J. Zool., Lond. (2002) 258, 269±276 # 2002 The Zoological Society of London Printed in the United Kingdom DOI:10.1017/S0952836902001371

Seasonal patterns of reproduction and abundance of leaf litter frogs in a Central American

James I. Watling* and Maureen A. Donnelly Florida International University, Department of Biological Sciences, University Park, Miami, FL 33199, U.S.A. (Accepted 16 November 2001)

Abstract Patterns of reproductive phenology and temporal variation in species composition and age structure were investigated for a sample of terrestrial leaf litter frogs from a lowland tropical rainforest in north-eastern Costa Rica. Recruitment of most species showed a seasonal pattern in which the growth of juveniles occurred during the dry season. The phenology of the assemblage was also seasonal, with a peak in abundance during the dry season. Variation in abundance was driven by seasonal patterns of juvenile recruitment in one species, Eleutherodactylus brandsfordii. We suggest that the timing of reproduction and patterns of frog phenology may be tied to the availability of arthropod prey items. A comparison of our data with data collected at other rainforest sites in Central America and the Amazon basin of South America indicates that patterns of recruitment and abundance, while correlated with arthropod abundance on both continents, show divergent seasonal patterns. This and other studies indicate that peaks in abundance and recruitment of juvenile frogs are concentrated in the dry season in Central America, whereas in South American , the wet season is the period of highest abundance and juvenile recruitment. We suggest that the length and severity of dry periods in the Amazon basin limits the ability of terrestrial frogs to reproduce successfully, while in Central America a more benign dry season, while strong enough to create distinct seasonal trends in the phenology of rainforest animals, is not strong enough to prohibit frogs from recruiting juveniles during the dry season.

Key words: age structure, amphibians, Costa Rica, reproductive phenology, species composition, temporal variation

INTRODUCTION species tropical assemblages (but see Stiles, 1980; Gascon, 1991a). If species composition and age struc- Field researchers have described seasonal reproductive ture differ throughout the year, interactions among patterns among terrestrial at several tropical species (e.g. predator±prey dynamics) may also be ex- locations (Fogden, 1972; Leigh, Rand & Windsor, 1982 pected to vary seasonally. Therefore, our understanding and references therein; van Shaik, Terborgh & Wright, of how communities are structured, as well as the 1993; Sinclair, Mduma & Arcese, 2000; Wikelski, Hau interactions among organisms at a site, hinges in part & Wing®eld, 2000). Data indicate that many tropical on understanding how individuals and species are dis- species time their reproduction to coincide with peaks in tributed in time. food resources, which generally occur during the rainy Crump (1974) quanti®ed reproductive patterns season (Russell, 1982; Goldizen et al., 1988; Poulin, among 74 sympatric species of frogs at a site in Amazo- Lefebvre & McNeil, 1992). Some species will reproduce nian Ecuador, making her study the most thorough during the dry season, however, if preferred food items description of anuran reproductive ecology in the Neo- are available at this time (Sinclair et al., 2000). Although tropics. Among 22 species of leaf litter frogs in her there are several studies describing seasonal patterns of sample, 11 (50%) were continuous breeders, two (9%) reproduction among individual species of tropical verte- were sporadic breeders (one of which bred sporadically brates, there are relatively few data quantifying seasonal during the wet season, while the other one was a variation in the composition and dynamics of multi- sporadic dry season breeder), and nine (41%) were unknown with respect to the timing of reproduction. In *All correspondence to: J. I. Watling. the central Amazon, Moreira & Lima (1991) described E-mail: jwatli01@®u.edu seasonal patterns of reproduction in four species of leaf 270 J. I. Watling and M. A. Donnelly litter frogs. They found that two species bred primarily dissected and gonad size and condition were recorded. in the wet season, whereas the other two species were For females of the genera Eleutherodactylus and Gastro- dry-season breeders. These studies show that Amazo- phryne, the number of mature ova contained in the nian leaf litter frogs exhibit some variability in the ovaries was counted. An ocular micrometer was used to timing of reproduction, though the most complete data measure the width of left and right oviducts at mid- set available indicates that most terrestrial species breed length and their condition described as straight, semi- continuously or during the wet season. However, these convoluted, or convoluted. Convoluted oviducts may two studies do not necessarily represent broad patterns indicate sexual maturity (Donnelly, 1999). For sub- of anuran reproductive phenology from throughout the adult females the presence of immature (unpigmented) Neotropics. We are interested in determining whether follicles was noted and the width and condition of left seasonal patterns of reproduction are characteristic of and right oviducts were recorded. For males, the length anurans at one site in Central America and to what and width of left and right testes were recorded. Total extent there is variation in the composition of the volume of the testes was calculated using the equation anuran community throughout the year. Therefore, our for the volume of a prolate spheroid (Johnson, 1999): goals in this study are: (1) to quantify the phenology of reproduction of several abundant frog species from a testis volume = 4/3p(1/2 testis length)(1/2 testis width)2. rainforest in northeastern Costa Rica and compare our ®ndings to what is known from South America; (2) to The volume of each testis was calculated separately and describe temporal patterns of species composition and then the 2 values combined to estimate total testis age structure based on the abundance of frogs in volume. monthly quadrat samples. Frogs were placed into 1 of 3 age±sex categories ( juvenile, adult male, or adult female) based on body size, gonad condition, and the presence of secondary MATERIALS AND METHODS sexual characteristics. Individuals were classi®ed as adult females if SVL was at least the minimum size at A sample of anurans collected over 14 months from which mature ovarian eggs were recorded for each November 1973 to December 1974 at the La Selva species. For males of all species except E. biporcatus, the Biological Station, Heredia Province, Costa Rica was minimum SVL at which vocal slits were noted was the examined. Most of the 1536 ha of the La Selva reserve is size at which individuals were considered adults. Since in primary forest, with the rest occurring in secondary E. biporcatus lacks vocal slits and nuptial pads, we were forest, pasture and abandoned plantations (McDade & not able to assign individuals to sex classes using Hartshorn, 1994). Rainfall at La Selva averages secondary sexual characteristics. Because E. biporcatus 3962 mm, with a short dry season from February to is comparable in size to E. rugulosus, we chose 25 mm April (Sanford et al., 1994). (approximately the size of the smallest adult male in Frogs were obtained in three ways. Most frogs E. rugulosus) as the minimum SVL of adult males in (n =1690) were collected in 1-ga pitfall traps containing E. biporcatus. picric acid. Traps were placed 10 m apart along a 100 m transect and emptied every 4±6 h during the 4 days per month that traps were opened. Some frogs (n = 1326) Reproductive phenology of individual species were collected from 868 m litter plots, which were sampled monthly by 2±4 observers. Six different focal The reproductive phenology for 6 species of frogs (Bufo litter plots were sampled each month during the study haematiticus, E. biporcatus, E. ®tzingeri, E. mimus, E. period, with the exception that the ®rst 6 quadrats were talamancae, and G. pictiventris) was quanti®ed based on sampled in late November and early December 1973. monthly variation in mean body size and mean testis November and December 1973 samples were combined volume. Variation in the size of the ovarian complement into 1 period, so samples used to describe patterns of during the study period was not analysed because of the community phenology re¯ect 13 sample periods across small sample sizes for adult females. To maximize the 14 months. The litter plots and pitfall-trap transects sample size available for analyses of body size and testis were located in primary forest and in an adjacent fallow size variation, data were included from individuals cacao grove. Finally, 508 individuals were collected collected using all 3 sampling methods. opportunistically in the laboratory clearing and along Variation in body size across the 14 months of the trails in both habitat types. All captured frogs were study was analysed because months with relatively low placed in plastic bags and transported to the laboratory SVLs may indicate periods of recruitment to the adult where they were killed by submersion in a chlorobutanol age classes (Donnelly, 1989, 1999). Because our data did solution, then preserved in 10% formalin and stored in not meet the assumption of equal variance across all 70% ethanol. months of the study, a Kruskall±Wallis nonparametric The snout±vent length (SVL) of each frog was mea- test was used to determine how mean body size varied sured to the nearest 0.5 mm with a plastic ruler. The among months for males, females, and juveniles of each presence of secondary sexual characteristics, including species. nuptial pads and vocal slits, was recorded. Frogs were Mean testis volume of all individuals for each month Leaf litter frog seasonality 271 was used as an indirect measure of the reproductive 35 Eleutherodactylus biporcatus activity of males. Seasonal variation in testis size has 30 been documented in other tropical taxa (Ka- 25 namadi & Jirankali, 1992; Kappeler, 1997; Wikelski et 20 al., 2000). Here it is assumed that signi®cant changes in 15 mean testis volume per month re¯ect differential allot- 10 N D J F M AMJ JAS O N D ment of energy to reproductive activity (Kanamadi & 50 Eleutherodactylus mimus Jirankali, 1992). Because testis volume was linearly 40 related to male SVL, a 1-way analysis of covariance 30 (ANCOVA), using (ln) SVL as a covariate to determine 20 if total testis volume varied signi®cantly by month once 10 the in¯uence of body size on testis volume was removed. 0 Months which did not have a minimum of 3 data points N D J F M AMJ JAS O N D 40 were excluded from this analysis. Eleutherodactylus talamancae 35 30 25 Snout–vent length (mm) Species composition and age structure 20 15 Data from quadrat sampling were used to describe 10 N D J F M AMJ JAS O N D patterns of abundance across the study period for the 35 Gastrophryne pictiventris most common leaf litter species at La Selva. Quadrats 30 are an effective method for sampling leaf litter amphi- 25 bians (Jaeger & Inger, 1994). Only the quadrat data 20 were used because more species were sampled using 15 this method than using pitfall traps, and the data are 10 easily standardized in terms of number of individuals/ N D J F M AMJ JAS O N D plot. The analyses described below include 5 species Month represented by > 20 individuals from quadrat sam- Fig. 1. Monthly variation in mean body size for juveniles of pling, including D. pumilio and E. brandsfordii, for four species of frogs. whom individual patterns of reproductive phenology have been described previously (Donnelly, 1989, 1999). study period. All other statistical methods were con- First, a 2-way analysis of variance (ANOVA) using ducted using SPSS 8.0 (SPSS, 1997). months and species as factors and quadrat counts as the dependent variable was used to test hypotheses about the distribution of species throughout the study RESULTS period. This analysis was run twice, once including all 5 species in the model, and a second time excluding Reproductive phenology E. brandsfordii (the most abundant frog at La Selva) to determine if monthly variation in abundance was attri- Adults of all six species showed no signi®cant differ- butable to E. brandsfordii alone. Post-hoc tests used ences in body size across the 14 month study period. Dunnett's C to determine which months and species Juveniles of four species, however, showed signi®cant differed signi®cantly from one another in quadrat monthly variation in body size (for G. pictiventris, counts. Another 2-way ANOVA with months and age± H = 30.19, P = 0.001; for E. biporcatus, H = 35.86, sex classes as factors and quadrat counts as the depen- P = 0.001; for E. mimus, H = 23.41, P = 0.003; for dent variable was used to investigate the temporal E. talamancae, H = 16.03, P = 0.042, Fig. 1). In three distribution of age±sex classes. As before, post-hoc tests species, juvenile body size was low at some point in the were conducted using Dunnett's C to determine which dry season (January±April) and increased monthly months and age-sex classes differed signi®cantly from through the wet season August±September 1974, when one another. the signal dampened. In E. talamancae, SVL was low w2 statistics were calculated to determine if the ap- during the dry season and increased every month from pearance of individuals in a species or age±sex class was March to September 1974 with the exception of June, evenly distributed throughout the year. First, we tested when SVL was lower than April and May. the hypothesis that the distribution of each species Males of most species did not show variation in among months did not differ from an even distribution gonadal condition during the 14-month study. Only throughout the study period, calculating a w2 value for G. pictiventris showed signi®cant variation in testis each species separately. Then 3 separate w2 tables were volume among months once the effect of body size on used to test the hypotheses that the total number of testis volume was removed (F = 3.312, P = 0.001; for individuals in each age class (male, female, or juvenile) E. ®tzingeri, F = 1.275, P = 0.297; for E. biporcatus, was evenly distributed among months throughout the F = 2.065, P = 0.112; for B. haematiticus, F = 0.981, 272 J. I. Watling and M. A. Donnelly

100 600 Table 1. Two-way ANOVA tables for quadrat counts of leaf E. biporcatus D. pumilio litter frogs: (a) species, months, and interaction; (b) the same E. bransfordii data excluding E. brandsfordii; (c) age structure, months, and 500 E. talamancae interaction 75 G. pictiventris Rainfall 400 Source d.f. MS FP

50 300 (a) Month 12 0.772 2.000 0.024 Species 4 47.13 122.11 < 0.001 Month6Species 48 0.35 0.906 0.652 200 Rainfall (mm) Error 325 0.386 Number of individuals 25 Total 389 100 (b) Month 12 0.257 0.724 0.728 0 0 Species 3 29.66 83.477 < 0.001 Nov Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Month6Species 36 0.171 0.48 0.995 and Dec Month Error 260 0.355 Total 311 Fig. 2. Variation in rainfall and monthly quadrat counts for ®ve frog species from November 1973 to December 1974. (c) Month 12 1.405 2.601 0.003 Age Class 2 1.001 1.853 0.160 Month6Age Class 24 0.499 0.925 0.568 P = 0.458). In G. pictiventris, testis volume was lowest Error 195 0.540 from January±April 1974. Total 233

Abundance 150

A total of 1205 individuals of ®ve species was repre- sented by > 20 individuals in quadrat surveys. The ®ve species represented three families: Dendrobatide (Den- drobates pumilio), Leptodactylidae (E. biporcatus, 100 E. brandsfordii,andE. talamancae), and Microhylidae (G. pictiventris). Eleutherodactylus brandsfordii and D. pumilio were the most abundant species in the sample, accounting for 86% of quadrat observations (Fig. 2). All ®ve species were caught in 9 of the 13 50 months of quadrat sampling. The 4 months in which Number of individuals fewer than ®ve species were recorded were August 1974 (four species), September 1974 (four species), October 1974 (three species), and November 1974 (four species). There were signi®cant differences in the abundance of 0 species across all months, and monthly abundance Nov Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec and across all species (Table 1a, Fig. 2). The interaction Dec Month between the main effects was not signi®cant, which indicates that there were no differences in the relative Fig. 3. Frequency histogram of monthly abundance of litter importance of each taxon in the community throughout frogs. the year. Post-hoc tests using Dunnett's C indicated that the abundance of E. biporcatus was not different from the abundance of E. talamancae or G. pictiventris across the quadrat counts of the three age±sex classes during months. All other combinations of species were signi®- the 14-month study (Table 1c, Fig. 4). Individuals cantly different from one another. Post-hoc tests did not (especially juveniles) were more abundant from Feb- indicate the months for which quadrat counts differed ruary to April 1974 than in other months. There were signi®cantly from one another, but the frequency histo- no differences in quadrat counts among age±sex classes gram of the abundance of all species across months across all months, and the interaction between age±sex indicates that frogs were more abundant from Feb- class and month was not signi®cant (Table 1c). ruary±July and December 1974 than the other 5 months The frequency with which individuals were encoun- of the study period (Fig. 3). When E. brandsfordii was tered during the study period differed from an even excluded from the analysis, abundance varied signi®- distribution in E. brandsfordii only (w2 = 155.8, cantly among species, but differences in quadrat counts P < 0.001). All other species were relatively evenly dis- among months were no longer signi®cant (Table 1b). tributed across the 14 months of the study (Fig. 2). Our The interaction between months and species was not data on the distribution of the three age classes across signi®cant. There were signi®cant monthly differences in the study period indicated that the observed frequency Leaf litter frog seasonality 273

70 600 Females adults is concentrated during the rainy season in this Juveniles Males species. The individuals in our sample probably depos- 60 Rainfall 500 ited ova late in the wet season of 1973 (November± December), with juvenile froglets emerging during the 50 dry season and showing the same pattern as most 400 terrestrial-breeding Eleutherodactylus in our sample: 40 recruitment and growth of juveniles was concentrated in

30 the dry season. 300 The recruitment of juveniles during the dry season at

Rainfall (mm) La Selva may be tied to the phenology of arthropods,

Number of individuals 20 200 the principal prey items of leaf litter frogs. Several 10 studies have indicated that leaf litter arthropod abun- dance is higher during the dry season and dry season± 0 100 wet season transition at sites in Central America (Toft, Nov Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec and 1980; Lieberman & Dock, 1982; Levings & Windsor, Dec Month 1984). At La Selva, the abundance of most litter arthro- pods, especially and orthopterans (important prey Fig. 4. Monthly quadrat counts of males, females, and juve- items for most of the species included in this study) niles of ®ve species of frogs from November 1973±December peaks in April±May, before the onset of the heaviest 1974. rains during the summer months (Lieberman & Dock, 1982). At other sites in the Neotropics, including the with which juveniles were encountered differed from south-western Amazon and the Caribbean, arthropod what would be expected based on an even distribution abundance peaks during the rainy season (Tanaka & (w2 = 125.9, P < 0.001), but that males and females were Tanaka, 1982; Pearson & Derr, 1986). We suggest that evenly distributed throughout the year (Fig. 4). many litter anurans time their reproduction in such a way that juveniles emerge during the season of peak arthropod abundance. In Central America, this may DISCUSSION result in increased recruitment of litter anurans during the dry season. In Amazonia and the Caribbean, arthro- Phenology of individual species pods are relatively more abundant in the wet season, which may explain the peaks in reproductive activity Our data on body size variation indicate that recruit- and juvenile growth documented from these areas (Ai- ment of juveniles occurred during the dry season at La chinger, 1987; Gascon, 1991b; Moreira & Lima, 1991; Selva for four out of six species analysed. Moreria & Ovaska, 1991). Other researchers have tied patterns of Lima (1991) interpreted monthly increases in SVL as juvenile recruitment to food availability among coatis in representing growth in recently metamorphosed indivi- Central America (Russell, 1982) and saddle-back ta- duals of leaf litter frogs in their sample from the marins in South America (Goldizen et al., 1988). Here Brazilian Amazon. We believe that the small juvenile we suggest a link between food availability and the body size in the dry season, followed by several months timing of reproduction among litter frogs in the tropics. of increase in mean SVL represents the emergence and Although predictable cycles of arthropod abundance growth of cohorts of juveniles in the four species for may in¯uence populations at sites in both Central and which we documented signi®cant temporal differences South America, seasonal patterns of recruitment differ in juvenile body size. Donnelly (1999) stated that repro- between the two continents. duction in E. brandsfordii was continuous at La Selva, though she noted that the high abundance of juveniles during the dry season in her sample may indicate some Temporal variation in abundance seasonality in reproductive output. We believe that her data in conjunction with ours indicate that the dry Our analyses of community phenology indicate that season is an important period of juvenile recruitment abundance of frogs was higher in the dry season than in for many species of litter frogs at this site in north- the wet season. The most abundant species in our eastern Costa Rica. sample, E. brandsfordii, is responsible for the signi®cant The dry season may be an important time for juvenile monthly differences in quadrat counts. When E. brands- recruitment among terrestrial species at La Selva and fordii was removed from the analysis we found no this is indicated by the pattern seen in the microhylid differences in the abundance of species among months. G. pictiventris. Gastrophryne pictiventris deposit their The patterns discussed below, then, are driven largely ova in ephemeral pools during rainy periods where they by variation in the abundance of one common frog at probably develop over a few weeks (Donnelly, de Sa & La Selva. Guyer, 1990). Adult G. pictiventris breed in water and Other researchers have found that litter amphibians adult males showed a decrease in testis volume during and reptiles at La Selva and other sites in Central the dry season, indicating that breeding activity in America are more abundant in the dry season than the 274 J. I. Watling and M. A. Donnelly

Table 2. Distribution of precipitation (‹ 1 sd when data were available) at eight sites in the neotropics

Site Mean annual rainfall (mm) No. months with No. months with rainfall < 200 mm rainfall < 100 mm

Central America La Selva, Costa Ricaa 3962 ‹ 723 3 0 Osa Peninsula, Costa Ricab 5296 ‹ 228 4 2 Barro Colorado Island, Panamac,d 2616 ‹ 422 4 3

South America Santa Cecilia, Ecuadore 4289 0 0 Panguana, Peruf 2634 4 3 Manu, Perug 2110 5 3 Manaus, Brazilh 2379 ‹ 300 6 4 Belem, Brazilh 3136 ‹ 382 6 0 a Sanford et al. (1994). b L. Gilbert (pers. comm.) c Dietrich, Windsor & Dunne (1982). d Rand & Rand (1982). e Crump (1974). f Aichinger (1987). g Rodriguez (1992). h NOAA. wet season (Toft, 1980; Lieberman, 1986). Guyer (1986) moist during development (Duellman & Trueb, 1986). documented a dry-season peak in abundance in Norops However, the dry season in Central America is shorter humilis, a leaf litter anole collected at the same time as and wetter than in much of the Amazon basin (Table the frogs in our sample. He attributed the higher 2). Furthermore, at La Selva the leaf litter layer, where abundance of animals during the late dry season to the many of the species included in this study deposit their high volume of leaf litter, which provides foraging and ova, is deeper in the dry season than in the wet season oviposition substrate for terrestrial amphibians and due to variation in decomposition rate throughout the reptiles. At relatively wet and dry sites in Panama, frogs year (Frankie, Baker & Opter, 1974). We suggest that are also more abundant in the dry season (Toft, 1980; the dry season in Central America is pronounced Toft, Rand & Clark, 1982). In contrast, researchers at enough to trigger seasonal variation in leaf fall and the sites with seasonal patterns of rainfall in the Amazon abundance of arthropods, but not so severe as to have found that anuran abundance is lower in the dry prevent some species from depositing terrestrial ova season than the wet season (Cuzco Amazonico, ; during the dry season. Duellman, 1995; Manaus, Brazil; Allmon, 1991). Of the On Barro Colorado Island, Panama, Andrews, Rand 14 species included in Allmon's (1991) sample, only & Guerrero (1982) reported that N. limifrons does not juveniles of Colostethus marchesianus were more abun- generally deposit ova in the litter layer until the begin- dant in the dry season than in the wet season. While ning of the wet season. We are not aware of any data total annual rainfall at Cuzco Amazonico, is much describing patterns of recruitment or ova deposition lower than La Selva (2387 mm at Cuzco Amazonico vs. among Eleutherodactylus, the largest group of terrest- 3962 mm at La Selva), rainfall at Cuzco Amazonico is rially breeding frogs, from other sites in Central similar to Toft's (1980) dry site in Panama (which America. At Panguana, Peru, Toft & Duellman (1979) receives 2200 mm of rain/year). However, annual pat- found indirect evidence that E. peruvianus and terns of anuran abundance differ between Panama and E. toftae, bred during the dry season, but Aichinger Peru, which suggests that the mechanism driving pat- (1987) categorized the same two species as primarily terns of anuran abundance acts in a fundamentally wet season breeders. In the central Amazon basin, different manner between Central and South America. Moreira & Lima (1991) found that juvenile recruitment The increase in the abundance of frogs during the in the terrestrial breeders Adenomera andreae and dry season is because of the increase in the number of Colostethus stepheni occurred during the rainy season. juvenile individuals observed from February±May More data describing reproductive patterns among 1974. As described above, we believe that many many species of terrestrial breeders from both Central anurans time their reproduction so that juveniles and South America are necessary to evaluate the emerge during periods of peak prey abundance, which hypothesis suggested by the data presented in this occur during the dry season or dry season±wet season study: the dry season in Central American rainforests is transition in Central America, and during the wet not severe enough to limit the ability of some terrest- season in much of the Amazon. At ®rst this seems rially breeding species to deposit ova and recruit counter-intuitive, given that frog ova, which lack a juveniles during dry periods. calci®ed shell, risk desiccation if they are not kept Although there was no signi®cant interaction between Leaf litter frog seasonality 275 species and month, indicating that the relative impor- changes in the relative importance of species in the tance of each taxon in the community did not vary community. temporally, the number of species present in the assem- blage was lowest during months when frogs and arthropods were least abundant. It is possible that a Acknowledgements reduction in arthropod abundance during rainy months may create a seasonal food shortage for litter frogs. As The specimens reported on here were collected by C. F. noted by Wiens (1977), ecological `crunches' may result Dock, C. S. Leib, J. J. Talbot and R. W. VanDevender in the local redistribution of individuals, affecting the as part of a study funded by NSF grant BMS ability of short-term censuses using small plots to relate 7301619A01 to J. M. Savage and I. R. Straughn. We resource abundance to the density of animals. Even if thank J. M. Savage for providing access to specimens. species in our sample do not experience population M. Crump, T. Doan, L. Fitzgerald and the Miami Herp declines during times of low prey availability, our data Group (D. Bickford, A. Catenazzi, K. Hines, K. Nichol- indicate that the composition of the litter frog commu- son, T. Ugarte, and H. Waddle) provided comments nity is in¯uenced either directly (by population declines that helped improve the quality of this paper. This is of some species) or indirectly (by changes in the distri- contribution number 54 to the Program in Tropical bution of frogs in the forest) by seasonal ¯uctuations in Biology at Florida International University. rainfall at La Selva. We found that the temporal distribution of juveniles varied throughout the year. The differential distribu- tion of juveniles among months may have important REFERENCES implications for the ecological in¯uence of litter frogs given the role of frogs as predators in rainforest Aichinger, M. (1987). Annual activity patterns of anurans in a seasonal neotropical environment. Oecologia (Berl.) 71: habitats (Stewart & Woolbright, 1996). Work at La 583±592. Selva and in the Brazilian Amazon indicates that the Allmon, W. D. (1991). A plot study of forest ¯oor litter frogs, diet of many litter frogs changes ontogenetically (Don- Central Amazon, Brazil. J. Trop. Ecol. 7: 503±522. nelly, 1991; Lima & Magnusson, 1998). In D. pumilio, Andrews, R. A., Rand, A. S. & Guerrero, S. (1982). Seasonal and for example, mites are more important prey items in spatial variation in the annual cycle of a tropical lizard. In juveniles than adults, and adults eat more ants than Advances in hepetology and evolutionary biology: 441±454. juveniles (Donnelly, 1991). Lima & Magnusson (1998) Rhodin, A. G. J. & Miyata, K. (Eds). Cambridge, MA: Harvard University Press. found that the diet of diurnal litter frogs varies as Arnold, S. J. (1993). Foraging theory and prey-size±predator-size much among size classes within a species as it does relations in snakes. In Snakes: 87±116. Seigel, R. A. & Collins, among species. If ontogenetic changes in diet occur J. T. (Eds). New York: McGraw-Hill. among many litter frogs at La Selva, then the cumula- Crump, M. L. (1974). Reproductive strategies in a tropical anuran tive effect of frogs as predators in the reserve probably community. Univ. Kansas. Mus. Nat. Hist. Misc. Pub. 61: 1±68. varies throughout the year. At the same time, the Dietrich, W. E., Windsor, D. M. & Dunne, T. (1982). Geology, climate, and hydrology of Barro Colorado Island. In The availability of frogs as prey items for larger predators ecology of a tropical forest: 21±46. Leigh, E. G., Rand, A. S. & (especially snakes, which eliminate relatively small prey Windsor, D. M. (Eds). Washington, DC: Smithsonian Institu- items as they grow; Arnold, 1993) also differs tion Press. throughout the year based on variation in the abun- Donnelly, M. A. (1989). Reproductive phenology and age struc- dance of juvenile and adult frogs. Therefore, any ture of Dendrobates pumilio in northeastern Costa Rica. J. attempt to understand the importance of frogs as Herpetol. 23: 362±367. predators and/or prey in rainforest habitats must ex- Donnelly, M. A. (1991). Feeding patterns of the strawberry poison frog, Dendrobates pumilio (Anura: Dendrobatidae). plicitly consider the effects of seasonal change on the Copeia 1991: 723±730. composition of the frog assemblages. Donnelly, M. A. (1999). Reproductive phenology of Eleutherodac- In conclusion, we found that patterns of abundance tylus brandsfordii (Anura: Leptodactylidae) in northeastern and recruitment of juveniles is seasonal for many litter Costa Rica. J. Herpetol. 33: 624±631. frogs at one site in north-eastern Costa Rica. We Donnelly, M. A., de Sa, R. O. & Guyer, C. (1990). Description of suggest that temporal variation in both frog abundance the tadpoles of Gastrophryne pictiventris and Nelsonophryne and juvenile recruitment may be attributable to ¯uctua- aterrima (Anura: Microhylidae), with a review of morpholo- gical variation in free-swimming microhylid larvae. Am. Mus. tions in the abundance of arthropod prey items. The Novit. 2976: 1±19. coupling of phenological patterns among both frogs and Duellman,W. E. (1995). Temporal ¯uctuations in abundances of arthropods with rainfall results in different seasonal anuran amphibians in a seasonal Amazonian rainforest. J. patterns between La Selva and other sites in Central Herpetol. 29: 13±21. America, where abundance and recruitment of frogs Duellman, W. E. & Trueb, L. (1986). Biology of Amphibians. New peak in the dry season, and the Amazon, where abun- York: McGraw-Hill. Fitzgerald, L. A., Cruz, F. B. & Perotti, G. (1999). Phenology of a dance and recruitment generally peak in the rainy lizard assemblage in the dry Chaco of Argentina. J. Herpetol. season. Finally, variation in the assemblage of leaf litter 33: 526±535. frogs at this site in north-eastern Costa Rica is based on Fogden, M. P. L. (1972). The seasonality and population dynamics variation in the age structure of individuals rather than of equatorial forest in Sarawak. Ibis. 114: 307±343. 276 J. I. Watling and M. A. Donnelly

Frankie, G. W., Baker, H. G. & Opler, P. A. (1974). Comparative forest ¯oor arthropod abundance in southeastern Peru. Biotro- phenological studies of trees in tropical wet and dry forests in pica 18: 244±256. the lowlands of Costa Rica. J. Ecol. 62: 881±919. Poulin, B., Lefebvre, G. & McNeil, R. (1992). Tropical avian Gascon, C. (1991a). Population- and community-level analysis of phenology in relation to abundance and exploitation of food species occurrences of central Amazonian rainforest tadpoles. resources. Ecology 73: 2295±2309. Ecology 75: 1731±1746. Rand, A. S. & Rand, W. M. (1982). Variation in rainfall on Barro Gascon, C. (1991b). Breeding of Leptodactylus knudseni: responses Colorado Island. In The ecology of a tropical forest: 47±59. to rainfall variation. Copeia 1991: 248±251. Leigh, E. G., Rand, A. S. & Windsor, D. M. (Eds). Wa- Goldizen, A. W., Terborgh, J., Cornejo, F., Porras, D. T. & shington, DC: Smithsonian Institution Press. Evans, R. (1988). Seasonal food shortage, weight loss, and the Rodriguez, L. O. (1992). Structure et organisation du peuplement timing of births in saddle-back tamarins (Saguinus fuscicollis). d'anours de Cocha Cashu, Parc National Manu, Amazonie J. Anim. Ecol. 57: 893±901. Peruvienne. Terre Vie 47: 151±197. Guyer, C. (1986). Seasonal patterns of reproduction of Norops Russell, J. K. (1982). Timing of reproduction by coatis (Nasua humilis (Sauria: Iguanidae) in Costa Rica. Rev. Biol. Trop. 34: narica) in relation to ¯uctuations in food resources. In The 247±251. ecology of a tropical forest: 413±431. Leigh, E. G., Rand, A. S. Jaeger, R. G. & Inger, R. F. (1994). Quadrat sampling. In & Windsor, D. M. (Eds). Washington, DC: Smithsonian Measuring and monitoring biological diversity: 97±103. Heyer, Institution Press. W. R., Donnelly, M. A., McDiarmid, R. W., Hayek, L. C. & Sanford, R. L. Jr, Paaby, P., Luvall, J. C. & Phillips, E. (1994). Foster, M. S. (Eds). Washington, DC: Smithsonian Institution Climate, geomorphology, and aquatic systems. In La Selva: Press. ecology and natural history of a Neotropical rainforest: 19±33. Johnson, G. (1999). Reproductive biology of the peninsula dragon McDade, L. A., Bawa, K. S., Hespenheide, H. S. & Hartshorn, lizard, Ctenophorous ®onni. J. Herpetol. 33: 694±698. G. S. (Eds). Chicago: University of Chicago Press. Kanamadi, R. D. & Jirankali, C. S. (1992). Testicular activity in Sinclair, A. R. E., Mduma, S. A. R. & Arcese, P. (2000). What Polypedates maculatus (Rhacophoridae): seasonal changes in determines phenology and synchrony of ungulate breeding in spermatogenesis and fat bodies. J. Herpetol 26: 329±335. Serengeti. Ecology 81: 2100±2111. Kappeler, P. M. (1997). Intrasexual selection in Mizra coquereli: SPSS (1997). SPSS base 8.0 for Windows user's guide. Chicago, evidence for scramble competition polygyny in a solitary IL: SPSS Inc. primate. Behav. Ecol. Sociobiol. 41: 115±127. Stewart, M. M. & Woolbright, L. L. (1996). Amphibians. In Leigh E. G., Rand, A. S. & Windsor, D. M. (1982). The ecology of The food web of a tropical rain forest: 273±320. Reagan, a tropical forest. Washington, DC: Smithsonian Institution D. P. & Waide, R. B. (Eds). Chicago: University of Chicago Press. Press. Levings, S. C. & Windsor, D. M. (1984). Litter moisture as a Stiles, F. G. (1980). The annual cycle in a tropical wet forest determinant of litter arthropod distribution and abundance hummingbird community. Ibis 122: 322±343. during the dry season on Barro Colorado Island, Panama. Tanaka, L. K. & Tanaka, S. K. (1982). Rainfall and seasonal Biotropica 16: 125±131. changes in arthropod abundance on a tropical oceanic island. Lieberman, S. S. (1986). Ecology of the leaf-litter herpetofauna of Biotropica 14: 114±123. a neotropical rainforest: La Selva, Costa Rica. Acta Zool. Toft, C. A. (1980). Seasonal patterns in populations of Panama- Mexicana 15: 1±72. nian litter frogs and their prey: a comparison of wetter and Lieberman, S. S. & Dock, C. F. (1982). Analysis of the leaf litter drier sites. Oecologia (Berl.) 47: 34±38. arthropod of a lowland tropical evergreen forest site (La Toft, C. A. & Duellman, W. E. (1979). Anurans of the lower Rio Selva, Costa Rica). Rev. Biol. Trop. 30: 27±34. Llullapichis, amazonian Peru: a preliminary analysis of com- Lima, A. P. & Magnusson, W. E. (1998). Partitioning seasonal munity structure. Herpetologica 35: 71±77. time: interactions among size, foraging activity and diet in leaf- Toft, C. A., Rand, A. S. & Clark, M. (1982). Population dynamics litter frogs. Oecologia (Berl.) 116: 259±266. and seasonal recruitment in Bufo typhonius and Colostethus McDade, L. A. & Hartshorn, G. S. (1994). La Selva Biological nubicola (Anura). In The ecology of a tropical forest: 397±403. Station. In La Selva: ecology and natural history of a Neotro- Leigh, E. G., Rand, A. S. & Windsor, D. M. (Eds). pical rainforest: 6±14. McDade, L. A., Bawa, K. S., Hespen- Washington, DC: Smithsonian Institution Press. heide, H. A. & Hartshorn, G. S. (Eds). Chicago: University of van Shaik, C. P., Terborgh, J. W. & Wright, S. J. (1993). The Chicago Press. phenology of tropical forests: adaptive signi®cance and con- Moreira, G. & Lima, A. P. (1991). Seasonal patterns of juvenile sequences for primary consumers. Annu. Rev. Ecol. Syst. 24: recruitment and reproduction in four species of leaf litter frogs 353±377 in central Amazonia. Herpetologica 47: 295±300. Wiens, J. A. (1977). On competition and variable environments. Ovaska, K. (1991). Reproductive phenology, population struc- Am. Scient. 65: 590±597. ture, and habitat use of the frog Eleutherodactylus johnstonei in Wikelski, M., Hau, M. & Wing®eld, J. C. (2000). Seasonality of Barbados, West Indies. J. Herpetol. 25: 424±430. reproduction in a neotropical rainforest . Ecology 81: Pearson, D. L. & Derr, J. A. (1986). Seasonal patterns of lowland 2458±2472.