Transactions of the Kansas Vol. 121, no. 3-4 Academy of Science p. 403-410 (2018)

Ontogenetic changes in tail-length and the possible relation to caudal luring in northeast Kansas Copperheads, Agkistrodon contortrix

George R. Pisani1 and J. Daren Riedle2 1. Kansas Biological Survey, Higuchi Hall, Lawrence, KS 66047 [email protected] 2. Wildlife Diversity Coordinator, Kansas Dept. of Wildlife, Parks, and Tourism, Pratt, KS

Electronic data capture of the nearly 60 years of field data on northeast Kansas snake populations collected by Henry Fitch enabled review of ontogenetic changes in tail- length from birth through adult size in Agkistrodon contortrix. Data from 5084 northeast Kansas Copperhead (Agkistrodon contortrix) records collected by Fitch from 1948-2003 (2287F:2797M) were examined to assess the nature of ontogenetic changes in relative tail length of sexes. We suggest that the longer relative tail length of neonate and juvenile copperheads, combined with tail color, enhances the effectiveness of caudal luring, and offer suggestions for further study.

Introduction for the possibility that one treatment group spent more time foraging and caudal luring,” or that “... Ontogenetic shifts in prey in the Crotalinae black-tailed snakes may have compensated for contribute to variation in morphology, reduced prey capture rates by spending more time physiology, and behavior between juveniles in ambush postures...” Ontogenetic tail coloration and adults (LaBonte 2008). Examples include in viperids merits more extensive study. ontogenetic shifts in foraging strategy, microhabitat use, activity period, and shifts in Similar to tail coloration, the influence of the chemical composition of venom (Mackessy ontogenetic and sex-specific differences in tail 1988; Andrade and Abe 2005; Eskew et al. 2009; length on foraging ability has yet to be fully Clark et al. 2016). One of the most obvious of explored. In his extensive documentation of these ontogenetic shifts is the brightly colored tail northeast Kansas Copperhead (Agkistrodon of juveniles of some species, which is used as a contortrix) ecology, Fitch (1960a, 1999) provided lure to attract frogs and lizards as prey (Carpenter an overview of ontogenetic changes in tail- and Gillingham 1990; Greene and Campbell length from birth through adult size, but did not 1972; Neill 1960). elaborate on the nature of the changes or their possible adaptive significance. He described the Juvenile tail coloration has been experimentally change as “... the ontogenetic change in each sex manipulated in other pit vipers, but with consists of shortening of the tail in relation to inconclusive results. Thus, Farrell, et al. (2011) snout-vent length...” (Fitch 1960b), and “sexual experimentally manipulated tail color in juvenile dimorphism is relatively slight and tends to be Pigmy Rattlesnakes (Sistrurus miliarius), obscured by ontogenetic changes” (Fitch 1960a) concluding that tail coloration did not affect and “as the young snakes grow the difference overall foraging success in this caudal-luring in proportions increases gradually… In both species. Though their findings are interesting, they sexes the tail becomes relatively shorter as size did not attempt to monitor foraging thereafter, increases” (Fitch 1960a). nor identify prey in subsequently recaptured snakes, and so no conclusions can be drawn To preserve the nearly 60 years of field data regarding the effectiveness of luring and tail color collected by Henry Fitch, his extensive field on any particular prey types. Additionally, they records on this and other species are being acknowledge that their model “...could not control migrated from paper to database format by one 404 Pisani and Riedle of us (GRP). This has provided an opportunity Results to re-examine this ontogeny in detail with the addition of data collected after the original In all instances, outcomes were equivalent, and publications (Fitch 1960a, b and summarized in are consistent with (thus supporting as well as Fitch 1999), and to suggest a possible selective elaborating) the general conclusions of Fitch mechanism for the observed changes. (1960a, b).

Materials and Methods Summary statistics are presented in Table 1; distributions of the two tail ratios examined We used 5084 Fitch Copperhead records (of a were (male vs female) significantly different total of 5462) from 1948-2003 (2287F:2797M) (Table 2). A histogram of Log10-transformed that had complete data (in mm) for Snout-Vent TTLs (Fig. 1) shows the very slight sexual Length (SVL) and Tail Length (TL). Also dimorphism in relative tail length noted by omitted from this total were records (>10) of Fitch (1960a, b) in this species. When Log10 snakes with tails not noted as broken but that transformed data from sexes are examined resulted in greatly reduced TTL values were via OLS (Fig. 2), it becomes apparent that regarded as original recording errors. the smallest SVL snakes (e.g., neonates) are effectively indistinguishable (though Data Analysis: Data were analyzed in three significantly different at p=0.05 in large sample primary ways in an attempt to minimize (even sizes) in relative tail length (TTL), and that given the large data set) the potential for TTL remains noticeably greater in juveniles, inference error due to SVL being a component decreasing with size as the snakes grow. of the ratios examined (TTL, TL÷SVL). A similar regression of untransformed (e.g., raw) data (Fig. 3) indicates the absolute Raw, and thereafter transformed, values of TL values of the TL-SVL relationship. Results and TTL as varying with SVL were analyzed of ANCOVA (Fig. 4) and both OLS tests initially by Ordinary Least Squares (OLS) (absolute and relative TLs) support the regression. Additionally, one-way ANCOVA ontogenetic difference. TL residuals of both was performed using Log-transformed SVLs sexes are normally distributed (Fig. 5), and and TTLs within sexes as column-paired showed weak but definite negative correlation correlated x-y data. Also non-parametric (Pearson r: -0.30) with SVLs. Non-parametric evaluations (Kruskal-Wallis tests for equal Kruskal-Wallis tests for equal medians using medians) of TL÷SVL and thereafter TTL were both absolute and relative tail lengths with SVL done to compare with parametric ANOVAs. by sex showed significant difference between sample medians (Table 3). Also, raw data for TL was regressed on raw data for SVL; residuals for TL were calculated, Since absolute (and hence relative) tail length in and then examined for negative correlation A. contortrix across SVL sizes varies considerably (indicating an ontogenetic shift) with SVL. through the extensive range of the species (Gloyd and Conant 1990; Mitchell 1994), with broad In all tests, significance was set to p<0.05. areas of intergradation through states along the Lower and upper 95% confidence intervals Atlantic coast (Mitchell 1994:287) we did not were calculated using simple bootstrapping, attempt comparisons of this character with distant with 9,999 bootstrap replicates. All statistics populations. Table 4 is condensed from Gloyd and were performed using PAST 3.2 (Hammer, et. Conant (1990) and contrasts Kansas copperheads al. 2001) and Microsoft Excel-2010. (A. c. phaeogaster) with the northern populations. Transactions of the Kansas Academy of Science 121(3-4), 2018 405

Table 1. Summary statistics for male and female Snout-Vent Length (SVL), Tail Length (TL), Ratio of Tail to Total Length (TTL). SVL and TL in mm.

Discussion shown here (neonate Kansas copperhead sexes less distinct from each other than are adult) The decrease in relative tail length with resembles patterns found for four natricids by increased age (as inferred from size) in A. King, et al. (1999) in their review of general contortrix is accompanied by slight, but sexual dimorphism and ontogeny, e.g. neonates increasing, sexual dimorphism as male of both sexes have similar (but not identical) hemipenes and the associated musculatures absolute TLs. There is no indication that mature; this sexual dimorphism is typical of the genera examined by King, et al (1999) viperids in general (Bonnet, et al. 1998; Shine actually engage in caudal luring, and so their et al. 1999), though the dichromatic change in explanatory hypotheses did not consider this copperheads and some other tail-luring viperids behavior and its adaptive significance. is not. The untransformed tail length pattern Table 2. Epps-Singleton tests of distributions, tail length ratios. 406 Pisani and Riedle

Figure 1. Distributions of relative tail-lengths (Log10 transformed) by sex, NE Kansas Agkistrodon contortrix. Magenta bars are areas of overlap; curved lines are fitted normal distributions for values. See Table 1 for untransformed data. Conclusions regarding diet of juvenile vs. adult squamates and anurans in the prey of neonates A. contortrix (Fitch 1960a, 1999; Lagesse and than in mid-size or adult snakes; the Fitch data Ford 1996) indicate the importance of small, relate to the population for which we here generally insect, prey to mid-sized copperheads. discuss caudal luring, and we hypothesize that However, both Fitch (1999, table 7) and Lagesse both these prey types MAY respond to caudal and Ford (1996) found a higher percentage of luring in natural circumstances. Our hypothesis

Figure 2. Regressions (with 95% confidence bands) of log-transformed male and female relative tail lengths on snout-vent lengths, NE Kansas Agkistrodon contortrix. Transactions of the Kansas Academy of Science 121(3-4), 2018 407

Figure 3. Regressions (with 95% confidence bands) of untransformed male and female tail lengths on snout-vent lengths, NE Kansas Agkistrodon contortrix. is not de novo, and is similar to that of Eskew, in eliciting the tail-waving behavior...” in et al. (2009) regarding juvenile cottonmouths captive neonate and juvenile copperheads, that selectively prey upon salamanders. Though the behavior is well-documented, though not Fitch (1960a) stated that he never “succeeded as prominent a display as noted for juvenile

Figure 4. Plot from ANCOVA. SVL vs TL÷SVL. 408 Pisani and Riedle

Figure 5. Distribution of residuals from OLS, untransformed SVL and TL. cantils (Agkistrodon bilineatus) (Neill 1960). In regard to efficiency of luring, an early Additionally, one of us (GRP) has observed and hypothesis was that if male snakes have filmed this behavior in the mid-1980s in captive longer tails then male snakes would be more local neonate copperheads presented with live efficient at luring prey (Neil 1960). Rabatsky prey. The sulfur-yellow tail coloration in neonate and Waterman (2005) tested this hypothesis and juvenile copperheads (Collins, et al. 2010: in Pygmy Rattlesnakes (Sistrurus miliarius), p178) and related viperids is known to serve as a where male juvenile snakes had longer tails prey attractant, persisting into adulthood in other than same age females. Female S. miliarius viperids not closely related to Agkistrodon (see females “spent significantly more time caudal review in Heatwole and Davison 1976). luring than males”, though females “did not lure Table 3. Non-parametric evaluation of tail length relation to SVL. Transactions of the Kansas Academy of Science 121(3-4), 2018 409

Table 4. Percent tail of total length for eastern vs. Kansas A. contortrix from Table 10, Gloyd and Conant 1990.

more lizards to move within striking distance custodian of the electronic databases constructed than males”. Because they did not present data by GRP. Neil Ford provided reference material. on snake body proportions, these findings are The constructive comments of three anonymous difficult to relate to our hypothesis. We know of reviewers are greatly appreciated, and have no similar study with Kansas Agkistrodon. for the most part been incorporated. We also acknowledge the exceptional efforts of Henry S. In light of the ontogenetic and behavioral Fitch (deceased) in amassing a phenomenal record patterns indicated above, we suggest that the of ecological data on eastern Kansas snakes. longer relative tail length of neonate and juvenile copperheads (essentially equivalent between Literature Cited neonate sexes) MAY enhance the effectiveness of caudal luring. It also might be expected to Andrade, D.V. and Abe, A.S. 1999. expose neonates and juveniles to increased Relationship of venom ontogeny and diet in predation risk, especially from avian predators, Bothrops. Herpetologica 55:200-204. though this may be mitigated by the effective Bonnet, X., Shine, R., Naulleau, G. and crypsis of juveniles. Juveniles of the congeneric Vacher-Vallas, M. 1998. Sexual dimorphism Cottonmouth (A. piscivorus) utilize different in snakes: different reproductive roles microhabitats than adults when foraging, favour different body plans. Proceedings of most likely to minimize predation risk while the Royal Society of London B: Biological increasing opportunity for prey capture (Eskew Sciences, 265(1392):179-183. et al. 2009). Additional field and laboratory Carpenter, C.C. and Gillingham, J.C. 1990. research on age-class habitat preferences and Ritualized behavior in Agkistrodon and caudal luring of A. contortrix are needed to allied genera. pp 523-531 in Gloyd, explore this possibility. Our treatment here of H.K. and Conant, R.C., Snakes of the the Fitch data on this species in Kansas presents Agkistrodon Complex. A Monographic a quantified overview of ontogenetic changes in Review. Contributions to Herpetology, relative tail length in Kansas copperheads. Number 6. Society for the Study of Amphibians and Reptiles. i-vi+614pp Acknowledgments Clark, R.W., Dorr, S.W., Whitford, M.D., Freymiller, G.A. and Putman, B.J. 2016. We are grateful to Kansas Dept. of Wildlife, Parks, Activity cycles and foraging behaviors of free- and Tourism Chickadee Checkoff Program for ranging Sidewinder Rattlesnakes (Crotalus financial support (to GRP) of the Fitch Snake Data cerastes): the ontogeny of hunting in a Archive project. GRP thanks Kansas Biological precocial vertebrate. Zoology 119:196-206. Survey (KBS) (Edward Martinko, Director) for Collins, J.T., Collins, S.L. and Taggart, T.T. providing work space and computational support 2010. Amphibians, Reptiles and Turtles in for an ongoing variety of research efforts. KBS Kansas. Eagle Mountain Publishing, LC, additionally houses the Fitch Data Archive, and is Eagle Mountain, Utah. xvi+312pp 410 Pisani and Riedle

Eskew, E.A., Willson, J.D. and Winne, C.T. King, R.B., Bittner, T.D., Queral-Regil, A. and 2009. Ambush site selection and ontogenetic Cline, J.H. 1999. Sexual dimorphism in shifts in foraging strategy in a semi-aquatic neonate and adult snakes. J. Zool., Lond. pit viper, the Eastern cottonmouth. Journal 247:19-28. of Zoology 277:179-186. LaBonte, J.P. 2008. Ontogeny of prey preference Farrell, T.M., May, P.G. and Andreadis, P.T. in the Southern Pacific Rattlesnake, Crotalus 2011. Experimental manipulation of tail oreganus helleri. pp. 169-174 in Hayes, color does not affect foraging success W.K., Beaman, K.R., Cardwell. M.D., in a caudal luring rattlesnake. Journal of and Bush, S.P. (eds.), The Biology of the Herpetology, 45(3):291-293. Rattlesnakes, Loma Linda University Press, Fitch, H.S. 1960a. Autecology of the Loma Linda, California. Copperhead. University of Kansas Lagesse, L.A. and Ford, N.B. 1996. Publications, Museum of Natural History. Ontogenetic variation in the diet of Vol. 13, No. 4, 288pp the southern copperhead, Agkistrodon Fitch, H.S. 1960b. Criteria for determining contortrix, in northeastern Texas. Texas sex and breeding maturity in snakes. Journal of Science 48(1):48-54. Herpetologica 16(1):49-51. Mackessy, S.P. 1988. Venom ontogeny in the Fitch, H.S. 1999. A Kansas snake community: Pacific rattlesnakesCrotalus viridis helleri composition and changes over 50 years. and C. v. oreganus. Copeia 188:92-101. Krieger Publishing, Malabar, Florida. xii + Mitchell, J.C. 1994. The Reptiles of Virginia. 165 pp. i-xv+352pp, Smithsonian Institution Press. Gloyd, H.K. and Conant, R.C. 1990. Snakes of Neill, W.T. 1960. The caudal lure of various the Agkistrodon Complex. A Monographic juvenile snakes. Quarterly Journal of the Review. Contributions to Herpetology, Florida Academy of Sciences, 23:173-200. Number 6. Society for the Study of Rabatsky, A.M. and Waterman, J.M. 2005. Amphibians and Reptiles. i-vi+614pp Ontogenetic shifts and sex difference Greene, H.W. and Campbell, J.A. 1972. Notes in caudal luring in the Dusky Pygmy on the use of caudal lures in arboreal green Rattlesnake Sistrurus miliarius barbouri. pitvipers. Herpetologica 28:32-34. Herpetologica 61:87-91. Hammer, Ø, Harper, D.A.T. and Ryan, P.D. Shine, R., Olsson, M.M., Moore, I.T., 2001. PAST: Paleontological statistics LeMaster, M.P. and Mason, R.T. 1999. software package for education and data Why do male snakes have longer tails analysis. Palaeontologia Electronica 4(1): than females? Proceedings of the Royal 9pp. [http://palaeo-electronica.org/2001_1/ Society of London B: Biological Sciences, past/issue1_01.htm Accessed 12 December 266(1434):2147-2151. 2017 from https://folk.uio.no/ohammer/past/] Heatwole, H. and Davison, E. 1976. A review of caudal luring in snakes with notes on its cccurrence in the Saharan Sand Viper, Cerastes vipera. Herpetologica 32(3):332-336.