRN, ShafferHB. 1996. The declineof amphibiansnCalifornia'sGreatCentralValley.Conserv.Biol. 10:1387-9777. Fite KV, BlausteinA, Bengston L, HewittHE. 1998. Evidenceof retinal ight damagein Rana cascadae: a declining amphibianspecies. Copeia 1998:906-14

78. FredaJ, Dunson WA. 1986. Effects of lowpH and other chemical variables on thelocal distributionof amphibians. Copeia1986:454-6679. FredaJ, SadinskiWJ, Dunson WA. 1991.Longtermmonitoringof amphibianpopu-lations with respectto the effects of acidicdeposition.Water,Air,Soil Pollut. 55:445-6280. FreedmanB, ShackellNL. 1992. Amphib-ians in the context of a national environ-mentalmonitoringprogram.See Ref. 22,pp. 101-10481. FriedlTWP,Klump GM. 1997. Some as-pects of populationbiology in the Euro-pean treefrog, Hyla arborea. Herpetolog-ica 53:321-3082. GamradtSC, Kats LB. 1996. Effect ofintroducedcrayfish and mosquitofish onCaliforniaNewts. Conserv.Biol. 10:1155-6283. Gill DE. 1978. The metapopulation col-ogy of the red-spotted newt, Notoph-thalmus viridescens (Rafinesque). Ecol.Monogr.48:145-6684. Gittins SP. 1983. Populationdynamicsof

the common toad (Bufobufo) at a lake inmid-Wales.J. Anim. Ecol. 52:981-8885. Grant KP, Licht LE. 1995. Effects of ul-travioletradiationon life-historystages ofanurans from Ontario, Canada. Can. J.Zool. 73:2292-30686. Green DM. 1992. Fowler's toads (Bufowoodhouseifowleri) at Long Point, On-tario: changing abundanceand implica-tions for conservation.See Ref. 22, pp. 37-4387. GreenDM. 1997.Perspectiveson amphib-ian populationdeclines: defining he prob-lem and searching for answers. In Am-phibiansin Decline. CanadianStudiesof aGlobalProblem,ed. DM Green, pp. 291-308. HerpetologicalConserv.,Vol 1.88. Green DM. 1997. Temporalvariationinabundanceand age structure n Fowler'stoads,Bufofowleri,atLong Point, Ontario.See Ref 87, pp.45-5689. Gyovai F. 1989. Demographicanalysisofthe moor frog (Rana arvalis olterstorffiFeje'rva'ry 1919) population in Fraxinopannonicae-Alnetumof the Tisza basin.Tiscia (Szeged) 24:107-2190. HairstonNG. 1983. Growth,survival,andreproduction f Plethodon ordani: trade-offs between selective pressures. Copeia1983:1024-3591. HairstonNG Sr, Wiley RH. 1993. No de-

cline in salamander(Amphibia:Caudata)populations: a twenty year study in thesouthern Appalachians. Brimleyana 18:59-6492. Halley JM, OldhamRS,ArntzenJW. 1996.Predicting the persistence of amphibianpopulations with the help of a spatialmodel.J. Appl.Ecol. 33:455-7093. HanskiI. 1997.Metapopulation ynamics:from conceptsand observations o predic-tive models. In MetapopulationBiology:Ecology, Genetics, and Evolution, ed. IHanski,M. Gilpin, pp. 69-91. San Diego,CA:AcademicPress. 512 pp.94. HanskiI. 1998.Metapopulation ynamics.Nature 396:41-49


30/34


95. Hanski I, Pakkala T, KuussaariM, LeiG. 1995. Metapopulationpersistenceofan endangeredbutterfly n a fragmentedlandscape.Oikos72:21-2896. HarteJ,HoffmanE. 1989. Possible effectsof acidic depositionon a RockyMountainpopulation of the tiger salamanderAm-bystoma tigrinum.Conserv.Biol. 3:149-5897. Hayes MP, Jennings MR. 1986. Declineof frog speciesinwesternNorthAmerica:arebullfrogs (Rana catesbeiana)respon-sible? J. Herpetol.20:490-50998. Hays JB, Blaustein AR, Kiesecker JM,Hoffman PD, Pandelova I, Coyle D,Richardson T. 1996. Developmentalre-sponsesof amphibians o solar and artifi-cial UVB sources: a comparative tudy.Photochem.Photobiol.64:449-5599. Hecnar SJ. 1997. Amphibianpond com-munities in southwestern Ontario. SeeRef. 87, pp. 1-15100. Hecnar SJ, M'Closkey RT. 1996. Theeffects of predatory fish on amphibianspecies richness and distribution.Biol.Conserv.79:123-31101. Hecnar SJ, M'Closkey RT. 1996. Re-gional dynamicsand he statusof amphib-ians. Ecology 77:2091-97102. HecnarSJ,M'CloskeyRT.1997. Changesin the composition of a ranidfrog com-munity ollowing bullfrogextinction.Am.Midl.Nat. 137:145-50103. HecnarSJ, M'Closkey RT. 1997. Spatialscale and determination f species statusof the green frog. Conserv.Biol. 11:670-82104. Henrikson B-I. 1990. Predationon am-phibian eggs and tadpoles by commonpredators in acidified lakes. HolarcticEcol. 13:201-6

105. HermanTB, Scott FW. 1992. Assessingthe vulnerabilityof amphibiansto cli-matic warming.See Ref. 22, pp. 46-49106. HeroJ-M, Gillespie GR. 1997.Epidemicdisease and amphibiandeclines in Aus-tralia.Conserv.Biol. 11:1023-25

107. HeyerWR. 1979. Annualvariation n lar-val amphibianpopulationswithin a tem-peratepond. J. Wash.Acad. Sci. 69:65-74108. Homolka M, Kokes J. 1994. Effect ofair pollution and forestrypractice on therangeandabundance f Salamandra ala-mandra.Folia Zoologica 43:49-56109. Home MT, Dunson WA. 1994. Exclu-sion of the Jefferson salamander,Am-bystoma effersonianum,from some po-tential breeding ponds in Pennsylvania:effects of pH, temperature, nd metals onembryonic development.Arch. Environ.ContaminationToxicol.27:323-30110. Home MT, DunsonWA. 1995. Effects oflow pH, metals,andwaterhardnesson lar-val amphibians.Arch. Environ.Contami-nation Toxicol.29:500-5111. HustingEL. 1965. Survivaland breedingstructure n a populationof Ambystomamaculatum.Copeia 1965:352-59112. IshchenkoVG. 1989. Populationbiologyof amphibians.Sov. Sci. Rev. F Physiol.Gen.Biol. 3:119-55113. JaegerRG. 1980. Density-dependent nddensity-independent auses of extinctionof a salamander opulation.Evolution34:617-21114. Jennings MR, Hayes MP. 1994. Declineof native ranidfrogs in the desert south-west. In SouthwesternHerpetol. Soc.,

Spec. Publ. No. 5, ed. PR Brown, JWWright,pp. 183-211115. JoglarRL,BurrowesPA.1996. Decliningamphibianpopulations n PuertoRico. InContributions o West Indian Herpetol-ogy: A Tributeto Albert Schwartz,ed.R Powell, RW Henderson, pp. 371-80.SSARContrib. o Herpetol.,Volume12.116. JohnsonB. 1992.Habitat oss and declin-ing amphibianpopulations.See Ref. 22,pp. 71-75117. KagariseShermanC, MortonML. 1993.Populationdeclines of Yosemitetoads inthe easternSierraNevadaof California.J.Herpetol.27:186-98118. Kats LB, PetrankaJW, Sih A. 1988.


31/34


Antipredator efenses andthepersistenceof amphibian arvaewith fishes. Ecology69:1865-70119. KerrJB,McElroyCT. 1993.Evidence forlarge upward rendsof ultraviolet-B adi-ation linked to ozone depletion. Science262:1032-34120. KieseckerJM, BlausteinAR. 1995. Syn-ergism between UV-B radiation and apathogen magnifies amphibianembryomortality nnature.Proc. Natl.Acad. Sci.,USA 92:11049-52121. KieseckerJM, BlausteinAR. 1997. Pop-ulation differences in responses of red-leggedfrogs (Rana aurora)to introducedbullfrogs.Ecology 78:1752-60122. Kiesecker JM, BlausteinAR. 1998. Ef-fects of introducedbullfrogs and small-mouthbass on microhabitatuse, growthand survival of native red-legged frogs(Rana aurora). Conserv. Biol. 12:776-87123. Koonz W. 1992. Amphibians in Mani-toba. See Ref. 22, pp.19-20124. KuckenDJ, Davis JS,Petranka W,SmithKC. 1994.Anakeestastreamacidificationand metal contamination: effects on asalamander ommunity. .Environ.Qual.23:1311-17125. KuzminS. 1994. The problemof declin-ing amphibianpopulationsin the Com-monwealthof IndependentStatesand ad-jacentterritories.Alytes 12:123-34126. LaanR, VerboomB. 1990.Effects of poolsize andisolationon amphibiancommu-nities.Biol. Conserv.54:251-62127. LannooMJ,Lang K,WaltzT, PhillipsGS.1994. An alteredamphibianassemblage:Dickinson County, Iowa, 70 years afterFrankBlanchard's urvey.Am. Midl. Nat.131:311-19

128. Laurance WF. 1996. Catastrophicde-clines of Australianrainforestfrogs: Isunusualweatherresponsible?Biol. Con-serv. 77:203-12129. LauranceWF,McDonaldKR, SpeareR.1996. Epidemic disease and the catas-

trophicdecline of Australianrain forestfrogs. Conserv.Biol. 10:406-13130. Licht LE, GrantKP. 1997. The effects ofultraviolet adiationon the biology of am-phibians.Am.Zool. 37:137-45131. Lips KR. 1998. Decline of a tropicalmontaneamphibian auna. Conserv.Biol.12:106-17132. LizanaM, PedrazaEM. 1998. The effectsof UV-B radiationon toad mortalityinmountainousareasof centralSpain. Con-serv. Biol. 12:703-7133. Long LE, SaylorLS, Soule ME. 1995. ApH/UV-Bsynergism n amphibians.Con-serv.Biol. 9:1301-3134. Martof B. 1956. Factors influencingthesize and composition of populations ofRana clamitans.Am. Midl. Nat. 56:224-45135. McDonald KR, Alford RA. 1999. Areview of declining frogs in northernQueensland. In Declines and Disap-pearances of AustralianFrogs, NationalThreatenedFrog Workshop 997, ed. ACampbell.Canberra:EnvironmentAus-tralia.Inpress136. Meyer AH, SchmidtBR, GrossenbacherK. 1998. Analysis of three amphibianpopulations with quarter-century ongtime series. Proc. R. Soc. Lond., Ser. B:523-28

137. MierzwaKS. 1998. Statusof northeasternIllinois amphibians.In Status and Con-servationof MidwesternAmphibians,ed.MJ Lannoo,pp. 115-24. Iowa City: Univ.IowaPress138. Nagle MN, Hofer R. 1997. Effects of ul-travioletradiationon early larval stagesof theAlpinenewt,Triturus lpestris,un-dernatural nd aboratory onditions.Oe-cologia 110:514-19139. Nee S, May RM, Hassell MP. 1997.Two-species metapopulationmodels. InMetapopulationBiology: Ecology, Ge-netics, and Evolution, ed. I Hanski, MGilpin, pp. 123-47. SanDiego, CA:Aca-demic Press. 512 pp.


32/34


140. Nicholls N. 1984. A system for predict-ing the onset of thenorthAustralianwet-season. J. Climatol.4:425-35141. Nyman S. 1986. Mass mortality in lar-val Ranasylvaticaattributableo thebac-terium,Aeromonashydrophilum. . Her-petol. 20:196-201142. Olson DH. 1989. Predation on breed-ing western toads (Bufo boreas). Copeia1989:391-97143. OvaskaK. 1997.Thevulnerability f am-phibians n Canada o global warmingandincreasedsolarradiation.See Ref. 87, pp.206-25144. Ovaska K, Davis TM, Flamarique IN.1997. Hatching success and larval sur-vival of the frogs Hyla regilla andRanaaurora underambientandartificiallyen-hanced solar ultraviolet adiation.Can.J.Zool. 75:1081-88145. Oza GM. 1990. Ecological effects of thefrog's legs trade.Environmentalist 0:39-41146. PechmannJHK,ScottDE, SemlitschRE,CaldwellJP,Vitt LJ, Gibbons JW. 1991.Declining amphibian populations: theproblem of separating human impactsfrom natural fluctuations. Science 253:892-95147. Pechmann JHK, Wake DB. 1997. De-clines and disappearancesof amphibianpopulations.In Principles of Conserva-tion Biology, ed. GK Meffe, CR Carroll,pp. 135-37. Sunderland,MA: Sinauer.2nd ed.148. Pechmann JHK, Wilbur HM. 1994.Puttingdeclining amphibianpopulationsin perspective: naturalfluctuations andhuman mpacts.Herpetologica 50:65-84149. PetrankaJW, Eldridge ME, Haley KE.1993. Effects of timber harvesting onsouthernAppalachian alamanders.Con-serv. Biol. 7:363-70150. Pierce BA, Wooten DK. 1992. Geneticvariationin tolerance of amphibianstolow pH. J. Herpetol.26:422-29151. PortnoyJW. 1990. Breeding biology of

the spottedsalamanderAmbystomamac-ulatum Shaw)in acidictemporarypondsatCapeCod, USA. Biol. Conserv.53:61-75152. PoundsJA, CrumpML. 1994. Amphib-ian declines andclimatedisturbance: hecase of the golden toadandthe harlequinfrog. Conserv.Biol. 8:72-85153. Pounds JA, Fogden MPL, Savage JM,Gorman GC. 1997. Tests of null mod-els for amphibiandeclines on a tropicalmountain.Conserv.Biol. 11:1307-22154. Power T, Clark KL, HarfenistA, PeakallDB. 1989.A review andevaluationof theamphibian oxicological literature.Tech.Rep. 61, Can. WildlifeServ.155. PreestMR. 1993.Mechanismsof growthratereduction n acid-exposed arvalsala-manders,Ambystomamaculatum.Phys-iol. Zool. 66:686-707156. Ramirez J, Vogt RC, Villareal-BenitezJ-L. 1998. Populationbiology of a neo-tropical rog (Ranavaillanti).J.Herpetol.32:338-44157. RamotnikCA. 1997. ConservationAs-sessment of the Sacramento MountainSalamander. Gen. Tech.Rep. RM-GTR-293. FortCollins, CO:USDAFS, RockyMountainFor.RangeExp. Stat.158. RaymondLR. 1991. SeasonalactivityofSiren intermediain northwesternLoui-siana(Amphibia:Sirenidae).Southwest-ernNat. 36:144-47159. Raymond LR, Hardy LM. 1990. De-mographyof a populationof Ambystomatalpoideum(Caudata:Ambystomatidae)innorthwesternLouisiana.Herpetologica46:371-82160. RaymondLR, HardyLM. 1991. Effectsof a clearcuton a populationof the molesalamander,Ambystomatalpoideum, inan adjacentunaltered orest.J. Herpetol.25:509-12161. Reading CJ, LomanJ, MadsenT. 1991.Breeding pond fidelity in the commontoad, Bufobufo.J. Zool. Lond. 225:201-11


33/34


162. Reed JM, Blaustein AR. 1995. Assess-ment of "nondeclining"amphibianpop-ulations using power analysis. Conserv.Biol. 9:1299-1300163. RichardsSJ, McDonaldKR, Alford RA.1993. Declines in populations of Aus-tralia'sendemic tropicalrainforest rogs.Pacific Conserv.Biol. 1:66-77164. Sarkar S. 1996. Ecological theory andanuran declines. BioScience 46:199-207

165. Schlupp I, PodlouckyR. 1994. Changesin breeding site fidelity: a combinedstudy of conservationand behaviourinthe common toad Bufo bufo. Biol. Con-serv.69:285-91166. Schwalbe CR, Rosen PC. 1988. Prelimi-nary reporton effect of bullfrogs on wet-land herpetofaunas n southeasternAri-zona. In Management of Amphibians,Reptiles and Small Mammals in NorthAmerica, pp. 166-73. US Dep. Agric.167. Semlitsch RD. 1998. Biological delin-eationof terrestrial ufferzones forpond-breedingsalamanders.Conserv.Biol. 12:1113-19168. SemlitschRD,BodieJR. 1998.Aresmall,isolated wetlands expendable? Conserv.Biol. 12:1129-33169. Semlitsch RD,ScottDE,PechmannJHK,GibbonsJW. 1996. Structure nddynam-ics of an amphibian ommunity. nLong-TermStudies of VertebrateCommunities,ed. MLCody,JASmallwood,pp.217-50.San Francisco: Academic Press170. Shirose LJ, Brooks RJ. 1997. Fluctua-tions in abundanceand age structure nthree species of frogs (Anura: Ranidae)in AlgonquinPark,Canada, rom 1985 to1993. See Ref. 87, pp. 16-26171. Shoop CR. 1974. Yearlyvariation n lar-val survival of Ambystomamaculatum.Ecology 55:440-44172. Sinsch U. 1991. Mini-review: the orien-tationbehaviour f amphibians.Herpetol.J. 1:541-44173. Sinsch U. 1992. Structureand dynamics

of a natterjack oad metapopulationBufocalamita). Oecologia 90:489-99174. Sinsch U. 1996. Population dynamicsof natterjack toads (Bufo calamita) inthe Rhineland: a nine-years study.Verh.Deutschen Zool. Ges. 89:1-127175. SjogrenP. 1991. Extinctionand isolationgradient n metapopulations: he case ofthe pool frog (Rana lessonae). Biol. J.Linn. S

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