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Jul 10, 2014 - Lincoln Park Zoo (Chicago, IL), embarked on a renovation project for its Kovler Lion House, the opportunity was taken to perform a scientific ...
Zoo Biology 33: 267–274 (2014)

RESEARCH ARTICLE

Behavioral and Physiological Responses in Felids to Exhibit Construction Julia Chosy,* Megan Wilson, and Rachel Santymire Conservation and Science Department, Lincoln Park Zoo, Chicago, Illinois Despite the growing body of literature examining the welfare of zoo‐housed animals, little standardized work has been published on the effect of construction and environmental disruption on the physiology and behavior of affected animals. When Lincoln Park Zoo (Chicago, IL), embarked on a renovation project for its Kovler Lion House, the opportunity was taken to perform a scientific study of behavioral and physiological markers in the resident felids to determine the effect of construction and environmental disruption. Fecal samples and behavioral observations were collected on four felid species (five individuals) before, during, and after the period of construction. As a group, the average z‐score for fecal glucocorticoid metabolite concentration increased during construction relative to baseline. Levels remained elevated after construction, but trended toward baseline. All individuals demonstrated a significant decrease in the frequency of pacing and time spent visible during construction. Overall activity levels also showed a significant decrease relative to baseline measures. As zoological institutions continue to recognize the importance of habitat design, construction and renovation become inevitable. It is important to be aware of the potential consequences this can have on animals in the vicinity and to work toward minimizing negative effects. One recommendation is the availability of ample retreat and hiding space for felids during disruption to their environment. © 2014 Wiley Periodicals, Inc. Zoo Biol. 33:267–274, 2014.

Keywords: zoo animal welfare; fecal hormone metabolites; glucocorticoids; housing; behavior; felids

INTRODUCTION Zoo animal welfare is routinely assessed through behavioral observations, with the understanding that the behavior of wild animals of a similar species represents an ideal to which zoo animal behavior can be compared [Carlstead, 1996]. Specifically, practices aimed at maximizing zoo animal welfare often seek to increase species typical behaviors and overall activity levels, while at the same time reduce abnormal or undesirable behaviors [Markowitz and LaForse, 1987; Forthman et al., 1992]. These abnormal behaviors are often described as “stereotypic,” and are subsequently defined as being invariant, regularly repeated, and having no apparent goal or function [Mason, 1991a]. The presence of stereotypic behaviors in a zoo animal’s behavioral repertoire suggests that the animal’s well‐being may be compromised [Mason, 1991b]. Indeed, some stereotypic behaviors, such as self‐mutilation, have a direct negative impact on the animal’s physical well‐being. Stereotypic behaviors are affected by a variety of factors in the captive environment, including elements of the enclosure [Clarke et al., 1988; Cooper et al., 1996; Bashaw

© 2014 Wiley Periodicals, Inc.

et al., 2007], certain aspects of animal care routines [Rushen, 1985; Carlstead et al., 1991; Krishnamurthy, 1994; Bloomsmith and Lambeth, 1995; Friend, 1999; Bloomsmith et al., 2001; Wilson et al., 2004; Ross, 2006], and construction noise [Powell et al., 2006]. Changes in activity levels, including increases in locomotion and “restlessness,” are also Grant sponsor: Davee Centre for Epidemiology and Endocrinology at Lincoln Park Zoo. Julia Chosy’s current address: is WriteStats, 445 Kaiolu Street, #402, Honolulu, Hawaii 96815 Megan Wilson’s current address: is Zoo Atlanta, 800 Cherokee Avenue, SE, Atlanta, Georgia 30315  Correspondence to: Julia Chosy, Writestats, 445 Kaiolu Street #402, Honolulu, Hawaii 96815. E‐mail: [email protected]

Received 06 October 2013; Revised 09 May 2014; Accepted 15 May 2014

DOI: 10.1002/zoo.21142 Published online 10 July 2014 in Wiley Online Library (wileyonlinelibrary.com).

268 Chosy et al. associated with noise [Owen et al., 2004; Powell et al., 2006]. Carnivores appear particularly susceptible to the development of stereotypic behaviors [Clubb and Mason, 2006]. Specifically, felids have been shown to engage in self‐ mutilation [Wielebnowski et al., 2002], hiding [Carlstead et al., 1993; Wielebnowski et al., 2002; Gusset, 2005] and pacing [Markowitz and LaForse, 1987; Carlstead et al., 1993; Markowitz et al., 1995; Jenny and Schmid, 2002; Mallapur and Chellam, 2002; Bashaw et al., 2003; Gusset, 2005]. Assessing welfare using both behavioral and physiological measures, such as adrenocortical activity using fecal glucocorticoid metabolite analysis, is considered superior to using only behavioral measures [Wielebnowski et al., 2002], although their relationship to welfare and stress is not entirely clear. Some animals that exhibit high rates of stereotypic behavior also have high cortisol concentrations [Redbo, 1993; Schmid et al., 2001; Wielebnowski et al., 2002; Liu et al., 2006; Laws et al., 2007], yet others exhibit high rates of stereotypic behavior and have low cortisol concentrations [Bildsoe et al., 1991; Mason, 1991a]. Some studies have found inconsistent associations between these two measures [Carlstead et al., 1993; Gusset, 2005]. For felids, fecal glucocorticoid metabolite concentrations have been validated and have been shown to change based on features of the enclosures and management [Wielebnowski et al., 2002; Fanson and Wielebnowski, 2013]. For example, clouded leopards (Neofelis nebulosa) housed in enclosures with more vertical space have significantly lower fecal glucocorticoid metabolites; available space on the enclosure floor does not have the same effect. Additionally, some felids that are housed in close proximity to or in visual contact with other large predators have higher cortisol concentrations [Carlstead et al., 1993; Wielebnowski et al., 2002; Quirk et al., 2012]. As carnivores have been shown to have a propensity for developing stereotypic behaviors [Clubb and Mason, 2006] and reports have shown that construction noise can affect stereotypic behaviors [Powell et al., 2006], a standardized study was designed to examine the effect of construction and environmental disruption on the physiology and behavior of captive felids. When Lincoln Park Zoo, embarked on a renovation project for its Kovler Lion House, the opportunity was taken to perform a scientific study including fecal hormone metabolite monitoring and behavioral observation of four felid species (five individuals) housed in the building.

We hypothesized that the five individuals would experience an increase in fecal glucocorticoid metabolite concentrations, corresponding to changes in behavior during the construction period. Behaviorally, we expect the animals to exhibit increased pacing and decreased visibility and over‐ all activity levels during construction. As with fecal glucocorticoid metabolite concentrations, we believe these values will begin to return to baseline during the post‐ construction period. METHODS Animals Subjects for the study included five cats housed on the south side of the Kovler Lion House at Lincoln Park Zoo. These included one female black leopard (Panthera pardus), two female servals (Leptailurus serval), one male Afghan leopard (Panthera pardus saxicolor), and one female snow leopard (Uncia uncia). Each animal had its own exhibit with the exception of the servals, who were housed together. None of the individuals were housed in a breeding situation and, therefore, none were contracepted. All of the animals had been with Lincoln Park Zoo for many years and were accustomed to their enclosures. Construction Timeline and Details Data were collected over four different phases: baseline, construction, new habitats, and follow‐up (Fig. 1). Baseline data were recorded for six consecutive weeks in December 2006 and January 2007. During this time, the cats were in their usual exhibits. The construction phase lasted 24 weeks and began with shifting one of the cats (the snow leopard) to an indoor exhibit, followed by renovation of the outdoor facilities. This phase lasted from mid‐January 2007 to early July 2007. The majority of the construction was aimed at enlarging three outdoor enclosures on the south side of the building. Additionally, some concrete areas were replaced with natural planted areas and extra overhangs and ledges were added to existing artificial rockwork. Upon completion of the construction, the animals were shifted to their new exhibits and the third phase of data collection, “new habitats,” was initiated. Data were collected for 13 weeks after construction, from early July 2007 till the end of September 2007. During the final phase, follow‐up, only fecal samples were collected and only from three of the cats, the servals,

Phase I

Phase 2

Phase 3

Baseline

Construcon

New habitats

6 weeks

24 weeks

13 weeks

Phase 4 Follow-up 6 weeks

Fig. 1. The three phases of data collection and the additional follow‐up. “Baseline” was the time frame when normal values of fecal glucocorticoid metabolite concentrations and behavior were collected. “Construction” was when construction activity took place. The ‘new habitats’ phase was the time frame when individuals were placed into the newly designed habitats. The “follow‐up” time was after individuals were well established in their enclosures long after the construction phase.

Zoo Biology

Felid Response to Exhibit Construction

and the black leopard. This phase lasted 6 weeks, from December 2010 to January 2011. Fecal Collection and Analysis Fecal sample collection coincided with behavioral data collection for the first three phases of data collection. Daily samples were collected from the cats’ enclosures. For the servals, one was given 1=2 tablespoon of blue liquid food coloring (Gordon Food Services, Grand Rapids, MI) to identify individual samples. In total, 1,245 fecal samples (approximately 220–275 collected per individual) were analyzed. Samples were stored in plastic bags in a freezer at 20°C. Fecal samples were dried using a lyophilizer (ModulyoD‐115, Thermo Fisher Scientific, Inc., Waltham, MA) and steroids were extracted from feces using protocols previously validated for other felid species [Brown et al., 1994; Brown et al., 1996; Graham and Brown, 1996]. Briefly, dried samples are pulverized and approximately 0.2 g (0.02 g) of fecal powder is boiled in 5 ml of 90% ethanol: distilled water for 20 min. After centrifugation (500 g, 20 min), the supernatant is recovered and the fecal pellet is re‐suspended in 5 ml of 90% ethanol:distilled water, vortexed for 1 min, and re‐centrifuged (500g, 15 min). Both supernatants are combined, dried under air, and redissolved in 1 ml methanol. Extracted samples are sonicated for 20 min and diluted for analysis. The fecal samples for all individuals except the Afghan leopard were analyzed for cortisol using an enzyme immunoassay (EIA) (R4866; provided by C. Munro, Davis, CA). Cortisol polyclonal antiserum and horseradish peroxidase (HRP) ligands were used at a 1:8,500 and 1:20,000 dilution, respectively. Cross‐reactivity to the cortisol antiserum was cortisol, 100%, prednisolone, 9.9%; prednisone, 6.3%; cortisone, 5%; corticosterone, 0.7%; deoxycorticosterone, 0.3%; 21‐deoxycortisone, 0.5%; 11‐deoxycortisol, 0.2%; progesterone, 0.2%; 17a‐hydroxyprogesterone, 0.2%; pregnenolone, 17a‐hydroxypregnenolone, anderostenedione, testosterone, androsterone, dehydroepiandrosterone, dehydroisoandrosterone‐3‐sulfate, aldosterone, estradiol‐17b, estrone, estriol, spironolactone and cholesterol, 0.1% [Young et al., 2004]. The cortisol EIA was validated for the four individuals by demonstrating: (1) parallelism between binding inhibition curves of fecal extract dilutions (1:2–1:2,048), and (2) significant recovery (>90%) of exogenous cortisol added to fecal extracts. Assay sensitivity was 3.9 pg/well and intra‐ and

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inter‐assay coefficients of variation were