Great Basin Naturalist

Volume 59 Number 4 Article 8

10-15-1999

Caudal distraction by rat snakes (Colubridae, Elaphe): a novel behavior used when capturing mammalian prey

Stephen J. Mullin University of Memphis, Memphis, Tennessee

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Recommended Citation Mullin, Stephen J. (1999) "Caudal distraction by rat snakes (Colubridae, Elaphe): a novel behavior used when capturing mammalian prey," Great Basin Naturalist: Vol. 59 : No. 4 , Article 8. Available at: https://scholarsarchive.byu.edu/gbn/vol59/iss4/8

This Article is brought to you for free and open access by the Western North American Naturalist Publications at BYU ScholarsArchive. It has been accepted for inclusion in Great Basin Naturalist by an authorized editor of BYU ScholarsArchive. For more information, please contact [email protected], [email protected]. Great Ba....in Naturalist 59(4), ©1999, pp. 361....167

CAUDAL DISTRACTION BY RAT SNAKES (COLUBHIDAE, ELAPHE): A NOVEL BEHAVIOR USED WHEN CAPTURING MAMMALIAN PREY

Stephen]. Mullin1

AJ3S11UCT.--el.mthtl movement in snakes trulY serve ei.ther a pl'Cdatory (e.g., caudal luring) or defensive (e.g., rattling, aposem,ttism) fUllction, I descliho n new behavioral pattern of tai.l movement in snakes. Gray rat snakl.'$ (Elaphe OhSO!etd spiloid.es) fi)raging on ~ma11 mmnmnls (Mus d01ne~·ticus) Inoved. their tails in un erratic, whiplike fashion uIter detecting prey in their vidnity. The thrashing movement in the horizontal plfme was audibly and visually obviolls, resulting in dis­ placement of leaf litter around the hlil. All subjects displayed the behavior, hilt not in all foraging episodes. Shorler durations ofcaudal distraction~1.l1lecl in greater predator SIIt.'t.'eSS during the 1st attempt snake.

Key words: caudal diJplalj, prerat snake, Cnlul.1t'hlae.

Visual communication by snakes (Carpenter 1993, Rahatsky and Farrell 1996) and at least 1 1977, Carpenter and Ferguson 1977) occurs in lizard specics (Morray et at. 1991). It is typi­ the absence of appendages used by many cally displayed by snakes foraging from lin other vertebrate taxa (CuUen 1972, Enquist et ambush posture (Chiszar et al. 1990). al. 1985). Limblessness necessitates the use of Both defensive tail vibration and caudal lur­ head, body, or tail for visual display. Snake de­ ing have been observed in rat snakes (Elaphe fens:ive displays frequently il1volve tail move­ obsoletspecies ofcolubrid snakes (Greene descrihe a heretofore undocurnented prellu­ 1988) and other elongate reptiles (Greene 1973) tory behavior of gray rat snakes that was dis­ also perform defensive tail displays. played only in tl,e presence of mammalian Another fonn of taU movement, termed prey. Frequency and duration of this behavior caudal/tIring, fucilitates prey capture. This be­ and its facilitation of prey capture arc also havior is described as a slow, undulatory or reported. Becaose this behavior parallels cau­ vermiform movement of the tail while it is dal luring and defensive tail vibration, I term held upright in close proximity to the snake's the novel behavior caudal distraction.. head (Heatwole ,uld Davison 1976). Caudallur­ ing is presumably mimetiC, in that the move­ MATERIALS AND METHODS ment is thought to resemble an insect huva OT worm and thus attracts potential prey to within r first noticcd caudal disb'action in a 113­ striking dLstance of the otherwise motionless em snout-vent length (SVL) female gray rat snake. Caudal luring has been documcnted in snake foraging for a mixed-sb'ain mouse (M. nearly aU fiunilies of snakes (Carpenter et at. domesticus). The snake was in an enclosure 1978, Radcliffe et al. 1980, Sazima and Puorto tllat simulated a bottomland hardwood forest

1Dellurtll1<:nt of 13inJO/,.'Y. University of Me,nphi~> Mell1phl~, TN 38152. l'r~enl (u::Idre$~' [kplll'tO\onl of 13iolOjl;1cul Scf«llOO&. EiI.I!I,,·n lllilmis UIlive-!'!'It.v. Charleston, IL 61920.

361 362 GREAT BASiN NATURALIST [Volume 59

habitat (see below). Behavior was documented Adult male lllic-e were placed in the enclo­ on videotape to permit detailed description. sure for a minimum of 10 min for acclimatiza­ Several other adult snakes displayed this tion. Only adult maJe mice having dark brown behavior with IitUe departure from the oligi­ pelage were used as prey duling the observa­ nal pattern. To examine possible differences in tions to minimize visual and vomeronasal dif­ capture success and latency to prey capture ferences among prey available to snakes (J ~oop that might be dependent on the use of this 1970) and provide prey visually similar to behavior, I recorded adult gray rat snakes (n those which sn.\kes encounter in the field. All =15) involved in {(>raging episodes under sim­ mice had similar mass (30.7 + 0.5 g, n = 30), ilar conditions. although the ratio of prey mass to snake mass Subjects (10 males and 5 females. >100 cm was not fixed during the study. A gray rat snake SVL) were obtained fi·OOl forested and semi· was placed in thc corner of the enclosure far­ rural areas within Shelby County, Tennessee, thest removed from the prey. Because observer and maintained 'in captivity at temperature presence may influence snake behavior (Drum­ and photopeliod regimes of 26-29°C and mond 198.3), behaviors were recorded by a 14:10 h light:dark, respectively. Suhjects had video carner.! on a tripod elevated over the spent between 1 and 16 months in captivity enclosure floor. The camera was always Oli­ prior to examination. Snakes were housed jn­ ented toward the snake, meauing that possible uividually in cages measuring a minimum of differences in prey behavior were not recorded. 30 x 60 x 30 ern, provided with water ad libi­ Occasionallv,, caudal distraction was initiated tum, and fed either KorUlem Bobwhite Quail with the b,il outside the field of view; bow­ (Colinus vir{"rinianlls) eggs or mixed-strain mice ever, tail movement was audibly discernible as weekly. Excepting; o<..:ca.~iona1 cage cleaning and leaf litte.- in the immediate vicinity was dis­ monthly SVL (±O.5 Col) measurements, sub­ turbed and could thus be recorded from its jects were handled as little as possihle to mini.· initial occurrence. mize any hehavioral modifications resulting The latency to suc(.--essfiIl mouse capture may from prolonged captivity (Warwick 1990, Ford lwve depended, in part, on initial distances 1995). Because recently fed snakes may exhibit separating the snake and its prey. Howevel; shilts in behavioral pattern (Beck 1996) or the colJlined, relatively sm,Jl euclosure proba­ alteTation of locomotor pClformance (Martin bly limited the influence of initial separation 1996), individuals were placed on a restricted distance. Missed attempts at capturing the diet (water alone) for 3 wk prior to experimen­ mouse and frequency and duration of caudal llJ trials. Between 23 April 1995 and 25 March distraction were recorded from videotaped 1996, snakes were allowed to forage indiVidu­ observations. A repeated-measures analysis of ally for mice on at least 2. different occasions, variance (ANOVAR; each mbject was recorded each separated by a 3-wk resmeted diet. on 2 occasions) was used to determine An enclosure (2.25 m2 and 2 m in height), whether those snakes exhibiting caudill dis­ c'Onstructed to simulate bottomland hardwood traction required fewer attempts to Sllccess­ forest ofthe wildlile m'magement area ofnearby /llily capture mke. l'aramemc statistics (Scheffe Mecman-Shelby Forest State Park (MSFSP), 1959, Cohen 1965) were also used to detect Tennessee, ,;vas maintained at the photoperiod any relationships between frequency and/or and temperature regimes described above. duration of caudal distraction and snake gen­ ArtHicial vegetation simulated mean recorded der (ANOVAR) or sile (Pearson's regression). level of vegetation density al MSFSP (mea­ Statistical tests were conducted using Super­ sured in June 19animal while the 1999J CAUDAL BEHAVIOR IN El..1I'H£ 363 predator's bead is moved to within slrildng distraction dJsplay; instances ofstationary t:au­ range ofthe prey. dal distraction were frequently accompanied In E. o. spiloides c-audal disb1lction displaL-ed by some time displaying the hehavior while leaves near the blil. was visually conspicnous advancing toward the mouse. There was no when unobscurcd by emergent vegetation, and difference in the amount of time a snake dis­ was audible from a distance ofseveral meters. played caudal distraction as a function of for­ Mice (M. domestu,~18) responded to caudal dis­ aging mode (ambush or pursuit) or trial nrder traction by ceasing all movement, often after (F1.J3 < 1.93, 1';:' 0.19). orienting their heads toward the undulating The ability of gray rat snakes to capture tail (Fig. 1). An ermtic lateral movement oftlw their prey on the .1st strike was influenL-eci by posterior 70% of the tail characterized the tail the duration of caudal distraction (Table 1; display. Undulations of the more proximal tail Pearson's r = 0.71, I' = 0.(03); longcr times portion appeared sinusoidal in fonn, but the spent performing caudal distraction \-\Tere tail til' moved similarly to the cnd of a whip, as:sociated with fewer successful 1st strikes. curving in a 1800 arc on either side of the tail Snakes failing to capLm·c their prey on the 1st Such movements were serially repeated 'with attempt typic-ally succ.eeded on the 2nd or 3rd an average (+1 .x) of 1.4 + 0.2 see elapsing for strike. Neither frequency nor duration of cau­ each whiplike pattern. Usually, but not always, dal distra<:tion was a tunction of snake gender caudal distraction was performed while the (Ftt3, < 0.1, I' > 0.9) or size (Pearson's r < body was laterally bent at an obtuse angle such 0.31, I' >0.26). Therc was no dilTerence in rate that tail movement was positioned to one side of successli,l capture on the 1st attempt as a of the hody axis with respect to the head. Dif~ function of whcther the snake displayed ean­ ferences between caudal distraction and other d~J distraction \vhile moving or stationary described tail movements are discussed below. (F113, = 0.15, I' = O.7J). AllIS gray rat snakes clisplayed the described behavior, although not in all foraging episodes DISCUSSION (caudal distraction was ohserved in 19 of 30 staged encounters and has been documented Caudal distraction most closely resembles in > 20 other occasions involving these and rapid tail movements that Carpenter ot al. other adult subjects foraging in different (1978) described as part of the caudal luring enclosure conditions; Mullin 1998). The behav­ sequence in death adders (Acanthophis). How­ ior, while most often displayed after snakes ever, caudal distmdion ditlers from luring in 2 visually detected miee, also oc'CUITcd when prey discernible l;,atures: (1) position of the tail rel­ was visually obscured (possibly a response to ative to the snake>s head---{Hstance separating tactile or chemosensory stimuli). Caudal dis­ head and tail is greater when disb-acting thml traction was always initiated before Ule head when luring, with UIC tail displaced laterally of tl,e snake was within striking distance of its away fi·om thc head (rather tl,an aligned in prey « 10 em). Dumtion ofthe behavior always fi·ont of, or behind, the head); 'md (2) speed of extended to the moment of sbiking the prey. taU movement--distmction movements are Subjects displaying caudal distraction did not generally faster than movements describcd for require less time (127 + 32 sec) to capture luring (approaching 2 undulations sec-I; Car~ prey than those not displaying the behavior penter et al. 1978). (140 + 36 sec; F1,13 =0.09, I' = 0.70). Subjects Caudal distraction was always initiated be­ did not display caudal distraction when offered fore snakes were within striking distance of other prey types (Colinus l:';-rginiutlus and their prey, and mice typically dirccted their Coturnix cotul"nix eggs, C. d-rginianus chicks. attention toward tl'e tail. Wnen using caudal Hemidtu:tylus turcicus juveniles, M. dome.ti<:us disb-action, snakes approached prey more slow· neonates) under similar test conditions. ly than when not displaying the behavior. Displays (n = W) averaged 27 + 8 sec in Although striking distance in fom!,~ng episodes duration and were usually initiated while tlu~ was not quantified in this study, the behavjor snakes were actively searching for prey, or less may permjt doser approach of snakes to their often from a stationary position (although not prey prior to attempting capture (Schmidt et necessarily a coiled posture). Snakes were rarely al. 1993), Foraging attempts involving display stationary for the entire duration of a caudal of caudal distraction did not result in gray rat [Volume 59 364 GlU:.H BASI'! NATVlIALlST

r'ig. 1. OnHbl (li~tnlclion in £lapfUl ofISofeta ~1J1loides (digitized £roOl viut.'ot'lp,;-:d obsel'vut.ions). Bhm'cd silhouettes of tail imli<:atc maximum eurvahn'c of tail during perfimmul<:c ufheh.wiol'. 1999] CAUDAL BEHAVIOR IN ELAPliE 365

TABLE L Capture stl(..'<..'t:ss as a function of the duration When performing caudal distraction, DO (!'iec; mean ± 1 sx-) of caudal distraction disphy in adult subject ever positioned its tail close «30 em) gray rat snakes (Elt.,phe obsolet.!:l spiloides). Sample sizes are given in pa.rentheses. Values in 2nd and 3rd columns to its head. Had mice been lured to the tail are different (Pearson's r = 0.71, P = 0.003). movement, they would not have been enticed to within striking distance of the snake. Thus, Omlltlon of Duration of Durati.on of caudal distraction caudal distraction the desclibed behavior appears to serve more caudal when 1st strike when 1st sbike as a distraction than it does as a lure to poten­ distraction succoodl.'rodent toward the mouse than when stationary, how­ species (Lima and Dill 1990). Subtle differences ever, indicating that any importance associated in response to snake presence by captive-bred with crypsis or stealth that might elicit a dis­ and wild-caught mice (Dell'omo and Alleva placement behavior was negligible. It is also 1994) suggest that caudal distraction would be worth noting that caudal distraction was of similar effect on small rodents in natural repeatedly displayed by snakes maintained in settings. captivity for durations of 1-16 months, 366 GREAT BASIN NATUHALlST [Volume 59 indicating that behavior was not suppressed special thanks for digitizing the figure of tJ,e hy conditions ofcaptivity (Warwick ]990). descrihed behavior. 1 am grateful for discus­ A few other cautions warrant (.'onsjderation: sions witJl G. Burghardt and comments from M. domesticus is not native to the geographic E.D. Brodie, Jr., R. Cooper, M. Ferkin, N. Ford, distribution of Elaphe; other small rodent taxa S. Fox, W Gutzke, A. Price, R. Reiserer, G. sympatric with gray rat snakes (e.g., Peromys­ Rodda, and 3 anonymous reviewers that im­ CIJS, Microtus, Sigmodon, etc.) may behave dif­ proved this mauuscript. Funding was provided ferently in response to caudal distraction by in pari by the Department of Biology, Univer­ snakes during a predator-prey encounter. Edge sity of Memphis. effects (a feature of noucircular enclosures; Krebs 1989) or space limitations of the enclo­ LITERATURE CITED sure may have ma.,ked a difference in ability to capture prey that wa!l' dependent upon cau­ AllNOLD. S.J. 1986. Laboratory and field approaches to the ~1:udy ofadaptation. Page-.s 157-179 in M.E. Feder and dal distraction frequency or duration. G.Y. Laudel; editors, Predator-prey relationships. The following observations suggest that Un.iversity ofChicago Press, Chicago, IL. much remains to be examined in the func­ BECK, OJ). 1996. Effects offeeding on body temperatures tional and ontogenetic development o( as well of rattJe.'makes: a field experiment. Pbysiological Zoology 69:1442-1455. as the importance of specific stimuli in elicit­ BUll(;~IAlmT, C.M. 1991. Cognitive ethology and critical ing, caudal hehaviors in Elaphe. (1) \Vhereas anthropomorphism: a snake with two heads and hog­ caudal luri,ng has heen documented in both nose snakes that play dead. Pages 53-90 in C.A.. Ris­ juveniles and adults of several taxa (Chiszar et I"nll, editor, C..ogniti.ve ethology: the minds of other animals. ErlbrlUm & Assoc., Hillsdale, NJ. al. 1990, and Jackson 1997, nebont 1997, Sisk CARPENTEIl, C.C. 1971. Communication and displays of and references therein), eaudal distraction has snakes. American Zoologist 12:217-223. not been observed in rat snakes <2.4 yr old CARPRNTER, C.C., AND C.w. FgI\GUSON. 1977. Variation (Mullin ]998). (2) Two adult gray rat snakes and evolution of stereotyped behavior in reptiles. were observed performing caudal luring, al­ Pages 335-554 in C. Gans and D.W Tinkle, edit.ors, The biology of the Reptilia. Volume- 7. Academic though without the tail in typical proximity to Press, New York the hcad (Carpenter et al. 1978, Jackson and CAHl'liNTElI, C.G, JR MURPHY, AND G.G CARPENTI<:R. 1978. Martin 1980, Tiebout 1997). (3) Luring in gray Thilluring in the death adder, Aca.ntlwphis untarcu.. rat snakes was recorded when foraging for CtM (Heptilia, Serpentes, Elapidae). Journal of Her­ petology 12,574-577. mammalian and avian prey, and in both cases CH1S7AtI, D., O. BOYER, H. LEE, J.B. MURPHY, AND C.w. waS elicited in response to prey movement. RAIX:I.U'FE. 1990. Calldalll1ling in the soutJlern dealh Differences in behavior patterns resulting addtlr, Acanthophis antarcticlls. Journal of Herpetol­ from the discrimination of prey types have ogy 24:253-260. CoHt::N, J. 1965. Some statistical issues in psychological hecn demonstrated in otller uua (Arnold 1986, research. Pages 95-121 in B.B. Wolman, editor, .Hand­ Ford and Burghardt 1993) and indieate an book ofclinical p~ychology. McCraw-Hill, New York. appropriate direction for further study of the CULLEN, J.M. 1972. Some principles of animal communi· described behavior. In particular, documenta­ catioll. Pages 101-1.22 in R.A. Hinde, editor, Non­ verbal communication. Cambridge University Pre.

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