inTroduCTion

Wildlife professionals are increasingly turningto translocation as a management tool tomaintain declining wildlife populations (Griffithet al. 1989). Translocation (the intentionalrelease of captive-propagated and/or wild-caughtanimals into the wild for the purpose ofestablishing a new population, reestablishing anextirpated population, or augmenting a criticallysmall population or managing nuisance animals;IUCN 2012), has been employed world-wide inhundreds of conservation programs withnumerous taxa (e.g., Seddon et al. 2007). Manyof these projects (33–52%) fail to establishsuccessfully reproducing individuals and the truesuccess rate is likely lower if failed projectsdisproportionately go unpublished (Scargle2000). Comprehensive reviews of translocationprojects have reported apparently greater successof reintroductions involving wild-to-wildtranslocations compared to the release of captiveanimals (Griffith et al. 1989; Wolf et al. 1996;Fischer and Lindenmayer 2000). Such reportshave raised concerns that captivity may decreasethe ability of individuals to survive in the wildfollowing release (Kleiman et al. 1994; Snyderet al. 1996; Mathews et al. 2005).

Captive animal populations may show rapidchanges (in three generations) in behavioralphenotypes (Connolly and Cree 2008; Guay and

Iwaniuk 2008) and genotypes (Kraaijeveld-Smitet al. 2006) as a consequence of stunted learningand development, or selection favoring traits thatare “adaptive” to captive conditions. Thesechanges are often unexpected and potentially thedetrimental consequences of captive rearing.Such changes can affect the success oftranslocation projects by promoting maladaptivebehaviors related to foraging or predatoravoidance. When released, many captive-bornanimals experience high rates of predation (Juleet al. 2008; Aaltonen et al. 2009) and starvation(Jule et al. 2008), or are reliant on anthropogenicfood sources (Champagnon et al. 2012).Evidence indicates that the more generations apopulation of animals is maintained in captivity,the less likely individuals are to retain high levelsof physical performance (Connolly and Cree2008) or to react normally to predators (McPhee2003; Kraaijeveld-Smit et al. 2006). Whiledecreased physical performance and predatoravoidance behavior of captive-born animals havebeen documented on a generational time scale(McDougall et al. 2006), effects on finertemporal scales for wild-born captives (within anindividual’s lifetime) have received much lessattention.

The use of captive-born animals confounds ourability to separate and understand changesarising from selection as opposed to phenotypicchanges arising during the course of captivity.

Herpetological Conservation and Biology

Time in CapTiviTy affeCTs foraging Behavior of raTsnakes:impliCaTions for TransloCaTion

Brett A. DeGreGorio1,2, PAtrick. J. WeAtherheAD1, trAcey D. tuBerville2, AnD Jinelle h. SPerry1,3

1Department of Natural Resources and Environmental Sciences. University of Illinois at Urbana – Champaign, 1102 S. Goodwin Avenue, Urbana, Illinois 61801, USA, e-mail: Bdegrego@illinois.edu

2University of Georgia Savannah River Ecology Lab, Drawer E, Aiken, South Carolina, 29802, USA3Engineer Research and Development Center, 2902 Newmark Drive, Champaign, Illinois 61826, USA

Abstract.—as wildlife populations decline or disappear, wildlife professionals are using management tools such astranslocation to maintain viable populations, often with mixed results. Wild-to-wild translocations are often more successfulthan when captive animals are released, raising concerns that captivity may have deleterious effects on animals. althoughthe effects of captivity have been documented on a generational time-scale, effects within the lifetime of an individual havereceived much less attention. here we examine how time in captivity affects foraging behavior of wild-caught ratsnakes(elaphe obsoleta). The longer ratsnakes had been in captivity, the less successful and slower they were to react to prey in asimple laboratory discrimination task. snakes that had been captive for a year or more performed no better than expectedby chance. Captivity-induced degradation of ecologically important behaviors provides a potential mechanism underlyingthe poor performance of animals that are released into the wild following prolonged captivity. our results also suggest thatresearch using captive snakes may not always document behaviors representative of wild snakes.

Key Words.—conservation; Elaphe obsoleta; prey detection; reintroduction; repatriation; snakes

Copyright © 2013. Brett DeGregorio. All RightsReserved. 581

Herpetological Conservation and Biology 8(3):581−590. Submitted: 15 April 2013; Accepted: 20 July 2013; Published: 31 December 2013.

Wild-caught animals maintained in captivity foran extended time experience similar influenceson their behavior as animals born in captivity.Indeed, long-term captive (but wild-born)animals in zoos and laboratories often displaybehaviors very different from those of free-ranging wild conspecifics (Fox 1968). Animalsmaintained in captivity are constrained fromdisplaying natural and flexible behavior, whichcan lead to a reduced behavioral repertoire(Poole 1992) and altered behaviors (Fox 1968).In the only translocation study to directlyinvestigate captivity effects on behavior of wild-caught individuals, Ben-David et al. (2002)showed that adult River Otters (Lontracanadensis) held in captivity for relatively shortdurations (nine months) suffered from increasedpredation and starvation upon release relative towild conspecifics. A recent review found thatbehavior of captive animals becomes lessrepeatable over time (Bell et al. 2009). However,no study has yet investigated the effect ofcaptivity duration on performance of wild-caught captive animals.

In many ways snakes appear to be idealcandidates for translocation because wild-caughtindividuals can be easily maintained and bred incaptivity. Furthermore, evidence that somesnake behaviors are “hard-wired” (Chiszar et al.1993) suggests that captivity might have limitedeffects on snake behavior. Despite thesecharacteristics, however, snake translocationshave had mixed results (Nowak et al. 2002;Germano and Bishop 2008; Kingsbury andAttum 2009; Roe et al. 2010), with failure oftendue to abnormal behavior of releasedindividuals. Future translocation andreintroduction efforts may therefore benefit fromexperimental assessment of how captivity affectssnake behavior, and how those effects vary withtime in captivity. In this study we compare theability of wild-caught Ratsnakes (Elapheobsoleta), held captive for varying lengths oftime, to react to and locate prey. If captivity hasa detrimental effect on behavior, snakeperformance should decline with increasing timein captivity.

maTerials and meThods

Study animals.—We compared the foragingability of 11 long-term captive Ratsnakes (1–60months in captivity) to that of 16 recently wild-caught Ratsnakes (< two weeks in captivity).

The long-term captive Ratsnakes were part of theSavannah River Ecology Lab’s (SREL) outreachprogram. These snakes were originally caughtas adults from the local area (Aiken andBarnwell counties, South Carolina, USA),usually as a result of human-animal conflict(e.g., in chicken coops, residences, etc.). Long-term captive Ratsnakes had been maintained atthe SREL animal care facility since capture. The16 short-term captive Ratsnakes were collectedopportunistically by hand from the same localarea. We weighed each snake to the nearestgram and measured to the nearest centimeter(snout to vent length; SVL). We only usedsnakes with an SVL > 70 cm for foraging trials(see below); we excluded gravid femalesbecause they may not have been as food-motivated as non-gravid snakes. We calculatedthe body condition of each snake using theresiduals of a regression of log transformed masson log transformed SVL. Because all snakeswere of similar size, this measurement of bodycondition avoids some of the potential biases ofbody condition calculations for snakes(Weatherhead and Brown 1996).

We housed all snakes individually in either 10-or 20-gallon glass aquaria or custom-built plasticand glass containers of similar size. Each had asubstrate of aspen shavings, a water bowl, and aretreat shelter. We kept all animals on a 12:12light:dark cycle at a constant temperature of 30°C. Long-term captive snakes had been fedthawed frozen mice weekly. Before being usedin a trial, we fasted each snake for a minimumof seven days (range = 7–11: mean = 9.9 d) toensure a strong appetitive response. Within theirfirst two days of captivity, we offered each short-term captive snake a dead mouse (Mus musculus;purchased commercially frozen then thawed inwarm water) weighing < 3% of their body mass.All snakes accepted the mouse, establishing thesight and smell of dead mice as desirable fooditems. After acceptance of the mouse, we thenheld snakes without food for a minimum ofseven days (range = 7–14: mean = 8.3 d). Weheld short-term captive snakes for < 2 weeksprior to testing and we released them at theirpoint of capture immediately after use.

Prey location trials.—Ratsnakes seasonallyshift from diurnal to nocturnal activity (Sperryet al. 2013), suggesting that they may be capableof locating prey both visually (Mullin andCooper 1998) and chemically (Saviola et al.

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2012). Because the long-term captive snakeshad become accustomed to diurnal feeding inwhich they were able to watch caretakers placefood in their enclosures, we examined theirability to locate prey nocturnally when visualstimuli were absent or minimized, a necessarytask for wild snakes. We presented all snakeswith a discrimination task requiring them to useeither chemical, visual, or coupled visual andchemical stimuli to locate prey in darkconditions. We performed all trials reported herein a room with a constant temperature of 30° Cand constant light of 1 lux to approximate lightconditions on a cloudy night. We placed snakesindividually in a plastic holding container (33.8cm L × 21.6 cm W × 11.9 cm H) with three cleartubes (10.2 cm diameter × 120 cm long)radiating out of it (one on each of three sides;Fig. 1). At the end of each tube was acompartment, one of which was baited with preyduring each trial. We initially prevented snakesfrom entering any of the tubes by clear screengates (aluminum window screen) placedbetween the holding container and the tubeentrances. In each trial, we placed both a dead-thawed mouse and a life-like toy mouse on astring at the end of one tube either behind opaquescreen made from six layers of charcoalfiberglass window screen (chemical stimulusonly), a clear, solid plastic screen (visual

stimulus only), or a clear barrier made fromaluminum window screen (visual and chemicalstimuli). Snakes were allowed access to all threetubes in each trial, but only one tube (randomlydetermined) contained prey in any given trial.Thus, in each trial there was one baited tube andtwo non-baited tubes. After allowing the snake30 min to acclimate to the holding container (tocease escape behavior and to react to the prey),we removed the gates, which provided the snakeaccess to all three tubes during the trial. Weinterpreted the snake entering one of the tubes ashaving reacted to the prey in that tube. Aftereach trial we cleaned the tubes thoroughly withpaper towels and an unscented commercialsurface disinfectant and then subsequentlyrearranged in a randomly determined order.

We recorded the response of each snake as amultinomial variable with snakes entering thebaited tube as having correctly “reacted to prey,”snakes entering one of the unbaited tubes as“failed to react to prey,” and snakes thatremained in the holding container for the entire30 minutes as “failed to respond.” One of theauthors (BAD) watching from behind a blind(and making the mouse on a string move in alife-like fashion) determined that a snake had“selected” a tube when its head was 25 cm fromthe holding container (marked by a piece ofblack tape around each tube). Under low light

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figure 1. A schematic of the experimental apparatus to determine prey detection inBlack Ratsnakes (Elaphe obsoletus).

conditions during trials, it was still (just) possibleto detect the dark snakes in the clear plastictubes. We also recorded the time from removalof the barriers to when the head of a snake was25 cm from the container (defined as latency).We tested all 27 snakes three times,incorporating prey stimulus type, with the preystimulus presented in a randomly selected order.The three tests for each snake occurred duringthe same day and we used “trial order” as avariable in our analyses to test for the ability ofa snake to learn between trials. All trials tookplace between 1 June and 15 August 2011 or 1May and 5 June 2012 from 0900 to 1400. Onlyone author (BAD) performed trials to eliminateinter-observer variability.

Data analysis.—We first compared the bodycondition of short and long-term captive snakesusing a t-test. We then compared the number ofshort and long-term captive snakes that reactedto prey to that expected by chance (33%) usingChi-square analysis. Because we recorded thereaction to prey as a categorical response (choiceof baited tube, choice of unbaited tube, or nochoice), we used a generalized linear mixedmodel (GLMM) with multinomial logisticregression to compare the effect of captivity onreaction to prey. We used group (short vs. long-term captive), stimulus type (visual, chemical, orchemical and visual), body condition, time sincelast meal, and trial order as fixed factors, withsnake ID as a random factor to account forindividual variability and the repeated measuresdesign. We compared latency to react to preyusing a univariate generalized linear model(GLM) with the fixed factors of group, bodycondition, time since last meal, and trial order,with snake ID included as a random factor in allanalyses. We explored the effect of time incaptivity on the ability and latency to react toprey using linear regression analysis. In thelinear regression analysis of captivity durationand reaction to prey success, we grouped trialsin which snakes failed to react to prey with trialsin which snakes failed to respond. In theanalysis of captivity duration and latency, weterminated trials in which snakes failed torespond after 30 min. Thus, latency for thesetrials was determined to be 30 min.

resulTs

We tested 16 short-term captive and 11 long-

term captive Ratsnakes for a total of 81 trials.Snakes failed to respond to prey in seven of 81trials (8.6%; four for short-term captives andthree for long-term captives). Short-term captiveRatsnakes moved into the baited prey tube at arate greater than expected by chance (63% vs.33%: χ2 = 29.44, df = 15, P = 0.01; Fig. 2);whereas, long-term captives did not (31% vs33%: χ2 = 22.31, df = 15, P = 0.99). Snake group(short- vs. long-term captive) had a significanteffect on the choice of a tube by an individual(F2,79 = 3.56, P = 0.03). Although long-termcaptive snakes tended to have a higher bodycondition, the difference was not significant (t =1.33, P = 0.10). Stimulus type, body condition,time since last meal, and trial order did not havea significant (P > 0.16) effect on a snake’s abilityto detect and approach prey (Fig. 2). Althoughstimulus type did not have a significant effect onthe reaction to prey by a snake (P = 0.26), long-term captive Ratsnakes reacted to prey at highrates (75%) when chemical and visual stimuliwere coupled, whereas short-term captivesreacted to prey at similar levels for all stimulustypes. Snake group also had a significant effecton latency to react to prey (F1,79 = 40.6, P =0.02), with short-term captive snakesapproaching prey faster (mean ± SE: 400 ± 52 s)than long-term captive snakes (594 ± 111 s).Neither trial order, body condition, stimulus, nortime since last meal had a significant effect (allP ≥ 0.26). Although not significant (P = 0.23),there was a trend for short-term captives toapproach prey more quickly when chemical (260± 48 s) or chemical and visual (384 ± 49 s)stimuli were presented compared to visualstimulus only (556 ± 83 s; Fig. 3). No trend wasdetected for long-term captive snakes (P = 0.72).Using time in captivity as a continuous variable,we found a negative relationship between timein captivity and successful reaction to prey (r2 =0.17, P = 0.03; Fig. 4a) and a positive correlationbetween time in captivity and latency to react toprey (r2 = 0.47, P = 0.02; Fig. 4b), indicating thatthe longer a snake had been in captivity, the lesslikely it was and the longer it took to approachprey.

disCussion

Compared to snakes that had been maintainedin captivity for longer periods, short-term captiveRatsnakes located and reacted to prey at a higherrate in a discrimination task. Short-term captive

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figure 2. Proportion of short- and long-term captive Ratsnakes (Elaphe obsoleta) that entered thebaited tube, an unbaited tube, or did not enter any tube in nocturnal foraging trials when the preystimulus present was either visual, chemical, or both.

figure 3. Latency to react to and approach prey of short- and long-term captiveRatsnakes (Elaphe obsoleta).

snakes successfully reacted to prey 63% of thetime, compared to 31% for long-term captivesnakes, which performed no better than wouldbe expected by chance. Short-term captiveRatsnakes also approached prey more quicklythan their long-term captive counterparts (400 vs594 s). When time in captivity was used as acontinuous variable, we found that foragingperformance declined with time in captivity. Ourresults indicate that Ratsnakes held in captivityfor as little as 10 months were less successful andtook longer to locate prey than snakes justbrought into captivity. Two of the long-termcaptives had been brought into captivity only oneand three months prior to being tested and

located prey in 67 and 100% of trials, whereasthree snakes held in captivity between 10 and 13months located prey levels not different than bychance (33%). Because all snakes were capturedas adults, the poor performance of long-termcaptives cannot be attributed to them neverhaving developed normal foraging abilities in thewild. Whether snakes can re-learn thesebehaviors after release, how long it might take,and how their compromised foraging abilitymight affect survival after release, are unknown.However, our results do suggest that whentranslocated or reintroduced animals starve (e.g.,Jule et al. 2008), a detrimental effect of time incaptivity prior to translocation, independent of

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figure 4. Effect of time in captivity on the ability of a Ratsnake (Elaphe obsoleta) A) to successfully react to preyand B) latency to react to prey. Diamonds are long-term captive Ratsnakes and squares are the means for the 16 short-term captive Ratsnakes.

(per

cent

[%])

(s)

developmental or selection effects of captivity,could be a contributing factor.

In the wild, Ratsnakes are often activenocturnally during the warmer months of theyear (Weatherhead et al. 2012; Sperry et al.2013). Presumably Ratsnakes must be able toshift their foraging strategy from a reliance onvisual stimuli during diurnal foraging (Mullinand Cooper 1998) to chemical stimuli whenforaging in the dark. Unsurprisingly, short-termcaptive Ratsnakes reacted to prey at greater thanchance levels using visual, chemical, orcombined stimuli. In fact, short-term captivesmost quickly approached prey when onlychemical stimuli were present. In constrast,long-term captive Ratsnakes chose the baitedtube in only 26% of trials, fewer than thatexpected by chance (33%). No trend wasdetected in the latency of long-term captiveRatsnakes to approach prey based on stimulusbecause they were slow to approach preyregardless of the available stimulus. Long-termcaptive snakes appear to have lost some capacityto shift between prey stimuli relative to short-term captive snakes.

The ability and speed with which snakesreacted to prey may be an artifact of theirmotivation to feed. We attempted to control forthis by feeding each snake a dead mouse whencaptured (establishing their experience with theprey item) and then fasting each snake for aminimum of a week. We evaluated the bodycondition of each snake used in the trial, andalthough long-term captive snakes tended to bein better condition, the difference between thegroups was not significant and condition did nothave a significant effect on snake behavior in thetrials.

The rapid degradation in foraging behavior weobserved in Ratsnakes is clearly inconsistentwith the notion that reptile behaviors are “hard-wired,” although different behaviors may vary intheir plasticity. For example, flight initiationdistance of captive-bred and released iguanas inresponse to a predator threat did not differ fromthose of wild iguanas (Alberts et al. 2004).Additionally, Chiszar et al. (1993) found thatforaging behaviors such as strike-inducedchemosensory searching and tongue flickingresponse to blood by captive-born rattlesnakesand cobras were similar to those observed inwild conspecifics. The effect of captivity likelyvaries both among species and behaviors, butuntil evidence to the contrary is presented, the

prudent assumption should be that traits that mayaffect survival in the wild should not be regardedas hard-wired.

Conservation practitioners involved in snaketranslocation or reintroduction projects shouldconsider the potential effects of captivity onsurvival-related behaviors when designinganimal handling and release protocols and whenconducting post-release monitoring. Forexample, current head-starting projects for raresnakes such as the Eastern Indigo Snake(Drymarchon couperi) focus on the collection ofeggs from wild-caught gravid females held intemporary captivity as the source of animals forreintroduction efforts (Godwin et al., unpubl.report). Because permanent removal of adultswould likely negatively impact sourcepopulations and translocated adults might fail tosettle at the release site (Kingsbury and Attum2009), releasing captive-reared offspring hasobvious benefits over release of wild-caughtadults. Because our study indicates thattemporary (one year or more) captivity mightnegatively affect animals, however, protocolsthat minimize animals’ time in captivity mayhelp increase post-release survivorship.

In some translocation projects, such asheadstarting or repatriation, animals must bemaintained in captivity for extended periods oftime as individuals grow, permits are approved,or suitable habitat is acquired and restored.Environmental enrichment and soft release aremanagement tools that can potentially offset thedetrimental effects of captivity on post-releasebehavior. Enrichment entails increasing thecomplexity of captive housing to simulatenatural conditions. Although enrichment fallsshort of providing the full range of naturalstimuli and behavioral challenges encountered inthe wild, it can provide increased sensory, motor,and cognitive demands (Poole 1992; Dinse2004). Enrichment may enhance the ability ofanimals to perform ecologically relevant taskssuch as refuge seeking, foraging, andreproducing (e.g., Almli and Burghardt 2006;Nicholson et al. 2007) and has been shown toimprove survival of released individuals(Biggins et al. 1999). Soft release entails placingindividuals in outdoor enclosures at the releasesite prior to being released, allowing animals toexperience local environmental conditions anddevelop fidelity to a site (Kingsbury and Attum2009). Soft release often allows animals toexhibit natural behaviors such as foraging and

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refuge seeking and has proven effective for anumber of successful translocation projects (e.g.,Tuberville et al. 2005). Research is needed todetermine how these tools can be used toenhance the ability of snakes to re-establishnatural behaviors.

In addition to the implications for translocationprograms, our results provide a note of cautionfor research on the behavior of captive snakes.For example, many studies examining snakeforaging behavior use animals that have been incaptivity for extensive periods of time (e.g.,Saviola et al. 2012). When feasible, the behaviorof captive and wild study subjects should becompared (Shivik 1998). Otherwise, cautionshould be used when inferring that the behaviorof captive snakes reflects the behavior of thosesnakes in the wild.

Acknowledgments.—Funding for this projectwas provided by the Construction EngineeringResearch Laboratory of the Engineer ResearchDevelopment Center (ERDC). We thank TimHayden for assistance in arranging funding. Thiswork would not have been possible without thegenerosity and meticulous record-keeping ofSean Poppy and Angela Tucker in the SRELoutreach program. Eric Nordberg, Mary MackGray, Brian Metts, Ashley Smith, PatrickBarnhart, Patrick Roberts, Caitlin Kupar, andPhil Vogrinc assisted in snake capture andhusbandry. Partial support for manuscriptpreparation by TDT and use of animal facilitieswas made possible by Award Number DE-FC09-07SR22506 from Department of Energy to theUniversity of Georgia Research Foundation.Animals were collected under South CarolinaDepartment of Natural Resources permits # G-11-03 and 23-2012A. Animal proceduresconformed to permits approved by theUniversity of Illinois (IACUC #11054) andUniversity of Georgia (AUP #A2011 04-007-Y2-A0).

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BreTT degregorio is a Ph.D. student at the Universityof Illinois. His current research project has allowed himto merge his love of birds and snakes to investigatepredator-prey interactions between the two taxa.(Photographed by Jacob Hill).

paTriCk J. WeaTherhead is a Professor at the Universityof Illinois. He received his B.Sc. in Biology from CarletonUniversity (1974) and M.Sc. and Ph.D. in Biology fromQueen’s University (in 1976 and 1978, respectively). Hisresearch focuses primarily on the behavior and ecology ofsnakes and birds, with a particular interest in snake-birdinteractions. (Photographed by Kit Muma).

TraCey d. TuBerville is an Assistant Research Scientistat the University of Georgia’s (UGA) Savannah RiverEcology Laboratory, near Aiken, South Carolina. Shereceived her B.S. in Biology from Furman University(1993), M.S. in Conservation Ecology and SustainableDevelopment (1998) and Ph.D. (2008) from UGA. Herresearch interests are in applied conservation andmanagement of reptiles and amphibians, includingtranslocation and reintroduction as conservation tools.(Photographed by Kurt A. Buhlmann).

Jinelle h. sperry is an Adjunct Assistant Professor atthe University of Illinois and a Research Scientist at theUS Army’s Engineer and Research Development Centerin Champaign, Illinois. Her research has focused on thecore theme of community ecology and the effects ofhuman-caused disturbances to multi-species interactions.(Photographed by Christopher Taylor).