Stress in Yucatan spider monkeys: effects of environmental conditions on fecal cortisol levels in wild and captive populations

In the Yucatán Peninsula, spider monkeys Ateles geoffroyi yucatanensis are generally found in two contrasting conditions: large tracts of conserved forest or small fragments surrounded by human populations. In the present study, we analyzed fecal cortisol levels of spider monkeys to investigate whether environmental conditions have an influence on stress; specifically, we compared fecal cortisol across individuals living in conserved forests, fragmented forests and captive conditions (zoos and pets). Radioimmunoanalysis of fecal samples from 121 individuals indicated significant differences in mean cortisol for A. g. yucatanensis based on habitat type, with the lowest levels found in the conserved forest condition. The higher cortisol levels in both fragmented forest populations and in captive individuals may be the result of metabolic and behavioral stress. The mean male fecal cortisol concentration was significantly higher than that of females, and the fecal cortisol concentration was higher in the dry season compared with the wet season in a conserved habitat. Therefore, we emphasize the importance of considering sex and seasonality when monitoring fecal cortisol concentrations of spider monkeys, and more generally of frugivores, as they face a seasonal variation in food availability. Finally, our results suggest that forest fragmentation may create long-term stressors for spider monkeys, affecting the viability of populations living under such conditions.     

Female Spider Monkeys (<Emphasis Type="Italic">Ateles geoffroyi</Emphasis>) Cope with Anthropogenic Disturbance Through Fission–Fusion Dynamics

Most primates live in habitats with some level of anthropogenic disturbance, and such disturbances have a larger impact on frugivorous primates that are more sensitive to ecological disruptions than folivores. Fecal glucocorticoid metabolites provide insight into how the external environment affects internal physiological state, and thus provide information on how anthropogenic pressures become embodied. Here, I examine how subgroup size and glucocorticoids vary with high and low fruit abundance, and how fruit abundance, subgroup size, and activity budget affect fecal glucocorticoid metabolites in female spider monkeys (Ateles geoffroyi) living in an anthropogenically disturbed habitat. I measured these variables via behavioral, ecological, and fecal sampling for 15 months in 17 female spider monkeys at El Zota Biological Field Station. Subgroup size was significantly larger during periods of high fruit abundance, but glucocorticoids did not differ between periods of low and high fruit abundance. Monthly fruit abundance predicted subgroup sizes significantly, but did not predict fecal glucocorticoid concentrations. Increased resting time and reproductive state predicted fecal glucocorticoid concentrations significantly, but travel and foraging time had no significant effect on glucocorticoid concentrations. Individual resting time over the study period correlated negatively with glucocorticoid concentrations. These results suggest that spider monkeys cope with variation in fruit abundance by adjusting subgroup size, and that these adjustments may mitigate environmental stress in this mildly seasonal environment. The large, relatively productive forest size at this site, and the availability of anthropogenic food sources, enable this population of spider monkeys to cope with human-induced habitat disturbance.     

Optimal group size and seasonal stress in ring-tailed lemurs (Lemur catta)

Adaptive explanations for social grouping assume that thereare fitness consequences associated with group size, and individualsmaintain membership in groups of favorable size to maximizefitness. Here I examine fecal cortisol concentrations as a hormonalmeasure of stress to assess the relative well-being of Lemurcatta in groups of different size and in seasons of normal andlow tamarind fruit availability. I test the hypotheses thatthere is an optimal group size at which cortisol is lowest andthat optimal group size changes in food-scarce conditions. Icollected 799 fecal samples from 87 individuals in seven free-rangingL. catta groups at Berenty Reserve, Madagascar, over a 1-yearperiod (August 1999–July 2000) and determined fecal cortisolconcentrations using a radioimmunoassay. Expressing these asresiduals from monthly population means to control for temporalfluctuations in cortisol concentration, I calculated mean fecalcortisol levels for each animal in seasons of normal and lowtamarind fruit abundance and over the entire year. Overall,females exhibited lowest mean cortisol levels in groups of intermediatesize, suggesting that there are benefits to maintaining membershipin these groups. Females in groups that were atypically largeor small for their habitat type had higher mean cortisol levelsthan typical groups. Cortisol levels increased in food-scarceconditions for larger groups, suggesting that intergroup competitiveadvantages do not outweigh intragroup feeding competition atthis time. Group size may be optimized for long-term averageconditions, and short-term stresses may intermittently alterthe costs associated with group size.     

Factors affecting fecal glucocorticoid levels in semi-free-ranging female mandrills (Mandrillus sphinx)

Subordinate female cercopithecine primates often experience decreased reproductive success in comparison with high-ranking females, with a later age at sexual maturity and first reproduction and/or longer interbirth intervals. One explanation that has traditionally been advanced to explain this is high levels of chronic social stress in subordinates, resulting from agonistic and aggressive interactions and leading to higher basal levels of glucocorticoids. We assessed the relationships among fecal cortisol levels and reproductive condition, dominance rank, degree of social support, and fertility in female mandrills (Mandrillus sphinx) living in a semi-free-ranging colony in Franceville, Gabon. Lower-ranking females in this colony have a reproductive disadvantage relative to higher-ranking females, and we were interested in determining whether this relationship between dominance rank and reproductive success is mediated through stress hormones. We analyzed 340 fecal samples from 19 females, collected over a 14-month period. We found that pregnant females experienced higher fecal cortisol levels than cycling or lactating females. This is similar to results for other primate species and is likely owing to increased metabolic demands and interactions between the hypothalamus-pituitary-adrenal axis, estrogen, and placental production of corticotrophin releasing hormones during pregnancy. There was no influence of dominance rank on fecal cortisol levels, suggesting that subordinate females do not suffer chronic stress. This may be because female mandrills have a stable social hierarchy, with low levels of aggression and high social support. However, we found no relationship between matriline size, as a measure of social support, and fecal cortisol levels. Subordinates may be able to avoid aggression from dominants in the large enclosure or may react only transiently to specific aggressive events, rather than continuously expecting them. Finally, we found no relationship between fecal cortisol levels and fertility. There was no difference in fecal cortisol levels between conceptive and nonconceptive cycles, and no significant relationship between fecal cortisol level and either the length of postpartum amenorrhea or the number of cycles before conception. This suggests that the influence of dominance rank on female reproductive success in this population is not mediated through chronic stress in subordinate females, and that alternative explanations of the relationship between social rank and reproduction should be sought.     

Foraging Success,Agonism, and Predator Alarms: Behavioral Predictors of Cortisol in <Emphasis Type="Italic">Lemur catta</Emphasis>

Primate social grouping is understood as an adaptive strategy for mitigating environmental selection pressures, but the relative importance of various pressures may vary. Physiological measures of well-being can show their short-term impacts and suggest their relative importance and capacity to provide ultimate or proximate control of group size. I examined correlations between pressures commonly proposed as causes of social grouping (foraging success, intergroup and intragroup agonism, and predation risk) and individual levels of fecal cortisol, a hormonal stress measure, in a free-ranging population of Lemur catta. I collected behavioral data on 45 female Lemur catta at Berenty Reserve, Madagascar, over 3 seasons (August 1999-July 2000) and determined individual cortisol levels from 474 fecal samples. Neither predator alarm rates nor intragroup agonism rates correlated with cortisol levels in any season. However, females with low daily food intake and high rates of escalated intergroup defense exhibited higher cortisol levels. The data suggest that acquisition and defense of food resources are principal challenges in Lemur catta, and may be important factors determining social grouping and other behavioral or life history adaptations.     

Effects of reproductive condition and dominance rank on cortisol responsiveness to stress in free‐ranging female rhesus macaques

The hypothalamic–pituitary–adrenal (HPA) axis modulates individuals' physiological responses to social stress, which is an inevitable aspect of the daily lives of group‐living animals. Previous nonhuman primate studies have reported that sex, age, rank, and reproductive condition influence cortisol levels under stressful conditions. In this study we investigated cortisol responses to stress among 70 multiparous, free‐ranging female rhesus macaques (Macaca mulatta) on the island of Cayo Santiago, PR. Plasma cortisol samples were collected in two consecutive years under similar conditions. Twenty‐two females were sampled both years, and most of those females were lactating in only one of the years. Individual differences in cortisol levels were stable across years, even though reproductive condition changed for most individuals. No relationship was found between age or social rank and cortisol levels. Of the females that changed reproductive conditions, cortisol levels were higher when they were lactating than when they were cycling, and the amount of change in cortisol from cycling to lactating was greatest for low‐ranking individuals. Heightened reactivity to stress during lactation may be the result of concerns about infant safety, and such concerns may be higher among low‐ranking mothers than among higher ranking mothers. Psychosocial stress and hyperactivation of the HPA axis during lactation can suppress immune function and increase vulnerability to infectious diseases, thus explaining why adult females in the free‐ranging rhesus macaque population on Cayo Santiago have a higher probability of mortality during the birth season than during the mating season. Am. J. Primatol. 72:559–565, 2010. © 2009 Wiley‐Liss, Inc.     

Aggression and social support predict long‐term cortisol levels in captive tufted capuchin monkeys (Cebus [Sapajus] apella)

Many nonhuman primates live in complex social groups in which they regularly encounter both social stressors such as aggression and social support such as that provided by long‐term affiliative relationships. Repeated exposure to social stressors may result in chronically elevated cortisol levels that can have deleterious physical effects such as impaired immune function, cardiovascular disease, and reduced brain function. In contrast, affiliative social relationships may act as a buffer, dampening the release of cortisol in response to acute and chronic stressors. Understanding how social stressors and social support predict cortisol levels is therefore essential to understanding how social situations relate to health and welfare. We studied this relationship in 16 socially housed captive brown capuchin monkeys (Cebus [Sapajus] apella) by comparing long‐term hair cortisol levels with behavioral measures of social stress (dominance rank, rank certainty, and amount of aggression received) and social support (amount of affiliation and centrality in the affiliative social network of the group). Dominance rank, rank certainty, amount of affiliation, and age were not significant predictors of long‐term cortisol levels in this population. Instead, long‐term cortisol levels were positively related to the amount of aggression received and negatively related to centrality in the affiliative social network of the group. This pattern may be attributed to the species’ socially tolerant dominance system and to the availability of social support across the dominance hierarchy.     

From process to pattern: how fluctuating predation risk impacts the stress axis of snowshoe hares during the 10-year cycle

Predation is a central organizing process affecting populations and communities. Traditionally, ecologists have focused on the direct effects of predation—the killing of prey. However, predators also have significant sublethal effects on prey populations. We investigated how fluctuating predation risk affected the stress physiology of a cyclic population of snowshoe hares (Lepus americanus) in the Yukon, finding that they are extremely sensitive to the fluctuating risk of predation. In years of high predator numbers, hares had greater plasma cortisol levels at capture, greater fecal cortisol metabolite levels, a greater plasma cortisol response to a hormone challenge, a greater ability to mobilize energy and poorer body condition. These indices of stress had the same pattern within years, during the winter and over the breeding season when the hare:lynx ratio was lowest and the food availability the worst. Previously we have shown that predator-induced maternal stress lowers reproduction and compromises offspring’s stress axis. We propose that predator-induced changes in hare stress physiology affect their demography through negative impacts on reproduction and that the low phase of cyclic populations may be the result of predator-induced maternal stress reducing the fitness of progeny. The hare population cycle has far reaching ramifications on predators, alternate prey, and vegetation. Thus, predation is the predominant organizing process for much of the North American boreal forest community, with its indirect signature—stress in hares—producing a pattern of hormonal changes that provides a sensitive reflection of fluctuating predator pressure that may have long-term demographic consequences.     

Cascading Effects of Climate Change: Do Hurricane‐damaged Forests Increase Risk of Exposure to Parasites?

Increased parasitism in animals in disturbed habitats is often understood to be the result of increased disease susceptibility due to low food availability resulting in nutritionally stressed and immunocompromised individuals. Such habitat change, however, might also lead to increased exposure to disease. In this article, we test measures of susceptibility and exposure to explain the prevalence and intensity of directly and indirectly transmitted helminths in black howler monkeys (Alouatta pigra) following a hurricane in Belize. None of these parasites were predicted by direct measures of susceptibility (as measured by fruit consumption and fecal cortisol levels). Rather, directly transmitted parasites (Trichuris sp. and strongylid type eggs.) were predicted by host density and group size, both measures of exposure. Similarly, only the consumption of Cecropia peltata, a fast growing pioneer that has a mutualistic relationship with ants predicted levels of the indirectly transmitted trematode Controrchis spp., also suggesting exposure. Cecropia peltata also increased in density post‐hurricane, was high in digestible protein, sugar, and salt and eaten by monkeys more frequently than predicted based on distribution. These data suggest that in this hurricane‐damaged forest the ingestion of this abundant and nutritious pioneer species increased exposure of the monkeys to Controrchis through ingestion of ant intermediate hosts. These results may point to a pattern true of pioneer species in general, leaving animals in disturbed forests with higher levels of parasitism as a result of changes to forest structure. As severe weather events are expected to increase, this suggests a cascading effect of climate change on ecosystem interactions and disease ecology.     

Blubber cortisol qualitatively reflects circulating cortisol concentrations in bottlenose dolphins

Stress hormones, released into circulation as a consequence of disturbance, are classically assayed from blood samples but may also be detected in a variety of matrices. Blubber and fecal samples can be remotely collected from free‐ranging cetaceans without the confounding hormone elevations associated with chase, capture, and handling required to collect blood samples. The relationship between cortisol concentrations in circulation with that of blubber and feces, however, is unknown. To assess these associations, we elevated cortisol by orally administering hydrocortisone for five days in five bottlenose dolphins. Voluntary blood and fecal samples were collected daily; blubber biopsies were collected on day one, just prior to hydrocortisone administration, and days three and five of hydrocortisone administration. We evaluated subsequent changes in several circulating stress hormones as well as cortisol and glucocorticoid metabolites in blubber and feces, respectively. There was a significant association between cortisol levels in serum and in blubber (F_1,12.7 = 14.3, P < 0.01, mR² = 0.57) despite substantial variability in blubber cortisol levels. Counterintuitively, fecal cortisol metabolite levels were inversely related to serum cortisol. The relationship between serum and blubber cortisol levels suggests blubber samples from remote sampling may be useful to detect stress loads in this species.     

Effects of forest fragmentation on the physiological stress response of black howler monkeys

Habitat loss and fragmentation can create severe environmental problems for forest species, and may ultimately lead to local population extinction. One mechanism that might play a role in this process is the physiological stress response of individuals, because animals that experience chronic stress might show reduced rates of reproduction and survival. In this study, we investigated whether black howler monkeys Alouatta pigra inhabiting forest fragments experienced greater physiological stress than those in continuous forest. Faecal cortisol metabolite levels were compared between monkeys inhabiting fragmented and continuous forests in Southern Mexico. The sex of the animals was taken into consideration, while activity patterns and aggressive events were also recorded to examine differences in behaviour and sociality. A chemiluminescent enzyme immunoassay was utilized to determine faecal cortisol metabolite levels. Our results showed that cortisol metabolite levels were higher in howler monkeys from forest fragments, and that they vary through time. Patterns of locomotion also differed between forest types, as monkeys from fragments travelled at higher frequencies, while monkeys from continuous forests performed more of their movements within tree crowns. There was no difference in the frequency of feeding, resting and social interactions between fragmented and continuous forest monkeys. Higher faecal cortisol metabolite levels in fragmented areas are likely the result of suboptimal environments and could have long-term adverse effects on monkey health, fertility and survival. We propose that faecal cortisol metabolite measurements can be a useful conservation tool for monitoring populations of long-lived species subsisting under suboptimal conditions.     

Proximal and Distal Predictors of the Spider Monkey’s Stress Levels in Fragmented Landscapes

The rapid loss, fragmentation and degradation of tropical forests threaten the survival of many animal species. However, the way in which these phenomena affect animal health has been poorly explored, thus limiting the design of appropriate conservation strategies. To address this, here we identified using linear mixed models the effect of proximal (diet, activity pattern, hunting and logging) and distal (sum of the basal areas of fruiting-tree species [SBAFS], landscape forest cover and degree of forest fragmentation) variables over fecal glucocorticoid metabolite (fGCM) levels–hormones associated with animal health and fitness–of six groups of spider monkeys (Ateles geoffroyi) inhabiting six landscapes with different spatial structures in Mexico. Proximal variables showed a stronger predictive power over fGCMs than distal. In this sense, increases in travel time, the occurrence of hunting, and reductions in rest time and fruit consumption resulted in higher fGCM levels. Regarding distal variables, increases in SBAFS were negatively related to fGCM levels, thus suggesting that food scarcity increases stress hormone levels. Nevertheless, contrary to theoretical expectations, spider monkeys living in smaller tracts of forest spent less time travelling, but the same time feeding on fruit as those in more forested areas. The lower net energy return associated with this combination of factors would explain why, contrary to theoretical expectations, increased forest cover was associated with increased levels of fGCMs in these groups. Our study shows that, at least in the short term, spider monkeys in fragmented landscapes do not always present higher levels of stress hormones compared to those inhabiting continuous forest, and the importance of preserving fruit sources and controlling hunting for reducing the levels of stress hormones in free ranging spider monkeys.     

Determinants of fruit removal in <Emphasis Type="Italic">Geonoma pauciflora</Emphasis>, an understory palm of neotropical forests

Competition for seed dispersers is supposedly a selective force that drives the evolution of plant reproductive traits. In the understory of tropical forests, such competition should be especially severe among bird-dispersed plant species because (i) the production of copious fruit crops is limited by low light availability; (ii) there usually is a high density of fleshy fruited plants, and (iii) understory frugivorous birds are not abundant. In this paper, we took advantage of a high-density population of Geonoma pauciflora, a bird-dispersed palm species growing in the understory of the Brazilian Atlantic forest, to investigate the influence of plant traits and its immediate neighborhood on fruit removal. Intrinsic (crop and fruit sizes) and extrinsic traits (related to light availability) affected the fruit removal of G. pauciflora. Crop size had a greater influence than fruit size on the absolute number of fruits removed, whereas none of the investigated traits influenced decisively fruit removal efficiency (i.e., the proportion of an individual’s crop removed). The influence of light availability was mostly indirect, through its positive influence on fruit production. A significant positive spatial autocorrelation in removal efficiency occurred among neighboring plants within a 7-m radius, which is indicative of facilitation among neighboring individuals. The consequence of such positive spatial autocorrelation in removal efficiency for clonal plants such as G. pauciflora is that by attracting a frugivore a given ramet may promote the removal of fruits of other ramets, thus enhancing the reproductive output of the genet as a whole.     

Fruit choice by red howler monkeys (Alouatta seniculus) in a tropical rain forest

This paper presents and discusses aspects of fruit selectivity by red howler monkeys (Alouatta seniculus) in relation with morphological characteristics of fruits. These data are used to provide an answer to the following questions: which are the fruit characteristics that lead fruit choice of howler monkeys and to what extent fruit characteristics play a role in seed dispersal by monkeys? The frugivorous diet of a troop of red howler monkeys was determined during a 2-year field study in French Guiana. The selection of fruit by howler monkeys was analyzed in relation to the fruit availability. Results showed that, although consumption followed availability, fruit species could be classified in three categories according to their selection ratio (percentage of consumption/percentage of abundance) as “high ranking,” “middle ranking,” and “low ranking” species. Also, the 97 species of fruit eaten by the monkeys were grouped according to the morphological characteristics thought to influence the monkeys' choice. This showed that howler monkeys consumed essentially fruits with juicy pulp, bright color, and a small number of well-protected seeds. Most of high ranking species had medium-sized fruits with yellow color, and low ranking species often had small fruits. However, howler monkeys are associated with the dispersal of seeds from fruit with a hard and indehiscent pericarp and/or large seeds, like those of the Sapotaceae family. Consequently, they can be considered as “specialized” frugivores for this fruit syndrome. © l996 Wiley-Liss, Inc.     

Ape conservation physiology: fecal glucocorticoid responses in wild Pongo pygmaeus morio following human visitation

Nature-based tourism can generate important revenue to support conservation of biodiversity. However, constant exposure to tourists and subsequent chronic activation of stress responses can produce pathological effects, including impaired cognition, growth, reproduction, and immunity in the same animals we are interested in protecting. Utilizing fecal samples (N = 53) from 2 wild habituated orangutans (Pongo pygmaeus morio) (in addition to 26 fecal samples from 4 wild unhabituated orangutans) in the Lower Kinabatangan Wildlife Sanctuary of Sabah, Malaysian Borneo, we predicted that i) fecal glucocorticoid metabolite concentrations would be elevated on the day after tourist visitation (indicative of normal stress response to exposure to tourists on the previous day) compared to samples taken before or during tourist visitation in wild, habituated orangutans, and ii) that samples collected from habituated animals would have lower fecal glucocorticoid metabolites than unhabituated animals not used for tourism. Among the habituated animals used for tourism, fecal glucocorticoid metabolite levels were significantly elevated in samples collected the day after tourist visitation (indicative of elevated cortisol production on the previous day during tourist visitation). Fecal glucocorticoid metabolite levels were also lower in the habituated animals compared to their age-matched unhabituated counterparts. We conclude that the habituated animals used for this singular ecotourism project are not chronically stressed, unlike other species/populations with documented permanent alterations in stress responses. Animal temperament, species, the presence of coping/escape mechanisms, social confounders, and variation in amount of tourism may explain differences among previous experiments. Acute alterations in glucocorticoid measures in wildlife exposed to tourism must be interpreted conservatively. While permanently altered stress responses can be detrimental, preliminary results in these wild habituated orangutans suggest that low levels of predictable disturbance can likely result in low physiological impact on these animals.     

Individual,social, and environmental factors affecting salivary and fecal cortisol levels in captive pied tamarins (Saguinus bicolor)

Pied tamarins (Saguinus bicolor) are endangered New World primates, and in captivity appear to be very susceptible to stress. We measured cortisol in 214 saliva samples from 36 tamarins and in 227 fecal samples from 27 tamarins, and investigated the effects of age, sex, pregnancy, rearing history, social status, weight, group composition, and enclosure type using generalized linear mixed models. There was no effect of age on either fecal or salivary cortisol levels. Female pied tamarins in late pregnancy had higher fecal cortisol levels than those in early pregnancy, or nonpregnant females, but there was no effect of pregnancy on salivary cortisol. Females had higher salivary cortisol levels than males, but there was no effect of rearing history. However, for fecal cortisol, there was an interaction between sex and rearing history. Hand‐reared tamarins overall had higher fecal cortisol levels, but while male parent‐reared tamarins had higher levels than females who were parent‐reared, the reverse was true for hand‐reared individuals. There was a trend towards lower fecal cortisol levels in subordinate individuals, but no effect of status on salivary cortisol. Fecal but not salivary cortisol levels declined with increasing weight. We found little effect of group composition on cortisol levels in either saliva or feces, suggesting that as long as tamarins are housed socially, the nature of the group is of less importance. However, animals in off‐show enclosures had higher salivary and fecal cortisol levels than individuals housed on‐show. We suggest that large on‐show enclosures with permanent access to off‐exhibit areas may compensate for the effects of visitor disturbance, and a larger number of tamarins of the same species housed close together may explain the higher cortisol levels found in tamarins living in off‐show accommodation, but further research is needed.     

The Influence of Temporal Changes in Fruit Availability on Diet Composition and Seed Handling in Blue Monkeys (Cercopithecus mitis doggetti)1

We investigated the relation between temporally varying resources, diet composition, and seed-handling behaviors in a group of blue monkeys (Cercopithecus mitis doggetti) in a tropical montane forest of Rwanda. Changes in diet composition were related to concurrent phenological studies of fruit-producing trees, and density and abundance of tree resources within the monkey's home range. Fruit composed nearly 50 percent of the diet. Over 50 percent of the fruits eaten had juicy fleshy pulp. Observations of seed handling behavior provided insights into the role of these animals as potential seed dispersal agents. The monkeys moved the seeds of 29 species out of parent canopies by defecating seeds intact and by potentially carrying seeds in cheek pouches and dropping them later. Seeds of 18 species were found intact in fecal piles. Our study showed community-level phenology patterns did not indicate a decrease in fruit availability during the study period, but an analysis of the preferred fruits consumed by the monkeys showed distinct periods of low fruit availability. The study period included two dry seasons; only one of these produced a period of fruit scarcity for the animals. The animals employed different strategies during times of preferred fruit scarcity. They increased consumption of leaves and other fleshy fruits, and diet diversity increased, or became mainly seed predators and diet diversity decreased. The variable responses of these monkeys to changes in food availability highlights their dietary plasticity and imposes significant variations in their role as potential seed dispersers.     

Temporal dynamics of nutrition, parasitism, and stress in colobus monkeys: implications for population regulation and conservation

The need to develop conservation plans calls for the ability to identify ecological factors that influence population density. Because stress is known to affect fecundity and mortality, increasing stress may provide a warning of potential population declines. We examined the effects of temporal variation in nutrition and parasitism on stress in endangered red colobus monkeys in Kibale National Park, Uganda. First, we tested the hypothesis that parasitism and nutrition would individually affect stress levels. We found that periods of poor-quality diet corresponded with an increase in cortisol. Similarly, increases in parasite infections were associated with increased cortisol. Next, we predicted that a poor-quality diet would facilitate increased parasite infections, and that together, they would lead to amplified stress. However, we found no support for such amplification, likely because the quality of the diet had little effect on parasite infections. Third, we tested whether individuals in a larger group were subject to food stress due to greater within-group competition, which would intensify nutritional stress and parasitism, and lead to reduced reproduction. Although we found no evidence to support a group size effect on parasites, cortisol levels in the large group tended to be higher than those in the small group, and the large group had fewer infants per female. The results suggest that parasitism and poor nutrition lead to increased stress which, because they are known to be associated with reduced fecundity and increased mortality, may lead to population declines.     

Comparison of Endocrine Response to Stress Between Captive-Raised and Wild-Caught Bighorn Sheep

ABSTRACT Stress hormones in Rocky Mountain bighorn sheep (Ovis canadensis canadensis), produced in response to environmental changes, road development, or high population density, may impact their immune systems to a threshold level that predisposes them to periodic, large-scale mortality. We compared the stress response to a novel environmental situation and repeated handling between bighorn sheep born and raised in captivity (CR) and bighorn sheep born in the wild (WC) and brought into captivity. We measured plasma epinephrine, norepinephrine, cortisol, and fecal glucocorticoid metabolites (FGM). Three weeks after each group's arrival we used a one-time drop-net event to elicit an acute stress response, and we collected blood samples from each sheep over 35 minutes, as well as one fecal sample. We collected blood and fecal samples from both groups on 7 other occasions over the subsequent 6 months. We also collected fecal samples from the pen at approximately 24-hour intervals for 3 days following every handling event to monitor the stress response to handling. We found that CR sheep had a stronger autonomic nervous system response than WC sheep, as measured by epinephrine and norepinephrine levels, but we found a very similar hypothalamic-pituitary–adrenal axis (HPA) response, measured by cortisol levels, to the acute stress event of a drop-net restraint. We also found that once the WC sheep had acclimated, as indicated by the return to the initial baseline FGM levels within 12 weeks, the CR and WC groups' HPA responses to sampling events were not significantly different from one another. Fecal samples can provide a noninvasive mechanism for managers to monitor baseline FGM for a given herd. Using long-term monitoring of FGM rather than values from a single point in time may allow managers to correlate these levels to outside influences on the herd and better understand the impacts of management changes, population density, or increased human developments on the health of the sheep population.     

环境丰容对笼养川金丝猴日常行为以及粪便皮质醇水平的影响

在笼养条件下,由于有限的空间和单调的笼舍结构,川金丝猴行为和生理指标发生变化,包括出现刻板行为和产生较高的粪便内应激激素。本论文旨在研究环境丰容对笼养川金丝猴日常行为以及粪便皮质醇水平的影响。于2013年8月1日至11月1日对杭州动物园内7只川金丝猴进行环境丰容后的行为观察。采用瞬时扫描法记录上午08:30-10:30和下午14:00-16：00的动物行为,并统计15种行为的发生频率。比较丰容前后每种行为的发生频率,结果表明环境丰容降低了川金丝猴的不活跃行为（P=0.021）和刻板行为（P=0.034）,增加了其活跃行为频率（P=0.018）。环境丰容后,动物表现出更多的攀爬（P = 0.012）、探究（P = 0.014）和环顾行为（P = 0.010）。粪便皮质醇激素的结果表明,除1只雄性个体激素上升外,其余6只个体的粪便皮质醇含量显著下降（P=0.028）。以上结果提示环境丰容可改善川金丝猴的福利状况。