Environmental enrichment of brown capuchins (Cebus apella): Behavioral and plasma and fecal cortisol measures of effectiveness

Boinski, Sue; Swing, Sonya P.; Gross, Timothy S.; Davis, J. K.

doi:10.1002/(sici)1098-2345(1999)48:1<49::aid-ajp4>3.0.co;2-6

Cited by 83 publications

(65 citation statements)

References 65 publications

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“…Indeed, there was a stronger correlation between serum and fecal cortisol measures than between corticosterone measures, which suggests that there are more cortisol metabolites in S. beldingi feces than there are corticosterone metabolites (although such a conclusion would have to be verified with high-performance liquid chromatography [HPLC] studies). Once it is determined that fecal hormone levels reliably reflect serum hormone levels (Graham and Brown 1996;Palme and Mostl 1997;Whitten et al 1998;Boinski et al 1999;Cavigelli 1999;this study), then non-invasive fecal monitoring can be used to compare basal levels across populations (which may differ in predation pressure, social stability, or food availability) or between environments (e.g., free-living vs. captive animals, breeding vs. overwintering sites).…”

Section: Discussionmentioning

confidence: 99%

“…Our next goal was to determine whether these fecal measures accurately reflect circulating glucocorticoid concentrations (as they do in some birds, carnivores, ungulates, and primates; Graham and Brown 1996;Palme and Mostl 1997;Wasser et al 1997;Boinski et al 1999;Cavigelli 1999). This step was important to confirm that our extraction methods detected fecal metabolites functionally related to circulating glucocorticoids.…”

Section: Study 2: Relationship Between Basal Concentrations Of Serum mentioning

confidence: 99%

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A Validation of Extraction Methods for Noninvasive Sampling of Glucocorticoids in Free‐Living Ground Squirrels

Mateo

Cavigelli

2005

Physiological and Biochemical Zoology

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Fecal hormone assays provide a powerful tool for noninvasive monitoring of endocrine status in wild animals. In this study we validated a protocol for extracting and measuring glucocorticoids in freeliving and captive Belding's ground squirrels (Spermophilus beldingi). We first compared two commonly used extraction protocols to determine which performed better with commercially available antibodies. We next verified the preferred extraction method by correlating circulating and fecal glucocorticoid measures from a group of individuals over time. For this comparison, we used both a cortisol and a corticosterone antibody to determine which had greater affinity to the fecal metabolites. Cortisol was the primary circulating glucocorticoid, but both hormones were present in well above detectable concentrations in the blood, which does not occur in other sciurids. In addition, the cortisol antibody showed greater binding with the fecal extracts than did the corticosterone antibody. Finally, we used adrenocorticotropic hormone and dexamethasone challenges to demonstrate that changes in adrenal functioning are reflected in changing fecal corticoid levels. These results suggest that our extraction protocol provides a fast, reliable assay of stress hormones in freeliving ground squirrels without the confounding influence of short-term rises in glucocorticoid concentrations caused by handling and restraint stress and that it can facilitate ecological and evolutionary studies of stress in wild species.

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Section: Discussionmentioning

confidence: 99%

Section: Study 2: Relationship Between Basal Concentrations Of Serum mentioning

confidence: 99%

A Validation of Extraction Methods for Noninvasive Sampling of Glucocorticoids in Free‐Living Ground Squirrels

Mateo

Cavigelli

2005

Physiological and Biochemical Zoology

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“…In many cases, however, these types of investigations require the detection of subtle differences in hormone concentrations among individuals and through time. When gross patterns are examined, fecal steroid profiles often appear ''noisy,'' with high variation around mean values, in comparison to urine or serum profiles (Boinski et al, 1999;Heistermann et al, 1996;Shideler et al, 1994;Ziegler et al, 1996). Therefore, when more subtle patterns are the target of interest, minimizing this noise is essential in order to detect real biological differences with strong resolution.…”

Section: Endocrinologymentioning

confidence: 99%

“…These initial applications continue for an increasing number of mammalian taxa (e.g., carnivores: Wasser et al, 1995;proboscids: Wasser et al, 1996;primates: Campbell et al, 2001;Heistermann et al, 2001;Jurke et al, 1997;Strier and Ziegler, 1994;Ziegler et al, 2000;ungulates: Garnier et al, 1998;M€ o ostl et al, 1999), and as fecal steroid analysis has become a more widely appreciated field technique, applications have expanded to consider steroid concentrations in relation to reproductive seasonality (Brockman et al, 2001;Cavigelli, 1999;Lynch et al, 2002;Strier et al, 1999;Ziegler et al, 2000), stress (Boinski et al, 1999;Creel et al, 1996;Dehnhard et al, 2001;Goymann et al, 1999), ontogeny (Strier and Ziegler, 2000), rank (Kraus General and Comparative Endocrinology 132 (2003) [264][265][266][267][268][269][270][271] www.elsevier.com/locate/ygcen GENERAL AND COMPARATIVE et al, 1999), and mating and aggression in males Lynch et al, 2002;Ostner et al, 2002). In these contexts, glucocorticoids and androgens have joined female reproductive hormones as markers of interest for fecal steroid analysis.…”

Section: Introductionmentioning

confidence: 99%

Concentrations of four fecal steroids in wild baboons: short-term storage conditions and consequences for data interpretation

Lynch

Khan

Altmann

et al. 2003

General and Comparative Endocrinology

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One source of both bias and ''noise'' in fecal steroid analysis is temporal change in steroid concentrations resulting from duration or conditions of fecal sample storage. However, no consensus currently exists regarding correct procedures or precautions necessary for fecal sample storage, and conditions vary widely within field endocrinology literature. This study considered the effects of shortterm, weeks-long, storage conditions on quantifiable fecal testosterone (fT), glucocorticoids (fGC), estrogens (fE), and progestagen (fP) metabolite concentrations in wild baboons (Papio cynocephalus). Quadruplicate subsamples of fecal samples (n ¼ 29) collected at Amboseli National Park and its environs were subjected to four different storage conditions prior to lyophilization, in order to determine the effects of storage on subsequent steroid concentrations, as assessed by 125 I radioimmunoassays. As expected, the best alternative to the ''initial condition'' of lyophilization at three days after collection was to freeze fecal samples at )20°C for two weeks prior to lyophilization. This storage method resulted in no significant change from initial steroid concentrations for fE, fT, or fP, although fGC showed a slight but significant decline. Storage for two weeks in a charcoal refrigerator caused a mean increase in all four steroid concentrations. However, the results from this storage condition were robust in terms of practical questions asked of the data: fE and fP values still reflected pregnant versus non-pregnant states in baboon females; a fGC profile constructed by age class resembled that created from the samples from the initial condition, although slightly inflated across age classes; and there were only moderate changes in relative fT concentrations across adult males. Knowledge of the effects of storage upon each steroid analyzed within oneÕs study is a necessary component in determining the optimal compromise for storage protocol in a particular research project.

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“…Various methods exist for improving housing conditions of zoo animals to minimize potential stress. Environmental enrichment, such as adding soil and vegetation or providing animals with special feeding devices, toys, and other novel objects, have become common practice in most zoos (Swaisgood and Sheperdson 2005;Vasconcellos et al 2009) and have been shown to reduce stress hormone (glucocorticoid) output (Boinski et al 1999;Buijs et al 2011;Moreira et al 2007;Pirovino et al 2011). Moreover, many modern keeping facilities provide hiding places that allow animals to withdraw from the sight of conspecifics, visitors, or keepers.…”

Section: Introductionmentioning

confidence: 99%

The Effect of Fission–Fusion Zoo Housing on Hormonal and Behavioral Indicators of Stress in Bornean Orangutans (Pongo pygmaeus)

2014

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The welfare of captive animals could be improved if zoos were to place more emphasis on their species-specific needs. In the wild, orangutans live in a fission-fusion social system and have a semisolitary lifestyle. However, most zoos keep orangutans in permanent groups, which may be stressful for them. Apenheul Primate Park in Apeldoorn, Netherlands, houses 14 Bornean orangutans in a simulated fissionfusion social system. To assess how this housing system affects indicators of stress, we measured fecal glucocorticoid metabolites (fGCM) and determined proportions of self-directed behavior (scratching and autogrooming). We compared fGCM concentrations of the Apenheul animals to those of zoo orangutans kept in permanent groups. In addition, we tested the effect of group size, visitor number, sex, age, and change of group composition on fGCM concentrations and proportions of self-directed behavior in the Apenheul orangutans. In contrast to Bornean orangutans housed in permanent groups, we did not find a group size effect on fGCM or on self-directed behavior in Apenheul's fission-fusion housing system. In addition, fGCM concentrations in Apenheul orangutans increased significantly with visitor numbers. Visitor number also affected proportions of self-directed behavior, and mean proportions of scratching were positively correlated with mean values of fGCM concentrations. Although these results suggest that the fission-fusion housing system in Apenheul reduces the group size effect leading to social stress in Bornean orangutans, they also show that visitors are an important factor that needs to be mitigated if the well-being of captive primates and other zoo animals is to be improved. Abstract The welfare of captive animals could be improved if zoos were to place more emphasis on their species-specific needs. In the wild, orangutans live in a fission-fusion social system and have a semisolitary lifestyle. However, most zoos keep orangutans in permanent groups, which may be stressful for them. Apenheul Primate Park in Apeldoorn, Netherlands, houses 14 Bornean orangutans in a simulated fission-fusion social system. To assess how this housing system affects indicators of stress, we measured fecal glucocorticoid metabolites (fGCM) and determined proportions of self-directed behavior (scratching and autogrooming). We compared fGCM concentrations of the Apenheul animals to those of zoo orangutans kept in permanent groups. In addition, we tested the effect of group size, visitor number, sex, age, and change of group composition on fGCM concentrations and proportions of self-directed behavior in the Apenheul orangutans. In contrast to Bornean orangutans housed in permanent groups, we did not find a group size effect on fGCM or on self-directed behavior in Apenheul's fissionfusion housing system. In addition, fGCM concentrations in Apenheul orangutans increased significantly with visitor numbers. Visitor number also affected proportions of self-directed behavior, and mean proportions of scratching were positively cor...

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Environmental enrichment of brown capuchins (Cebus apella): Behavioral and plasma and fecal cortisol measures of effectiveness

Cited by 83 publications

References 65 publications

A Validation of Extraction Methods for Noninvasive Sampling of Glucocorticoids in Free‐Living Ground Squirrels

A Validation of Extraction Methods for Noninvasive Sampling of Glucocorticoids in Free‐Living Ground Squirrels

Concentrations of four fecal steroids in wild baboons: short-term storage conditions and consequences for data interpretation

The Effect of Fission–Fusion Zoo Housing on Hormonal and Behavioral Indicators of Stress in Bornean Orangutans (Pongo pygmaeus)

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