Notes on the diets of seven sympatric snakes in the genera Agkistrodon, Nerodia, Sistrurus, and Thamnophis
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1 Herpetology Notes, volume 7: (2014) (published online on 16 April 2014) Notes on the diets of seven sympatric snakes in the genera Agkistrodon, Nerodia, Sistrurus, and Thamnophis Donald T. McKnight*, Joshua R. Harmon, Jennifer L. McKnight and Day B. Ligon Abstract. Diet samples were collected from seven snake species at a site in southeastern Oklahoma. New diet records were identified for five of the species (10 new records total). Southern copperheads (Agkistrodon contortrix contortrix) were generalists, consuming insects, mammals, lizards, and snakes. Western cottonmouths (Agkistrodon piscivorus leucostoma) also exhibited generalist tendencies, consuming fish, anurans, snakes, and a salamander. Broad-banded watersnakes (Nerodia fasciata confluens) consumed only anurans, and diamond-backed watersnakes (Nerodia rhombifer) ate only fish and anurans. An observation of feeding behaviour at a drying pool is also presented. Keywords: Serpentes, Foraging, Ecology, Predation Introduction Snakes are gape-limited, obligate predators with diets that are highly variable among species and, to a certain extent, even within species (Shine, 1991; King, 2002; Himes, 2003; Luiselli, 2006a). While there are dietary specialists among Serpentes, many snakes are dietary generalists, and ontogenetic diet shifts and dietary niche partitioning are common (Mushinsky, Hebrard, and Vodopich, 1982; Toft, 1985: Luiselli, 2006b; Luiselli, Akani, and Capizzi, 1988; Burghardt and Krause, 1999). This dietary elasticity and tendency towards dietary niche partitioning make it important to study a species diet across its range in order to get a full understanding of its ecology. This goal is often accomplished through multiple independent studies that, collectively, span a wide geographical range. In this paper, we present data on the diets of seven sympatric species of snake at a site in southeastern Oklahoma. These data include 10 new diet records for five of the species and notes on feeding behaviour at a drying pool. Department of Biology, Missouri State University, 901 South National Avenue, Springfield, MO *Corresponding author; donald222@live.missouristate.edu Materials and Methods Study Site This research was conducted at Boehler Seeps and Sandhills Preserve, located in Atoka County, Oklahoma. This site has two beaver-formed lakes (Boehler Lake and Hassel Lake) and several seasonal seeps and streams that connect to the lakes. These seeps and lakes form a rich wetland habitat, but away from the water the habitat rapidly transitions into a dry, upland, bluejack oak (Quercus incana) forest. This combination of habitats has resulted in a very diverse herpetological community (Patton and Wood, 2009). Collection Methods From April August of 2012 and 2013, snakes were captured as part of a general herpetological survey. They were captured by hand, in terrestrial funnel traps, and in collapsible crawfish traps that were placed in lakes, seeps, and streams. Snakes were palpated to determine whether or not they contained a food bolus. When food was detected in the stomach, it was gently massaged up the oesophagus until the snake regurgitated. Clear plastic tubes were used to restrain venomous snakes heads until the food had been moved far enough up the oesophagus that the snakes would regurgitate voluntarily. When food was detected in the colon, it was massaged caudally until the snake defecated (Diller and Wallace, 1996). Prey items were then identified to the
2 172 lowest taxonomic level possible. Additionally, when dead snakes were encountered they were dissected and the stomach and colon contents were examined. When possible, the snout-vent length (SVL) of the snakes and prey items were recorded (for fish the length from the snout to the base of the caudal fin was recorded [standard length; SL]). Because of the difficulties of accurately measuring a snake on occasions when only one researcher was present, it was not always possible to measure each individual. Also, prey were occasionally too digested to obtain accurate measurements. Finally, when snakes were observed feeding, the species of both the snake and prey item were recorded but they were otherwise left undisturbed. No snakes were sexed. Results/Discussion General Diet Donald T. McKnight et al. Diet data were obtained from 11 southern copperheads (Agkistrodon contortrix contortrix (Linnaeus 1766)), 23 western cottonmouths (Agkistrodon piscivorus leucostoma (Troost 1836)), four plain-bellied watersnakes (Nerodia erythrogaster (Forster 1771)), 13 broad-banded watersnakes (Nerodia fasciata confluens Blanchard 1923), seven diamond-backed watersnakes (Nerodia rhombifer (Hallowell 1852)), one western pygmy rattlesnake (Sistrurus miliarius streckeri Gloyd 1935), and one western ribbon snake (Thamnophis proximus proximus (Say 1823)) (Table 1). These data Table 1. Stomach and gut contents of southern copperheads (Agkistrodon contortrix contortrix), western cottonmouths (Agkistrodon piscivorus leucostoma), plain-bellied watersnakes (Nerodia erythrogaster), broad-banded watersnakes (Nerodia fasciata confluens), diamond-backed watersnakes (Nerodia rhombifer), one western pygmy rattlesnake (Sistrurus miliarius streckeri), and one western ribbon snake (Thamnophis proximus proximus). Prey size is reported as snout-vent length (SVL) for snakes, adult frogs, newts, and tadpoles, length from the snout to the base of the caudal fin for fish, and as total length for the siren. Lakes = snakes found in the lakes or in traps beside the lakes, Pools = snakes found in or around the drying pools in the seeps and streams, Woods = snakes found in the forest, not associated with water. 10 Snake SVL Prey Size Snake Species Location Prey Item (mm) (mm) A. c. contortrix 620 Woods 2 cicadas - A. c. contortrix 475 Woods 2 cicadas - A. c. contortrix 617 Woods 1 cicada - A. c. contortrix 373 Woods 1 cicada - A. c. contortrix 300 Woods 1 cicada - A. c. contortrix a 437 Woods 1 caterpillar 57 A. c. contortrix a 437 Woods 1 unidentified mammal - A. c. contortrix 433 Woods 1 unidentified mammal - A. c. contortrix b - Woods 1 unidentified vertebrate - A. c. contortrix b - Woods 1 Hurter's spadefoot toad (Scaphiopus hurterii)* - A. c. contortrix 419 Woods 1 flat-headed snake (Tantilla gracilis)* - A. c. contortrix 455 Woods 1 prairie lizard (Sceloporus consobrinus)* - A. c. contortrix 253 Woods Unidentified scales (not keeled) - A. p. leucostoma 519 Lake 1 green sunfish (Lepomis cyanellus) - A. p. leucostoma - Lake 1 green sunfish (Lepomis cyanellus) - A. p. leucostoma 661 Lake 1 red-finned pickerel (Esox americanus) 133 A. p. leucostoma 672 Lake 1 red-finned pickerel (Esox americanus) 139 A. p. leucostoma 549 Lake 1 red-finned pickerel (Esox americanus) - A. p. leucostoma 555 Lake 1 red-finned pickerel (Esox americanus) - A. p. leucostoma 620 Lake 1 red-finned pickerel (Esox americanus) - A. p. leucostoma - Lake 1 unidentified fish - A. p. leucostoma 536 Lake 1 western lesser siren (Siren intermedia nettingi) 293 A. p. leucostoma 787 Lake 1 American bullfrog (Lithobates catesbeianus) 87 A. p. leucostoma 593 Lake 1 American bullfrog (Lithobates catesbeianus) 105 A. p. leucostoma - Lake 1 green frog (Lithobates clamitans) - A. p. leucostoma - Lake 1 green frog (Lithobates clamitans) - A. p. leucostoma - Lake 1 southern leopard frog (Lithobates sphenocephalus utricularius) - A. p. leucostoma 282 Lake 1 unidentified frog (Lithobates sp) - A. p. leucostoma 884 Lake 1 diamond-backed watersnake (Nerodia rhombifer) 570 A. p. leucostoma 643 Lake 1 unidentified snake - A. p. leucostoma 690 Lake 1 unidentified snake - A. p. leucostoma 619 Pool 1 unidentified fish -
3 Notes on the diets of seven sympatric snakes 173 Table 1 (continued) A. p. leucostoma - Pool 1 green sunfish (Lepomis cyanellus) - A. p. leucostoma c - Pool 5 green sunfish (Lepomis cyanellus) A. p. leucostoma c - Pool 1 unidentified snake - A. p. leucostoma 573 Pool 1 green frog (Lithobates clamitans) 37 A. p. leucostoma 586 Pool 14 southern leopard frog larvae (Lithobates sphenocephalus utricularius) - N. erythrogaster 456 Lake 2 unidentified anuran larvae (Lithobates sp) - N. erythrogaster 400 Lake 1 unidentified anuran larva (Lithobates sp) 32 N. erythrogaster d - Pool 56 green sunfish (Lepomis cyanellus)* N. erythrogaster d - Pool 16 goldstripe darters (Etheostoma parvipinne)* 35 N. erythrogaster d - Pool 5 central newt larvae (Notophthalmus viridescens louisianensis)* 15 N. erythrogaster d - Pool 2 grey treefrog larvae (Hyla versicolor)* 16 N. erythrogaster 849 Woods 1 unidentified vertebrate - N. f. confluens - Lake 1 southern leopard frog (Lithobates sphenocephalus utricularius) - N. f. confluens - Lake 1 southern leopard frog (Lithobates sphenocephalus utricularius) - N. f. confluens 610 Lake 4 American bullfrog tadpoles (Lithobates catesbeianus) 53, 53, 54, 56 N. f. confluens 611 Lake 2 American bullfrog tadpoles (Lithobates catesbeianus) 50, 55 N. f. confluens 425 Lake 1 American bullfrog tadpoles (Lithobates catesbeianus) 55 N. f. confluens 645 Lake 1 American bullfrog tadpoles (Lithobates catesbeianus) 49 N. f. confluens 507 Lake 1 unidentified frog (Lithobates sp) - N. f. confluens 602 Lake 1 unidentified frog (Lithobates sp) - N. f. confluens - Lake 1 unidentified frog (Lithobates sp) - N. f. confluens 484 Lake 4 unidentified tadpoles (Lithobates sp) 25, 28, 28, 31 N. f. confluens 411 Lake 1 unidentified tadpole (Lithobates sp) - N. f. confluens 477 Lake 1 unidentified tadpole (Lithobates sp) - N. f. confluens - Pool 3 southern leopard frog tadpoles (Lithobates sphenocephalus utricularius) - N. rhombifer 825 Lake 1 green sunfish (Lepomis cyanellus) - N. rhombifer - Lake 1 green sunfish (Lepomis cyanellus) - N. rhombifer 348 Lake 1 red-finned pickerel (Esox americanus)* 141 N. rhombifer - Lake 1 unidentified catfish (Ameiurus sp) 142 N. rhombifer 500 Lake 2 American bullfrog larvae (Lithobates catesbeianus) 28, 49 N. rhombifer 570 Lake 2 unidentified anuran larvae (Lithobates sp) - N. rhombifer 556 Lake 1 unidentified frog (Lithobates sp) - S. m. streckeri 209 Woods 1 flat-headed snake (Tantilla gracilis)* 118 T. p. proximus - Lake 1 Blanchard's cricket frog (Acris blanchardi)* - a,b,c,d Superscript letters denote individual snakes that had consumed multiple prey species (i.e., records with the same letter are from a single individual). *new diet records include observations of A. p. leucostoma foraging at a drying pool and new diet records (10 total) for every species except A. p. leucostoma and N. f. confluens (reviewed in Ernst and Ernst, 2003). Agkistrodon contortrix contortrix Among the 11 A. c. contortrix sampled, 6 (54.5%) had consumed insects, 2 (18.2%) mammals, 1 (9.1%) anurans, 1 (9.1%) snakes, and 1 (9.1%) lizards. Additionally, one specimen contained an unidentified vertebra, and another contained unidentified scales. Several aspects of these results are interesting. First, A. c. contortrix have typically been described as generalists, and mammals typically make up the bulk of their diet (Garton and Dimmick, 1969; Fitch, 1982). In contrast, mammals were only present in 18.2% of our samples. Second, while cicadas have frequently been reported in the diet of A. contortrix (Savage, 1967), Lagesse and Ford (1996) reported that only adult A. contortrix (SVL > 350 mm) consumed cicadas. In our study, however, a cicada was found in the gut of a juvenile (SVL = 300 mm). Interestingly, 80% of the snakes with cicadas were captured in 2012, but there were no obvious differences
4 174 JDonald T. McKnight et al. Agkistrodon piscivorus leucostoma Diet Agkistrodon piscivorus leucostoma in our study consumed a wider range of prey than any of the other aquatic species (Figure 1). Of the 18 A. p. leucostoma sampled at the lakes, 8 (44.4%) contained fish, 6 (33.3%) adult frogs, 3 (16.7%) snakes, and 1 (5.6%) sirens (five additional snakes were captured in drying pools; Table 1). These results are consistent with previous studies that have reported that A. p. leucostoma are generalists (Gloyd and Conant, 1990; Ernst and Ernst, 2003). It is interesting to note that the only A. p. leucostoma that had eaten tadpoles was found at a drying pool, which contained almost nothing but tadpoles. Given that tadpoles were detected multiple times in the diets of N. f. confluens and N. rhombifer (both of which were represented by smaller sample sizes), it seems likely that tadpoles are not a common component of the diet of A. p. leucostoma at this site. Agkistrodon piscivorus leucostoma Feeding Behaviour Figure 1. Diet composition of 18 western cottonmouths (Agkistrodon piscivorus leucostoma), 12 broad-banded watersnakes (Nerodia fasciata confluens), and seven diamondbacked watersnakes (Nerodia rhombifer) at beaver-formed lakes at Boehler Seeps and Sandhills Preserve, Atoka County, Oklahoma. in cicada abundance between the two years (McKnight, pers. obs.). Three new diet records were obtained for A. c. contortrix: (flat-headed snake [Tantilla gracilis], prairie lizard [Sceloporus consobrinus], and Hurter s spadefoot [Scaphiopus hurterii]). Although A. contortrix have been reported eating members of the Tantilla and Sceloporus genera, this is the first record of them depredating T. gracilis or S. consobrinus (Ernst and Ernst, 2003). To our knowledge, this is also the first record of A. contortrix consuming any Scaphiopus species. Neither the snake nor the spadefoot were measured, but the spadefoot was approximately the size of the snake s head, and was largely undigested. At 19:20 h on 25 May 2012, five A. p. leucostoma were observed feeding at a pool near Boehler Lake that was in the final stages of drying. The pool had previously covered 1,900 m 2 and was m deep, but it had been reduced to less than two square meters and was <1 cm deep in most areas. The pool was writhing with young green sunfish (Lepomis cyanellus) ( mm SL), goldstripe darters (Etheostoma parvipinne), grey treefrog larvae (Hyla versicolor), southern leopard frog larvae (Lithobates sphenocephalus utricularius), central newt larvae (Notophthalmus viridescens louisianensis), and dragonfly larvae (Odonata). Lepomis cyanellus appeared to be the most abundant species. Three of the A. p. leucostoma were already bulging with prey at 19:20 h, and almost immediately began to leave (the snakes were roughly evenly spaced in the pool prior to the departure of these three). The other two individuals remained in the pool and continued to consume prey. They were positioned in the shallowest portions of the water, moving only their heads and necks, and rapidly consuming the fish around them. All of the fish were much smaller than the snakes heads, so to grab the prey they arched their necks off the substrate so that their noses touched the water, then they opened their jaws and grabbed the prey with the front of their mouth (Figure 2). After securing the prey, the snakes returned their heads to a horizontal position, quickly swallowed, and moved on to the next fish. They ate the fish one at a time, but handling time was very brief. One A. p.
5 Notes on the diets of seven sympatric snakes 175 Figure 2. A western cottonmouth (Agkistrodon piscivorus leucostoma) feeding on small fish in a drying pool at Boehler Seeps and Sandhills Preserve, Atoka County, Oklahoma on 25 May Figure 3. A plain-bellied watersnake (Nerodia erythrogaster) beside part of its regurgitated meal (green sunfish [Lepomis cyanellus], goldstripe darters [Etheostoma parvipinne], and central newt larvae [Notophthalmus viridescens louisianensis] can be seen) at Boehler Seeps and Sandhills Preserve, Atoka County, Oklahoma on 25 May 2012.
6 176 leucostoma was observed eating one fish every seven seconds. Lepomis cyanellus were the only prey item that could be confirmed during the observed foraging event. These snakes were not palpated to obtain stomach contents. While this was the only detailed observation of feeding behaviour that we recorded, A. p. leucostoma were frequently found in and around other drying pools where fish and tadpoles were highly concentrated and likely provide a rich intermittent food source. Hill and Beaupre (2008) reported a similar observation of A. p. leucostoma congregating around drying pools in Arkansas. Interestingly, other snake species at our site were rarely encountered at these pools. This may be merely a result of A. p. leucostoma being more abundant (i.e. A. p. leucostoma were frequently seen at pools because they are highly abundant, whereas the Nerodia species were not encountered frequently because they are less abundant), or it may result from the fact that A. p. leucostoma will eat potential competitors such as Nerodia spp. It also may be an artefact of the tendency of Nerodia spp. to inhabit areas closer to the main lakes than A. p. leucostoma (McKnight unpublished data). Nerodia erythrogaster Four new prey items were detected for N. erythrogaster (Figure 3). All four came from a single individual that was feeding at the same pool where A. p. leucostoma were observed on 25 May Upon capture, the snake voluntarily regurgitated 56 young L. cyanellus, 16 E. parvipinne, five N. v. louisianensis larvae, and two H. versicolor tadpoles. Nerodia erythrogaster has previously been reported eating other Lepomis, Etheostoma, and Hyla species, but previous records of salamander (caudate) prey are limited to the genera Ambystoma, Amphiuma, and Siren (Ernst and Ernst, 2003). Nerodia fasciata confluens Of the 12 N. f. confluens sampled at the lakes, 7 (58.3%) had consumed tadpoles, and 5 (41.6%) had consumed adult frogs (Figure 1). The result that N. fasciata ate entirely anurans at this site is unusual. While N. fasciata often consume anurans, they generally have a more varied diet (Kofron, 1978; Hampton et al., 2009). For example, Clark (1949) reported 60 fish, 85 frogs, and 5 birds in stomach contents, and Mushinsky and Hebrard (1977) reported that 77.8% of their diet (by volume) consisted of fish while anurans comprised just 21.8%. Nerodia rhombifer Fish and anurans are the most common prey reported for N. rhombifer (Ernst and Ernst, 2003). Bowers (1966) reported that fish were present in 54.2% of N. rhombifer examined, and Mushinsky and Hebrard (1977), reported that fish constituted 92.9% of prey items taken by 40 N. rhombifer. Of the seven N. rhombifer that we examined, 4 (57.1%) contained fish, 2 (28.6%) tadpoles, and 1 (14.3%) adult frogs (Figure 1). One of the fish that had been consumed was a redfinned pickerel (Esox americanus), which is a new diet record for N. rhombifer. Sistrurus miliarius streckeri We obtained a diet sample from one S. m. streckeri. On 5 June 2013, a S. m. streckeri (SVL = 209 mm, total length = 238 mm) was captured in a funnel trap, and its stomach contained a recently consumed flat-headed snake (Tantilla gracilis; SVL = 118 mm, total length = 154 mm). Sistrurus miliarius are known to eat other snakes, but this is the first record of any member of the Tantilla genus being consumed (Ernst and Ernst, 2003). Thamnophis proximus proximus We obtained diet data from one T. p. proximus. On 1 August 2012, a young T. p. proximus was observed near one of the lakes, where it captured an adult Blanchard s cricket frog (Acris blanchardi) by a rear leg and swallowed it backwards (one rear leg in its mouth, the other extended) as the frog thrashed in an attempt to escape. The frog was approximately 2 3 times the size of the snake s head, and the feeding event took less than one minute. Thamnophis proximus have been previously reported eating both Acris crepitans and Acris gryllus, but this is the first report of consumption of A. blanchardi (Ernst and Ernst, 2003). Conclusion Jeffrey W. Streicher et al. Our study presents multiple new diet records from a single site and highlights the need for continued research on species that are often considered to be well-studied. Both A. p. leucostoma and A. c. contortrix exhibited generalist tendencies, consuming a wide range of prey. Nerodia fasciata confluens and N. rhombifer had more restricted diets, with N. f. confluens consuming only anurans, and N. rhombifer consuming only fish and anurans. Our data provide some evidence that niche partitioning may be influencing the diets of snakes at
7 Notes on the diets of seven sympatric snakes 177 our study site, and explicit tests of this possibility could reveal important insights about interactions within the snake community. Acknowledgements. We are indebted to the many people who have assisted us with this research, especially the preserve manager, J. Tucker, and our field assistant T. Dean. We would also like to thank the Oklahoma Department of Wildlife Conservation and the Delta Foundation for funding this study. We conducted this research under Oklahoma Department of Wildlife Conservation scientific collecting permits #5269 and 5610 and with the approval of the Missouri State University Institutional Animal Care and Use Committee (IACUC protocol #10014). References Bowers, J.H. (1966): Food habits of the diamond-backed watersnake, Natrix rhombifera rhombifera, in Bowie and Red River counties, Texas. Herpetologica 22: Burghardt, G.M., Krause, M.A. (1999): Plasticity of foraging behavior in garter snakes (Thamnophis sirtalis) reared on different diets. Journal of Comparative Psychology 113: Clark, R.F. (1949): Snakes of the hill parishes of Louisiana. Journal of the Tennessee Academy of Science 24: Diller, L.V., Wallace, R.L. (1996): Comparative ecology of two snake species (Crotalus viridis and Pituophis melanoleucus) in southwestern Idaho. Herpetologica 52: Ernst, C.H, Ernst, E.M. (2003): Snakes of the United States and Canada. Smithsonian Books. Fitch, H.S. (1982): Resources of a snake community in prairiewoodland habitat of northeastern Kansas. In: Herpetological Communities, p Scott, N.J. Jr. Ed., US Department of Interior. Garton, J.S., Dimmick, R.W. (1969): Food habits of the copperhead in middle Tennessee. Journal of the Tennessee Academy of Science 44: Gloyd, H.K., Conant, R. (1990): Snakes of the Agkistrodon complex: a monographic review. Society for the Study of Amphibians and Reptiles, Contributions to Herpetology 6. Ithaca, NY. Hampton, P.M., Haertle, N., Dartez, S.F., Monterio, C. (2009). Prey of the broad-banded watersnake (Nerodia fasciata) and the diamondback watersnake (Nerodia rhombifer). Southwestern Naturalist 54: Hill, J.G., Beaupre, S.J. (2008): Body size, growth, and reproduction in a population of western cottonmouths (Agkistrodon piscivorus leucostoma) in the Ozark Mountains of Northwest Arkansas. Copeia 2008: 105:114. Himes, J.G. (2003): Diet composition of Nerodia sipedon (Serpentes: Colubridae) and its dietary overlap with, and chemical recognition of Agkistrodon piscivorus (Serpentes: Viperidae). Amphibia-Reptilia 24: King, R.B. (2002): Predicted and observed maximum prey size snake size allometry. Functional Ecology 16: Kofron, C.P. (1978): Food and habitats of aquatic snakes (Reptilia, Serpentes) in a Louisiana swamp. Journal of Herpetology 12: Lagesse, L.A., Ford, N.B. (1996): Ontogenetic variation in the diet of the southern copperhead, Agkistrodon contortrix, in northeastern Texas. Texas Journal of Science 48: Luiselli, L. (2006a): Broad geographic, taxonomic and ecological patterns of interpopulation variation in the dietary habits of snakes. Web Ecology 6: Luiselli, L. (2006b): Resource partitioning and interspecific competition in snakes: the search for general geographical and guild patterns. Oikos 114: Luiselli, L., Akani, G.C., Capizzi, D. (1988): Food resource partitioning of a community of snakes in a swamp rainforest of south-eastern Nigeria. Journal of Zoology 246: Mushinsky, H.R., Hebrard, J.J. (1977): Food partitioning by five species of water snakes in Louisiana. Herpetologica 33: Mushinsky, H.R., Hebrard, J.J., Vodopich, D.S. (1982): Ontogeny of water snake foraging ecology. Ecology 63: Patton, T., Wood, J. (2009): A herpetofaunal survey of the Boehler Seeps Preserve, with reports of new county records and recommendations for conservation efforts. Proceedings of the Oklahoma Academy of Science 89: Savage, T. (1967): The diet of rattlesnakes and copperheads in the Great Smoky Mountains National Park. Copeia 1967: Shine, R. (1991): Why do larger snakes eat larger prey items? Functional Ecology 5: Toft, C.A. (1985): Partitioning in amphibians and reptiles. Copeia 1985: Accepted by Philip de Pous; Managing Editor: Christoph Liedtke
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