Reproductive Phenology of Three Lizard Species in Costa Rica, with Comments on Seasonal Reproduction of Neotropical Lizards

Reproductive Phenology of Three Lizard Species in Costa Rica, with Comments on Seasonal Reproduction of Neotropical Lizards Author(s): James I. Watling, J. Hardin Waddle, David Kizirian, and Maureen A. Donnelly Source: Journal of Herpetology, 39(3):341-348. 2005. Published By: The Society for the Study of Amphibians and Reptiles DOI: http://dx.doi.org/10.1670/80-02a.1 URL: http://www.bioone.org/doi/full/10.1670/80-02a.1 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.

Journal of Herpetology, Vol. 39, No. 3, pp. 341 348, 2005 Copyright 2005 Society for the Study of Amphibians and Reptiles Reproductive Phenology of Three Lizard Species in Costa Rica, with Comments on Seasonal Reproduction of Neotropical Lizards JAMES I. WATLING, 1 J. HARDIN WADDLE, 2 DAVID KIZIRIAN, 3 AND MAUREEN A. DONNELLY Florida International University, Department of Biological Sciences, University Park, Miami, Florida 33199, USA ABSTRACT. We quantified reproductive phenology for three lizard species collected in northeastern Costa Rica over a 14-month sampling period from November 1973 to December 1974. Two species, a gecko (Lepidoblepharis xanthostigma) and a skink (Sphenomorphus cherriei), reproduced continuously at this site, whereas an anole (Norops limifrons) showed a slight decline in reproduction during the dry season. The decrease in reproduction of N. limifrons may reflect a response to moisture stress during the driest part of the year. When seasonal patterns of reproduction among 32 populations of Neotropical lizards with small clutch sizes were analyzed with the effect of phylogenetic relatedness removed, we found that seasonality of reproduction was strongly related to mean annual rainfall but not to number of dry season months. Much research has focused on quantifying reproductive strategies of lizards, with many studies describing clutch size variation (Vitt and Price, 1982; Ballinger, 1983; Sinervo, 1994), evolution of parental care (Shine, 1994), and reproductive seasonality (Fitch, 1973; Vitt, 1990; Colli et al., 1997). One of the best-studied assemblages of tropical lizards occurs in the caatinga habitat of northeastern Brazil (Vitt and Lacher, 1981; Vitt, 1982a,b, 1986). Research in the caatinga revealed that even in a habitat characterized by a strongly seasonal rainfall pattern, species vary considerably in the phenology of reproduction (Vitt, 1995). Data from the caatinga assemblage demonstrate that the local environment does not necessarily play the dominant role in determining the reproductive phenology of tropical lizards and highlight the importance of considering multiple factors when trying to infer the mechanism(s) responsible for generating phenological patterns. To put existing data in a broader geographic and taxonomic context and better understand the combined influence of environment and history on lizard reproduction, data describing reproductive patterns of species occurring sympatrically as well as closely related species living in different habitats are needed. Although such data are available for some temperate-zone taxa (Pianka and Pianka, 1976; James, 1991; Niewiarowski, 1994), comparative data for tropical taxa are still scant. Therefore, the 1 Corresponding Author. E-mail: jwatli01@fiu.edu 2 Present address: Florida Cooperative Fish and Wildlife Research Unit, Department of Wildlife Ecology and Conservation, University of Florida, Gainesville, Florida 32611-0458, USA. 3 Present address: Department of Ecology and Evolutionary Biology, University of California-Los Angeles, Los Angeles, California 90095-1606, USA. goals of this paper are to (1) describe the reproductive phenology of three species of lizards at La Selva, Costa Rica, and (2) evaluate the relationship between two local environmental factors (mean annual precipitation and length of the dry season) and seasonality of reproduction of lizards from sites throughout the New World tropics. MATERIALS AND METHODS We examined a sample of 559 individuals of three species of lizards, Lepidoblepharis xanthostigma (Gekkonidae; N 5 179), Norops limifrons (Polychrotidae; N 5 209), and Sphenomorphus cherriei (Scincidae; N 5 171) collected at the La Selva research station in northeastern Costa Rica during a 14-month period from November 1973 to December 1974. Rainfall at La Selva is high (mean 5 3962 mm per year; Sanford et al., 1994), though a distinct dry season occurs from February to April when precipitation averages less than 200 mm per month. Most of La Selva is covered by primary lowland rain forest, although part of the reserve consists of abandoned cacao plantations and disturbed, nonforest habitat. Lizards were collected in one of three ways. Approximately equal numbers of lizards were caught by opportunistic collection (N 5 279) and quadrat sampling (N 5 245). A few additional lizards (N 5 35) were caught in pitfall traps established along a 100 m transect (for details, see Lieberman, 1986). All lizards were euthanized, fixed in formalin, and stored in 70% ethanol. In the laboratory, we measured snout vent length (SVL) of each specimen before dissecting it to assess reproductive condition. For males, we measured length of the left testis to the nearest millimeter with an ocular micrometer and recorded the condition of the epididymis as

342 J. I. WATLING ET AL. convoluted or straight. For females, we measured length of all oviductal eggs or yolking follicles (>0.3 mm) to the nearest tenth of a millimeter. Individuals were then assigned to one of three age-sex classes (adult female, adult male, or juvenile) based on body size (SVL) and gonadal condition. Females that were at least as long as the smallest individual containing oviductal eggs or yolking follicles were classified as adults. For males, we classified adult body size as the length at which more than 50% of individuals had convoluted epididymi. All other individuals of both sexes were classified as juveniles. We used three approaches to describe the reproductive phenology of lizards. Because variation in body size may be indicative of recruitment events (Donnelly, 1989, 1999), we used a one-way analysis of variance (ANOVA) to test the hypothesis that mean body size varied among months. We performed this analysis for each age class of each species separately. We then used a one-way analysis of covariance (ANCOVA) using body size as a covariate to test the hypothesis that gonad size varied among months independently of monthly variation in body size. We analyzed variation in gonad size for adult males and adult females for each species. Months in which fewer than three individuals were captured were excluded from the above analyses. Finally, we calculated the percentage of adult females of each species that contained at least one oviductal egg or yolking follicles during each month of the study. We analyzed data in two ways: (1) using pooled data from all sampling methods; and (2) based on a random sample of four individuals from each age-sex class per month. We chose to select four individuals at random so that we would be able to generate the variance estimates required for ANOVA and ANCOVA analyses but minimize biases resulting from overrepresentation of certain age-sex classes in some months. Because the results from the random dataset were qualitatively similar to results based on the entire dataset, we present the pooled results throughout the rest of the paper. To meet assumptions of normality, we used the natural logarithm of SVL and gonad length in all analyses. We surveyed the primary literature for data describing seasonal patterns of reproduction for 32 populations of 19 Neotropical lizard species. We limited our analysis to those species in which clutch size is fixed at one to two ova per clutch. Species with larger clutches may be constrained to reproduce seasonally because of energetic constraints rather than responding to seasonal changes in the environment (L. Vitt, pers. comm.). We focused on mainland taxa because insular organisms undergo morphological and ecological changes that may influence the reproductive parameters of interest here (for an ecological comparison of island and mainland Anolis lizards, see Irschick et al., 1997). Species were categorized as continuous breeders if output of ova was relatively constant throughout the year, with little variation in body size among months. Seasonal breeders were defined as species in which output of ova and body size varied throughout the sampling period, with these changes occurring during a period of consecutive months, as opposed to discontinuously throughout the year. To overcome the problem of nonindependence of samples with a shared history, we used Program CAIC (Purvis and Rambaut, 1995) to calculate phylogenetically independent contrasts for our three variables (seasonality of reproduction, mean annual rainfall and number of dry season months). Although seasonality of reproduction is a categorical variable, for the purposes of our analysis, we assumed it was continuous since CAIC requires that variables included in multivariate analyses be continuous. Separate analyses using seasonality of reproduction as a categorical variable yielded similar results to the multivariate analysis; thus, we are confident that the coding of reproduction as a continuous variable did not alter the results presented below. We derived a cladogram of lizard relationships (Fig. 1) from multiple sources: Estes et al. (1988; squamata), Zug et al. (2001; squamata), Frost and Etheridge (1989; Iguania), Pellegrino et al. (2001; Gymnopthalmidae); Presch (1974; Teiidae), Nicholson (2002; Norops), and Kluge (1987, gekkonids). We used the brunch algorithm in CAIC to calculate independent contrasts because it has less restrictive evolutionary assumptions than other algorithms, and we assumed equal branch lengths among all taxa. The analysis provided 11 independent contrasts for each variable, which we analyzed using multiple regression. Independent contrasts were calculated in CAIC, and all other statistical analyses were conducted using JMP 4.0 (SAS Institute, Cary, NC, 2000). RESULTS Lepidoblepharis xanthostigma. Snout vent length of adult females ranged from 27.0 35.0 mm (mean 5 31.5 mm, N 5 50), adult males ranged from 26.0 34.0 mm (mean 5 30.1 mm, N 5 70), and juveniles ranged from 11.0 27.0 mm (mean 5 19.9 mm, N 5 58). Mean body size of males, females, and juveniles did not vary significantly among months (Table 1). However, both mean testis length and mean ovum length showed significant variation during the study period (Table 1). Mean ovum length was lowest during February 1974, whereas mean testis length varied throughout the year but showed no seasonal signal (Fig. 2). During months when adult

NEOTROPICAL LIZARD PHENOLOGY 343 TABLE 1. Analysis of variance tables describing variation in snout vent length (SVL), testis length (males), and ovum length (females) from November 1973 to December 1974 for three lizard species at La Selva. FIG. 1. Cladogram of lizard relationships used in phylogenetic analysis. Numbers beside species names indicate independent populations used in analysis. females were present and ovum condition was recorded (all months except July, September, and October 1974), all individuals contained at least one oviductal egg or yolking follicles (Table 2). Sphenomorphus cherriei. Adult females ranged from 44.0 56.0 mm in SVL (mean 5 50.6 mm, N 5 56), males ranged from 40.0 58.0 mm (mean 5 48.8 mm, N 5 67), and juveniles ranged from 20.0 43.0 mm (mean 5 29.3 mm, N 5 47). Mean body size in all three age-sex classes did not vary significantly among months (Table 1). Gonadal length varied significantly in both males and females (Table 1). Mean testis length was shortest during the last six months of 1974, whereas mean ovum length was shortest from L. xanthostigma Source df SS F P SVL females Month 7 0.01191 0.4769 0.85 Error 34 0.12138 Total 41 0.1333 males Month 11 0.06428 1.0948 0.38 Error 57 0.3043 Total 68 0.3685 juveniles Month 6 0.4363 1.5103 0.2 Error 41 1.9739 Total 47 2.4102 Testis length Model 12 6.3999 13.9152,0.0001 Error 55 2.1079 Total 67 8.50795 Ovum length Model 8 1.44617 2.6164 0.03 Error 24 1.65819 Total 32 3.10436 S. cherriei SVL females Month 8 0.03144 0.7883 0.62 Error 42 0.2094 Total 50 0.24087 males Month 11 0.12659 1.3614 0.22 Error 52 0.43959 Total 63 0.56619 juveniles Month 7 0.2674 0.8652 0.54 Error 30 1.3245 Total 37 1.5919 Testis length Model 12 1.3029 6.5923,0.001 Error 51 0.84 Total 63 2.1429 Ovum length Model 9 12.10118 3.1118 0.0061 Error 41 17.7155 Total 50 29.8167 N. limifrons SVL females Month 10 0.102 2.1316 0.04 Error 56 0.2681 Total 66 0.3702 males Month 11 0.0409 0.7484 0.69 Error 67 0.3331 Total 78 0.37407 juveniles Month 7 0.89 3.7677 0.003 Error 42 1.4174 Total 49 2.3075 Testis length Model 12 1.5666 11.0225,0.001 Error 57 0.6751 Total 69 2.2417 Ovum length Model 11 26.252 7.1525,0.001 Error 50 16.6833 Total 61 42.9354 September to December 1974 (Fig. 3). With the exception of one individual in June 1974, all adult

344 J. I. WATLING ET AL. Mean ovum length was lowest during January and February 1974, and mean testis length was lowest during September 1974 (Table 1, Fig. 5). The production of eggs varied among months, with fewer females containing an oviductal egg or yolking follicles in January and February 1974 than during the rest of the year (Table 2). Environmental Influence on Reproductive Phenology. Summary data and climate variables at study sites for 32 populations of lizards included in multiple regression analyses are presented in Table 3. The multiple regression model of independent contrasts of the three variables was significant (F 2,9 5 4.50, P 5 0.0442). The effect test indicated that the independent contrasts representing annual rainfall were a significant predictor of reproductive seasonality (F 1,1 5 5.97, P 5 0.0371), but the independent contrasts representing number of dry season months were not (F 1,1 5 2.38, P 5 0.1574). That is, after the effects of phylogeny were controlled for, populations at sites with high annual rainfall tended to reproduce continuously, whereas populations at sites with low annual rainfall reproduced seasonally. FIG. 2. Variation (mean 6 one standard error) in ln(testis length) and ln(ovum length) in Lepidoblepharis xanthostigma from November 1973 to December 1974. In all figures, dry season months are indicated by a black bar. females contained oviductal eggs or yolking follicles throughout the year (Table 2). Norops limifrons. Adult females ranged in size from 32.0 44.0 mm (mean 5 37.1 mm, N 5 71), males ranged from 30.0 40.0 mm (mean 5 34.6 mm, N 5 83), and juveniles ranged from 12.0 31.0 mm (mean 5 24.5 mm, N 5 55). Male body size did not vary among months, but females were smaller in January 1974 than they were in other months. Juveniles showed significant variation in body size among months (Table 1) and were smallest in July and August 1974 (Fig. 4). DISCUSSION Although gonadal size varied among months in both the gecko Lepidoblepharis xanthostigma and the skink Sphenomorphus cherriei, that variation did not show a pronounced seasonal pattern. In the anole N. limifrons, females were smallest in January 1974 and showed decreased egg output during the height of the dry season (January and February 1974). Juveniles of N. limifrons were smallest during the middle of the rainy season, which may be indicative of a recruitment event. Based on these data, we conclude that L. xanthostigma and S. cherriei probably reproduce continuously at La Selva, whereas N. limifrons is a seasonal breeder with a short but distinct decline in reproduction during the dry season. This paper represents the second report on reproductive phenology for L. xanthostigma (for another description, see Fitch, 1973), which, like many gekkonids, reproduces continuously throughout the year (Table 1). Fitch (1973) also TABLE 2. Number (top) and percentage (bottom) of females containing oviductal eggs. An X indicates that no females were captured, and XX indicates that we have no record of ova condition because specimens were damaged. Lepidoblepharis xanthostigma Sphenomorphus cherriei Norops limifrons Nov Dec Jan Feb March April May June July Aug Sept Oct Nov Dec 2 1 3 3 6 6 8 5 XX 1 XX X 1 1 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 2 5 4 8 10 9 4 3 X 1 5 X 2 3 100% 100% 100% 100% 100% 100% 100% 67% 100% 100% 100% 100% 0 3 6 4 12 6 8 3 9 4 6 2 2 3 100% 17% 25% 100% 83% 88% 100% 100% 100% 100% 100% 100% 100%

NEOTROPICAL LIZARD PHENOLOGY 345 FIG. 4. Variation (mean 6 one standard error) in ln(svl) of juvenile Norops limifrons from November 1973 to December 1974. FIG. 3. Variation (mean 6 one standard error) in ln(testis length) and ln(ovum length) in Sphenomorphus cherriei from November 1973 to December 1974. arthropods is higher in the dry season than the wet season at that site (Lieberman and Dock, 1982). In reviewing studies of N. limifrons on BCI, Andrews and Wright (1994) concluded that reduced reproduction during the dry season is most likely caused by changes in dryness per se rather than a change in food availability. They provided experimental data suggesting that concluded that S. cherriei showed signs of seasonal reproduction at Turrialba, Costa Rica. Other researchers have found that N. limifrons is variable with respect to the phenology of reproduction (Andrews and Rand, 1982; Sexton et al., 1971). Both S. cherriei and N. limifrons seem to show geographic variation in reproductive phenology. Norops limifrons has been the subject of longterm population studies on Barro Colorado Island (BCI) in Panama. These studies have indicated that reproduction of N. limifrons is seasonal at BCI, with a decrease in egg production during the dry season (Andrews et al., 1983). Proposed explanations for decreased reproductive output during the dry season include a decrease in food abundance, or moisture stress (i.e., a decrease in soil moisture, affecting eggs, or an increased risk of desiccation for hatchlings). Although arthropods are less abundant during the dry season than the wet season on BCI (Levings and Windsor, 1982), Andrews et al. (1983) noted that this does not necessarily indicate that reproduction in anoles is food limited. Food limitation is not likely to be responsible for decreased reproduction of N. limifrons at La Selva because the abundance of FIG. 5. Variation (mean 6 one standard error) in ln(testis length) and ln(ovum length) in Norops limifrons from November 1973 to December 1974.

346 J. I. WATLING ET AL. TABLE 3. Summary data describing lizard reproduction (S 5 seasonal, C 5 continuous) and climate at study sites for 32 populations used in multiple regression analyses. Taxon Site Annual rainfall (mm) Dry season (months) Reproduction Source Gekkonidae Gonatodes albogularis Limon, CR 3431 3 C Fitch, 1973 Gonatodes albogularis Puntarenas, CR 1600 5 S Fitch, 1973 Gymnodactylus geckoides caatinga, Brazil 725 6 C Vitt, 1986 Hemidactylus mabouia caatinga, Brazil 725 6 C Vitt, 1986 Lepidoblepharis xanthostigma La Selva, CR 3962 3 C this study Lygodactylus klugei caatinga, Brazil 725 6 C Vitt, 1986 Phyllopezus pollicaris caatinga, Brazil 725 6 C Vitt, 1986 Gymnophthalmidae Vanzosaura rubricauda caatinga, Brazil 725 6 C Vitt, 1982b Gymnophthalmus speciosus Panama City, Panama 1779 4 S Telford, 1971 Leposoma rugiceps Panama City, Panama 1779 4 S Telford, 1971 Neusticurus ecpleopus Tingo Maria, Peru 3157 4 C Sherbrooke, 1975 Polychrotidae Norops auratus Balboa, Panama 1779 4 S Sexton et al., 1971 Norops auratus BCI, Panama 2616 4 S Sexton et al., 1971 Norops cupreus San Jose, CR 2115 5 S Fitch, 1973 Norops cupreus Puntarenas, CR 1600 5 S Fitch, 1973 Norops cupreus Sardinal, CR 1633 5 S Fitch, 1973 Norops cupreus La Irma, CR 1599 5 S Fitch, 1973 Norops humilis San Miguel, CR 4521 1 C Fitch, 1973 Norops humilis La Selva, CR 3962 3 C Guyer, 1986 Norops humilis Beverly, CR 3134 4 C Fitch, 1973 Norops intermedius San Jose, CR 2115 5 S Fitch, 1973 Norops limifrons La Selva 3962 3 S this study Norops limifrons Limon, CR 3431 3 C Fitch, 1973 Norops limifrons Gatun, Panama 3140 3 C Sexton et al., 1971 Norops limifrons Turrialba, CR 2606 4 C Fitch. 1973 Norops limifrons Pacific Panama 1779 4 S Sexton et al., 1971 Norops limifrons BCI, Panama 2616 4 S Andrews and Rand, 1982 Norops lionotus San Miguel, CR 4521 1 C Fitch, 1973 Norops tropidogaster Balboa, Panama 1779 4 S Sexton et al., 1971 Norops tropidolepis Hacienda Prado, CR 3707 3 C Fitch, 1973 Scincidae Sphenomorphus cherriei Turrialba, CR 2606 4 S Fitch, 1973 Sphenomorphus cherriei La Selva, CR 3962 3 C this study desiccation of eggs during the dry season might play a role in creating observed variation in population density within and among years. Desiccation of terrestrial eggs may also occur at La Selva, although the dry season is shorter and less severe there than at many rain-forest sites in Panama, including BCI (see Table 1 in Sexton et al., 1971). A controlled experiment in which soil moisture and food abundance are manipulated and the interactions between those factors quantified may help to determine the mechanisms creating observed dry-season declines in lizard reproduction on Barro Colorado Island and at La Selva. Environmental and Phylogenetic Effects. Our results based on an analysis of previously published data indicated that, when phylogenetic effects are removed from the analysis, mean annual rainfall was a significant predictor of reproductive seasonality, whereas dry season length was not. Although many studies have shown that squamate reproduction is related to rainfall patterns over the course of a year at a site (i.e., Ameiva ameiva in the Brazilian Cerrado, Colli, 1991; Kentropyx lizards in Brazilian grasslands, Vitt and DeCarvalho, 1992; snakes in a tropical Australian floodplain, Madsen and Shine, 2000), our analyses indicate that even across multiple taxa and sites, local environmental conditions in the form of total annual rainfall play a role in determining the phenology of reproduction of at least some Neotropical lizards. In conclusion, we found that two lizard species at La Selva (the gecko L. xanthostigma and the

NEOTROPICAL LIZARD PHENOLOGY 347 skink S. cherriei) probably reproduce continuously throughout the year, whereas the anole N. limifrons shows a short but distinct decline in reproduction during the dry season. A similar pattern has been seen in N. limifrons at Barro Colorado Island in Panama, where desiccation of eggs during the dry season is thought to inhibit reproduction and Guyer (1986) reported a decline in juvenile recruitment during the dry season in N. humilis at La Selva. Finally, a phylogenetically independent analysis indicated that the reproduction of Neotropical lizards with one- and two-egg clutches tended to be continuous in areas with high annual rainfall and seasonal in areas with low rainfall. This indicates that, although phylogenetic effects certainly play a role in determining whether a species can reproduce continuously, local environmental conditions are also important, at least for the taxa included in our analysis. Acknowledgments. 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