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Home , Cerberus rynchops, Cylindrophis, Cylindrophis ruffus, Elapidae, Enhydris, Erpeton

Copeia 2009, No. 1, 7–20

Reproductive and Trophic Ecology of an Assemblage of Aquatic and Semi-Aquatic in Tonle Sap,

Sharon E. Brooks1, Edward H. Allison2, Jennifer A. Gill3, and John D. Reynolds4

We studied the reproductive and trophic ecology of a group of aquatic and semi-aquatic snakes that face severe hunting pressure in Cambodia. Over a two-year period we sampled hunters’ catches, measuring and dissecting a total of 8982 specimens of seven , five of which belong to the family . The seven species— enhydris, Enhydris longicauda, buccata, Enhydris bocourti, tentaculatus, Xenochrophis piscator, and ruffus—all inhabit Tonle Sap Lake, the largest lake in South-East . All species are sexually dimorphic in either body size or tail length. The larger species, E. bocourti and H. buccata, have a larger size at maturity, and the non- homalopsids, X. piscator and C. ruffus, have the highest and lowest fecundities, respectively. Clutch size increases significantly with female body size in all species, and with body conditioninE. enhydris. Our data also suggest that relative investment in reproduction increases with size in E. enhydris, which has the largest sample size. All species except one are synchronized in their timing of reproduction with the seasonally receding flood waters of the lake. There was variation in both the frequency of feeding and the prey size and type among species, with the homalopsids more similar to one another than to the other non-homalopsid species. The prey to predator mass ratio ranged from 0.04 to 0.1 in the homalopsids, compared to 0.15 to 0.17 in the non-homalopsids. There was also variation in the feeding frequency between the sexes that differed between species and six species continued to feed while gravid. These detailed life history analyses can help provide a basis for assessing conservation options for these heavily exploited species.

ONLESapLakeinCambodiaishometoan in the 1970’s (Saint Girons and Pfeffer, 1971; Saint Girons, assemblage of aquatic and semi-aquatic snakes that 1972). T are heavily exploited and traded as a food supply for Tonle Sap Lake is the largest wetland in South-East Asia the numerous crocodile farms surrounding the lake (Stuart and exhibits an extraordinary seasonal fluctuation in water et al., 2000). As a result of the growing demand from this level and size. As a result of the rising waters of the Mekong industry over the last 20 years, this exploitation now River during the monsoon season each year, the Tonle Sap represents the world’s largest snake hunting operation, with River reverses and Mekong water flows into the Tonle Sap an estimated 6.9 million snakes removed annually (Brooks Lake, inundating a large expanse of forest (Bonheur and et al., 2007a, 2007b), yet it proceeds without knowledge of Lane, 2002). This lake receives intense fishing pressure, and the basic population biology of the species involved. This it has been suggested that homalopsids thrive in such areas study aims to increase our understanding of the reproduc- due to reductions in size composition of communities, tive and trophic ecology of these snake populations as part increasing the snakes’ food supply while decreasing the of a program to assess the severity of this threat. abundance of their natural predators (Murphy, 2007). Five of the species in this community belong to the family However, in recent years, decreasing fish catches from the Homalopsidae. There is also a member of the Natricidae lake have led to human exploitation of several snake species, (Xenochrophis) and a member of the Cylindrophiidae primarily to provide food for the growing number of (Cylindrophis). Homalopsidae consists of approximately 37 crocodile farms, and some snake species now face the viviparous species distributed throughout South and South- likelihood of population declines (Brooks et al., 2007a). East Asia from to North (Gyi, 1970; Voris et While most of the species in this study are widely distributed al., 2002; Murphy, 2007). The greatest diversity and throughout the region, the Tonle Sap Water Snake, Enhydris abundance is in South-East Asia, where the snakes are longicauda, is endemic to the Tonle Sap Lake and River. The largely found in lowland freshwater habitats (Voris and status of this species has not been assessed, but its limited Karns, 1996). Homalopsids can comprise a large part of the distribution and high level of exploitation throughout its vertebrate biomass of the aquatic systems they inhabit range raises strong conservation concerns. (Voris and Karns, 1996), and there is speculation that some The extreme level of exploitation of snakes at this study species may thrive in areas dominated by human activities site allowed assessment of a large number of specimens that such as rice cultivation, which may provide suitable habitat had been killed during routine hunting operations. Here we and food supplies (Gyi, 1970; Murphy and Voris, 1994). explore life history variation within and among species While there is a growing literature on the ecology of throughout the year, to identify breeding seasons and to homalopsid species (Jayne et al., 1995; Voris and Karns, describe the ecological traits of this aquatic and semi-aquatic 1996; Murphy et al., 1999; Karns et al., 1999–2000), snake community. Inter-specific comparisons are included reviewed by Murphy (2007), the Cambodian populations as they can be useful for predicting how species will differ in have received little attention since the work of Saint Girons their response to exploitation. The large sample sizes

1 Department of Geography, University of Cambridge, CB2 3EN, Cambridge, U.K.; E-mail: [email protected]. Send reprint requests to this address. 2 The WorldFish Center, P.O. Box 500, GPO, 10670 Penang, , and School of Development Studies, University of East Anglia, Norwich NR4 7TJ, U.K. 3 School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, U.K. 4 Department of Biological Sciences, Simon Fraser University, Burnaby, BC, V5A 1S6, Canada. Submitted: 20 April 2007. Accepted: 11 June 2008. Associate Editor: G. Haenel. F 2009 by the American Society of Ichthyologists and Herpetologists DOI: 10.1643/CE-07-102 8 Copeia 2009, No. 1 available for some species have allowed us to adopt some used as an indication, which we include here for compar- analytical approaches used by fish biologists for studies of ative purposes (Fitzgerald et al., 1993; Blouin-Demers et al., population dynamics. 2002). However, variation between individuals in size at maturity makes this method heavily sample-size dependent. MATERIALS AND METHODS We therefore also adopted a more representative and statistically robust method, which is widely used in fisheries research (Jennings et al., 2001), to estimate the length at Study site.—Biological monitoring programs were based at which 50% of the female population is mature (SVL50), Chong Khneas landing site in Siem Reap province on the based on a logistic regression of the length of mature versus northern side of Tonle Sap Lake in Cambodia. This is the immature females: most important location for snakes being transported from . { z the lake as a result of the high number of crocodile farms in PMðÞ~ 1 1 z e ðÞa bðÞSVL , Siem Reap province. where P(M) is the probability of being mature, a is the y- Study species.—We purchased a total of 8982 dead snakes intercept, and b is the coefficient for the predictor variable from traders on a weekly basis during two hunting seasons (SVL). The SVL when the probability of being mature is 50% that extended from June 2004 to March 2005 and June 2005 was then calculated as: to March 2006. Seven species that occur regularly in the ~ trade were included in the study, with sample sizes that vary SVL a=b: according to their abundance in catches. We measured (snout to vent length [SVL] and total length), weighed, and An alternative indicator of size is mass, which might be sexed 4356 Enhydris enhydris, 1634 Enhydris longicauda, 1609 more appropriate for comparisons among species, due to , 141 Enhydris bocourti,869Erpeton differences in shape. As our mass measurements included tentaculatus, 234 Xenochrophis piscator, and 139 Cylindrophis gravid females, we could not use the above method to make ruffus. We analyzed each species for sexual dimorphism of direct calculations of the mass at which 50% of the female body mass, length, and tail length and for the relationship population is mature. Instead, we used length–mass rela- between body length and mass, which we square-root tionships within each species to convert the length at 50% transformed. Only non-reproductive females were used in female maturity to mass at 50% female maturity. analyses using mass, as the mass of the clutch could bias the We measured the right testis of dissected males and results. estimated volume from length and width based on the formula for a prolate spheroid (vol 5 4/3p (K teste length) N 2 Sampling issues.—We sampled snakes by haphazardly select- (K teste width) (Harlow and Taylor, 2000). As the mass of ing crates of snakes as they arrived at the landing site to the gonads was unknown, the gonadosomatic index (GSI), ensure the data were as representative of catch composition which is a measure of the mass of the testis relative to the as possible. The size composition of the catch is influenced mass of the , could not be calculated. Instead we by the size-selective capture technique. The gill nets used in calculated the testis volume per 100 g snake in order to take Tonle Sap capture a large range of sizes of reproductive-aged account of the varying size of males. individuals of most species, but large adults of the two larger species, H. buccata and E. bocourti, are not caught by this Trophic ecology.—We examined stomach contents of indi- method. For these two species, we therefore sampled the viduals of all seven species between June 2004 and March larger adults from those that had been caught by baited 2006. Presence or absence of food items was noted and hooks and traps. identified into broad taxonomic groups where possible. When prey items were intact, we weighed and measured Reproductive biology.—For each female we recorded the them and where possible identified the species. We retrieved reproductive state as inactive, vitellogenic, or embryonic. 277 intact prey items, of which 249 were from the stomachs Embryonic eggs were categorized as follows: A1—egg of three species; E. enhydris, E. longicauda, and H. buccata. All fertilized and oviducal but no embryo yet visible, A2—small of the data in these analyses were checked for a normal embryo present, A3—scales present on the embryonic snake, distribution and log transformed where necessary. A4—pigmentation of the embryonic snake present but not complete and brain still visible, A5—fully developed, RESULTS resembling a neonate. This classification was adapted from the 37 stages identified in Thamnophis sirtalis (Zehr, 1962). We considered females as reproductively mature when they Sexual dimorphism and sex ratios.—All species, except H. contained vitellogenic follicles or oviducal eggs or showed buccata, show sexual dimorphism of body size with females evidence of being post-partum, indicated by a thickened and significantly longer and/or heavier than males (Table 1). muscular oviduct. Reproductively inactive females showed a The lack of sexual size dimorphism in H. buccata and E. ribbon-like oviduct. However, as the oviduct regresses after bocourti with regard to length is likely to be the result of each reproductive bout, mature females that have bred insufficient sampling in the upper range of body size by the previously but have yet to thicken their oviduct in this size-selective gill net fishery. Sexual size dimorphism is season would be scored as immature, resulting in a slight reflected in the maximum sizes of individuals in our samples bias in this method, particularly if females do not breed where females are two to three times heavier than males. every year (Harlow and Taylor, 2000; Keogh et al., 2000). This difference is also illustrated in the mass–length There is no standard method for determining the size or relationships, where females of all species except C. ruffus age at maturity in . Often the minimum size at which accrue a greater mass per unit length increase (Table 1). All gravid or reproductively active individuals are observed is species, other than C. ruffus, exhibit significant sex differ- rose l—clg fepotdsnakes exploited of al.—Ecology et Brooks

Table 1. Sex Ratios and Sexually Dimorphic Traits of the Seven Water Snake Species. Sex ratios are reported as the number of males/females. Where two values are given, these represent two samples of smaller snakes (captured by gillnet; 25–86 cm SVL) and larger ones (captured by baited hooks and traps; 56–135 cm SVL). The linear relationships between mass and SVL are given. P values are derived from t–tests comparing differences between the sexes for mass, SVL, and tail length (**** P , 0.0001, *** P , 0.001, ** P , 0.01, * P , 0.05).

Sqrt mass (y) 2 Sqrt SVL (x) Tail length as proportion of regression equation (R2) Mass (g) mean 61 SE (max) SVL (cm) mean 61 SE (max) SVL mean 61SE Sex ratio Species (M:F) female male female male P female male P female male P Enhydris 1.44 y 5 3.938x 2 y 5 2.854x 2 97.8 6 1.2 81.5 6 0.5 **** 50.5 6 0.2 47.6 6 0.1 *** 0.28 6 0.32 6 *** enhydris 17.617 (0.70) 10.747 (335) (285) (74.1) (69.3) 0.001 0.001 (0.54) n 5 1154 n 5 2448 n 5 1826 n 5 2371 Enhydris 0.83 y 5 4.810x 2 y 5 4.143x 2 150.9 6 2.6 117.5 6 4.6 **** 48.9 6 0.2 44.2 6 0.2 **** 0.27 6 0.34 6 **** longicauda 21.258 (0.79) 17.025 (518) (260) (89) (59.7) 0.002 0.002 (0.57) n 5 892 n 5 725 n 5 911 n 5 691 Homalopsis 1.18 / 0.72 y 5 4.109x 2 y 5 3.835x 2 242.4 6 5.5 249.8 6 3.8 NS 74.0 6 0.5 74.0 6 0.5 NS 0.29 6 0.34 6 **** buccata 19.434 (0.80) 17.478 (1740) (615) (134.5) (100.0) 0.002 0.002 (0.78) n 5 730 n 5 722 n 5 875 n 5 698 Enhydris 1.2 / 0.55 y 5 4.947x 2 y 5 3.671x 2 267.9 6 31.8 196.9 6 14.7 * 57.3 6 2.6 53.2 6 1.7 NS 0.15 6 0.22 6 **** bocourti 21.32 (0.91) 13.192 (1110) (559) (105) (98.5) 0.006 0.008 (0.65) n 5 65 n 5 71 n 5 70 n 5 71 Erpeton 1.06 y 5 3.559x 2 y 5 3.460x 2 104.1 6 2.3 81.8 6 1.3 **** 50.1 6 0.3 45.9 6 0.2 **** 0.43 6 0.52 6 **** tentaculatus 14.939 (0.62) 14.386 (387) (297) (77.5) (70) 0.004 0.004 (0.54) n 5 323 n 5 443 n 5 366 n 5 380 Xenochrophis 0.70 y 5 4.81x 2 y 5 3.601x 2 160.1 6 10.1 103.1 6 3.8 **** 60.6 6 1.0 50.4 6 0.7 **** 0.36 6 0.41 6 *** piscator 25.18 (0.78) 15.586 (620) (222) (89) (67) 0.012 0.011 (0.66) n 5 106 n 5 98 n 5 113 n 5 75 Cylindrophis 0.54 y 5 3.69x 2 y 5 5.31x 2 224.4 6 8.0 220.9 6 10.5 NS 71.5 6 0.8 68.6 6 1.2 * 0.021 6 0.019 6 NS ruffus 16.22 (0.41) 29.05 (0.73) (410) (379) (86.4) (80.5) 0.003 0.0004 n 5 79 n 5 48 n 5 78 n 5 37 9 10 Copeia 2009, No. 1

Table 2. The Estimated Size at Maturity of Water Snakes from Logistic Regression Models of Percentage Mature Females in Relation to Snout–Vent

Length (SVL). SVL at 50% maturity (SVL 50) is shown and converted to mass at 50% maturity (Mass 50) using the linear relationships given in Table 1 (** P , 0.0001, * P , 0.01). Exp b represents the change in probability of an individual being mature with a unit change in SVL according to the model for each species. The % predicted correctly indicates how accurately the model can predict maturity based on SVL. The minimum size (SVL) of mature females observed is also shown with the total number of mature females observed (n).

Minimum SVL at SVL50 (SVL at Log- Chi- % predicted Mass50 (Mass at Species maturity (cm) (n) maturity (cm)) likelihood squared Exp b (95% CI) correctly maturity (g)) Enhydris enhydris 41.0 (836) 48.73** 392.6 194.8 1.387 80.8 96.44** (1.302–1.478) Enhydris longicauda 38.8 (319) 44.75** 461.5 88.6 1.207 74.6 119.23** (1.153–1.263) Homalopsis buccata 67.2 (291) 81.26** 369.5 493.3 1.411 89.1 310.05** (1.337–1.490) Enhydris bocourti 66.5 (16) 71.32** 12.7 31.7 1.198 90.6 418.39** (1.053–1.362) Erpeton tentaculatus 37.8 (188) 47.23** 250.7 68.6 1.287 74.1 90.55** (1.196–1.384) Xenochrophis piscator 45.4 (38) 60.51* 69.9 3.4 1.052 54.7 149.40* (0.995–1.113) 61.2 (37) 63 (P50.1) 32.1 2.5 1.153 79.4 170.50 (0.953–1.395) ences in tail length, with males having considerably longer estimated size at maturity as a minimum and the maximum tails—a widely reported sexually dimorphic trait in snakes observed female body size as a maximum (Fig. 2). The size- (Table 1). selective capture method may influence the estimated mean The sex ratios reported here show considerable variation clutch size for some of the populations, particularly H. between species and, for five of the seven, they deviate buccata and E. bocourti. Figure 2 illustrates considerable significantly from 1:1, with E. enhydris the most male-biased variation in fecundity among species, with the non-homa- and C. ruffus the most female-biased (Table 1). In H. buccata lopsids, X. piscator and C. ruffus, showing the highest and and E. bocourti, the observed sex ratio shifts from male- lowest fecundities, respectively. The homalopsids had inter- biased in smaller snakes (first value) to female-biased in mediate clutch sizes, which appear similar to one another. larger snakes (second value), and therefore sex ratios become Body condition (BC), measured as mass of females with skewed in favor of the females at upper ranges of body sizes. litters removed divided by SVL, has a significant positive relationship with clutch size (CS) in E. enhydris (CS 5 2 Size at maturity.—For all species other than C. ruffus, the 5.41(BC) 2 2.11, R 5 0.35, F1,197 5 101.3, P , 0.0001) and SVL50 could be estimated using logistic regression. These the same trend is apparent in E. longicauda, although the 2 values are converted into mass at maturity (Table 2) using relationship is weaker (CS 5 2.60(BC) + 5.57, R 5 0.36, F1,9 the linear length–mass relationships given in Table 1. There 5 5.0, P , 0.052). Sample sizes were too small to test for was considerable variation among the species in mass at relationships in the other species. maturity, with H. buccata and E. bocourti maturing at a much An ANCOVA with egg stage as a fixed factor and SVL as a larger size than the other species, and E. tentaculatus covariate showed that, for any given size of snake, clutch followed by E. enhydris maturing at the smallest size. Size sizes of vitellogenic eggs are significantly larger than those at maturity for males is unknown for all species as we did of embryonic eggs in E. enhydris (F1,647 5 493.7, P , 0.0001). not record any immature males. Enhydris longicauda shows a similar trend of a reduction in clutch size from vitellogenic to embryonic stages, but this Reproductive output.—Females of all species exhibit a strong was not significant (F1,183 5 0.66, P 5 0.42; Table 3). For E. positive relationship between clutch size and body size enhydris the decline in clutch size occurs post-fertilization, as (Fig. 1). An ANCOVA with clutch size as the dependent post hoc analysis of a one-way ANOVA shows that the variable, species as a factor, and SVL as a covariate showed number of eggs at stages A2 to A5 are significantly lower that clutch sizes differed significantly between species than those at the vitellogenic (yolk) or fertilized (A1) stage (F6,1069 5 5.33, P , 0.0001). Bonferroni-corrected post hoc (F5,671 5 17.63, P , 0.0001). In contrast, for E. longicauda comparisons showed X. piscator had significantly larger there is some decline in clutch size between vitellogenic and clutch sizes than all other species, and C. ruffus, E. bocourti, fertilized eggs and then again between fertilized and full and H. buccata had significantly smaller clutches than the term embryos (A5), although these differences are not other species (P , 0.05). An interaction effect between SVL statistically significant (F2,189 5 1.56, P 5 0.21). For both and species demonstrated that there were significant of these examples, there is greater variation for the more differences between the species in the relationship between developed stages due to smaller sample sizes. No significant clutch size and SVL (F6,1069 5 15.78, P , 0.0001), with the differences were seen between the clutch sizes of vitellogen- most notable difference being the weak relationship shown ic and embryonic eggs in any of the other species, although by E. longicauda (Fig. 1). this may partly be an artifact of low sample sizes, The potential ranges of fecundities can be estimated from particularly for E. bocourti and C. ruffus. Xenochrophis piscator the linear fit of clutch size against SVL and using the is oviparous and therefore does not appear in this analysis. Brooks et al.—Ecology of exploited snakes 11

Fig. 1. Fecundity–body length relationships for seven snake species. Clutch size is measured as the number of eggs per breeding bout and is combined for vitellogenic and embryonic eggs. Each data point represents a gravid female. Linear regression equations and R2 values can be found in Table 3. 12 Copeia 2009, No. 1

Neonate size also varies significantly between species (F3,174 5 22.72, P , 0.0001) with the largest species, E. bocourti, producing larger offspring (Table 3). No full-term neonates were observed in individuals of H. buccata, E. tentaculatus, or X. piscator.

Timing of reproduction.—All species, except C. ruffus, breed at the same time. Females undergo vitellogenesis in November and December, which matches the timing of the seasonal reduction in water levels in the lake (Fig. 3). Developing embryos were observed in successive months, and, although this varies between species, embryogenesis appears to be taking place mostly in February and March. Enhydris enhydris is an exception because it displays two breeding seasons. The Fig. 2. Fecundity ranges for seven snake species, based on the linear first period of vitellogenesis occurs as the water starts to rise regressions of clutch size (number of eggs) versus SVL shown in Fig. 1. in July and August with embryogenesis taking place between Minimum values are based on the estimated clutch size at length at August and October, and the second period matches the maturity (Table 2) and maximum values are based on the estimated other five species (Fig. 3). In all species, peaks in testis size clutch sizes at maximum observed female length. The mean observed are synchronized with female vitellogenesis (Fig. 3). For E. clutch sizes are also shown. enhydris, this occurs in both July and December, and for all other species, except for C. ruffus, the peaks occur between The relative clutch mass (RCM), calculated as the mass of October and December. the clutch/maternal mass, was derived from females con- taining embryonic eggs for four of the species. This is a Trophic ecology.—The diet of this assemblage shows a measure of the reproductive effort made by a female per striking difference between the five homalopsids and the breeding bout. Cylindrophis ruffus shows a considerably two non-homalopsids, X. piscator and C. ruffus (Table 4). higher RCM than the others, and H. buccata exhibits the Whereas the homalopsids fed nearly exclusively on , lowest (Table 3). Enhydris enhydris showed a slight positive the other two species ate a significant amount of non-fish relationship between RCM and body length (RCM 5 prey (Table 4). Xenochrophis piscator has the most diverse 2 0.004(SVL) 2 0.078, R 5 0.11, F1,200 5 25.94, P , 0.0001). diet, with the major components being fish (77%) and frogs A similar trend was seen in E. longicauda, although the (16%). For C. ruffus, 40% of the diet was composed of snakes sample size was small and the relationship was not and 60% (family Synbranchidae). The prey species of statistically significant (RCM 5 0.008(SVL) 2 0.217, R2 5 snake identified were E. enhydris (80%) and E. tentaculatus 0.04, F1,9 5 0.41, P 5 0.54). SVL is strongly correlated with (20%), n 5 5. One individual of H. buccata contained a frog mass, which is the denominator for RCM. Existence of a in its stomach. positive relationship therefore provides evidence that the In total, ten fish families were identified within the relative investment in reproduction increases with an stomachs of this snake assemblage, with the two common- increase in body size. There were insufficient data to est families being Cyprinidae (minnows and carps) and determine if this relationship existed in the other species. Osphronoemidae (gouramies). Of the cyprinids, all fish

Table 3. Reproductive Allocation for Seven Water Snake Species. R2 values and linear regression equations are given for the relationships between clutch size and body size shown in Figure 1 (* P , 0.05, ** P , 0.001, *** P , 0.0001). Mean sizes of vitellogenic and embryonic clutches are given. Mean relative clutch mass (RCM) and neonate length are given for species for which data exist.

Clutch size Mean relative clutch mass Mean Clutch size–SVL relationship Vitellogenic Embryonic (litter mass / neonate total Mean Mean maternal mass) length (cm) Species R2 Linear equation Range (6 1 SE) Range (6 1 SE) (61 SE) (61 SE) Enhydris enhydris 0.43 *** y 5 0.602x–20.28 4–34 13.5 6 0.30 2–28 10.6 6 0.32 0.15 6 0.001 18.9 6 0.16 (n 5 414) (n 5 263) (n 5 213) (n 5 75) Enhydris longicauda 0.44 *** y 5 0.865x–25.98 6–44 19.4 6 0.57 5–24 16.23 6 1.2 0.15 6 0.03 17.5 6 0.33 (n 5 179) (n 5 13) (n 5 12) (n 5 23) Homalopsis buccata 0.39 *** y 5 0.404x–23.98 4–23 11.7 6 0.35 4–24 12.4 6 1.1 0.10 6 0.02 (n 5 106) (n 5 19) (n 5 5) Enhydris bocourti 0.72 * y 5 0.345x–16.88 6–20 13.6 6 2.66 11 11.0 (n 5 1) 25.0 6 0.14 (n 5 5) (n 5 4) Erpeton tentaculatus 0.28 *** y 5 0.432x–9.834 3–29 12.2 6 0.49 6–29 13.9 6 1.21 (n 5 79) (n 5 24) Xenochrophis piscator 0.73 *** y 5 1.24x–46.075 9–74 33 6 3.28 (n 5 29) Cylindrophis ruffus 0.90 ** y 5 0.293x–11.869 4 4 (n 5 1) 6–14 9.4 6 0.85 0.41 6 0.04 19.4 6 0.23 (n 5 9) (n 5 8) (n 5 76) Brooks et al.—Ecology of exploited snakes 13

Fig. 3. Breeding seasons for the seven snake species. The bars represent the percentage of all females that were reproductive, including vitellogenic (white bars) and embryonic (solid bars). The line represents the mean testis volume 6 standard error. Data shown are from June 2004 until March 2006 and no data exist for April and May 2005. The sparse amount of data for 2004, for all species except E. enhydris, is the result of lower sampling effort that year. The graph in the bottom left-hand corner illustrates the seasonal fluctuation of water level in the lake (data extracted from MRC/FIN Water Utilisation program, 2000). species belonged to the Trichogaster and of the and prey mass as the dependent variable, with sex and ophronoemids most belonged to the genera Henichorynchus species of snake as factors and SVL as the covariate. Only E. (56%), Cyclocheilichthys (19%), and Opsarius (15%). enhydris, E. longicauda, and H. buccata were included in this Across all species, prey size increased with snake SVL. A analysis due to the low sample sizes for all other species. two-factor ANCOVA was conducted using both prey length Unsurprisingly, snakes with a larger SVL consumed larger 14

Table 4. Dietary Data for Both Sexes of All Seven Species. % containing food represents feeding frequency. Prey size (length and weight) taken from a smaller sample of intact prey items. Prey type identified into broad taxonomic groups and into fish families for a smaller sub-sample.

Enhydris Homalopsis Erpeton Xenochrophis Enhydris enhydris longicauda buccata Enhydris bocourti tentaculatus piscator Cylindrophis ruffus MFMFMFMFMFMFMF % containing food (n) 42.0 53.3 44.4 47.6 38.1 43.3 44.1 47.1 34.1 33.7 75.3 60.7 20.8 17.1 (2341) (1658) (720) (906) (707) (874) (68) (68) (443) (424) (97) (135) (48) (88) Number of measured prey 25 58 14 41 49 62 5 4 3 2 2 4 1 7 Mean prey length 6 SE (mm) 69.3 6 81.9 6 79.5 6 93.7 6 97.6 6 110.3 6 92.7 6 80.5 6 49.4 6 101.0 6 97.9 6 69.9 6 106.3 6 3.4 2.8 6.3 3.5 2.8 5.3 23.3 26.6 1.2 40.9 44.9 15.1 57.8 57.6 Mean prey weight 6 SE (g) 3.2 6 7.1 6 7.7 6 10.7 6 15.1 6 21.3 6 13.5 6 10.9 6 2.2 6 10.7 6 9.0 6 12.7 6 51.5 6 0.27 0.63 1.8 1.3 1.4 3.4 6.0 4.4 0.4 7.7 4.1 2.4 61.0 10.5 Prey types No. identified to broad 307 376 80 153 139 199 15 10 33 37 28 47 5 15 taxonomic gp % Serpente 0 0 000000000040.0 42.3 % Anuran 0 0 0 0 0 0.5 0 0 0 0 14.3 17.0 0 0 % Rodent 0 0 000000003.63.200 % Bird 0 0 0000000002.100 % Insect 0 0 0000000002.100 % Fish 100 100 100 100 100 99.5 100 100 100 100 82.1 75.5 60.0 57.7 Number fish identified to family 26 34 11 35 50 66 5 4 2 1 0 3 0 3 % Family Anabantidae 3.9 8.8 18.2 17.1 56.0 59.1 0 0 0 0 0 33.3 0 0 % Family Bagridae 0 0 0 8.6 0 0 20.0 0 50.0 0 0 0 0 0 % Family Channidae 0 0 0 2.9 6.0 9.1 0 0 0 0 0 0 0 0 % Family Cyprinidae 73.1 52.9 27.3 42.9 2.0 3.0 0 0 0 0 0 0 0 0 % Family Mastacembilidae 0 0 0 0 0 3.0 0 0 0 0 0 0 0 0 % Family Nandidae 3.9 11.8 18.2 2.9 0 0 0 0 0 0 0 0 0 0 % Family Osphronemidae 19.2 26.5 36.4 25.7 36.0 25.8 40.0 50.0 50.0 100.0 0 33.3 0 0 % Family Pangasiidae 0 0 0000025.0 0 0 0 0 0 0 % Family Siliridae 0 0 000020.0 0 0 0 0 0 0 0 % Family Synbranchidae 0 0 000020.0 25.0 0 0 0 33.3 0 100.0 Copeia 09 o 1 No. 2009, Brooks et al.—Ecology of exploited snakes 15

Fig. 4. Prey mass relative to predator mass (6 standard error). Symbols a, b, and c denote homogeneous subsets to which the species belong, derived from post hoc analyses following a one-way ANOVA of mean prey/predator mass ratio. Those with different symbols are therefore statistically significantly different from one another.

prey (prey length F1,232 5 62.78, P , 0.0001, log prey weight DISCUSSION F1,234 5 45.79, P , 0.0001), but both species identity and sex had an independent effect on prey size (species effect: prey Sexual dimorphism and sex ratios.—All species are sexually length F 5 4.49, P , 0.05, log prey mass F 5 10.37, P 2,232 2,234 dimorphic either in overall size, with females heavier or , 0.0001 and sex effect: prey length F 5 3.21, P , 0.05, 3,232 longer than males, or in tail length, with males having log prey mass F 5 3.68, P , 0.05). Homalopsis buccata 3,234 longer tails. Sexual size dimorphism may be the result of consumed much larger prey, followed by E. longicauda with females growing more quickly rather than living longer, as E. enhydris consuming the smallest prey. Females of all has been shown in studies of northern water snakes, Nerodia species consumed larger prey than males both in absolute sipedon (Weatherhead et al., 1995). The direction and terms (Table 4) and after controlling for SVL (statistics magnitude of sexual size dimorphism depends on relative above). Analyses of prey to predator mass ratios showed benefits and costs of growth and size in each sex (Andersson, that the two non-homalopsids ate much larger prey items 1994). These are typically determined by size–fecundity relative to their body size than did the homalopsids (Fig. 4). benefits in females and size–competitive benefits in males Contingency table analysis revealed that there were (Fairbairn, 1997; Sze´kely et al., 2004). We have shown strong significant differences between the species in their feeding size–fecundity relationships in females of most species, 2 frequency (x 6 5 86.74, P , 0.0001), with most of the suggesting that larger body size could be favored by variation resulting from the low count for C. ruffus (Fig. 5). selection for greater reproductive output. Cylindrophis ruffus, Within some species, there were significant differences however, showed weak sexual size dimorphism, despite a between the sexes; E. enhydris and H. buccata showed strong size–fecundity relationship in females. It is possible significantly higher feeding frequencies in females and less that a large male size offers advantages that are absent in the 2 2 in males than expected (x 1 5 48.88, P , 0.0001 and x 1 5 other species, for example, through combat or displacement 4.37, P , 0.05, respectively), and X. piscator showed of other males in mating aggregations (Weatherhead et al., significantly higher feeding frequencies in males and less 1995). In species for which male–male combat has been 2 in females than expected (x 1 5 72.03, P , 0.0001; Fig. 5). shown, males usually reach a larger size than females (Shine, Comparisons were also made between feeding frequencies 1978, 1994a). Tail length relative to body length has been for breeding and non-breeding females. When breeding, E. shown to be another sexually dimorphic trait in many snake 2 enhydris fed less frequently (x 1 5 25.07, P , 0.0001) and E. species, with males having longer tails than females, as a 2 longicauda fed more frequently (x 1 5 7.0, P , 0.001). No result of sexual selection for male mating success (Shine et breeding individuals of C. ruffus were found with food in al., 1999). In this study, the lack of tail size dimorphism in their stomachs, but this finding did not differ from the other C. ruffus again implies that this species may have a different species due to the low number of breeding individuals mating system than the others. encountered and the low feeding frequency for this species The size dimorphism exhibited by these snakes translates 2 (x 1 5 2.95, P 5 0.086; Fig. 5). into changes in sex ratios with size for H. buccata and E. 16 Copeia 2009, No. 1

Fig. 5. Proportion of individuals containing food in the stomachs. This is shown for males, females, non-breeding and breeding females for all species separately. Values above bars denote sample sizes. Where the number of females in the sample is greater than the sum of the breeding and non-breeding females, this is due to missing data on the reproductive status of females due to putrefication of specimens. bocourti, and consequently size-selective capture techniques reduction in fecundity between the years of the two studies. will be biased with regard to sex ratio. Most snakes show a Nonetheless, the clutch sizes and RCM values reported here 1:1 sex ratio at birth, although skewed sex ratios have been for the Cambodian populations of E. enhydris are still observed in a few species (Shine and Bull, 1977). Sex ratios considerably larger than those reported for this species in are difficult to determine due to differing activity patterns both and (Murphy et al., 2002). The between males and females (Shine, 1994b). Our study of E. Tonle Sap Lake in Cambodia is famous for its productive enhydris is a case in point. This species may form mating fisheries (Lim et al., 1999; Lamberts, 2006), and it is aggregations during the breeding season, as indicated therefore possible that there is a more abundant supply of through sightings by local fishers in Thailand (Murphy, fish available to the snakes here than in other parts of their 2007), and it has also been reported that males are attracted range. This could increase their body condition and account to fishing traps containing females. Such behavior could for the greater clutch sizes observed in Cambodia, compared account for the strong male-biased sex ratio seen for this with Thailand and Myanmar. species. The clutch sizes shown for H. buccata are consistent with the ranges seen in previous studies (Berry and Lim, 1967), Size at maturity.—Size and age at maturity are key life history and the larger average clutch size in our study may be due to variables that affect population vulnerability to exploitation a greater sampling of adults, which are sought and traded for (Reynolds, 2003). We report both mass and length as size their skins. Since Berry and Lim did not present size– parameters. Mass may be a better indication of inter-specific fecundity relationships, we cannot test whether this is the variation in age at maturity, as it indicates the biomass that correct explanation, but this underscores the importance of must be accumulated before a female is able to breed and is reporting fecundities as a function of body size. Clutch sizes independent of body shape. Enhydris bocourti, which for E. tentaculatus are higher than previously recorded, with matures at a smaller length than H. buccata, has a documented litter sizes ranging from 5 to 12 (Martinez and considerably greater mass at maturity. Similarly, E. long- Behler, 1988), compared to the range of 3 to 29 shown here. icauda, which matures at a relatively small length compared The range of SVL of females in our study is considerably to the other similar-sized homalopsids, has a greater mass at higher, and this could account for the difference. maturity. The use of mass, however, may be confounded by Relative clutch mass (RCM) is used as a measure of current body condition and stomach contents, which will reproductive effort and is often thought to reflect trade-offs vary independently of the sexual maturity of the snake. in allocation of resources among maintenance, storage, growth, and reproduction. The low RCM values reported Reproductive output and strategies.—The clutch sizes and here for the homalopsid species support previous research, mean relative clutch mass (RCM) reported here for E. which showed that aquatic viviparous snakes have a lower enhydris are considerably lower than those documented level of reproductive investment than terrestrial egg-laying previously in this lake (Murphy et al., 2002). This cannot be species (Seigel and Fitch, 1984; Shine, 1988). The long explained solely by differences in sample sizes because, reproductive season of viviparous species and the mobility despite our large sampling effort with this species, we did restriction of a large clutch mass when swimming are not find any female with a litter size as large as in this suggested to have resulted in selection for a low RCM. This previous study. This suggests that there may have been some is further supported by the higher RCM value reported here Brooks et al.—Ecology of exploited snakes 17 for C. ruffus and the large clutch size of X. piscator, the more whereby testis mass peaks prior to ovulation, a characteristic terrestrial species within this assemblage. of many tropical snake populations (Maunaga et al., 2003). Life history theory predicts a trade-off between clutch size For all species in this study, sperm production occurs while and offspring size, as has been reported within and among the majority of females are undergoing vitellogenesis. species (Fleming and Gross, 1990; Olsson and Shine, 1997; However, given the likelihood that the females have the Kolm et al., 2006). Across the species in this study, we see ability to retain sperm (Sever and Ryan, 1999), this suggestions of a negative trend between offspring size and synchronized timing of sperm production by the males to number, but this is confounded by variation in maternal the female’s fertile period is likely to be the result of sperm body size between the species. Our study suggests that H. competition. buccata and E. bocourti show a lower reproductive effort than Females of E. enhydris appear to breed all year round, but the other homalopsids, as a result of their smaller clutch there are two distinct peaks per year. This concurs with sizes at maturity. This is reflected in the low RCM of H. previous studies of this species (Saint Girons and Pfeffer, buccata. This has strong conservation implications for the 1971; Murphy et al., 2002). It is unknown whether a single relative vulnerability of these larger-bodied species (Brooks female is capable of breeding twice a year or whether the et al., 2007a). The relationship between RCM and body size pattern stems from different individuals breeding at differ- seen in E. enhydris suggests that reproductive effort increases ent times. We observed females that contained fat stores with age, at least for this species. This suggests that the when heavily gravid, whereas, in most snakes, fat stores allocation of resources to reproduction changes over time, become depleted during vitellogenesis (Scott et al., 1995). It perhaps with more energy being allocated to growth earlier is likely that this is typical of tropical aquatic snakes that on in life, given the advantages of large body size for lifetime show a high frequency of feeding, even while gravid, thus reproductive success. enabling them to undergo vitellogenesis soon after parturi- The reduction in clutch sizes between vitellogenic and tion. embryonic staged females shown for two of the species in Cylindrophis ruffus is the only species in this assemblage this study, E. enhydris and E. longicauda, indicates a lack of that does not breed when the lake is receding, but is efficiency in converting eggs into neonate snakes. It is synchronized with the first breeding season of E. enhydris. unclear whether this difference is due to lack of fertilization, We speculate that this species could be out of synchrony or whether eggs are aborted post-fertilization. There is no with flooding periods in order to synchronize with the evidence that squamate reptiles are able to resorb abortive periods of productivity of their prey, which include the eggs, based on the functional morphology of the oviduct other snakes in this assemblage. (Blackburn, 1998). Observations made during our study of solidified vitellogenic eggs in the oviduct alongside devel- Trophic ecology.—Previous studies of the two non-homalop- oping embryonic eggs in E. enhydris further support the view sids in this assemblage show them both to be top predators, that abortive eggs would be expelled rather than resorbed. with X. piscator feeding largely on frogs, and C. ruffus on and other snakes (Kupfer et al., 2006). This Reproductive synchrony and timing.—The flood pulse in river- matches our findings, although eels and other fish comprise floodplain systems is considered the principal driving force a significant proportion of their diet. The local Khmer name behind the seasonal patterns in productivity of the flora and for X. piscator is ‘poh sumlap gon gaeb’ which literally fauna of this region (Junk et al., 1989). The reproductive translates as ‘snake that eats frog.’ Cylindrophis ruffus has synchrony of all species except for C. ruffus therefore previously been reported to be a predator of homalopsids suggests that the flood pulse may be driving the seasonal (Voris and Murphy, 2002; Karns et al., 2005) but has never reproduction of this snake assemblage. Based on estimates of been reported to prey on E. tentaculatus. This snake has the gestation period of E. enhydris as 2 to 2.5 months, and H. clearly specialized to a diet of relatively large elongated prey buccata as 2 to 3 months (Saint Girons and Pfeffer, 1971; items, i.e., snakes and eels. Saint Girons, 1972), we expect that for all species except for The homalopsids in this study are almost entirely C. ruffus, parturition occurs during the dry season between piscivorous. This is in accordance with what was previously April and June. The newborn neonates would therefore be known for these species, although Deuve (1970) reported present in the floodplain at the onset of the rainy season crustaceans in the stomachs of H. buccata in , along with (May to June), prior to or just as the Mekong water floods fish and frogs (Voris and Murphy, 2002). There is a great deal the lake. This is when the majority of fish species within the of overlap between the fish diet of this snake community floodplain of Tonle Sap reproduce (Lim et al., 1999). The and the fish composition taken by the fishery on Tonle Sap, timing of reproduction by the snakes may therefore be with species of the family Cyprinidae dominating both (Lim timed to match the presence of optimal conditions for the et al., 1999). This highlights a potential connection between newborn snakes, such as availability of prey items (fish fry) human fishing activities and the snake populations. Tonle and the presence of nursery conditions when the grasslands Sap Lake is currently undergoing intense fishing at levels are beginning to flood. This information can help to inform that may be unsustainable (Bonheur and Lane, 2002), and conservation management strategies, such as closed hunting this is likely to have conservation implications for this snake seasons to protect species during the breeding season assemblage. However, based on this study, the homalopsids, (Brooks et al., 2007a). although restricted to a diet of fish, appear to be fairly non- The seasonal changes in testis volume reported here specialized feeders, which should increase their resilience to provide evidence for seasonal sperm production in these such effects. snakes. For most species, males show peak testicular activity The prey-to-predator mass ratios reported here for homa- between October and December prior to the presence of lopsids are lower than for other groups of snakes (Rodrı´guez- ovarian eggs in females. Spermatogenic cycles in the Robles et al., 1999; Greene and Rodrı´guez-Robles, 2003), and homalopsids can therefore be said to be pre-nuptial, given that larger prey items are available, at least for the 18 Copeia 2009, No. 1 smaller of the species, this suggests they are restricted in Councils (NERC and ESRC). This is WorldFish contribution their choice of prey with regard to size. Other homalopsids number 1879. have been shown to consume relatively small prey items (Jayne et al., 1988), and some have been shown to tear large LITERATURE CITED prey items into smaller pieces, thus overcoming gape limitations (Jayne et al., 2002). Andersson, M. 1994. Sexual Selection. Princeton University Sex differences in feeding biology shown in this study can Press, Princeton, New Jersey. be explained by sexual dimorphism in body size, with the Berry, P. Y., and G. G. Lim. 1967. The breeding pattern of larger snakes taking larger prey items. However, it has been the Puff-Faced Water Snake, Homalopsis buccata Boulen- suggested in other studies that the difference in choice of ger. Copeia 1967:307–313. prey size between males and females may drive this sexual Blackburn, D. G. 1998. Structure, function, and evolution size dimorphism (Shetty and Shine, 2002; Shine et al., 2002). of the oviducts of squamate reptiles, with special reference In this study we see considerable overlap between the sexes to and placentation. The Journal of Experimen- in their choice of prey, providing no evidence that males tal Zoology 282:560–617. and females follow separate allometric trajectories with Blouin-Demers, G., K. A. Prior, and P. J. Weatherhead. regard to prey size. 2002. Comparative demography of black rat snakes We found high and consistent feeding rates throughout (Elaphe obsoleta) in Ontario and Maryland. Journal of the wet season, even through pregnancy, which matches Zoology 256:1–10. previous studies of tropical aquatic snakes (Shine et al., Bonheur, N., and B. D. Lane. 2002. Natural resources 2004; Karns et al., 2005). The homalopsids do not bask, and management for human security in Cambodia’s Tonle Sap their body temperature remains very stable (Murphy et al., Biosphere Reserve. Environmental Science and Policy 1999; Karns et al., 2002). They may therefore need to feed 5:33–41. continuously to sustain this metabolic rate as they cannot Brooks, S. E., E. H. Allison, and J. D. Reynolds. 2007a. seek out cooler refuges to digest food slowly. Cylindrophis Vulnerability of Cambodian water snakes: initial assess- ruffus, which feeds on larger prey, is more likely to be ment of the impact of hunting at Tonle Sap Lake. restricted in feeding while gravid, due to the physiological Biological Conservation 139:401–414. constraint of containing both eggs and large food items. Brooks, S. E., J. D. Reynolds, E. H. Allison, and B. Touch. This would also account for the lack of females observed 2007b. 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Murphy, and B. Stuart from the Field Gyi, K. K. 1970. A revision of colubrid snakes of the Museum of Natural History, Chicago and D. Karns from subfamily Homalopsinae. University of Kansas Publica- Hanover College, Chicago, who assisted us greatly with tions, Museum of Natural History 20:47–223. setting up the methodologies for this project and for sharing Harlow, P. S., and J. E. Taylor. 2000. Reproductive ecology their knowledge of homalopsid snakes. In particular we of the jacky dragon (Amphibolurus muricatus): an agamid thank J. Murphy and D. Karns who advised us in the field in lizard with temperature-dependent sex determination. Cambodia. We are grateful to C. Poole, J. Walston, S. Visal, Austral Ecology 25:640–652. H. Sovannara, and L. Kheng from the Wildlife Conservation Jayne, B. C., H. H. Voris, and K. B. Heang. 1988. Diet, Society Cambodia program and K. Davies, F. 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