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Detritus type alters the outcome of interspecificcompetition between Aedes aegypti and Aedesalbopictus (Diptera Culicidae)Ebony G MurrellIllinois State University

Steven A JulianoIllinois State University

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Recommended CitationMurrell Ebony G and Juliano Steven A Detritus type alters the outcome of interspecific competition between Aedes aegypti andAedes albopictus (Diptera Culicidae) (2008) Faculty Publications ndash Biological Sciences Paper 12httpirlibraryillinoisstateedufpbiosci12

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Detritus Type Alters the Outcome of Interspecific CompetitionBetween Aedes aegypti and Aedes albopictus (Diptera Culicidae)Author(s) Ebony G Murrell and Steven A JulianoSource Journal of Medical Entomology 45(3)375-383 2008Published By Entomological Society of AmericaDOI httpdxdoiorg1016030022-2585(2008)45[375DTATOO]20CO2URL httpwwwbiooneorgdoifull1016030022-258528200829455B3753ADTATOO5D20CO3B2

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POPULATION AND COMMUNITY ECOLOGY

Detritus Type Alters the Outcome of Interspecific CompetitionBetween Aedes aegypti and Aedes albopictus (Diptera Culicidae)

EBONY G MURRELL1 AND STEVEN A JULIANO

Department of Biological Sciences Illinois State University Campus Box 4120 Normal IL 61790

J Med Entomol 45(3) 375ETH383 (2008)

ABSTRACT Many studies of interspeciTHORNc competition betweenAedes albopictus (Skuse) andAedesaegypti (L) (Diptera Culicidae) larvae show that Ae albopictus are superior resource competitorstoAe aegypti Single-species studies indicate that growth and survival ofAe albopictus andAe aegyptilarvae are affected by the type of detritus present in containers which presumably affects the amountand quality of microorganisms that the mosquito larvae consume We tested whether different detritustypes alter the intensity of larval competition by raising 10 different densityspecies combinations ofAe albopictus and Ae aegypti larvae under standard laboratory conditions with one of four detritustypes (oak pine grass or insect) provided as a nutrient base IntraspeciTHORNc competitive effects onsurvival were present with all detritus typesAealbopictus survivorship was unaffected by interspeciTHORNccompetition in all treatments Negative interspeciTHORNc effects on Ae aegypti survivorship were presentwith three of four detritus types but absent with grass Estimated THORNnite rate of increase (Otilde) was lowerwith pine detritus than with any other detritus type for both species Furthermore Ae aegypti Otilde wasnegatively affected by high interspeciTHORNc density in all detritus types except grass Thus our experimentconTHORNrms competitive asymmetry in favor of Ae albopictus with oak pine or insect detritus but alsodemonstrates that certain detritus types may eliminate interspeciTHORNc competition among the larvae ofthese species which may allow for stable coexistence Such variation in competitive outcome withdetritus type may help to account for observed patterns of coexistenceexclusion ofAe albopictus andAe aegypti in the THORNeld

KEY WORDS Culicidae Aedes aegypti Aedes albopictus condition-speciTHORNc competition artiTHORNcialcontainers

InterspeciTHORNc resource competition can be a majordeterminant of species distributions and ultimatelycommunity structure (Connell 1983 Schoener 1983)Often interspeciTHORNc resource competition is asymmet-rical which is expected to lead to the competitiveexclusion of the species that is more negatively af-fected by interspeciTHORNc competition (Lawton and Has-sell 1981 Schoener 1983 Vandermeer and Goldberg2003) However in some cases environmental factorsmay alter the presence or severity of interspeciTHORNccompetition At the population level this alterationof competitive effects may reduce asymmetry or re-verse competitive advantage yielding respectivelystable coexistence or even a reversal of competitiveadvantage (Welden and Slauson 1986 Dunson andTravis 1991 Taniguchi and Nakano 2000 Costanzo etal 2005) This effect is referred to as ldquocondition-spe-ciTHORNc competitionrdquo and it seems to be an importantphenomenon in some systems affecting competitorcoexistence (Taniguchi and Nakano 2000) or localvariation in the success and impact of invasive speciesFacon et al 2004 Costanzo et al 2005 Thomas and

Holway 2005) Most investigations of condition-spe-ciTHORNc competition have focused on differences in thephysical variables that affect competitive interactions(Dunson and Travis 1991 Taniguchi and Nakano 2000Holway et al 2002 Facon et al 2004 Costanzo et al2005 Thomas and Holway 2005) Despite its basic andpotential practical importance we know relativelylittle about the prevalence of condition-speciTHORNc com-petition

A good model system for investigating condition-speciTHORNc competition is the interaction between twoinvasive mosquitoes Aedes albopictus (Skuse) andAedes aegypti (L)Ae albopictus (Diptera Culicidae)was introduced into Florida in the 1980s and within adecade had established populations throughout thestate (OOtildeMeara et al 1995) Its spread throughoutFlorida (Hornby et al 1994 OOtildeMeara et al 1995) andsouthern North America (Hobbs et al 1991 Mekuriaand Hyatt 1995) coincided with the decline of Aedesaegypti which has inhabited southeastern UnitedStates since colonial times (Christophers 1960 Louni-bos 2002) Larvae of both species occur in water-THORNlledartiTHORNcial containers and THORNlter-feed on microorganisms(Juliano et al 2004 Walker et al 1996 Merritt et al1 Corresponding author e-mail egmurreilstuedu

0022-2585080375ETH0383$04000 2008 Entomological Society of America

1992) making interspeciTHORNc resource competitionamong larvae possible Laboratory and THORNeld studiesalso indicate that under most conditionsAe albopictusis the superior competitor (Barrera 1996 Juliano 1998Daugherty et al 2000 Braks et al 2004 Yee et al 2004)which is consistent with the relative dominance ofAealbopictus at many Florida sites Despite this there aresome areas where Ae aegypti and Ae albopictus co-exist and in a few areas Ae aegypti remains dominantand Ae albopictus has been unable to establish resi-dent populations (OOtildeMeara et al 1995 Juliano et al2004)

The mechanisms producing coexistence of thesespecies at some sites andAe aegyptiextinction at othersites are unknown Experiments have shown how avariety of environmental factors may affect the spreadof Ae albopictus (Alto and Juliano 2001ab) and thepattern of coexistence or exclusion of Ae aegypti andAe albopictus in Florida (Juliano et al 2002 Costanzoet al 2005) Condition-speciTHORNc competition has beendocumented for one physical variable (container dry-ing due to drought) in this system (Costanzo et al2005) One environmental factor that has receivedrelatively little investigation concerning its effects oncompetition among mosquitoes is the type of detrituspresent in containers (Daugherty et al 2000 Yee et al2007a) Different types of detritus support differentquantities (and possibly different species) of micro-organisms (Walker et al 1991 Yee and Juliano 2006)which could in turn affect the quantity or quality offood available for mosquito larvae Differential feed-ing of mosquito species on microorganism species oran overabundance of microorganisms available toboth species could lead to elimination or reversal ofinterspeciTHORNc competitive advantage between mos-quito species allowing regional coexistence of the twospecies (Yee et al 2007a)

Differences in food quality of different detritustypes for mosquito larvae have been shown by Daugh-erty et al (2000) and Barrera (1996) who demon-strated that larvae raised with animal detritus developfaster and attain larger adult body mass than do larvaeraised with plant detritus Larvae raised with rapidlydecaying plant detritus have faster development andlarger adult body mass than do larvae raised withslow-decaying plant detritus (Fish and Carpenter1982 Dieng et al 2002) Daugherty et al (2000)showed that addition of insect carcasses to containersprimarily based on leaf detritus could eliminate inter-speciTHORNc competition between Ae Albopictus and Aeaegypti

As part of our investigations of the sources of vari-ation in the outcome of competition among theseinvasive container mosquitoes we conducted a labo-ratory experiment on the effects of different detritustypes on competition and its population level outcomefor Ae aegypti and Ae albopictus Four types of de-tritus were tested across different density combina-tions of Ae aegypti and Ae albopictus We hypothe-sized that detritus type would alter the presence oroutcome of interspeciTHORNc competition and thus couldcontribute to observed pattern of coexistence or ex-

clusion in Florida We expected that reductions ofpopulation growth survival development or massgain due to interspeciTHORNc competition would be moreextreme for Ae aegypti than for Ae albopictus in mostdetritus types However we also expected that detri-tus types that decay rapidly (grass and insect detritus)would reduce or eliminate interspeciTHORNc competitiveeffects or reverse competitive asymmetry betweenthese species

Materials and Methods

Container Setup Forty different treatments wereestablished for this experiment with three replicatesper treatment (120 containers) Each treatment in-cluded one of four detritus typesNtildesenescent live oak(Quercus virginianaMill) leaves senescent slash pine(Pinus elliotti Engelm) needles fresh grass clippings(Zoysia sp) and insects consisting of a 5050 mix bymass of Drosophila and crickets (Gryllodes sigilla-tus)Ntildeand one of 10 different density combinations ofAe albopictus Ae aegypti (010 020 040 1010 20201030 3010 400 200 and 100) thus testing bothintraspeciTHORNc and interspeciTHORNc competition at low me-dium and high densities Larvae were added as THORNrstinstars synchronously hatched in 044 gliter nutrientbroth Detritus types for this experiment were chosenbased on the types of detritus commonly found inFlorida cemetery vases (SAJ unpublished data)With the exception of insect detritus which was ob-tained from laboratory colonies all detritus we usedwas collected from the Florida Medical EntomologyLaboratory Vero Beach FL and it was pesticide-freeAe aegypti larvae were from a laboratory colony (gen-eration unknown) originally collected in south Flor-ida The Ae albopictus larvae were from an F2 gener-ation colony originally collected at Indrio Rd FtPierce FL and Myakka State Park Florida

Each container received 350 ml of deionized (DI)water 100 l of microbial inoculum of tree hole watercollected from Parklands Merwin Preserve north ofNormal IL and either 05 0003 g plant detritus or005 0003 g insect detritus A lower amount of insectdetritus was used because preliminary data indicatedthat more animal material resulted in fouling of thewater and toxicity to larvae Containers were supple-mented with the same amounts of detritus on days 1428 and 49 to maintain larval food supply and DI waterwas added as needed to maintain the initial volumeThe containers were randomized and held in an en-vironmental chamber at 28C on a photoperiod of1410 (LD) cycle When the containers had beenestablished for 4 d (day 0 of the experiment) weadded Ae albopictus and Ae aegypti larvae (24 h old)to the containers in the ratios listed above

Pupae were removed daily and placed in individualvials foreclosionEclosedadultswere sexed identiTHORNedto species and their date of eclosion dry mass andwing lengths of females were recorded We ended theexperiment on day 65 when we collected and iden-tiTHORNed remaining larvae Pupae collected on day 65were allowed to eclose and they were included in the

376 JOURNAL OF MEDICAL ENTOMOLOGY Vol 45 no 3

adult data set Once the experiment ended we cal-culated survivorship to adulthood for each species ineach containerPopulation GrowthWe estimated the THORNnite rate of

increase (Otilde) for each species in each container by THORNrstcalculating the estimated instantaneous rate of in-crease (rOtilde Livdahl and Sugihara 1984)

rOtilde ln1N0x

AxfwxD

x

xAxfwxx

AxfwxwhereN0 is the initial number of females per container(assumed to be 50 of the larvae) Ax is the numberof females eclosing on day x and f(wx) is a functiondescribing size dependent fecundity for each speciesestimated from the mean wing length on day x wx offemale mosquitoes (Livdahl and Sugihara1984 Juliano1998) The function for Ae aegypti was f(wx) 250wx 8616 where wx is the cube of wing length(millimeters) (Briegel 1990) The function for Aealbopictuswas f(wx) 121240 7802wxwherewxis wing length (millimeters) (Lounibos et al 2002)Finite rate of increase was then estimated from rOtilde asOtilde exp(rOtilde) For cohort studies like this Otilde is estimableeven if there are no surviving females (Otilde 0)whereas in that circumstance rOtilde is not estimable(Juliano 1998)Tannins In addition to the 120 containers of detri-

tus and mosquitoes larvae we also established a set ofnine containers for each detritus type that did notcontainer larvae These containers were used to mea-sure decay rate tannin concentration and microbialgrowth rate for each detritus type Tannin concentra-tions 100 mgliter can reduce mosquito growth(Sota 1993) and we expected major differences intannin content among types

One day before addition of mosquitoes we col-lected 10 ml of water from each of the 36 containersthat did not receive mosquitoes These water sampleswere analyzed for tannins (milligrams per liter) byusing a Hach D800 meter and its Hach tannin test kit(Hach Loveland CO)Microbial GrowthOn days 0 4 and 7 we collected

two 1-ml samples from each of the 36 containers thatdid not receive mosquitoes We used these samples to

quantify microbial growth using the method of leucineincorporation described by Yee et al (2007a) Triti-ated leucine was added to each sample at a concen-tration of 25 nM After the samples were incubated for30 min 100 trichloroacetic acid was added to eachsample (5 THORNnal concentration) to halt leucine incor-poration (Yee et al 2007a) We randomly collectedone additional 1-ml sample from two of the 36 con-tainers and we added trichloroacetic acid to thesesamples to measure baseline radiation levels of aquaticmicroorganisms before the addition of radioactiveleucine All killed samples were then centrifugedrinsed and analyzed via liquid scintillation by using aBeckman LS 6500 scintillation counter (BeckmanCoulter Fullerton CA) This procedure measures theleucine incorporation into microbial biomass whichquantiTHORNes microbial growth (Kirchman 2001)Detritus Decay Rate On days 7 14 and 21 we

destructively sampled three containers of each detri-tus type that received no mosquitoes We used a106-m sieve to remove remaining detritus from eachcontainer dried the detritus at 50C for at least 24 hand recorded its dry massAnalysesForeachspeciesweanalyzedsurvivorship

and sex-speciTHORNc mean adult mass and median days toeclosion (collectively ldquoperformance variablesrdquo) by us-ing a linear model (PROC GLM SAS 91) with num-bers of Ae aegypti and Ae albopictus as continuousvariables and detritus type as a class variable Wetested among detritus types for equality of slopes ofperformance variables versus numbers of the twoAedes species If detritus type altered the competitiveeffect of these species on one another or on them-selves we expected that slopes would differ amongdetritus types yielding a signiTHORNcant mosquito den-sity detritus type interaction We used factorial

Fig 1 Decay of different detritus types over time Valuesplotted are means SE Absence of error bars indicates thatSE was too small to show Statistical results in Table 2

Table 1 ANOVA and pairwise comparisons for effects of de-tritus types on tannins

Source Comparison df F value Pr F

Detritus 3 7327 00001Grass vs insect 1 7427 00001Oak vs pine 1 12650 00001Grass vs oak 1 1944 00001Grass vs pine 1 4676 00001Insect vs oak 1 16959 00001Insect vs pine 1 315 00853

Error 32

SigniTHORNcant effects and pairwise comparisons are in bold

Table 2 ANOVA results for proportion decay of detritus atthree time periods 7 14 and 21 d

Source df F value Pr F

Detritus 3 565247 00001Day 2 1425 00001Detritus day 6 616 00005Error 24

Detritus data was square root transformed SigniTHORNcant P values arein bold

May 2008 MURRELL AND JULIANO EFFECTS OF DETRITUS ON Aedes LARVAL COMPETITION 377

analysis of variance (ANOVA) to test effects of Aealbopictus Ae aegypti density combinations on Otilde(which was clearly nonlinearly related to densities)and to test for treatment effects on decay rate andtannin concentrations The effect of detritus type onleucine incorporation rate was analyzed using repeated-measures multivariate analysis of variance (MANOVA)(Scheiner 2001 von Ende 2001) We arcsine square-rootETHtransformed proportions surviving and log trans-formed mass and time data to meet assumptions ofnormality and homogeneity of variances For Otilde datadid not meet the assumption of normality and we alsotested for effects using a randomization ANOVA (RT21 Manly 1991) Randomization ANOVA yielded thesame signiTHORNcant effects as the parametric ANOVAhence we report only the parametric results

Results

Tannins Decay Rate and Microbial Growth Tan-nin concentrations differed signiTHORNcantly among detri-tus types (Table 1) All detritus types were signiTHORN-cantly different from one another except for pine andinsect Tannins were highest in oak (152 mgliter)and lowest in insect (119 mgliter) Decay rate alsodiffered signiTHORNcantly among detritus types at threetimes (Table 2) with insect detritus having the great-

est percentage of decay followed by grass (Fig 1)Oak and pine had low decay and they were not sig-niTHORNcantly different from one another Leucine incor-poration differed signiTHORNcantly among detritus types(Table 3) Grass had the highest leucine incorpora-tion followed by insect Oak and pine had the lowestincorporation and they were not signiTHORNcantly differ-ent from one another (Fig 2)Mosquito Data Survivorship for both species dif-

fered signiTHORNcantly among detritus types and was neg-atively affected by conspeciTHORNc density (Table 4) Inaddition there was a signiTHORNcant interaction betweenheterospeciTHORNc density and detritus type forAe aegyptisurvivorship indicating that the impact of interspe-ciTHORNc competition differed with detritus type Het-erospeciTHORNc (Ae albopictus) density had a signiTHORNcantand negative effect on Ae aegypti survivorship withpine oak and insect detritus but with grass detritussurvivorship was not signiTHORNcantly affected by Ae al-bopictus density (Fig 3)

Developmental time (Table 5) and mass (Table 6)inboth species andsexeswere signiTHORNcantlyaffectedbyboth con- and heterospeciTHORNc densities Time to eclo-sion increased signiTHORNcantly and adult mass decreasedsigniTHORNcantly as larval densities increased There was asigniTHORNcant interaction of heterospeciTHORNc density anddetritus type for female Ae albopictus developmentaltime (Table 5 Fig 5) Development to adulthood ofAe albopictus females was less affected by heterospe-ciTHORNc density with pine detritus than with other detritus

Fig 2 Leucine incorporation (mean SE) measured at three times for each detritus type Statistical results in Table 3

Table 3 Repeated-measures MANOVA results for leucineincorporation

SourcePillaiOtildes trace

(F)df Pr F

Standardizedcanonical

coefTHORNcients

Day7

Day14

Day21

Detritus type 564 996 00001 248 054 090Insect vs all

vegetation700 330 00010 203 004 090

Grass vs alltree detritus

7183 330 00001 201 245 077

Oak vs pine 135 330 02781Time 7959 231 00001 156 093Time detritus

type406 664 00016 158 069

Data were square root transformed for analysis SigniTHORNcant P valuesare in bold

Table 4 Linear model results for mean Ae aegypti and Aealbopictus survival (arcsine-square root transformed)

Source

Ae aegypti Ae albopictus

dfF

valuePr F df

Fvalue

Pr F

Detritus 3 511 00030 3 365 00167albopictus 1 3210 00001 1 1511 00002aegypti 1 5280 00001 1 051 04789albopictus

detritus3 478 00044 3 141 02485

aegypti detritus

3 050 06855 3 092 04375

Error 67 69

SigniTHORNcant effects are in bold


types (Fig 5B) Also male Ae albopictus develop-mental time showed signiTHORNcant interaction effects be-tween both hetero- and conspeciTHORNc density and de-tritus type (Table 5) with larval densities having agreater effect on male Ae albopictus developmentwith pine and insect detritus than with grass and oakdetritus (Fig 5D) There was no interaction for Aeaegypti males (Fig 5C) Female masses yielded nosigniTHORNcant interactions (Table 6 Fig 4 A and B) Incontrast male Ae albopictus masses showed a signif-icant interaction between heterospeciTHORNc density anddetritus type (Table 6) with male adult mass of Aealbopictus more affected by Ae aegypti density withoak than with other detritus types (Fig 4D)

Estimated THORNnite rate of increase (Otilde) of both specieswas signiTHORNcantly affected by species density combi-nation and detritus type (Table 7)Ae aegypti showeda signiTHORNcant interaction between combination and de-tritus type SpeciTHORNcally grass detritus yielded signiTHORN-cantly higher Otilde for Ae aegypti than did all other

detritus types at the 3010 Ae albopictusAe aegypticombination (ie with high interspeciTHORNc density)pine yielded signiTHORNcantly lower Otilde than did grass at 040combination and pine also yielded signiTHORNcantly lowerOtilde than all other detritus types at 1030 and 2020combinations (Fig 6A) For Ae albopictus Otilde wassigniTHORNcantly lower in pine than in all other detritustypes and lower at the 1010 combination than at allothers (Fig 6B)

Discussion

It is clear from these data that detritus types not onlyaffect mosquito performance and population growthbut also can affect the outcome of competition Thepatterns of impacts of larval density on survival and Otildeare consistent when compared with the microbialgrowth and decay rate data across detritus types Sur-vival and Otilde values for both species were greater withdetritus types that had greater decay rates and micro-

Fig 3 Mean proportion survival by detritus type ofAe aegypti (A) andAe albopictus (B) as affected by both conspeciTHORNcand heterospeciTHORNc densities Scatter plots represent back-transformed means for each detritus type and surfaces representpredicted model values for each detritus type Note that appearance of nonlinearity of both scatter plot and surfaces areproducts of back-transformation

Table 5 Linear model results for log10-transformed mediandays to eclosion for each speciessex

Sex Source


dfF

valuePr F df

Fvalue

Pr F

Female Detritus 3 3760 00001 3 2223 00001albopictus 1 1360 00005 1 9156 00001aegypti 1 4019 00001 1 6512 00001albopictus

detritus3 014 09365 3 178 01607

aegypti detritus

3 163 01942 3 533 00025

Error 41 46Male Detritus 3 4058 00001 3 1294 00001

albopictus 1 2654 00001 1 4357 00001aegypti 1 4143 00001 1 1833 00001albopictus

detritus3 105 03785 3 460 00055

aegypti detritus

3 244 00734 3 502 00034

Error 44 49


Table 6 Linear model results for log10-transformed meanmass for each speciessex

Sex Source


dfF

valuePr F df

Fvalue

Pr F


detritus3 083 04838 3 004 09877

aegypti detritus

3 030 08275 3 159 02011



detritus3 209 01115 3 260 00594

aegypti detritus

3 016 09258 3 470 00049

Error 44 49



bial growth (eg grass and insect) and lower withdetritus types that had slower decay and microbialgrowth (eg oak and pine) These results suggests thatlarval survival and Otilde are directly related to the amountof available food (microorganisms as suggested by themicrobial growth data) each detritus type supportsThese data are consistent with previous laboratorystudies of effects of detritus types on mosquito per-formance (Fish and Carpenter 1982 Walker et al1991 Yee and Juliano 2006)

Both the survival and Otilde data support our hypothesisthat detritus type can alter the outcome of interspe-ciTHORNc competition The strong negative effect of inter-speciTHORNc competition on Ae aegypti survival with in-sect oak and pine detritus with Ae albopictussimultaneously unaffected by interspeciTHORNc competi-tion implies strong competitive asymmetry with Aealbopictus the superior competitor with those sub-strates which is also consistent with previous studies(Barrera 1996 Juliano 1998 Daugherty et al 2000 Yeeet al 2004) This competitive asymmetry would beexpected to lead to competitive exclusion of Ae ae-gypti However with grass detritus neither speciesOtildesurvival was affected by interspeciTHORNc competition al-though intraspeciTHORNc competition was still evidentWeak interspeciTHORNc competition along with signiTHORNcantintraspeciTHORNc competition is consistent with stable co-existence of these two species being possible in con-

tainers dominated by grass detritus as each speciesOtildepopulation would be regulated by its own densityrather than the density of the other species (Vander-meer and Goldberg 2003) This change from Ae al-bopictus dominance to potential coexistence depend-ing on the detritus type could help to explain howthese species continue to coexist at some sites in Flor-ida despite the frequently observed competitive su-periority of Ae albopictus (Barrera 1996 Juliano 1998Braks et al 2004) Geographic variation in the mix ofdetritus types available may affect the outcome ofcompetition leading to coexistence at some sites andexclusion at others Sites where coexistence occurswhich are predominantly urban areas of South Florida(OOtildeMeara et al 1995 SAJ unpublished data) wouldbe predicted to have a greater relative abundance ofhigh-quality detritus (eg grass) whereas sites dom-inated by Ae albopictuswould be predicted to have agreater relative abundance of lower quality detritustypes (eg oak leaves and pine needles)

How may grass as a detritus source yield no inter-speciTHORNc competition but still yield signiTHORNcant intraspe-ciTHORNc competition We cannot answer this questionbased on this experiment but we offer a hypothesisbesides producing greater microbial growth (as indi-cated by leucine incorporation) grass as a resourcemay yield a greater diversity of microbial types (bothtaxonomic groups and functional groups) and this

Fig 4 Mean mass by detritus type of adult females (A and B) and males (C and D) of each species as affected byconspeciTHORNc and heterospeciTHORNc densities As in Fig 3 scatter plots represent back-transformed means and surfaces representpredicted model values Appearance of nonlinearity is a product of back transformation of data


diversity may allow these species to specialize on cer-tain classes of microorganisms Yee et al (2004) doc-umented signiTHORNcant interspeciTHORNc differences in forag-ing behaviors with Ae albopictus directing moreforaging at detritus surfaces and Ae aegypti spendingmore time at the wall and bottom Under the rightenvironmental circumstances (high microbial abun-dance and diversity) these differences in foragingbehavior may result in differential use of microbialresources sufTHORNcient food for Ae aegypti (the poorercompetitor in many circumstances) and thus reducedinterspeciTHORNc competition Several other studies sug-gest that rich rapidly decaying detritus (usually ani-mal material) can reduce the competitive disadvan-

tage of Ae aegypti (Barrera 1996 Daugherty et al2000 Alto et al 2005) To test this hypothesis we needdata on the diversity of microorganisms associatedwith grass as a detritus source

Mass and developmental time of both speciesshowed similar responses to detritus types This sug-gests competitive symmetry of the two species foreffects on these variables contrary to our originalpredictions However the profound asymmetry of ef-fects on survival seems to be more important as adeterminant of overall population performance (Otilde)The most consistent and most notable difference be-tween the species is that development time of Aealbopictus is less affected by interspeciTHORNc densities inpine detritus than with other detritus types This re-sponse could be in part a result of high mortality ofAeaegyptiwith pine detritus (Fig 3) severe reduction orelimination ofAe aegypti from high-density pine treat-ments would alleviate negative interspeciTHORNc effects onAe albopictus producing the signiTHORNcant interactioneffect observed This asymmetric response in devel-opment with pine detritus could provide anothermechanism by which Ae albopictus is competitivelysuperior to Ae aegyptiHowever because survivorshipand Otilde for both species with pine detritus were very lowit is more likely that this competitive asymmetry serves

Fig 5 Median days to eclosion by detritus type of adult females (A and B) and males (C and D) of each species asaffected by conspeciTHORNc and heterospeciTHORNc densities As in Fig 3 scatter plots represent back-transformed means and surfacesrepresent predicted model values Apparent nonlinearity is a product of back-transformation of data Note that colors for thisgraph have been reversed to better display all detritus types

Table 7 ANOVA results for rsquo for each species

Source


dfF

valuePr F df

Fvalue

Pr F

Detritus 3 3049 00001 3 1397 00001Combination 6 1062 00001 6 347 00056Detritus

combination18 292 00012 18 107 04046

Error 55 55



only to exacerbate competitive dominance ofAe albop-ictus with pine detritus and it does not ultimately alterthe outcome of interspeciTHORNc competition

Understanding how environmental factors such asdetritus type may affectAe albopictus andAe aegyptidistributions is not only of basic ecological interestbut it may be medically important Both species havebeen introduced worldwide to tropical and subtrop-ical locations (Hawley 1988) and both are carriers ofhuman diseases such as dengue yellow fever andpotentially West Nile Virus (Yuill 1986 Sardelis et al2002) The ability of both species to live in artiTHORNcialcontainer habitats (Juliano et al 2004) brings them intoproximity to human population and along with theirability to transmit human diseases makes them poten-tially serious threats to human health on a wide geo-graphic scale The possibility of stable coexistence be-tween these two vectors under some circumstancesraises the question of whether transmission of a diseasecarried by both (eg dengue) might be more frequentor more persistent when these species coexist

This laboratory experiment provides us with at leastone environmental variable detritus type that couldpredict where Ae aegypti and Ae albopictus may co-occur or where Ae albopictus may eliminate Ae ae-gypti Logically the next step should be to determinewhether variation in detritus types in nature is corre-lated with distributions of Ae aegypti and Ae albop-ictus Previous studies have shown that Aedes speciesdistributions are correlated with urbanization and cli-mate differences with Ae aegypti more prevalent in

highly urbanized areas and in locations with greaterperiods of seasonal drought whereas Ae albopictus ishighly dominant in rural areas without seasonaldrought (Juliano et al 2002 Braks et al 2003) We donot yet know urbanization and climate differences arelinked to these species distributions Detritus variationis apossibility as thequantityandcompositionofplantand animal communities are generally different alongboth climatic and urbanization gradients (Mather andYoshioka 1968 McDonnell and Pickett 1990) There-fore quaniTHORNcation of geographic variation in detritustypes and distributions of these species will be nec-essary to determine if detritus is in fact an importantdeterminant ofAedes species distributions in the THORNeldFurther laboratory or THORNeld studies on the chemical andmicrobial properties of detritus types would help todeTHORNne the mechanistic relationship between detritustypes and their effects on competition

Acknowledgments

We thank L P Lounibos B W Alto E Gunawardene CJaniec W L Perry and S K Sakaluk for aid in the THORNeld orlaboratory comments and useful discussion and three anon-ymous referees for comments on the manuscript This re-search was funded by National Institute of Allergy and In-fectious Diseases grant R01 AI44793 and by Beta LambdaChapter of Phi Sigma at Illinois State University

References Cited

Alto B W and S A Juliano 2001a Precipitation and tem-perature effects on populations of Aedes albopictus(Diptera Culicidae) implications for range expansionJ Med Entomol 38 646ETH656

AltoBW andSA Juliano 2001b Temperature effects onthe dynamics of Aedes albopictus (Diptera Culicidae)populations in the laboratory J Med Entomol 38 548ETH556

Alto BW L P Lounibos S Higgs and S A Juliano 2005Larval competition differentially affects arbovirus infec-tion in Aedes mosquitoes Ecology 86 3279ETH3288

Barrera R 1996 Competition and resistance to starvationin larvae of container-inhabiting Aedesmosquitoes EcolEntomol 21 112ETH127

Braks MAH N A Honorio L P Lounibos R L Oliveiraand S A Juliano 2004 InterspeciTHORNc competition be-tween two invasive species of container mosquitoesAedes aegypti andAedes albopictus (Diptera Culicidae)in Brazil Ann Entomol Soc Am 97 130ETH139

BraksMAHNAHonorioRLOliveira SA Juliano andL P Lounibos 2003 Convergent habitat segregation ofAedes aegypti and Aedes albopictus (Diptera Culicidae)in southeastern Brazil and Florida USA J Med Entomol40 785ETH794

Briegel H 1990 Metabolic relationship between femalebody size reserves and fecundity of Aedes aegypti J In-sect Physiol 36 165ETH172

Christophers R S 1960 Aedes aegypti The yellow fevermosquito its life history bionomics and structure Cam-bridge University Press Cambridge United Kingdom

Connell J H 1983 On the prevalence and relative impor-tance of interspeciTHORNc competition evidence from THORNeldexperiments Am Nat 122 661ETH696

Costanzo K S B Kesavaraju and S A Juliano 2005 Con-dition-speciTHORNc competition in container mosquitoes the

Fig 6 Comparison of least squares means for Otilde of Aeaegypti (A) and Ae albopictus (B) Values with the sameletters are not signiTHORNcantly different from one another withinthe same species combination


role of non-competing life-history stages Ecology 863289ETH3295

Daugherty M P B W Alto and S A Juliano 2000 In-vertebrate carcasses as a resource for competing Aedesalbopictus andAedes aegypti (Diptera Culicidae) J MedEntomol 37 364ETH372

Dieng H C Mwandawiro M Boots R Morales T Satho TNobuko Y Tsuda and M Takagi 2002 Leaf litter decayprocess and the growth performance of Aedes albopictuslarvae (Diptera Culicidae) J Vector Ecol 27 31ETH38

Dunson W A and J Travis 1991 The role of abiotic fac-tors in community organization Am Nat 138 1069ETH1091

Facon B E Machline J P Pointier and P David 2004Variation in desiccation tolerance in freshwater snails andits consequences for invasion ability Biol Invasions 6283ETH293

Fish D and S R Carpenter 1982 Leaf litter and larvalmosquito dynamics in tree-hole ecosystems Ecology 63283ETH288

HawleyW A 1988 The biology of Aedes albopictus J AmMosq Control Assoc 1 1ETH40

Hobbs J H E A Hughes and B H Eichold I I 1991Replacement of Aedes aegypti by Aedes albopictus in Mo-bile Alabama J Am Mosq Control Assoc 7 488ETH489

Hornby J AD EMoore andTWMiller Jr 1994 Aedesalbopictus distribution abundance and colonization inLee County Florida and its effect onAedes aegypti J AmMosq Control Assoc 10 397ETH402

Juliano S A 1998 Species introduction and replacementamong mosquitoes interspeciTHORNc resource competition orapparent competition Ecology 79 255ETH268

Juliano S A G F OrsquoMeara J R Morrill andMM Cutwa2002 Desiccation and thermal tolerance of eggs and thecoexistence of competing mosquitoes Oecologia (Berl)130 458ETH469

Juliano S A L P Lounibos andG FOrsquoMeara 2004 A THORNeldtest for competitive effects of Aedes albopictus on Aedesaegypti in south Florida differences between sites of coex-istence and exclusion Oecologia (Berl) 139 583ETH593

Kirchman D 2001 Measuring bacterial biomass productionand growth rates from leucine incorporation in naturalaquatic environments Methods Microbiol 30 227ETH237

Lawton J H and M P Hassell 1981 Asymmetrical com-petition in insects Nature (Lond) 289 793ETH795

Livdahl T P and G Sugihara 1984 Non-linear interac-tions of populations and the importance of estimating percapita rates of change J Anim Ecol 53 573ETH580

Lounibos L P S Saurez Z Menedez N Nishimura R LEscher S M OrsquoConnell and J R Rey 2002 Does tem-perature affect the outcome of larval competition be-tweenAedes aegypti andAedes albopictus J Vector Ecol27 86ETH95

Lounibos L P 2002 Invasions by insect vectors of humandisease Annu Review Entomol 47 233ETH266

Manly BFJ 1991 Randomization and Monte Carlo meth-ods in biology Chapman amp Hall New York

Mather J R and G A Yoshioka 1968 The role of climatein the distribution of vegetation Ann Assoc Am Geogr58 29ETH41

McDonnell M J and STA Pickett 1990 Ecosystem struc-ture and function along urban-rural gradients an unex-ploited opportunity for ecology Ecology 71 1232ETH1237

Mekuria Y and M G Hyatt 1995 Aedes albopictus inSouth Carolina J Am Mosq Control Assoc 9 352ETH355

Merritt RWRHDadd andEDWalker 1992 Feedingbehavior natural food and nutritional relationships oflarval mosquitoes Annu Rev Entomol 37 349ETH376

OrsquoMeara G F L F Evans A D Gettman and J P Cuda1995 Spread of Aedes albopictus and decline of Ae ae-gypti (Diptera Culicidae) in Florida J Med Entomol 32554ETH562

SardelisMRM J TurrellMLOrsquoGuinnRGAndre andDRRoberts 2002 Vector competence of North Amer-ican strains of Aedes albopictus for west Nile virus J AmMosq Control Assoc 18 284ETH289

Scheiner S M 2001 MANOVA multiple response vari-ables and multispecies interactions chapter 6 pp 99ETH115In S M Scheiner and J Gurevitch Design and analysis ofecological experiments 2nd ed Oxford University PressLondon United Kingdom

Schoener T W 1983 Field experiments on interspeciTHORNccompetition Am Nat 122 240ETH285

Sota T 1993 Performance of Aedes albopictus and Aedesriversi larvae (Diptera Culicidae) in waters that containtannic acid and decaying leaves is the treehole speciesbetter adapted to treeholewaterAnnEntomol SocAm86 450ETH457

Taniguchi Y and S Nakano 2000 Condition-dependentcompetition implications for the distributions of streamTHORNshes Ecology 81 2027ETH2039

Thomas M L and D A Holway 2005 Condition-speciTHORNccompetition between invasive Argentine ants and Aus-tralian Iridomyrmex J Anim Ecol 74 532ETH542

Vandermeer J H and D E Goldberg 2003 Populationecology THORNrst principles Princeton University PressPrinceton NJ

von Ende C N 2001 Repeated-measures analysis growthand other time-dependent measures Chapter 8 pp 134ETH157 In S M Scheiner and J Gurevitch [eds] Design andanalysis of ecological experiments 2nd ed Oxford Uni-versity Press London United Kingdom

Walker E D D L Lawson R W Merritt W T Morganand M J Klug 1991 Nutrient dynamics bacterial pop-ulations and mosquito productivity in tree hole ecosys-tems and microcosms Ecology 72 1629ETH1546

Walker E D G F OrsquoMeara and W T Morgan 1996Bacterial abundance in larval habitats of Aedes albopictus(Diptera Culicidae) in a Florida cemetery J VectorEcol 21 173ETH177

Welden C W and W L Slauson 1986 The intensity ofcompetition versus its importance an overlooked distinc-tion and some implications Q Rev Biol 61 23ETH44

YeeDA and S A Juliano 2006 Consequences of detritustype in an aquatic microsystem effects on water qualitymicro-organisms and performance of the dominant con-sumer Freshw Biol 51 448ETH459

Yee D A B Kesavaraju and S A Juliano 2004 Interspe-ciTHORNc differences in feeding behavior and survival underfood-limited conditions for larval Aedes albopictus andAedes aegypti (Diptera Culicidae) Ann Entomol SocAm 97 720ETH728

Yee D A M G Kaufman and S A Juliano 2007a ThesigniTHORNcance of ratios of detritus types and microorganismproductivity to competitive interactions between aquaticinsect detritivores J Anim Ecol 76 1105ETH1115

Yuill T M 1986 The ecology of tropical arthropod-borneviruses Annu Rev Ecol Syst 17 189ETH219

Received 20 August 2007 accepted 8 February 2008


Illinois State University

ISU ReD Research and eData

5-1-2008

Detritus type alters the outcome of interspecific competition between Aedes aegypti and Aedes albopictus (Diptera Culicidae)

Ebony G Murrell

Steven A Juliano

Recommended Citation

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Detritus Type Alters the Outcome of Interspecific CompetitionBetween Aedes aegypti and Aedes albopictus (Diptera Culicidae)Author(s) Ebony G Murrell and Steven A JulianoSource Journal of Medical Entomology 45(3)375-383 2008Published By Entomological Society of AmericaDOI httpdxdoiorg1016030022-2585(2008)45[375DTATOO]20CO2URL httpwwwbiooneorgdoifull1016030022-258528200829455B3753ADTATOO5D20CO3B2

BioOne (wwwbiooneorg) is a nonprofit online aggregation of core research in thebiological ecological and environmental sciences BioOne provides a sustainable onlineplatform for over 170 journals and books published by nonprofit societies associationsmuseums institutions and presses

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J Med Entomol 45(3) 375ETH383 (2008)



















rOtilde ln1N0x

AxfwxD

x

xAxfwxx












Error 32








Results








(F)df Pr F


coefTHORNcients

Day7

Day14

Day21


vegetation700 330 00010 203 004 090


7183 330 00001 201 245 077


type406 664 00016 158 069



Source


dfF

valuePr F df

Fvalue

Pr F


detritus3 478 00044 3 141 02485

aegypti detritus

3 050 06855 3 092 04375

Error 67 69






Discussion




Sex Source


dfF

valuePr F df

Fvalue

Pr F


detritus3 014 09365 3 178 01607

aegypti detritus

3 163 01942 3 533 00025



detritus3 105 03785 3 460 00055

aegypti detritus

3 244 00734 3 502 00034

Error 44 49



Sex Source


dfF

valuePr F df

Fvalue

Pr F


detritus3 083 04838 3 004 09877

aegypti detritus

3 030 08275 3 159 02011



detritus3 209 01115 3 260 00594

aegypti detritus

3 016 09258 3 470 00049

Error 44 49














Source


dfF

valuePr F df

Fvalue

Pr F


combination18 292 00012 18 107 04046

Error 55 55







Acknowledgments


References Cited























































5-1-2008


Ebony G Murrell

Steven A Juliano






J Med Entomol 45(3) 375ETH383 (2008)



















rOtilde ln1N0x

AxfwxD

x

xAxfwxx












Error 32








Results








(F)df Pr F


coefTHORNcients

Day7

Day14

Day21


vegetation700 330 00010 203 004 090


7183 330 00001 201 245 077


type406 664 00016 158 069



Source


dfF

valuePr F df

Fvalue

Pr F


detritus3 478 00044 3 141 02485

aegypti detritus

3 050 06855 3 092 04375

Error 67 69






Discussion




Sex Source


dfF

valuePr F df

Fvalue

Pr F


detritus3 014 09365 3 178 01607

aegypti detritus

3 163 01942 3 533 00025



detritus3 105 03785 3 460 00055

aegypti detritus

3 244 00734 3 502 00034

Error 44 49



Sex Source


dfF

valuePr F df

Fvalue

Pr F


detritus3 083 04838 3 004 09877

aegypti detritus

3 030 08275 3 159 02011



detritus3 209 01115 3 260 00594

aegypti detritus

3 016 09258 3 470 00049

Error 44 49














Source


dfF

valuePr F df

Fvalue

Pr F


combination18 292 00012 18 107 04046

Error 55 55







Acknowledgments


References Cited























































5-1-2008


Ebony G Murrell

Steven A Juliano














rOtilde ln1N0x

AxfwxD

x

xAxfwxx












Error 32








Results








(F)df Pr F


coefTHORNcients

Day7

Day14

Day21


vegetation700 330 00010 203 004 090


7183 330 00001 201 245 077


type406 664 00016 158 069



Source


dfF

valuePr F df

Fvalue

Pr F


detritus3 478 00044 3 141 02485

aegypti detritus

3 050 06855 3 092 04375

Error 67 69






Discussion




Sex Source


dfF

valuePr F df

Fvalue

Pr F


detritus3 014 09365 3 178 01607

aegypti detritus

3 163 01942 3 533 00025



detritus3 105 03785 3 460 00055

aegypti detritus

3 244 00734 3 502 00034

Error 44 49



Sex Source


dfF

valuePr F df

Fvalue

Pr F


detritus3 083 04838 3 004 09877

aegypti detritus

3 030 08275 3 159 02011



detritus3 209 01115 3 260 00594

aegypti detritus

3 016 09258 3 470 00049

Error 44 49














Source


dfF

valuePr F df

Fvalue

Pr F


combination18 292 00012 18 107 04046

Error 55 55







Acknowledgments


References Cited























































5-1-2008


Ebony G Murrell

Steven A Juliano



Results








(F)df Pr F


coefTHORNcients

Day7

Day14

Day21


vegetation700 330 00010 203 004 090


7183 330 00001 201 245 077


type406 664 00016 158 069



Source


dfF

valuePr F df

Fvalue

Pr F


detritus3 478 00044 3 141 02485

aegypti detritus

3 050 06855 3 092 04375

Error 67 69






Discussion




Sex Source


dfF

valuePr F df

Fvalue

Pr F


detritus3 014 09365 3 178 01607

aegypti detritus

3 163 01942 3 533 00025



detritus3 105 03785 3 460 00055

aegypti detritus

3 244 00734 3 502 00034

Error 44 49



Sex Source


dfF

valuePr F df

Fvalue

Pr F


detritus3 083 04838 3 004 09877

aegypti detritus

3 030 08275 3 159 02011



detritus3 209 01115 3 260 00594

aegypti detritus

3 016 09258 3 470 00049

Error 44 49














Source


dfF

valuePr F df

Fvalue

Pr F


combination18 292 00012 18 107 04046

Error 55 55







Acknowledgments


References Cited























































5-1-2008


Ebony G Murrell

Steven A Juliano





Discussion




Sex Source


dfF

valuePr F df

Fvalue

Pr F


detritus3 014 09365 3 178 01607

aegypti detritus

3 163 01942 3 533 00025



detritus3 105 03785 3 460 00055

aegypti detritus

3 244 00734 3 502 00034

Error 44 49



Sex Source


dfF

valuePr F df

Fvalue

Pr F


detritus3 083 04838 3 004 09877

aegypti detritus

3 030 08275 3 159 02011



detritus3 209 01115 3 260 00594

aegypti detritus

3 016 09258 3 470 00049

Error 44 49














Source


dfF

valuePr F df

Fvalue

Pr F


combination18 292 00012 18 107 04046

Error 55 55







Acknowledgments


References Cited























































5-1-2008


Ebony G Murrell

Steven A Juliano













Source


dfF

valuePr F df

Fvalue

Pr F


combination18 292 00012 18 107 04046

Error 55 55







Acknowledgments


References Cited























































5-1-2008


Ebony G Murrell

Steven A Juliano






Acknowledgments


References Cited























































5-1-2008


Ebony G Murrell

Steven A Juliano












































5-1-2008


Ebony G Murrell

Steven A Juliano


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