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Temporal and spatial changes in the diet of Hylapulchella (Anura, Hylidae) in southern UruguayRaúl Maneyro1,2 and Inés da Rosa1

1 Sección de Zoología de Vertebrados, Facultad de Ciencias, Universidad de la República. Iguá 4225, 11400,Montevideo, Uruguay E-mail: [email protected].

2 Laboratório de Herpetologia, Museu de Ciências e Tecnologia & Faculdade de Biociências da PontifíciaUniversidade Católica do Rio Grande do Sul. Av. Ipiranga 6681, 90619-900, Porto Alegre, RS, Brazil.

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AbstractTemporal and spatial changes in the diet of Hyla pulchella (Anura, Hylidae) insouthern Uruguay. In this article we report the diet of a population of the hylid frogHyla pulchella from southeastern Uruguay. We collected the specimens in ponds,where we identified microenvironments defined by the invertebrate assemblage, duringone year divided into two seasons (warm and cold). We taxonomically determined10365 invertebrates belonging to 21 categories in the digestive tracts of frogs. Weestimated the diversity of the diet and alimentary preference according tomicroenvironments and seasons. We estimated the expected richness of both diet andprey availability using a null model based on the hypergeometric distribution. Weperformed Discriminant Analyses and Kruskal-Wallis tests to detect changes in preyavailability among microenvironments and between seasons. The overall diet in termsof frequencies was composed primarily of arthropods (mainly Araneae, Diptera,Hymenoptera, and Coleoptera) and in terms of volume, by larvae. The most relevantitems to study the microenvironmental and seasonal variation in the available preyswere Araneae, Collembola, Homoptera, Hymenoptera, Diptera, Dictioptera,Lepidoptera, Coleoptera, and larvae. Based on the null model curves and preferenceindexes we inferred positive selection by larvae, Isopoda, Dictioptera, Lepidoptera,and Diptera, and negative selection by Collembola and Hymenoptera. The diversityof diet and the null model curves indicated that the diet changes amongmicroenvironments and seasons. This frog may be considered as a middle generalistpredator, with some selective behavior and a combined search strategy (active andsit-and-wait). We conclude that the knowledge about the availability of preys is arelevant tool for trophic studies.

Keywords: Anura, Hylidae, Hyla pulchella, diet, trophic ecology.

Introduction

Amphibians play a pivotal role linkingaquatic and terrestrial ecosystems. However,

studies in diets of adult amphibians based onprey availability are scarce, particularly intemperate ecosystems (Hirai and Matsui 1999).Although Schoener (1974) recommended thatthe study of a trophic niche of species shouldinclude the availability of preys, only a fewstudies have done so (Toft 1980, 1981, Jones1982, MacNally 1983, Lizana et al. 1986). This

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failure may be significant, due to the potentialinfluence of prey distribution on the feedingbehavior the frogs (Labanick 1976, Hirai andMatsui 1999).

An extensive literature has been publishedabout the trophic niche of many Neotropicalanurans, although dietary preference were notconsidered because the environmentalavailability was unknown (Zug and Zug 1979,Guix 1993, Filipello and Crespo 1994,Lajmanovich 1995, 1996, Teixeira et al. 1999,Brandão et al. 2003, Santos et al. 2003, Teixeiraand Vrcibradic 2003, Maneyro et al. 2004). Themost extensive works in niche overlap betweentemperate South American amphibian speciesare those from Argentinean localities, likeBuenos Aires (Basso 1990) and Corrientes(Duré 1999, Duré and Kehr 2001). Recently,Peltzer and Lajmanovich (1999) studied dietvariation between two populations of hylid frogsat Santa Fé; da Rosa et al. (2002) analyzed theseasonal changes in the diet of four anuranspecies in Uruguay. None of the above-mentioned works considered prey availability,therefore the observed patterns of preyconsumption cannot be explained.

The tree frog Hyla pulchella Duméril andBibron, 1841 is one of the most commonanurans in Uruguay. This species is a middle-sized hylid (up to 50 mm SVL in adult females)that lives in natural wetlands but can also befound in anthropized environments (Achavaland Olmos 2003). This species shows repro-ductive activity during the whole year in naturalor artificial ponds, and the egg clutches are laidin a gelatinous mass attached to aquatic vegeta-tion (Langone 1994). This reproductive modecan be described as Type I (sensu Duellman andTrueb 1994), which means a non-specializedbehavior. Bibliographic references indicate thatH. pulchella is an insectivorous frog, ingestingmainly hymenopterans and dipterans (Gallardo1987, Basso 1990, Langone, 1994).

The aim of this work was to describe thediet of H. pulchella and its variation in threemicroenvironments and along one year divided

Maneyro and da Rosa

into two seasons. We also explored how changesin seasonal and microenvironmental preyavailabilities could be reflected in the diet ofthis frog.

Material and Methods

Fieldwork was conducted in a privatereserve (Reserva Privada de Fauna y Flora “ElRelincho”) located in southern Uruguay (34º20’S, 57º00’ W) (Figure 1). This area has a tempe-rate climate (average annual temperature 16.6°C, cumulative annual rainfall 1031.6 mm) withfour seasons. This is a protected area with amanagement plan that includes the preservationof natural ecosystems with some extensive cattleactivities. Many ponds were built in grasslandareas several years ago. The specimens (frogsand invertebrate prey) were collected in three ofthese ponds (Ponds 1, 2, and 3), which werebuilt on the same stream (as a way to minimizeenvironmental variability). In each pond, weidentified three microenvironmental categories:straw zone, wet grassland and bank (Figure 2).The straw zone was determined as the placewhere the pond receives the water supply,characterized by dense vegetation, includingmainly Scirpus sp. and Typha sp. The wetgrassland covered both margins of the pond; itsflora was dominated by grass and aquaticvegetation (Azolla, Polygonum). This locationwas periodically flooded after heavy rains andthus is characterized by a fluctuating hydricregime. The bank was a sloping artificial grassdam where water retention occurs (2 – 3 mhigh). These microenvironments were classifiedto reflect the assemblage of the invertebrates(from here “invertebrate assemblage”).

The invertebrate assemblage was estimatedthrough pitfall traps, consisting of 300 ml canswith a solution of liquid soap and 10% formalin.In all ponds, five traps were placed in eachmicroenvironment, resulting in a design withforty-five traps (5 ´ 3 ´ 3). The traps wereactivated during two successive nights, monthly,from January to December 1998. One of the

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For all statistical and descriptive analysisabout the trophic ecology of the frogs, onlyitems in the diet were considered as availableprey (named as “available assemblage”),because not all the groups in the invertebrateassemblage are potential preys. The invertebrateassemblage is therefore a good biologicaldescriptor of the microenvironments but it doesnot reflect the real availability of prey for thefrogs (i.e., snails).

Spatial and temporal variation was studiedfor both prey availability and diet of the frogs.The spatial variation was evaluated within thedefined microenvironments (straw zone, wetgrassland, bank). The temporal variation wasexplored by grouping observations as was donein other studies on species of temperate region(da Rosa et al. 2002, Maneyro et al. 2004). Twoseasons were defined: a cold season (datacollected from April to September, meantemperature below 17°C) and a warm season(from January to March, and October toDecember, mean temperature above 18°C).

All analyses were performed using theStatistica 5.5 (StatSoft 1999). The set of fivetraps and two days were grouped as a singleobservation, resulting in 108 independentreplicates (three microenvironments in each ofthe three ponds during 12 months).

Temporal and spatial changes in the diet of Hyla pulchella (Anura, Hylidae) in Uruguay

Figure 2 - Schematic representation of one of the ponds.B, bank; WG, wet grassland; SZ, straw zone.

Figure 1 - Study Area. References in the detailed map: a.Juan Lacaze City; b. Ecilda Paulier Town; c.San José de Mayo City; d. Cardona City.Shadded lines represent National routes. Solidlines are rivers and streams.

goals of this study was to verify if zonificationbased on invertebrate assemblage was consistentwith the biophysical architecture of the ponds.To do so, we tested differences amonghypothesized microenvironments and ponds by amultivariate analysis of variance (MANOVA)and described them by a Discriminant Analysis(DA). For these analyses the independentvariables were the microenvironments (threestages: straw zone, wet grassland, and bank) andthe ponds (Ponds 1, 2, and 3). The frequenciesin each invertebrate group were the dependentvariables (for MANOVA only the variables inthe model obtained from the DA were tested).The assumptions of variance homogeneity andnormality were tested by the Levenne test andthe Shapiro Wilks’ W test, respectively.

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Maneyro and da Rosa

The frogs were collected during the sameperiod; date, pond number andmicroenvironment type were recorded. Eachfrog constituted an independent replicate for thespatial analysis. The anurans were caught byhand and immediately euthanized. Allprocedures were approved by the HonoraryComission for Animal Experimentation at theUniversity of Uruguay. Specimens weredeposited in Vertebrate Zoology Collection,Facultad de Ciencias, Uruguay (ZVCB). Theentire alimentary tract was removed in eachspecimen to obtain individual prey (Schoener1989). The preys found in each gastrointestinalcontent were taxonomically determined to Orderlevel recording their frequencies. Taking intoaccount the biases reported by Magnusson et al.(2003), the volume of each prey was estimatedby the ellipsoid method proposed by Dunham(1983). Diversity of diet was calculated by theShannon-Weaver Index (Shannon and Weaver1949), H = –S p

i x (log p

i), where p

i is the

proportion of each prey item found in the diet.Dietary preference was calculated by Ivlev

Index (Ivlev 1961) II = )nr(

)nr(

ii

ii

+−

, where ri is

the proportion of each prey item found in thediet and n

i is the proportion of each prey item in

the available assemblage (from –1 for avoidedpreys to +1 for preferred preys). Bothparameters were calculated for the overallsample and for each microenvironment andseason sub-samples.

As the observed richness depends on thetotal number of observations (Gotelli andGraves 1996), the expected richness for eachsample size was estimated using a rarefactionnull model (Magurran 1988, Krebs 1989).This model can be applied to calculate theexpected richness in several samples for thesame sample size (Gotelli and Graves 1996).The model is based on the hypergeometricdistribution and the expected values can becalculated as follows:

expected richness = ,

where S is the total number of observed itemsin diet or in available assemblage samples, N is thetotal sample size, m

i is the total number of

individuals of the “i” item and n is the sample.Additional DAs were performed in order to

understand the environmental and seasonalchanges in the available assemblage and in theconsumed prey. The Kruskal-Wallis analysis byitems was used as “a posteriori” test(significance at 0.05). To avoid Type 1 error(because of high number of analyzed variables)the alpha value for significant results wascorrected by Bonferroni test.

Results

Microenvironmental Variation of theInvertebrate Assemblage

A total of 10365 invertebrates wereclassified into 21 categories including 19arthropod orders (four Arachnida, twoMyriapoda, 11 Hexapoda, and two Crustacea),annelids and insect larvae. Prey availabilityvaried among the three microenvironments, aswas suggested by the DA classification (Figure3). The items (variables) included in the model[F(

14,198) = 2.35, p < 0.005] were Hymenoptera,

Homoptera, Collembola, Diptera, Acarina,Coleoptera, and Isopoda. This microenvi-ronmental effect was also detected by theMANOVA (Wilks’ l = 0.71, F = 1.93, df =18,182, p = 0.02). In this analysis, neither pondeffect (Wilks’ l = 0.82, F = 1.07, df = 18,182, p= 0.39) nor interaction effect (Wilks’ l = 0.72, F= 0.89, df = 36,342, p = 0.65) were detected.Therefore, the three ponds were considered asreplicates, and the microenvironments, as threetreatments.

∑

−

−S

1

i

n

N

n

mN

1

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The Available Assemblage:microenvironmental and seasonal changes

The available prey assemblage was esti-mated based on 9543 individuals and includedAraneae, Collembola, Orthoptera, Coleoptera,Hymenoptera, Diptera, Lepidoptera, Hemiptera,Homoptera, Dictioptera, larvae, and Isopoda.The most frequent item was Collembola(65.1%), followed by Hymenoptera (23.4%) andAraneae (6,2%). The excluded items (present inthe invertebrate assemblage) were Scorpiones,Acarina, Opiliones, Chilopoda, Diplododa,Isoptera, Crustacea other than Isopoda, andAnnelida. The microenvironments could bedistinguished by available prey assemblage[F(

18,50) = 1.88, p < 0.04]. Two roots were

extracted and graphically presented in Figure4A, showing these groups (microenvironments).The variables in the model were Araneae,Collembola, Homoptera, Hymenoptera, Diptera,Dictioptera, Lepidoptera, Coleoptera, andlarvae. However, none of these taxa showedstatistically significant variation in theirfrequency between microenvironments after theKruskal-Wallis test (Table 1).

The available assemblage in the warmseason differed from that in the cold season(Figure 4B) [F(

8,99) = 12.28, p < 0.000]. The

variables in the model were Araneae,Collembola, Homoptera, Hymenoptera, Diptera,Dictioptera, Hemiptera, and larvae. OnlyAraneae and Hymenoptera showed significantdifferences between seasons by the Kruskal-Wallis test (Table 1).

Overall Diet

A total of 105 frogs were captured, 35 ofwhich had empty digestive tracts, and 256 preyitems were identified. The average number ofprey items per individual (N = 70) was 3.66 ±4.05 (x ± SE), ranging from 1 to 28 (Table 2).Four arthropod orders predominated in number(82.5%) in the overall sample. Araneae showedthe largest proportion in number, followed by

Figure 3 - Graphic representation of the first two roots ofthe Discriminant Analysis in the environmentalavailability (Method: Forward Stepwise, F toremove = 0, F to enter = 1). F(

14,198) = 2.35 (p

< 0.005). Solid circles, bank; Open circles,straw zone; Crosses, wet grassland.

Figure 4 - Graphic representation of the roots of theDiscriminant Analysis with availablecommunity’s data (Method: Forward Stepwise,F to remove = 0, F to enter = 1). A. first tworoots of microenvironmental avaliability’s data,F(

18,50) = 1.88 (p < 0.004). Solid circles, bank;

Open circles, straw zone; Crosses, wetgrassland. B. the only one extracted root ofseasonal avaliability’s data, F(

8,99) = 12.29 (p

< 0.000). C, cold season; W, warm season.

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Table 1 - Results of the Kruskal-Wallis tests for each variable in the model of the Discriminant Analysis bymicroenvironment (bank, straw zone, and wet grassland) and by season (warm season: from October to March,cold season: from April to September) for the available community. H, Kruskal-Wallis statistics; df, degreeof freedom; p, probability. * indicates significant differences. Alpha values (Bonferroni test corrected) were0.005 (microenvironmetal analyses) and 0.006 (Seasonal analyses).

MICROENVIRONMENT SEASON

H df p H df p

Homoptera 1.06 2 0.59 2.75 1 0.10Lepidoptera 3.50 2 0.17Coleoptera 0.84 2 0.66Larvae 0.95 2 0.62 2.66 1 0.10Collembola 1.57 2 0.46 1.26 1 0.26Hymenoptera 1.61 2 0.45 26.30 1 * 0Dictioptera 3.83 2 0.15 4.12 1 0.04Araneae 0.77 2 0.68 3.36 1 * 0Diptera 0.14 2 0.93 0.19 1 0.66Hemiptera 5.81 1 0.02

Table 2 - Diet composition of Hyla pulchella in each microenvironment. SZ (straw zone), WG (wet grassland), B (bank),OS (Overall Sample). Total numbers of preys were 91 (SZ), 93 (WG), and 72 (B). Total numbers of frogswere 22 (SZ), 28 (WG), and 20 (B). Total volumes of preys (in mm3) were 2611.99 (SZ), 1303.38 (WG), and1518.90 (B). For the overall sample total number of preys was 256, total number of frogs was 70, and totalvolume of preys was 5434.27 mm3.

NUMERICAL VOLUMETRICFREQUENCY (%) PROPORTIONS (%) PROPORTIONS (%)

SZ WG B OS SZ WG B OS SZ WG B OS

ArachnidaAraneae 54.5 6.7 6.0 58.6 22.0 32.3 31.9 28.5 13.4 35.2 17.0 19.6HexapodaCollembola 7.1 2.8 2.2 0.8 < 0.1 < 0.1Orthoptera 9.1 7.1 1.0 8.6 2.2 2.2 2.8 2.3 2.1 4.3 2.7 11.4Coleoptera 22.7 28.6 3.0 27.1 6.6 1.8 13.9 1.2 2.7 9.9 11.3 6.8Hymenoptera 13.6 21.4 1.0 15.7 37.4 1.8 2.8 18.0 2.1 3.3 0.8 2.0Diptera 27.3 53.6 45.0 42.9 2.9 28.0 29.2 25.8 7.6 15.1 15.4 11.6Lepidoptera 13.6 4.3 3.3 1.2 19.0 9.1Hemiptera 5.0 1.4 2.8 0.8 1.4 0.4Homoptera 14.3 1.0 8.6 4.3 4.2 2.7 3.8 11.1 4.0Dictioptera 4.5 3.6 2.9 1.1 1.1 0.8 1.8 9.5 3.2Larvae 13.6 17.9 15.0 15.7 3.3 7.5 4.2 5.1 29.0 14.5 2.2 23.1CrustaceaIsopoda 4.5 3.6 2.0 8.6 3.3 1.1 8.3 3.9 4.3 4.4 2.1 8.7

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Diptera, Hymenoptera, and Coleoptera (Table2). In the volumetrical analysis four invertebrategroups were predominat (65.7%), larvae (mainlylepidopterans larvae) comprised the largestproportion, followed by Araneae, Diptera, andOrthoptera (Table 2).

The diversity of the diet calculated for theoverall sample was 0.82 in frequencies and 0.92in volume. The rarefaction curve indicated thatthe maximum expected richness was 12 items(Figure 5). Additionally, this curve showed thatthe calculated diet of the frog is richer thanenvironmental calculated availability, thereforeany kind of selectivity could be occurring. Themost preferred preys sensu Ivlev Index were

larvae (II = 0.96) followed by Isopoda (0.95),Dictioptera (0.90), Lepidoptera (0.90), andDiptera (0.87). Collembola (-0.98) was the mostavoided prey followed by Hymenoptera (-0.13).

Microenvironmental and Seasonal Variationin Diet

The average numbers of prey items perindividual were 4.14 ± 5.86 (range 1–28) in thestraw zone, 3.32 ± 2.74 (1–12) in the wetgrassland, and 3.60 ± 3.25 (1–11) in the bank (F= 0.25, df = 2, p = 0.78). Araneae was the mostfrequent category (%) in the threemicroenvironments (straw zone = 54.5, wetgrassland = 60.7, bank = 60.0), followed byDiptera (27.3, 53.6, 45.0) and Coleoptera (22.7,28.6, 30.0). In the wet grassland and the bankresults for numerical proportions were similar tothose observed in frequency. However, the mainprey item (highest numerical proportion) in thestraw zone was Hymenoptera (37.4), followedby Araneae (22.0) and Diptera (20.9). Takinginto account volumetrical proportions, the mostconsumed item in the straw zone were larvae(29.0), followed by Orthoptera (20.1), andLepidoptera (19.0). In the wet grassland, themain items were Araneae (35.2), Diptera (15.1),and larvae (14.5), while in the bank were larvae(20.2), Isopoda (20.1), and Araneae (17.0).

The diversity of the diet based in frequen-cies for each microenvironment was 0.73, 0.78,and 0.77 in straw zone, wet grassland, and bank,respectively; and in volume was 0.80, 0.82, and0.84. For each microenvironment, therarefaction curves indicated that the wetgrassland was the richest (Figure 5). The bankand the straw zone were similar, but bank wasricher than straw zone.

The most preferred preys sensu Ivlev Indexat the straw zone were Isopoda (0.93) andLepidoptera (0.93), at the wet grassland werethe larvae (0.97) and Dictioptera (0.94), whereasat the bank were Isopoda (0.98) and Diptera(0.93). When consumed (only at wet grassland),Collembola was the most avoided prey (-0.98),

Figure 5 - Graphic representation of rarefaction analysis.(A) Overall sample for diet and environmentalavailability; (B) diet in each of the threemicroenvironments, (C) diet in each of the twoseasons (Cold Season = April to September;Warm Season = October to March).

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Maneyro and da Rosa

followed by Hymenoptera at everymicroenvironment.

A graphic representation of the DA is shownin Figure 6. The variables in the model wereHomoptera, Orthoptera, Lepidoptera,Coleoptera, larvae, and Collembola, butsignificant differences between groups were notfound [F(

12, 34) = 1.33, p < 0.25]. The

significance of each variable in the model wasevaluated by Kruskal Wallis test, and nosignificant differences were found among them(Table 3).

The total number of frogs and preys in eachseason is given in Table 4. The average numberof prey items per stomach was 3.79 ± 3.41(range 1–11) in the cold season, and 3.59 ± 4.38(1–28) in the warm season (t = -0.2, df = 68, p =0.85). Araneae was the most frequent item inboth seasons (70.8 and 52.2 respectively in coldand warm season), followed by Diptera (54.2,37.0) and Coleoptera (29.2, 26.1). In numericalproportions, the main prey item in the coldseason was Araneae (32.6), followed by Diptera(28.9) and Coleoptera (14.1). However, in thewarm season the major numerical proportionwere showed by Hymenoptera (36.4), followedby Araneae (24.0) and Diptera (22.3). Involumetrical proportions the main item in thecold season were the larvae (35.3), followed byAraneae (24.5) and Isopoda (14.2), whereas inthe warm season were Lepidoptera (23.7),Orthoptera (22.3), and Diptera (16.8).

The diversity of the diet calculated infrequencies in each season were 0.74 and 0.77respectively in cold and warm season, and involume were 0.73 and 0.89. The rarefactioncurves for each season indicated that the warmseason is richer than the cold season (Figure 5).

The most preferred prey sensu Ivlev Indexat the cold season were Isopoda and larvae (bothreach value 0.98 for the preference Index),followed by Diptera (0.85), Araneae (0.78), andOrthoptera (0.77). At the warm season, the mostpreferred preys were the larvae (0.95), followedby Lepidoptera (0.92), Diptera (0.90), andDictioptera (0.88). Collembola was onlyconsumed in the warm season, however, as inthe overall analysis, it was the most avoidedprey (-0.94). In the case of Hymenoptera, it wasavoided along both seasons (-0.86 and -0.07 incold season and warm season respectively).

Only one root could be extracted from theDA and its distribution between groups(seasons) is shown in Figure 6. The variables inthe model were Hymenoptera, Coleoptera,Homoptera, Orthoptera, Lepidoptera andDiptera; significant differences between groupswere found [F(

6, 18) = 2.63, p < 0.05]. No

Figure 6 - Graphic representation of the roots of theDiscriminant Analysis with the microenviron-mental and seasonal variation of consumedpreys’ data (Method: Forward Stepwise, F toremove = 0, F to enter = 1). A. first two rootsof diet’s data by microenvironment, F(

12, 34) =

1.33 (p < 0.25). Solid circles, bank; Opencircles, straw zone; Crosses, wet grassland. B.the only one extracted root of diet’s data byseason, F(

6,18) = 2,63 (p < 0.05). C, cold

season; W, warm season.

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MICROENVIRONMENT SEASON

H df p H df p

Homoptera 3.04 2 0.22 0.55 1 0.46Ortoptera 0.71 2 0.70 0.49 1 0.48Lepidoptera 2.13 2 0.35 1.08 1 0.30Coleoptera 0.61 2 0.73 4.57 1 0.03Larvae 0.88 2 0.65Collembola 1.78 2 0.41Diptera 0.55 1 0.46Hymenoptera 5.65 1 0.01

Table 3 - Results of the Kruskal Wallis tests for each prey item in the model of the Discriminant Analysis bymicroenvironment and season. H, Kruskal Wallis statistics; df, degree of freedom; p, probability; * significantdifferences. Microenvironmental and seasonal analyses (Bonferroni test corrected), alpha = 0.009.

NUMERICAL VOLUMETRICFREQUENCY (%) PROPORTIONS (%) PROPORTIONS (%)

CS W S CS WS CS WS

ArachnidaAraneae 70.8 52.2 32.6 24.0 24.5 12.0HexapodaCollembola 8.3 1.5 <0.1Orthoptera 8.3 8.7 2.2 2.5 4.6 22.3Coleoptera 29.2 26.1 14.1 5.8 9.2 3.1Hymenoptera 4.2 21.7 1.5 36.4 1.0 3.7Diptera 54.2 37.0 28.9 22.3 8.3 16.8Lepidoptera 6.5 2.5 23.7Hemiptera 2.2 1.5 0.7Homoptera 4.2 10.9 3.0 2.5 2,3 6,7Dictioptera 4.3 1.7 8,2Larvae 16.7 15.2 7.4 2.5 35,3 3,7CrustaceaIsopoda 25.0 7.4 14,2

Table 4 - Diet composition of Hyla pulchella in each season. CS, cold season; WS, warm season. Total number of preys= 91 (CS) and 165 (WS). Total number of frogs = 46 (CS) and 24 (WS). Total volume of preys (in mm3) =1945.17 (CS) and 3489.10 (WS).

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significant differences were found betweengroups in the variables in the model (results ofKruskal-Wallis test are showed in Table 3).

Discussion

An organism can be classified as generalistor specialist depending on the broadness of theirtrophic niche, whereas to be an opportunist orselective it is related to capture strategies (Jaksic2001). Hyla pulchella has been considered ageneralist species (Basso 1990, da Rosa et al.2002), as confirmed by the results of this study.However, this species is selective for some oftheir preys (taking into account availability inthe environment). We inferred selectivity fromthe positive values of the Ivlev Index for somecategories (i.e. larvae, Isopoda, Dictioptera,Lepidoptera, Diptera) and the negative valuesfor other categories (i.e. Collembola, perhapsbecause of their small size, or Hymenoptera,generally ants with formic acid). This result isconsistent with other studies including estimatesof prey availability (e.g., Toft 1980, 1981). Thisis in agreement with the rarefaction curves; theyshowed an expected richness (predicted by thenull mode) higher in the diet than in theavailable assemblage (Figure 5). This factreaffirms the importance of estimating preyavailability when hypothesizing about feedingstrategies.

The absence of variation in the diet in thespatial analysis, while the available assemblagediffers among microenvironments, could beinterpreted as the expression of a selectivebehavior. However, spatial changes in theavailability were detected mainly on the wholeanalysis, and significant differences by itemwere not detected.

Considering the temporal analysis, the preyassemblage also differs between seasons. Thesedifferences were detected both in the wholeanalysis and when the items are comparedindividually. This pattern is reflected in the diet,and in agreement with da Rosa et al. (2002),differences among seasons have been observed.

Seasonal changes have been observed indiet not only in amphibians but also in reptiles(Lizana et al. 1986, Magnusson and Vieira1993, Feria Ortiz et al. 2001). The seasonalvariation indicates that diet of H. pulchellacould be interpreted as a response to theavailable assemblage. This pattern has beenreported for others frogs (Hirai and Matsui,1999, 2000, 2001). The diversity of the diet ofthis species did not vary seasonally, although itsdiet did so. One of the predictions of the nicheoverlap hypothesis is that the changes in the axisof the resources could be associated to thepresence of other species sharing that resource,minimizing this overlap (Jaksic 2001). Thechanges observed in the diet of H. pulchellamay also be related with the presence of otheranuran species in the assemblage (Maneyro2000).

The prey-capture strategies are related withtwo opposite tactics: opportunistic or selective.A predator that exibits electivity for its preyshould look for or wait for the most profitableone from an energetic point of view (Jaksic2001). Huey and Pianka (1981) proposed thatprey type in the diet is correlated with foragingmode of the predators. If the prey is mobile thepredator will behave in a sit-and-wait way, whileif the prey possesses sedentary habits, then itwill be captured by an active predator. Thebroad diversity of the diet (H

frequency = 0.82 and

Hvolume

= 0.92) and the predominant consumptionof Araneae, Coleoptera and Diptera (medium-sized and mobile preys), suggest that H.pulchella is a sit-and-wait predator (Toft 1981),as would be expected for a hylid frog (Freed1980).

On the other hand, the higher consumptionof Hymenoptera (mainly ants) during the warmseason (36.4%) contradicts this pattern, becauseants are an aggregated resource and it wouldimply an active foraging strategy (Toft 1981). Inthe warm season the frogs ingest hymenopteransin approximately the same proportion as theyoccur in the environment, but when this itembecomes twice as abundant in the available

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assemblage (cold season), it is strongly avoided.Our results do not state whether the frogs searchactively for this resource. The leptodactylidZachaenus parvulus shows a high consumptionof ants (Van Sluys et al. 2001) although theleptodactylids belong to the non-ant specialistguild. Perhaps this pattern reflects mixedcapture strategies. The ingestion of ants wasinterpreted historically as a way to incorporateskin toxins for antipredatory functions (Caldwell1996). In this case, the myrmecophagy may havephysiological consequences, as proposed foranother hylid, Phyllomedusa hypocondrialis(Peltzer et al. 2000). Another interpretation maybe the behavioral consequence of the combinedprey search strategy (active and sit-and-wait).This frog may behave as an active forager whenit finds an ant nest or trial, like some little leaflitter frogs, such as Dendrobates pumilio(Donnelly 1991) and becoming in that situation,a sit-and-wait predator.

In conclusion, Hyla pulchella presents ageneralist diet that responds in great measure tothe seasonal variation of the available prey, butwith possible trophic interactions with otherfrogs. This species possesses preference (andthen selectivity) for several prey types, probablybased on a sit-and-wait strategy of capture.

Acknowledgements

We are grateful to the colleagues andstudents of the Sección Zoología Vertebrados(Facultad de Ciencias, UDELAR) for valuablehelp, especially to Prof. Federico Achaval forlogistical support during field and laboratoryworks. We also thank to Axel Kwet, CatherineToft and two anonymous reviewers for criticalsuggestions on the manuscript. To ArleyCamargo and Andrés Canavero for suggestions,to Guadalupe Tiscornia and Ronald McGregorfor language corrections. Guillermo Maccióallowed us to collect and stay at ReservaPrivada de Fauna y Flora “El Relincho”. RMreceived a grant from PEDECIBA, Biología andhas a doctoral fellowship from Coordenação de

Aperfeiçoamento de Pessoal de Nível Superior(CAPES) at the Pontifícia Universidade Católicado Rio Grande do Sul, Brazil.

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