Fecal glucocorticoid metabolite response of captive koalas (Phascolarctos cinereus) to visitor encounters
Introduction
Glucocorticoid hormones (GCs) are secreted by the adrenal glands and regulate many aspects of vertebrate physiology. Their primary role is in the regulation of energy and maintenance of homeostasis (Sapolsky et al., 2000), and only at high levels do they live up to their typical designation of being ‘stress’ hormones (O’Connor et al., 2000). When the hypothalamic-pituitary-adrenal (HPA) axis is activated by a perceived threat to homeostasis, the physiological stress response is initiated, resulting in elevated GC levels circulating in the blood. Acutely elevated GCs act on many different physiological and behavioural systems to help the individual cope with the stressor, including increasing blood flow, mobilising glucose stores, enhancing memory, suppressing reproductive behaviours and promoting appropriate survival behaviours (Busch and Hayward, 2009). Chronic stress can result in dysfunction of the HPA-axis and maladaptive glucocorticoid secretions that can cause negative effects on functionally important biochemical processes, such as immune-response and metabolism (Herman, 2013). Circulating GCs can be measured directly from blood samples (Breuner et al., 2013), but monitoring of GC levels can also be done non-invasively through measurements of GC metabolites in excreta (Palme, 2005). In particular, fecal glucocorticoid metabolite (FGM) monitoring is a useful tool for managers of wildlife in captivity, since fecal samples are readily available and may be identified to individuals if required (Hogan et al., 2012, Narayan, 2017). Technical considerations of FGM analysis, such as sample collection and storage protocols, assay system design and validation have been thoroughly discussed in recent reviews (Fanson et al., 2017, Millspaugh and Washburn, 2004, Palme et al., 2013, Sheriff et al., 2011).
Many years of behavioural research into the effect of unfamiliar humans (zoo visitors) on zoo animals have demonstrated that responses are inconsistent between taxa (Hosey, 2008). In some cases animals show no behavioural response to visitors, in others they are enriched by human contact, and in others (e.g. primates) zoo visitors appear to have a stressful effect (Hosey and Melfi, 2015). Whether a stressful effect on behaviour is reflected in GC levels is not well understood, since few studies have investigated the physiological impact of zoo visitors. However, in the studies thus far, there appears to be evidence of a physiological stress response to zoo visitors in some contexts. Increased FGM levels were demonstrated in these studies occurring at peak times of visitation: Indian blackbuck (Antilope cervicapra) (Rajagopal et al., 2011), Mexican wolves (Canis lupus baileyi) (Pifarré et al., 2012) and Père David’s deer stags (Elaphurus davidianus) (Li et al., 2007). Similar observations were made using salivary cortisol levels of jaguars (Panthera onca) (Montanha et al., 2009) and urinary cortisol levels in spider monkeys, Ateles geoffroyii rufiventris (Davis et al., 2005). A significant correlation between human exposure (based on the proportion of enclosure perimeter exposed to zoo visitors) and mean FGM concentrations has also been reported for black rhinos, Diceros bicornis (Carlstead and Brown, 2005). In koalas, there was a significant difference in mean FGMs (over a 20 day period) between ‘handled’ and ‘unhandled’ males (but not females); males were ‘handled’ for 5–30 min for a variety of purposes, but primarily for photography sessions with zoo visitors (Narayan et al., 2013). In other contexts, captive mammals may not respond physiologically to anthropogenic stressors; this appears to be the case with numbats, Myrmecobius fasciatus (Hogan et al., 2012). Alternatively, regular exposure to humans may lead to potential habituation, as is the case with the greater bilby (Macrotis lagotis): when used regularly for educational displays (school visits and shows) there was no significant increase in FGMs (Narayan et al., 2011).
The difference between handled and unhandled koalas in the study of Narayan et al. (2013) drew our attention to the investigating the effect of ‘animal encounter’ experiences on zoo animals. These encounters provide zoo visitors an opportunity to interact with zoo animals at closer quarters, and are offered by many zoos as an additional feature to enhance the visitor experience of the zoo. The welfare of the individual animals used in visitor encounters is closely monitored by zoo staff during each encounter, but there is still the potential for GC-modulated stress responses, either acutely in response to a specific encounter event or a chronic elevation in GCs in response to long-term exposure. In the present study, we monitored FGMs of koalas in a photography encounter program where zoo visitors stood in close proximity to the animals, but were not permitted to touch or handle the animals. Since an acute stress response is more likely in response to a change in circumstances, in the present study we manipulated the photography encounter frequency (‘standard’ or ‘intensive’) following a ‘baseline’ period of no encounters. We hypothesised that the intensive photography frequency would result in higher FGMs than both baseline and standard photography frequency. We also hypothesised that this effect may interact with the sex of the koalas, due to the interaction between sex and handling effects seen in the study of Narayan et al. (2013). To our knowledge, this is the first experimental test of the effect of changes in visitor encounters on the FGM response of animals in captivity.
Section snippets
Study animals
Captive koalas (Phascolarctos cinereus) used in this study were housed at Taronga Zoo, Sydney. The animals were housed in the Koala Encounters enclosure (KE3), which is used for photography sessions with zoo visitors. This enclosure is divided into seven sections (‘Bays’), each of which contains one to three individual adult koalas. Koalas were provided with fresh browse daily.
Fecal samples were collected during May to July 2010 from 12 koalas (6 female and 6 male). Koalas ranged in age from 11
Sex, enclosure (bay) and visitor encounter treatment
Mean fecal cortisol metabolite (FCM) levels for male and female koalas in each enclosure bay are shown in Table 3. The koalas in Bay 6, which did not experience any photography events, had the lowest mean FCMs. In all bays in which both males and females were housed, males had higher FCM levels.
The GLMM analysis did not include bays as a factor because the photography treatment regime was designed to include or exclude certain bays. The GLMM showed that male FCMs were significantly different
Discussion
Early observations of glucocorticoid responses in koalas were made by Oddie et al. (1976) as part of a comprehensive examination of marsupial blood glucocorticoids. Recently several studies have investigated the topic of stress responses in koalas using non-invasive fecal sampling, including validation of FCM EIAs in the koala (Narayan et al., 2013, Davies et al., 2013a, Johnston et al., 2013), and evaluation of physiological stress in relation to climate (Davies et al., 2013b, Davies et al.,
Author contributions
KNW designed the study, arranged sample collection, prepared samples, performed statistical analyses and collaborated on the manuscript. EJN prepared samples, performed the EIAs, collated data and collaborated on the manuscript. NdV coordinated sample collections and changes to the koala visitor encounter schedule and collaborated on the manuscript.
Funding
Financial support for this project was provided by Taronga Zoo and by a grant from the James N Kirby Foundation, Australia to KNW and EJN [IRIS ID: 9201300452].
Acknowledgments
The authors wish to acknowledge the significant support of current and former staff at Taronga Zoo, Sydney, Australia. The project arose from discussions with Mr William Meikle, and was developed with Mr Nicholas de Vos and other staff from the Australian Mammals section. The Australian Mammals staff collected fecal samples from koalas, and coordinated the two visitor encounter treatments, without which this project could not have proceeded. In addition, Dr Rebecca Spindler and Dr Vicky Melfi
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Contributed equally to this research.