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

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1 Transactions of the Kansas Academy of Science Vol. 121, no. 3-4 p (2018) Ontogenetic changes in tail-length and the possible relation to caudal luring in northeast Kansas Copperheads, Agkistrodon contortrix George R. Pisani 1 and J. Daren Riedle 2 1. Kansas Biological Survey, Higuchi Hall, Lawrence, KS gpisani@ku.edu 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 taillength from birth through adult size in Agkistrodon contortrix. Data from 5084 northeast Kansas Copperhead (Agkistrodon contortrix) records collected by Fitch from (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 Ontogenetic shifts in prey in the Crotalinae contribute to variation in morphology, physiology, and behavior between juveniles and adults (LaBonte 2008). Examples include ontogenetic shifts in foraging strategy, microhabitat use, activity period, and shifts in the chemical composition of venom (Mackessy 1988; Andrade and Abe 2005; Eskew et al. 2009; Clark et al. 2016). One of the most obvious of these ontogenetic shifts is the brightly colored tail of juveniles of some species, which is used as a lure to attract frogs and lizards as prey (Carpenter and Gillingham 1990; Greene and Campbell 1972; Neill 1960). Juvenile tail coloration has been experimentally manipulated in other pit vipers, but with inconclusive results. Thus, Farrell, et al. (2011) experimentally manipulated tail color in juvenile Pigmy Rattlesnakes (Sistrurus miliarius), concluding that tail coloration did not affect overall foraging success in this caudal-luring species. Though their findings are interesting, they did not attempt to monitor foraging thereafter, nor identify prey in subsequently recaptured snakes, and so no conclusions can be drawn regarding the effectiveness of luring and tail color on any particular prey types. Additionally, they acknowledge that their model...could not control for the possibility that one treatment group spent more time foraging and caudal luring, or that... black-tailed snakes may have compensated for reduced prey capture rates by spending more time in ambush postures... Ontogenetic tail coloration in viperids merits more extensive study. Similar to tail coloration, the influence of ontogenetic and sex-specific differences in tail length on foraging ability has yet to be fully explored. In his extensive documentation of northeast Kansas Copperhead (Agkistrodon contortrix) ecology, Fitch (1960a, 1999) provided an overview of ontogenetic changes in taillength from birth through adult size, but did not elaborate on the nature of the changes or their possible adaptive significance. He described the change as... the ontogenetic change in each sex consists of shortening of the tail in relation to snout-vent length... (Fitch 1960b), and sexual dimorphism is relatively slight and tends to be obscured by ontogenetic changes (Fitch 1960a) and as the young snakes grow the difference in proportions increases gradually In both sexes the tail becomes relatively shorter as size increases (Fitch 1960a). To preserve the nearly 60 years of field data collected by Henry Fitch, his extensive field records on this and other species are being migrated from paper to database format by one

2 404 Pisani and Riedle of us (GRP). This has provided an opportunity to re-examine this ontogeny in detail with the addition of data collected after the original publications (Fitch 1960a, b and summarized in Fitch 1999), and to suggest a possible selective mechanism for the observed changes. Materials and Methods We used 5084 Fitch Copperhead records (of a total of 5462) from (2287F:2797M) that had complete data (in mm) for Snout-Vent Length (SVL) and Tail Length (TL). Also omitted from this total were records (>10) of snakes with tails not noted as broken but that resulted in greatly reduced TTL values were regarded as original recording errors. Data Analysis: Data were analyzed in three primary ways in an attempt to minimize (even given the large data set) the potential for inference error due to SVL being a component of the ratios examined (TTL, TL SVL). Raw, and thereafter transformed, values of TL and TTL as varying with SVL were analyzed initially by Ordinary Least Squares (OLS) regression. Additionally, one-way ANCOVA was performed using Log-transformed SVLs and TTLs within sexes as column-paired correlated x-y data. Also non-parametric evaluations (Kruskal-Wallis tests for equal medians) of TL SVL and thereafter TTL were done to compare with parametric ANOVAs. Also, raw data for TL was regressed on raw data for SVL; residuals for TL were calculated, and then examined for negative correlation (indicating an ontogenetic shift) with SVL. In all tests, significance was set to p<0.05. Lower and upper 95% confidence intervals were calculated using simple bootstrapping, with 9,999 bootstrap replicates. All statistics were performed using PAST 3.2 (Hammer, et. al. 2001) and Microsoft Excel Results In all instances, outcomes were equivalent, and are consistent with (thus supporting as well as elaborating) the general conclusions of Fitch (1960a, b). Summary statistics are presented in Table 1; distributions of the two tail ratios examined were (male vs female) significantly different (Table 2). A histogram of Log 10 -transformed TTLs (Fig. 1) shows the very slight sexual dimorphism in relative tail length noted by Fitch (1960a, b) in this species. When Log 10 transformed data from sexes are examined via OLS (Fig. 2), it becomes apparent that the smallest SVL snakes (e.g., neonates) are effectively indistinguishable (though significantly different at p=0.05 in large sample sizes) in relative tail length (TTL), and that TTL remains noticeably greater in juveniles, decreasing with size as the snakes grow. A similar regression of untransformed (e.g., raw) data (Fig. 3) indicates the absolute values of the TL-SVL relationship. Results of ANCOVA (Fig. 4) and both OLS tests (absolute and relative TLs) support the ontogenetic difference. TL residuals of both sexes are normally distributed (Fig. 5), and showed weak but definite negative correlation (Pearson r: -0.30) with SVLs. Non-parametric Kruskal-Wallis tests for equal medians using both absolute and relative tail lengths with SVL by sex showed significant difference between sample medians (Table 3). Since absolute (and hence relative) tail length in A. contortrix across SVL sizes varies considerably through the extensive range of the species (Gloyd and Conant 1990; Mitchell 1994), with broad areas of intergradation through states along the Atlantic coast (Mitchell 1994:287) we did not attempt comparisons of this character with distant populations. Table 4 is condensed from Gloyd and Conant (1990) and contrasts Kansas copperheads (A. c. phaeogaster) with the northern populations.

3 Transactions of the Kansas Academy of Science 121(3-4), 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 The decrease in relative tail length with increased age (as inferred from size) in A. contortrix is accompanied by slight, but increasing, sexual dimorphism as male hemipenes and the associated musculatures mature; this sexual dimorphism is typical of viperids in general (Bonnet, et al. 1998; Shine et al. 1999), though the dichromatic change in copperheads and some other tail-luring viperids is not. The untransformed tail length pattern Table 2. Epps-Singleton tests of distributions, tail length ratios. shown here (neonate Kansas copperhead sexes less distinct from each other than are adult) resembles patterns found for four natricids by King, et al. (1999) in their review of general sexual dimorphism and ontogeny, e.g. neonates of both sexes have similar (but not identical) absolute TLs. There is no indication that the genera examined by King, et al (1999) actually engage in caudal luring, and so their explanatory hypotheses did not consider this behavior and its adaptive significance.

4 406 Pisani and Riedle Figure 1. Distributions of relative tail-lengths (Log 10 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 A. contortrix (Fitch 1960a, 1999; Lagesse and Ford 1996) indicate the importance of small, generally insect, prey to mid-sized copperheads. However, both Fitch (1999, table 7) and Lagesse and Ford (1996) found a higher percentage of squamates and anurans in the prey of neonates than in mid-size or adult snakes; the Fitch data relate to the population for which we here discuss caudal luring, and we hypothesize that both these prey types MAY respond to caudal 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.

5 Transactions of the Kansas Academy of Science 121(3-4), 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, et al. (2009) regarding juvenile cottonmouths that selectively prey upon salamanders. Though Fitch (1960a) stated that he never succeeded in eliciting the tail-waving behavior... in captive neonate and juvenile copperheads, the behavior is well-documented, though not as prominent a display as noted for juvenile Figure 4. Plot from ANCOVA. SVL vs TL SVL.

6 408 Pisani and Riedle Figure 5. Distribution of residuals from OLS, untransformed SVL and TL. cantils (Agkistrodon bilineatus) (Neill 1960). Additionally, one of us (GRP) has observed and filmed this behavior in the mid-1980s in captive local neonate copperheads presented with live prey. The sulfur-yellow tail coloration in neonate and juvenile copperheads (Collins, et al. 2010: p178) and related viperids is known to serve as a prey attractant, persisting into adulthood in other viperids not closely related to Agkistrodon (see review in Heatwole and Davison 1976). Table 3. Non-parametric evaluation of tail length relation to SVL. In regard to efficiency of luring, an early hypothesis was that if male snakes have longer tails then male snakes would be more efficient at luring prey (Neil 1960). Rabatsky and Waterman (2005) tested this hypothesis in Pygmy Rattlesnakes (Sistrurus miliarius), where male juvenile snakes had longer tails than same age females. Female S. miliarius females spent significantly more time caudal luring than males, though females did not lure

7 Transactions of the Kansas Academy of Science 121(3-4), Table 4. Percent tail of total length for eastern vs. Kansas A. contortrix from Table 10, Gloyd and Conant more lizards to move within striking distance than males. Because they did not present data on snake body proportions, these findings are difficult to relate to our hypothesis. We know of no similar study with Kansas Agkistrodon. In light of the ontogenetic and behavioral patterns indicated above, we suggest that the longer relative tail length of neonate and juvenile copperheads (essentially equivalent between neonate sexes) MAY enhance the effectiveness of caudal luring. It also might be expected to expose neonates and juveniles to increased predation risk, especially from avian predators, though this may be mitigated by the effective crypsis of juveniles. Juveniles of the congeneric Cottonmouth (A. piscivorus) utilize different microhabitats than adults when foraging, most likely to minimize predation risk while increasing opportunity for prey capture (Eskew et al. 2009). Additional field and laboratory research on age-class habitat preferences and caudal luring of A. contortrix are needed to explore this possibility. Our treatment here of the Fitch data on this species in Kansas presents a quantified overview of ontogenetic changes in relative tail length in Kansas copperheads. Acknowledgments We are grateful to Kansas Dept. of Wildlife, Parks, and Tourism Chickadee Checkoff Program for financial support (to GRP) of the Fitch Snake Data Archive project. GRP thanks Kansas Biological Survey (KBS) (Edward Martinko, Director) for providing work space and computational support for an ongoing variety of research efforts. KBS additionally houses the Fitch Data Archive, and is custodian of the electronic databases constructed by GRP. Neil Ford provided reference material. The constructive comments of three anonymous reviewers are greatly appreciated, and have for the most part been incorporated. We also acknowledge the exceptional efforts of Henry S. Fitch (deceased) in amassing a phenomenal record of ecological data on eastern Kansas snakes. Literature Cited Andrade, D.V. and Abe, A.S Relationship of venom ontogeny and diet in Bothrops. Herpetologica 55: Bonnet, X., Shine, R., Naulleau, G. and Vacher-Vallas, M Sexual dimorphism in snakes: different reproductive roles favour different body plans. Proceedings of the Royal Society of London B: Biological Sciences, 265(1392): Carpenter, C.C. and Gillingham, J.C Ritualized behavior in Agkistrodon and allied genera. pp in Gloyd, H.K. and Conant, R.C., Snakes of the Agkistrodon Complex. A Monographic Review. Contributions to Herpetology, Number 6. Society for the Study of Amphibians and Reptiles. i-vi+614pp Clark, R.W., Dorr, S.W., Whitford, M.D., Freymiller, G.A. and Putman, B.J Activity cycles and foraging behaviors of freeranging Sidewinder Rattlesnakes (Crotalus cerastes): the ontogeny of hunting in a precocial vertebrate. Zoology 119: Collins, J.T., Collins, S.L. and Taggart, T.T Amphibians, Reptiles and Turtles in Kansas. Eagle Mountain Publishing, LC, Eagle Mountain, Utah. xvi+312pp

8 410 Pisani and Riedle Eskew, E.A., Willson, J.D. and Winne, C.T Ambush site selection and ontogenetic shifts in foraging strategy in a semi-aquatic pit viper, the Eastern cottonmouth. Journal of Zoology 277: Farrell, T.M., May, P.G. and Andreadis, P.T Experimental manipulation of tail color does not affect foraging success in a caudal luring rattlesnake. Journal of Herpetology, 45(3): Fitch, H.S. 1960a. Autecology of the Copperhead. University of Kansas Publications, Museum of Natural History. Vol. 13, No. 4, 288pp Fitch, H.S. 1960b. Criteria for determining sex and breeding maturity in snakes. Herpetologica 16(1): Fitch, H.S A Kansas snake community: composition and changes over 50 years. Krieger Publishing, Malabar, Florida. xii pp. Gloyd, H.K. and Conant, R.C Snakes of the Agkistrodon Complex. A Monographic Review. Contributions to Herpetology, Number 6. Society for the Study of Amphibians and Reptiles. i-vi+614pp Greene, H.W. and Campbell, J.A Notes on the use of caudal lures in arboreal green pitvipers. Herpetologica 28: Hammer, Ø, Harper, D.A.T. and Ryan, P.D PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1): 9pp. [ past/issue1_01.htm Accessed 12 December 2017 from Heatwole, H. and Davison, E A review of caudal luring in snakes with notes on its cccurrence in the Saharan Sand Viper, Cerastes vipera. Herpetologica 32(3): King, R.B., Bittner, T.D., Queral-Regil, A. and Cline, J.H Sexual dimorphism in neonate and adult snakes. J. Zool., Lond. 247: LaBonte, J.P Ontogeny of prey preference in the Southern Pacific Rattlesnake, Crotalus oreganus helleri. pp in Hayes, W.K., Beaman, K.R., Cardwell. M.D., and Bush, S.P. (eds.), The Biology of the Rattlesnakes, Loma Linda University Press, Loma Linda, California. Lagesse, L.A. and Ford, N.B Ontogenetic variation in the diet of the southern copperhead, Agkistrodon contortrix, in northeastern Texas. Texas Journal of Science 48(1): Mackessy, S.P Venom ontogeny in the Pacific rattlesnakes Crotalus viridis helleri and C. v. oreganus. Copeia 188: Mitchell, J.C The Reptiles of Virginia. i-xv+352pp, Smithsonian Institution Press. Neill, W.T The caudal lure of various juvenile snakes. Quarterly Journal of the Florida Academy of Sciences, 23: Rabatsky, A.M. and Waterman, J.M Ontogenetic shifts and sex difference in caudal luring in the Dusky Pygmy Rattlesnake Sistrurus miliarius barbouri. Herpetologica 61: Shine, R., Olsson, M.M., Moore, I.T., LeMaster, M.P. and Mason, R.T Why do male snakes have longer tails than females? Proceedings of the Royal Society of London B: Biological Sciences, 266(1434):