Behavioral and Physiologic Responses to Environmental Enrichment in the Maned Wolf (Chrysocyon brachyurus)

Transcription

1 Zoo Biology 0:1 13 (2007) RESEARCH ARTICLE Behviorl nd Physiologic Responses to Environmentl Enrichment in the Mned Wolf (Chrysocyon rchyurus) Dwn Cummings, Jnine L. Brown, Meliss D. Rodden, nd Nuchrin Songssen Conservtion nd Reserch Center, Smithsonin s Ntionl Zoologicl Prk, Front Royl, Virgini The ex situ popultion of mned wolves is not self-sustining due to poor reproduction, cused primrily y prentl incompetence. Studies hve shown tht environmentl enrichment cn promote nturl prentl ehviors in zoo nimls. The ojective of this study ws to determine the effects of environmentl enrichment on ehviorl nd physiologicl responses of mned wolves. During n 8-week experimentl period, dily ehvior oservtions nd fecl smple collection were conducted on four dult wolves (2.2) individully housed in environments without enrichment. After 2 weeks, the wolves were chronologiclly provided with 2-week intervls of hiding ded mice round the exhiit, no enrichment, nd introduction of oomer lls. Responses of the wolves to enrichment were ssessed sed on ctivity levels nd explortory rtes, s well s the level of corticoid metolites in fecl smples collected dily throughout the study period. Providing wolves with environmentl enrichment significntly incresed explortory ehviors (Po0.05), especilly when mice were hidden in the enclosure. Fecl corticoid concentrtions were incresed during periods of enrichment in mles (Po0.05), ut not in femles. Overll, there were no correltions etween ehviorl responses to enrichment nd fecl corticoid levels. Behviorl results suggest tht environmentl enrichment elicits positive effects on the ehvior of cptive mned wolves. There is evidence suggesting tht providing nimls with ility to forge for food is more effective enrichment strtegy thn introducing ojects. There is need for longer term study to determine the impct of environmentl enrichment in this species. Zoo Biol 0:1 13, c 2007 Wiley-Liss, Inc. Keywords: mned wolf; enrichment; ehvior response; corticoids D. Cumming s present ddress is Denver Zoo, 2300 Steel Street, Denver, CO Grnt sponsor: Sichel Endowment Fund. Correspondence to: Nuchrin Songssen, Conservtion nd Reserch Center, Smithsonin s Ntionl Zoologicl Prk, Front Royl, VA E-mil: songssenn@si.edu Received 15 Novemer 2005; Accepted 22 Mrch 2007 DOI /zoo Pulished online in Wiley InterScience ( r 2007 Wiley-Liss, Inc.

2 2 Cummings et l. INTRODUCTION The mned wolf (Chrysocyon rchyurus) is Neotropicl cnid tht lives in hitts eing severely compromised y griculturl development. Listed s ner thretened on the IUCN Red List [IUCN, 2004], the species is ntive to South Americn grsslnds nd found primrily in Brzil, lso rnging into res of Bolivi, Argentin, Prguy, Peru, nd possily Uruguy [Dietz, 1984; Rodden et l., 2004]. Despite its flgship sttus, the numer of mned wolves living in nture is unknown, nd wild popultions re incresingly t risk due to hitt loss to griculture [Dietz, 1984; Rodden et l., 2004]. A Popultion nd Hitt Viility Assessment held in Brzil in 2005 estimted there my e 20,000 wolves living in the wild; the vst mjority re in Brzil. Becuse wild popultions hve declined sustntilly, mintining selfsustining, vile cptive popultion is vitl. Mned wolves mintined in zoos hve three functions: 1) mssdors for the disppering grsslnds; 2) reserch resource; nd 3) hedge ginst ctstrophe ffecting the remining wild popultion. Although reeding of mned wolves in cptivity hs improved during the pst few yers (Rodden, unpulished), neontl mortlity remins high [Interntionl Studook, 2003], due to ndonment nd cnnilism of young [Mi nd Gouvei, 2002]. This my e cused y lck of pup rering experience nd inpproprite housing environments such s insufficient den sites [Wielenowski, 1998]. It hs een suggested tht prentl cre ehvior in zoo nimls cn e esily disrupted even t low levels of stress when other spects of reproduction re norml [Shepherdson et l., 1998; Wielenowski, 1998]. Providing cptive nimls with pproprite environmentl enrichment cn promote nturl prentl ehviors, which in turn enhnces reproductive success in cptive individuls [Shepherdson et l., 1998]. Overwhelming evidence exists to support the enefits of enrichment for reducing norml or stereotypic ehviors, prticulrly in cptive primtes nd crnivores [Shepherdson et l., 1998]. Enrichment hs een shown to increse ctivity levels nd norml explortory ehviors, while reducing norml pcing nd hiding in ers nd felids [Forthmn et l., 1992; Crlsted et l., 1993,; Shepherdson et l., 1993; Wielenowski et l., 2002,; Bshw et l., 2003]. Environmentl enrichment includes wide rnge of ctivities iming to enhnce the environment of cptive nimls. These ctivities cn e divided into two mjor ctegories iming to provide: 1) opportunities for explortion nd ply; or 2) control over the environment [Mrkowitz nd Ady, 1998; Mench, 1998; Shepherdson nd Crlsted, 2000]. Explortion is n importnt component of most species life strtegies [Mench, 1998]. Animls need to continuously explore the environment to sty wre of food nd wter sources, shelters, trils, predtors, hzrds, territory intruders, nd potentil mtes. Animls in cptivity re typiclly mintined in sttic environments nd hve limited opportunities to explore [Mench, 1998]. Novel ojects, scents, nd exhiit chnges re techniques used to stimulte explortory ehvior. However, these tctics cn ecome sttic themselves, only requiring few minutes to investigte in typiclly smll enclosures [Hre nd Worley, 1995; Mench, 1998]. Control or choice is the other mjor component missing in the lives of cptive nimls [Mrkowitz nd Ady, 1998; Shepherdson nd Crlsted, 2000]. Freeroming nimls mke choices dily out when nd where to forge, wht to et,

3 Environmentl Enrichment nd Mned Wolf 3 whom to interct with nd where to sleep. All of these choices re limited for nimls in the strictly controlled environments of cptivity. Studies hve suggested tht this lck of control leds to most stereotypic ehviors [Shepherdson et l., 1998; Mellen nd McPhee, 2001]. Control is given ck to cptive nimls y providing choices nd opportunities to work (e.g., multiple shelters nd puzzle feeders), thus providing empowerment for the niml. The complexity of this enrichment strtegy is limited only y humn cretivity, nd seems to offer the est opportunity to elicit nturl nd complex ehviorl repertoires [Mrkowitz nd Ady, 1998]. Formultion of effective environmentl enrichment strtegies is dependent on species, ge, sex, socil structure nd individul vritions [Mench, 1998]. The principl gol of this study ws to identify n pproprite environmentl enrichment regimen for cptive mned wolves. This study ws designed to determine whether: 1) enrichment cn improve the ehviorl repertoire of cptive mned wolves; 2) chnges in ehvior re reflected in fecl corticoid levels; nd 3) there re differences in ehviorl nd physiologic responses to empowerment nd explortion enrichment strtegies. In this study, improving the ehviorl repertoire is defined s n increse in nturl ehviors nd decrese in stereotypic ehviors or pthy. In this study, we compre two types of enrichment: 1) oomer lls were used, referred to s novel ojects [Poole, 1998] in ttempt to increse explortory opportunity; nd 2) food hiding ws used to provide wolves the opportunity to serch for food, referred to s empowerment [Mrkowitz nd Ady, 1998]. MATERIALS AND METHODS Animls Experimentl sujects were four dult mned wolves; two femles (Wolves L nd R) nd two mles (Wolves C nd Z) mintined t the Conservtion nd Reserch Center (CRC) in Front Royl, Virgini. All wolves were orn nd rised in cptivity; Wolves R nd Z were hnd-rised, wheres Wolves C nd L were prentrered. Ech wolf ws housed lone, ut in similr enclosures. Enclosures consisted of lrge fenced in yrd (10 30 m) nd n outdoor den with ccess to heted uilding (3 5 m). The CRC is not open to the pulic; thus, wolves were not exposed to visitors. Three of four wolves (1.2) hd successfully produced nd rised t lest one litter. All four wolves were fed the sme diet of dog chow, fruit nd mice, nd were cred for y the sme primry keeper. This study ws conducted from Ferury April, the non-reeding seson for this species. All procedures were reviewed nd pproved y the CRC Institutionl Animl Cre nd Use Committee. Experimentl Design The experimentl schedule ws s follows: ehviorl oservtions were conducted nd fecl smples collected dily for: 1) 2 weeks of no enrichment; 2) 2 weeks of hiding mice enrichment; 3) 2 weeks of no enrichment; nd 4) 2 weeks of oomer lls enrichment. The first 2-week period of no enrichment served s seline control. The second period with no enrichment ws intended to void interctions etween the two enrichment periods. The hiding mice enrichment consisted of the primry keeper hiding vried numer of ded mice, which re preferred food items of mned wolves, round the

4 4 Cummings et l. enclosure ech dy in different loctions, providing unpredictility. The wolves were ccustomed to their primry keeper, nd thus were not distrcted y humn odor. Other food items (i.e., dog chow nd fruit) lso were provided to the nimls t the sme time; thus, the wolves hve choices etween serching for mice or eting offered food. Boomer lls of vrious sizes nd shpes ( totl of 5 lls were used) were lso plced in the enclosure y the primry keeper. All wolves hd een living t CRC for t lest 4 yers, nd hd never een exposed to lls of ny kind during this time. A different sized nd shped ll ws plced in n enclosure ech dy, lwys in different loction nd removed t the end of ech oservtion period. After ech session, the lls were wshed with mild detergent to remove niml scent. Cre ws tken to ensure tht exposure to the sme sized (or shped) ll ws not repeted on 2 consecutive dys for the sme individul, nd tht ech wolf ws exposed to ech ll the sme numer of times. All enrichment items were plced in the enclosures t the sme time ech dy (i.e., in the morning fter feeding). Behvior Oservtions Quntittive ehviorl dt were collected dily on ech wolf in 30-min oservtion sessions in the morning fter feeding, y the sme oserver using the focl smpling method [Mrtin nd Bteson, 1986]. Behviors of interest were predetermined nd divided into two mjor ctegories: ctivity levels nd explortory chrcteristics. Activity levels were determined y recording the ehviorl stte every 30 sec. When the wolves were sitting, lying down or sleeping, the ctivity level ws recorded s inctive. When the wolves were grooming, sniff, stnding, wlking, pcing, or scent mrking, the ctivity level ws recorded s ctive. Explortory ehvior levels were determined y recording ll events determined to est represent nturl nd desired ehviors (sniff oject or ground, pw or dig t ground nd scent mrk). According to Rodden et l. [1996], scent mrking ehvior includes repetedly ruing of the cheek or neck on the surfce of the oject, urinting or defecting; however, in the present study, only urintion ws counted s scent mrking ehvior. Dily ctivity rtes were clculted y dividing times tht wolves were ctive y the totl oservtion period (i.e., 30 min). Explortory rtes were clculted y dividing the totl numer of ehviorl events y the totl oservtion period. Anlysis of Fecl Corticoid Metolites Fecl smples from ech wolf were otined dily throughout the experimentl period. The smples were plced in Ziploc gs nd leled with the suject s nme nd dte of collection. Smples were stored t 201C until processing nd nlysis. Fecl smples were collected in the morning nd were ssumed to hve een deposited the previous dy. An ACTH chllenge conducted on the gry wolf (Cnis lupus) showed hr lg time for pek glucocorticoid concentrtions in fecl mteril [Snds nd Creel, 2004]. A study in which rdioleled testosterone ws infused into mned wolf showed tht ll isotope excretion occurred within 16 hr [Velloso, 1996]. However, it hs een shown tht excretion rte of steroid hormones vries gretly mong individuls within the sme species s well s mong species [Plme et l., 1996]. Therefore, fecl corticoid level for given dy ws correlted with 2-dy verge of ehvior dt oserved efore the dy of fecl collections.

5 Environmentl Enrichment nd Mned Wolf 5 Smples were dried in lyophilizer, then 0.2 g of fecl powder ws oiled for 20 min in 90% ethnol nd 10% distilled wter followed y centrifugtion t 500 g for 20 min. The first superntnt ws recovered nd the pellet re-dissolved in 5 ml of 90% ethnol nd centrifuged t 500 g for 15 min. The second superntnt ws recovered nd comined with first one; oth were dried down under ir nd redissolved in 1 ml of methnol (100%). Averge fecl extrction efficiency ws 87% with coefficient of vrition o10%. Corticoid metolites were quntified y enzyme immunossy (EIA) [Munro et l., 1991] using n nti-cortisol ntiserum (R4866; 1:85,000 dilutions) otined from Corlie Munro (University of Cliforni, Dvis, CA). Before nlysis, fecl extrcts were diluted in phosphte uffered sline (1:500). Seril dilutions of pooled fecl extrcts produced displcement curves prllel to those of the cortisol stndrd curve. Inter- nd intr-ssy vritions were o10%. Assy sensitivity ws 3.9 pg/well. Sttisticl Anlysis Becuse of the smll niml numer (n 5 4) nd highly vrile responses cross wolves, dt nlysis nd interprettion were done seprtely for ech individul. Dily ctivity nd explortory rtes were clculted for ech wolf during ech period of 1) no enrichment; 2) empowerment (i.e., hiding mice); nd 3) novel oject (i.e., oomer lls) nd nlyzed for differences using Wilcoxon tests. Fecl corticoid concentrtions re reported s men7stndrd error (SEM). Overll, seline, pek corticoid concentrtion, nd coefficient of vrition (CV) for ech enrichment period for ech individul were clculted. Bseline vlues were clculted y n itertive process, wherey high vlues exceeding the men11.5 stndrd devition (SD) were excluded. The verge ws then reclculted, nd the elimintion process repeted until no vlues exceeded the men11.5 SD. A pek verge included only vlues 41.5 SD. Before further nlysis, ll dt were trnsformed using the common logrithm, log 10, to djust for skewed, non-norml distriution, nd then tested for normlity using Sigm Stt 3.0 (SPSS Inc., Chicgo, IL). Comprisons of men fecl corticoid concentrtions mong tretments within the sme individul were conducted using nlysis of vrince followed y Duncn s multiple rnge tests. Spermn-rnk correltion nlyses were conducted to determine the correltion etween ctivity/explore rtes nd fecl corticoid metolites. Differences were considered significnt t Po0.05. RESULTS Behviorl Response to Environment Enrichment Figure 1 shows ctivity nd explortory rtes of four mned wolves fter one of two types of enrichment or no enrichment. In ll wolves, there were no significnt differences in ehviorl responses etween the two no enrichment periods (P40.05); thus, dt were comined nd compred to those of hiding mice nd oomer lls periods. Behviorl responses to enrichment seemed to differ mong wolves. There were no differences in ctivity rtes of Wolf L mong tretments (Fig. 1A), lthough explortory rte significntly incresed when enrichment ws

6 6 Cummings et l. A Activity rtes Hiding mice Boomer lls C Z L R B 3 Hiding mice c Explortory rte (events/minute) Boomer lls c c C Z L R Fig. 1. Activity (A) nd explortory (B) rtes of four mned wolves (C, Z, L, nd R) without enrichment or when enrichment ws provided y hiding mice or introducing oomer lls. Different letters within the sme wolf indicte significnt differences (Po0.05). provided (Po0.05, Fig. 1B). For the remining wolves, providing them with enrichment, especilly hiding mice resulted in overll positive ehviorl chnges (i.e., incresed ctivity or explortory rtes, Po0.05) (Fig. 1A,B). Explortory rtes during the period when mice were hidden round the enclosure were significntly higher thn when oomer lls were introduced (Po0.05). Interestingly, only mle wolves, especilly Wolf Z, significntly responded to the oomer lls. A significnt increse in the rte of scent mrking ws oserved in Wolf Z when ll ws provided (Po0.01, Fig. 2).

7 Environmentl Enrichment nd Mned Wolf 7 Scent mrking rte (events/minute) No Enrichment Hiding mice Boomer lls Tretments Fig. 2. Rte of scent mrking when Wolf Z ws provided with no enrichment, hiding mice, or oomer lls. Physiologic Response to Environmentl Enrichment Figure 3 shows profiles of fecl corticoid metolites of the four wolves for the entire study. Inter-individul vrition nd ptterns were high in overll men fecl corticoid concentrtions, regrdless of the sence or presence nd types of enrichment (Fig. 3, Tle 1). Enrichment significntly ffected pek nd seline levels of fecl corticoids in mles (Po0.05), ut not in femles (Tle 1). Overll, seline, nd pek levels of fecl corticoids were higher during hiding mice enrichment thn during introduction of oomer lls (Po0.01). There ws no correltion etween ehviorl responses nd corticoid concentrtions for ny of the wolves evluted. DISCUSSION This is the first study to quntittively exmine ehviorl nd physiologic responses of cptive mned wolves to environmentl enrichment. The enrichment pproches exmined were introduction of oomer lls nd hiding mice in the enclosure. It ws found tht: 1) there re individul nd gender vritions in ehviorl nd physiologic responses to different types of enrichment; 2) hiding mice in the enclosure ws more effective t promoting positive ehviors thn oomer lls; nd 3) providing wolves with enriched environments promoted explortory ehvior. Assocition of Zoos nd Aquriums nd Behvior Scientific Advisory Group defines environmentl enrichment s process (chnges in structure or husndry prctices) for improving or enhncing zoo niml s environment within the context of their ehviorl iology nd nturl history [Dley nd Linsey, 2002]. The gol of this dynmic process is to increse ehviorl choices ville to nimls nd to drw out species pproprite ehviors nd ilities [Dley nd Linsey, 2000]. However, types of environmentl enrichment re sometimes chosen more for their

8 8 Cummings et l Fecl corticoid metolites (ng/g feces) Wolf Z Wolf C Fecl corticoid metolites (ng/g feces) Wolf L Wolf R Fig. 3. Fecl corticoid metolites of mles (A) nd femles (B) mned wolves during the entire study period (i.e. 8 weeks). durility, sfety, vilility, nd cost thn other properties tht my e of greter enefit to the nimls [Kreger et l., 1998]. A survey conducted in 1999 showed tht most North Americn zoos holding mned wolves provided vriety of enrichment items. Fruit nd mice were the two food items most frequently provided to wolves for enrichment, wheres tree trunks nd long grsses were the most common furniture in mned wolf enclosures [Dley nd Lindsey, 2000]. Although most institutions tht responded to the survey indicted tht wolves showed some level of interest in the enrichment items provided, quntittive responses were not mesured. In this study, providing enrichment to individully housed mned wolves incresed oth ctivity nd explortory rtes. Explortory rtes seemed to e the

9 Environmentl Enrichment nd Mned Wolf 9 TABLE 1. Men (7SEM) fecl corticoid concentrtions of four mned wolves during enrichment nd non-enrichment periods Wolf Gender Fecl corticoids (mg/ml) No enrichment Boomer lls Hiding mice P-vlue C Mle Overll Bseline Pek c o0.001 CV (%) Z Mle Overll o0.001 Bseline Pek o0.001 CV (%) L Femle Overll Bseline Pek CV (%) R Femle Overll Bseline Pek CV (%) CV, coefficient of vrince.,,c Different superscripts within the sme row indicte significnt differences. etter indictor of enrichment method effectiveness in this species. It hs een shown in other species tht incresed explortory ehvior is response of nimls to environmentl enrichment [Shepherdson et l., 1993; Crlsted nd Shepherdson, 1994; Mench, 1998]. Mny reserchers consider n incresed ctivity level s desirle for cptive nimls. However, the results of two studies on cptive wolves (Cnis lupus ileyi nd Cnis lupus lupus) re prticulrly noteworthy. Bernl nd Pckrd [1997] compred wolves living in non-enriched vs. nturlistic enclosures. They found tht wolves living in the non-enriched environments hd higher ctivity nd ggression levels. Frezrd nd Le Ppe [2003] found tht wolf pcks living in lrger, more nturlistic enclosures used less ville spce nd spent more time resting. It is common knowledge tht wolves in the wild spend mjority of their time resting, conserving energy until the next mel. Perhps in cptivity, wolf tht spends more time resting nd is less ctive is wolf ehving more nturlly. In this cse ctivity level my therefore not provide the est indictor for incresed welfre (or well-eing, nd lower levels of stress). It would seem tht incresing the overll ehviorl repertoire my e etter index of welfre sttus in cptive wolves thn ny single ehvior. Inter-individul vritions in ehviorl responses to environmentl enrichment were consistent with those previously reported in other species [Kreger et l., 1998]. These vritions re likely to due to individul gender differences nd the conditions under which nimls were rered (e.g., wild-cught vs. cptive orn or hnd rered vs. prent-rered). In the present study, hiding mice elicited ehviorl response in oth mles nd femles. However, only mle wolves responded to the oomer lls. A significnt increse in the rte of scent mrking ws oserved in Mle Z when oomer lls were provided (Fig. 2); such ehvior ws not oserved in the other wolves. It is worth noting tht Mle Z hd een housed lone for most of his dult

10 10 Cummings et l. life, unlike others in the study, which hve een pired for the mjority of their dult life. This my explin his unique response to ojects. Inter-individul vrition in fecl corticoid concentrtions ws high nd my in prt reflect the inherent individul vriility in response to environmentl enrichment. Scent mrking ehvior of Mle Z ws ssocited with temporry increse in rousl, which my e eneficil or could hve resulted from fer. An nlysis of fecl corticoids during this enrichment period showed concentrtions tht were significntly lower thn those during the no enrichment nd hiding mice intervls. This suggests introducing oomer lls to this prticulr wolf my hve een eneficil. When enrichment strtegies were compred, hiding mice seemed to result in more positive responses thn introducing oomer lls with respect to incresing ehviorl repertoire. This is not surprising, s severl studies hve shown tht nimls prefer to work for their food rther thn e fed d li [Inglis nd Fergusson, 1986; Kreger et l., 1998; Shepherdson et l., 1993; Shepherdson, 1998, Mellen nd McPhee, 2001]. Although ojects plced in n niml s enclosure presented the opportunity to explore, the result ws short-lived. Animls in the wild my spend n entire dy or night exploring home rnges for ny chnges. However, in cptivity the niml s home re is comprtively smll nd sttic. It only tkes few minutes to inspect single oject plced in the enclosure. As shown y oservtions in this study, the rte of explortory ehviors ws low for the oomer lls. Three of the four wolves inspected the oject for o5 min, nd then ignored it for the rest of the oservtion period. By contrst, when mice were hidden round the enclosure, the rte of explortory ehviors incresed. Most interesting ws tht serching nd forging ehviors often continued for severl minutes fter ll the mice hd een locted nd consumed. Thus, the ehviorl repertoire of nturl ehviors ws incresed. The strongest evidence to support tht hiding mice is more effective thn oomer lls is tht ll four wolves in this study hd significntly higher rtes of explortory ehvior with the hidden mice thn with the lls. Shepherdson et l. [1993] showed tht minimizing predictility of food vilility in smll felids ws n effective enrichment technique s it reduced stereotyped pcing nd incresed ehvior diversity. It is the lck of opportunity to explore tht my led to stereotypic ehviors. It mkes sense tht hving nimls serch for food gives them something to do, nd engges them more thoroughly thn simply plcing novel ojects in their spce. Studies in felids hve shown tht enrichment cn decrese corticoid excretion rtes, nd potentilly stress levels [Crlsted et l., 1993,; Wielenowski et l., 2002,]. In the present study, there were lrge vritions mong individuls in physiologicl responses to enrichment; however, in generl, hiding mice round the enclosure incresed drenl responses. It hs een suggested tht otining prey is good stressor tht stimultes the hypothlmic-pituitry drenocorticl xis [Moerg, 2000]. This my explin the increse in corticoid levels during the hiding mice enrichment period. Yet, the rise in corticoid levels could lso suggest negtive effect of this type of enrichment. Although it seems nimls were given choice to serch for food, it is uncler if such explortion is positive or negtive stressor. A long-term evlution to determine whether hiding mice elicits eneficil elevtions in corticoid production is needed to identify how nimls re ffected y this enrichment method. It hs een shown in leoprd cts tht there is n inverse correltion etween urinry corticoid levels nd explortory ehvior [Crlsted et l., 1993]. However,

11 Environmentl Enrichment nd Mned Wolf 11 we did not find ny correltions etween fecl corticoid concentrtions nd explortory ehvior of ny of the four mned wolves studied. This finding is consistent with tht reported in the cheeth [Wielenowski et l., 2002] where fecl corticoid ptterns were unrelted to ehvior. The lck of greement etween these two studies my e due to species-specific vritions (smll vs. lrge cts) in responses to husndry conditions. It is worth noting tht erlier studies focused on the influence of husndry conditions on ehvior nd drenl ctivity, wheres the present study imed to determine the impct of enrichment items on these responses. Thus, results otined for the mned wolf my not e directly compred to those conducted in leoprd cts nd cheeths. It should e noted tht ech enrichment type ws given to wolves for only 2 weeks, which would e insufficient to determine long-term effects. Wielenowski et l. [2002] studied drenl ctivity of cheeths sujected to socil stress for 6 months. In tht study, pprent chnges in concentrtion of fecl corticoid were not oserved until nimls were housed s housed lone or pired for t lest 2 months. Therefore, further investigtions tht include longer period of enrichment re needed. Interesting oservtions regrding ehvior responses nd corticoid levels were recorded in femle Wolf R. This individul ws hnd-rered nd ws the only wolf to disply stereotypic pcing. Behviorl responses of this individul to enrichment were not mrkedly different from the other three sujects, ut ssessment of fecl corticoid metolites showed no physiologic response to enrichment. Corticoid concentrtions remined stle nd were consistently lower thn those for the other wolves evluted during the study period. There re two possile explntions for the lck of corticoid response. It hs een shown in domestic species tht chronic stress cn result in shutdown of drenl ctivity [Jmes, 1979]. Given her tendency to pce, Wolf R my hve experienced stress-relted suppression in norml corticoid production. Further studies using ACTH chllenges my e necessry to determine whether this individul suffers from chronic stress. Another explntion is tht the ct of pcing my e self-soothing ctivity. It hs een resonly rgued tht there is little evidence tht pcing is hrmful to n niml [Moerg, 1987; Mson, 1991]. In ddition, pcing hs een correlted with lower corticosteroid levels nd drenl glnd weights [Mson, 1991]. It hs een suggested recently tht some stereotypic ehviors my ctully improve welfre in poor environments [Mson nd Lthm, 2004]. Becuse stereotypic ehviors cn rise from either poor or good conditions, nd non-stereotyping individuls cn hve poor welfre, this pttern of ehvior should not e used s sole index of well eing [Mson nd Lthm, 2004]. CONCLUSIONS Bsed on the ehvior dt, we showed tht environmentl enrichment elicits positive effects on cptive mned wolves. The results of this study provide evidence tht hiding mice my e more effective enrichment devise thn providing wolves with oomer lls. Hiding mice incresed drenl ctivity significntly; however, further studies re needed to exmine the nture of the reltionship etween corticoid production nd enrichment in mned wolves. Behviorl oservtions were confined to 30-min period dily for 2 weeks, only long enough to ssess short-term

12 12 Cummings et l. effects. Further studies involving multiple sessions of ehviorl oservtion with longer durtion of enrichment will e required to determine the long-term impct of enrichment on overll dily ctivity. Detiled study lso is required to determine whether providing wolves with environmentl enrichment would enhnce reproductive success in this species. ACKNOWLEDGMENTS The uthors thnk J. McLughlin for ssistnce in conducting this study. The uthors lso thnk E. Freemn for her invlule dvice in dt interprettion. REFERENCES Bshw MJ, Bloomsmith MA, Mrr MJ, Mple TL To hunt or not to hunt? A feeding enrichment experiment with cptive lrge felids. Zoo Biol 22: Bernl JF, Pckrd JM Differences in winter ctivity, courtship, nd socil ehvior of two cptive fmily groups of Mexicn wolves (Cnis lupus ileyi). Zoo Biol 16: Crlsted K, Brown JL, Strwn W Behviorl nd physiologicl correltes of stress in lortory cts. Appl Anim Behv Sci 38: Crlsted K, Brown JL, Seidensticker J Behviorl nd drenocorticol responses to environmentl chnges in leoprd cts (Felis englensis). Zoo Biol 12: Crlsted K, Shepherdson D Effects of environmentl enrichment on reproduction. Zoo Biol 13: Dley B, Lindsey SL A survey of mned wolf enrichment prctices in North Americn zoos. Proc Am Zoo Aqur Regionl Conf. p Dietz JM Ecology nd socil orgniztion of the mned wolf (Chrysocyon rchyurus). Wshington DC: Smithsonin Institution Press. Dietz JM Chrysocyon rchyurus. Mmm Species 231:1 4. Frezrd A, Le Ppe G Contriution to the welfre of cptive wolves (Cnis lupus lupus): ehviorl comprison of six wolf pcks. Zoo Biol 22: Forthmn DL, Elder SD, Bkemn R, Kurkowski TW, Nole CC, Winslow SW Effects of feeding enrichment on ehvior of three species of cptive ers. Zoo Biol 11: Hre VJ, Worley KE The shpe of enrichment: the first genertion. Proc Am Zoo Aqur Annu Conf. p Hilserg S Interntionl Mned Wolf Studook Chrysocyon rchyurus. Frnkfurt: Zoologischer Grten Frnkfurt m Min 26p. Inglis IR, Fergusson NJK Strlings serch for food rther thn et freely ville, identicl food. Anim Behv 34: Interntionl Union for Conservtion of Nture nd Nturl Resource IUCN Red List of Thretened Species. Aville t: redlist.org. Jmes VHT The drenl glnd. In: Comprehensive endocrinology. New York: Rven Press. Kreger MD, Hutchins M, Fscione N Context, ethics nd environmentl enrichment in zoos nd quriums. In: Shepherdson DJ, Mellen JD, Hutchins M, editors. Second nture: environmentl enrichment for cptive nimls. Wshington DC: Smithsonin Institution Press. p Mi OB, Gouvei AM Birth nd mortlity of mned wolves (Chrysocyon rchyurus) in cptivity. Brz J Biol 62: Mrkowitz H, Ady C Power for cptive nimls: contingencies nd nture. In: Shepherdson DJ, Mellen JD, Hutchins M, editors. Second nture: environmentl enrichment for cptive nimls. Wshington DC: Smithsonin Institution. p Mrtin P, Bteson P Mesuring ehvior: n introductory guide. Cmridge: Cmridge Press. Mson GJ Stereotypics: criticl review. Anim Behv 41: Mson GJ, Lthm NR Cn t stop, won t stop: is stereotypy relile niml welfre indictor? Anim Welf 13(Suppl): Mellen J, McPhee MS Philosophy of environmentl enrichment: pst, present nd future. Zoo Biol 20: Mench JA Environmentl enrichment nd the importnce of explortory ehvior. In: Shepherdson DJ, Mellen JD, Hutchins M, editors. Second nture: environmentl enrichment for cptive nimls. Wshington DC: Smithsonin Institution. p Moerg GP Prolems in defining stress nd distress in nimls. J Am Vet Med Assoc 191: Moerg GP Biologicl response to stress: implictions for niml welfre. In: Moerg GP, Mench JA, editors. The iology of niml stress. New York: CABI Pulishing. p Munro CJ, Stenfeldt GH, Crgun JR, Addiego LA, Overstreet JW, Lsley BL

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