Sources of morbidity in lorises and pottos in North American zoos: A retrospective review, 1980-2010.

Delineating patterns of morbidity can reveal management practices in need of reassessment to improve individual welfare, as well as population health and sustainability. We reviewed medical records from 38 North American zoological institutions for 276 slender lorises, slow lorises, and pottos born between January 1, 1980 and December 31, 2010. This sample included animals identified as 116 Nycticebus pygmaeus, 84 N. coucang, 48 Loris tardigradus tardigradus, 6 L.t. nordicus (now classified as L. lydekkerianus nordicus), and 22 Perodicticus potto. Taxonomy for lorises and pottos is developing, and two of these populations (N. coucang and P. potto) likely included hybrids and/or multiple species. Our focus was to examine trends based on species and age. Across all species, whole body disease events, abnormalities of bloodwork, and dental diseases were the most common sources of morbidity. Other major sources of morbidity varied by species and included trauma, respiratory disease, and ocular disease. A recent upsurge in research has informed feeding practices for slow lorises living in human care, and a similar, evidence-based approach is needed to improve diets for other species. Given the prevalence of trauma in this sample, social needs and reproductive management practices are also important areas for further investigation. Species-level health trends reveal risk factors for individual welfare that can guide husbandry practices in zoos, as well as in sanctuaries caring for the influx of lorises and pottos rescued from the growing wildlife trade.

Fecal glucocorticoid metabolite responses to management stressors and social change in four species of callitrichine monkeys.

The use of enzyme immunoassays (EIA) for the non-invasive measurement of glucocorticoids provides a valuable tool for monitoring health and welfare in sensitive species. We validated methods for measuring fecal glucocorticoid metabolites (FGM) using the response to veterinary exams for four species of callitrichine monkeys: golden lion tamarin (Leontopithecus rosalia, n = 7), callimico (Callimico goeldii, n = 2), pied tamarin (Saguinus bicolor, n = 2), and white-fronted marmoset (Callithrix geoffroyi, n = 2). Routine veterinary exams were performed for the golden lion tamarins and callimicos, but exams for the pied tamarins and white-fronted marmosets were prompted by the death of a social partner. Prior to veterinary exams, fecal markers were evaluated to allow collection of individual samples and estimate approximate gut transit times. Based on this assessment, individual markers were fed in the afternoon, and fresh morning fecal samples were collected throughout this study. Following a veterinary exam, FGM increased roughly 3- to 28-fold above baseline in all species. Although FGM for most species returned to baseline concentrations within 24-48 h, the marmosets exhibited a progressive increase in FGM after an exam in response to the death of a breeding female and subsequent hand-rearing of a neonate. Individual differences were noted in the callimicos and tamarins, with higher baseline FGM levels in females vs. males, although small sample size precluded a clear determination of sex differences. To our knowledge, this is the first study to measure FGM in callimicos and white-fronted marmosets and the first to compare FGM across callitrichine species. These findings highlight the broad applicability of this EIA to measure the stress response of callitrichine monkeys. The progressive increase in FGM in the marmosets during hand-rearing of a neonate suggests that care should be taken to minimize this disturbance as much as possible.

Behavioral thermoregulation in a group of zoo-housed colobus monkeys (Colobus guereza).

Although wild primates are known to modify behavior in response to thermal stress, less is known about behavioral thermoregulation in zoo-housed primates. Zoo exhibits expose individuals to unique thermal environments and may constrain the thermoregulatory strategies available to individual animals. In this study, we observed a group of seven colobus monkeys (Colobus guereza) living on a concrete "Monkey Island" style exhibit that featured limited shade and limited arboreal space. Behaviors were recorded using continuous focal animal sampling (n = 63 days, 97.7 hr). Logistic regression revealed 23°C was the temperature at which monkeys began resting more in shade than in sun. When temperatures exceeded 23°C, animals spent more time in open sitting postures with limbs extended from the body; sat less frequently in closed, hunched postures; spent more time in social contact; and performed more self-directed behaviors. Exhibit use also shifted under higher temperatures, with more time spent in areas with shade and lower surface temperatures. Lastly, when provided with access to an indoor holding area, the colobus monkeys spent more than half the time indoors when temperatures exceeded 23°C, yet only 10% of their time indoors when the temperature was below this value. Although postural changes have been reported in wild colobus, the postural and other behavioral changes observed in the current study occurred at temperatures lower than expected based on the published thermoneutral zone of colobus monkeys and highlight the importance of considering the specific thermoregulatory responses of zoo animals.

A survey of husbandry practices for lorisid primates in North American zoos and related facilities.

Zoos and related facilities in North America currently manage five species in the primate family Lorisidae: the greater (Nycticebus coucang), Bengal (N. bengalensis) and pygmy (N. pygmaeus) slow lorises, red slender loris (Loris tardigradus), and potto (Perodicticus potto). We used an online survey to describe institutional housing and husbandry practices for these species and assess the extent to which practices are consistent with established guidelines. Our results show that most captive lorisids are housed solitarily or in pairs. Most individuals occupy a single exhibit space in a building dedicated to nocturnal animals. Facilities are commonly meeting recommendations for abiotic exhibit design and are providing animals with an enriched environment. However, pottos and slender lorises currently occupy exhibit spaces smaller than the recommended minimum, and the impact of cleaning protocols on olfactory communication should be critically evaluated. Few facilities are taking advantage of the benefits of positive reinforcement training for promoting animal welfare. Research is greatly needed on the effects of exhibit lighting on behavior, health, and reproduction; and to determine how best to manage the social needs of lorisids with naturally dispersed social structures. Although captive populations of slender lorises, pottos, and slow lorises are declining, we suggest that improved husbandry knowledge has the potential to positively influence population sustainability and to enhance future efforts to manage the growing pygmy loris population.

Female nile hippopotamus (Hippopotamus amphibius) space use in a naturalistic exhibit.

Zoological institutions provide naturalistic exhibits for their animals in order to offer a more appealing look for visitors and give the animal the opportunity to engage in more natural behaviors. Examining space use of the animals in the naturalistic exhibit may aid in the management of these animals and inform future naturalistic exhibit design. The hippopotamus is an amphibious ungulate that spends much of its days in the wild in the water but may be found along the banks of the rivers basking in the sun. Our objective was to determine how captive female hippos utilize their exhibit by examining whether hippos selected for certain areas of a naturalistic exhibit. Scan sample data were collected on a group of nine captive female hippos housed at Disney's Animal Kingdom®. Using ArcView, the data were analyzed to determine distribution of hippos in the exhibit and their utilization of depth categories while in the water. Hippos were found to aggregate in preferred areas of the exhibit, mostly water, and selected most for water depths of 0.6-1.0 m. These results will aid in the understanding of hippopotamus space use and may aid zoological institutions in the design of naturalistic exhibits for hippos.

Behavioral responses of silverback gorillas (Gorilla gorilla gorilla) to videos.

This study examined the impact of video presentations on the behavior of 4 silverback, western lowland gorillas (Gorilla gorilla gorilla). On each of 5 occasions, gorillas viewed 6 types of videos (blue screen, humans, an all-male or mixed-sex group engaged in low activity, and an all-male or mixed-sex group engaged in agonistic behavior). The study recorded behavioral responses and watching rates. All gorillas preferred dynamic over static videos; 3 watched videos depicting gorillas significantly more than those depicting humans. Among the gorilla videos, the gorillas clearly preferred watching the mixed-sex group engaged in agonistic behavior; yet, this did not lead to an increase in aggression or behavior indicating agitation. Further, habituation to videos depicting gorillas did not occur. This supports the effectiveness of this form of enrichment, particularly for a nonhuman animal needing to be separated temporarily due to illness, shipment quarantine, social restructuring, or exhibit modification.

How access to exhibit space impacts the behavior of female tigers (Panthera tigris).

Little is known about how socially housed captive carnivores respond to temporary reductions in available space. We documented rates of aggression and affiliation in our group of six female tigers, under their normal housing conditions and during a period of exhibit renovations which resulted in a 50% reduction in time spent in an outdoor enclosure. During the period of reduced availability of space, significant declines in aggression and affiliation were observed indicating that these tigers responded in a manner consistent with a strategy of conflict avoidance. These reductions in rates of social behavior remained in place during the year following the return to their original housing conditions. Thus, even temporary alterations to housing practices have the potential to have lasting impacts on the social behavior of this species.

Siamangs (Hylobates syndactylus) and white-cheeked gibbons (Hylobates leucogenys) show few behavioral differences related to zoo attendance.

The effect of visitors on behavior and welfare of nonhuman animals in the zoo has been an active research topic during the last few decades. Although research has variously shown negative or positive impacts of zoo visitors on animals in captivity, previous primate research at Disney's Animal Kingdom suggests the importance of visual barriers in allowing animals to cope with large crowds. Examining this further, this study monitored the behavior of white-cheeked gibbons (Hylobates leucogenys) and siamangs (Hylobates syndactylus) in large, open exhibits. Behavioral data showed rates of social behavior and percentage of time engaged in solitary behavior did not differ between low and high visitor-attendance days. Both gibbons and siamangs spent more time in areas away from the public on high attendance days. Supporting previous findings, results imply visual barriers and ability to retreat from crowds may have provided these animals with choice and minimized potential negative visitor impact. Future research should focus on the relationship between attendance and actual crowds at exhibits; it should utilize multi-institutional methodologies to control for variance and look for individual and demographic differences between individuals.

Behavioral response of captive western lowland gorillas (Gorilla gorilla gorilla) to the death of silverbacks in multi-male groups.

In both free-ranging and captive western lowland gorillas, a silverback provides protection and leadership, mediating conflict within a group. In the wild, when a dominant silverback dies the group will disperse or transfer to a solitary male, unless a subsequent male is present to inherit the group. In captivity, studies have focused on groups containing one male and therefore it is unclear how gorillas respond to the death or removal of a silverback in multi-male groups. This study examined the behavior of a bachelor group (Cleveland Metroparks Zoo) and a multi-male, mixed-sex group (Pittsburgh Zoo and PPG Aquarium) following the death of two older silverbacks in 2005. Both of the younger but dominant males maintained their same level of dominance after the death. We predicted that agonism would increase after the death as groups struggled for social stablility. We did observe an increase in both agonism and displacements among the bachelor group, but only observed an increase in displacements among the mixed-sex group. Although we predicted that there would be no change in solitary behavior, both groups decreased feeding and the mixed-sex group increased self-directed behavior post-death. In the bachelor group, self-directed behavior decreased and undesirable behavior increased. We also observed a difference in spatial distance after the death with members of the mixed-sex group becoming more dispersed and members of the bachelor group more converged. This study demonstrates that there is a period of transition for multi-male groups after the death or removal of the oldest silverback. Future research could integrate physiological measures with behavioral analyses before and after the death or removal of a prominent member of the group.

Long-term monitoring of social behavior in a grouping of six female tigers (Panthera tigris).

Although literature on the reproduction of captive tigers is plentiful, there is little information on other social behaviors, particularly within large social groupings. Here we report on the long-term monitoring of social behaviors in six female tigers (Panthera tigris). Over a period of 6 years, behavioral data were collected on spraying, vocalizations, non-contact aggression, and contact aggression during outdoor observations, as well as nearest neighbors in the morning, as a proxy measure of affiliation. Regression analyses showed that non-contact aggression and vocalizing were increasing, whereas spraying and social proximity were decreasing over the 6 years of the study. Paired t-tests showed no seasonal differences in aggression, but animals had higher social proximity scores during the mornings of the colder winter months. Correlations showed that spraying was positively related to contact aggression whereas social proximity was negatively correlated with non-contact aggression. In addition to documenting levels of contact and non-contact aggression over time, this study showed these behaviors correlated with behaviors that were more easily scored (spraying and social proximity). Behavioral monitoring has played a key role in the management and husbandry of this large social grouping of female tigers. In addition to providing keepers with the opportunity to observe their animals in regularly scheduled sessions, behavioral monitoring has provided baseline information on social relationships in this grouping over time. If future research validates the relationship between aggression and spraying/social proximity, this can be a valuable tool for long-term monitoring of groups of tigers. Zoo Biol 27:89-99, 2008. (c) 2007 Wiley-Liss, Inc.