Evaluating the Use of Chemical Weapons for Capturing Prey by a Venomous Mammal, the Greater Slow Loris (Nycticebus coucang).

Few mammals are venomous, including one group of primates-slow (Nycticebus spp.) and pygmy (Xanthonycticebus spp.) lorises. Hypotheses for the evolutionary function of venom in these primates include defense from predators or ectoparasites, communication or competition with conspecifics, and the capture of prey. We tested the prey capture hypothesis in 75 trials with 22 wild-caught greater slow lorises (N. coucang) housed in a rescue center in Java, Indonesia. We experimentally offered the slow lorises arthropod prey items varying in size, escape potential, and toxicity and recorded venom-related and predatory behaviors using live and video observations. The slow lorises visually targeted arthropod prey, approached it quickly and efficiently, and captured it with a manual grasping motion. They rarely performed venom-related behaviors and seemed to do so in a defensive context. The slow lorises exhibited little variation in pre-capture behavior as a function of prey size or escape potential. In response to noxious prey, the slow lorises performed tongue-flicking and other investigative behaviors that indicate they are using chemosensory input to assess prey characteristics. These data suggest it is unlikely that slow lorises use chemical weapons to subdue arthropod prey and may support, instead, a defensive function for slow loris venom.

Behavior of polar bear (Ursus maritimus) cubs post-den emergence at the Detroit Zoo.

In the wild, female polar bears (Ursus maritimus) with cubs may spend extended periods of time within the den following initial emergence. As a result, studying behavioral development of cubs at the denning site has been difficult and unreliable. Although care staff at zoological institutions have easier access to animals, every effort is made to minimize intrusions to maternal groups, which presents research limitations. Detroit Zoological Society staff used audio-equipped cameras installed in behind-the-scenes spaces to conduct approximately 9 weeks of monitoring on two female polar bear cubs of the same litter, one of whom (Laerke) was hand-reared while the other (Astra) was mother-reared. Monitoring spanned ages 14-24 weeks and consisted of 12, 5-min focal observations per observation day timed to evenly cover the entire 24-h day. Using generalized linear mixed models, we examined relationships between behavior and time of day, hour, and age. We also conducted descriptive analyses and used these to draw comparisons between the two cubs where appropriate. Despite different rearing environments, both cubs had highly comparable patterns of inactive, locomotory, and independent play behaviors. Astra generally decreased time spent nursing and in proximity to Suka as she aged. Data presented here represent a continuation of previous neonatal observations conducted on Astra, adding to the minimal body of knowledge currently available on first year polar bear cub development. We also report successful mitigation of stereotypic behavior in Laerke. Further studies of captive maternal groups can provide insight into this critical developmental stage, supporting both captive-based breeding efforts and in situ conservation efforts.

The Benefits of Increased Space and Habitat Complexity for the Welfare of Zoo-Housed King Penguins (Aptenodytes patagonicus).

Zoos and aquariums accredited by the Association of Zoos and Aquariums embrace animal welfare as a foundational principle of habitat design. Modern habitats are designed to provide animals with choices and agency over their environment, and to encourage species-appropriate behavior and space use. In 2016, the Detroit Zoological Society opened the Polk Penguin Conservation Center, a 3065.80 m2 facility that features a naturalistic design. The building was designed to optimize animal welfare by incorporating various substrates, nesting sites, and a 1234 kL pool with elements of underwater complexity. The facility houses a mixed-species group of penguins that were previously housed in a smaller habitat that opened in 1968. Between 2015 and 2022, we opportunistically monitored the behavior of ten king penguins (Aptenodytes patagonicus) as they moved back and forth between the two buildings while additional modifications were made to the new habitat. We collected 695 h of behavioral observations and 10,416 h of data from flipper-mounted time-depth recorders. We found that the king penguins spent less time engaged in aggression and more time engaged in swimming and positive social behaviors in the redesigned space. They also spent less time in proximity to other species of penguins and more time alone. These behavioral trends suggest that increased space and environmental complexity had positive welfare benefits for these penguins.

Behavioral development of a captive polar bear (Ursus maritimus) cub in the maternal den.

Two female polar bear (Ursus maritimus) cubs were born to mother Suka at the Detroit Zoo on November 17, 2020. One cub (Laerke) was hand-reared out of medical necessity, while the other cub (Astra) was mother-reared. Using audio-equipped video cameras previously installed in the maternal den, staff were able to conduct uninterrupted continuous monitoring on Suka and Astra for an unprecedented 12 weeks. Data collected during this time were analyzed descriptively. Astra spent a maximum of approximately 20% of any given 24 h period in nursing behaviors. Distribution of time spent nursing was relatively even across the 24 h day. In contrast to the limited data currently available, Astra spent only approximately 11% of the over 2000 h of behavioral data engaged in nursing behaviors. Astra left the nest for the first time in her fourth week of life, and time spent out of the nest gradually increased with age. Suka was observed guiding Astra back to the nest the first few times Astra ventured out. However, maintenance of maternal proximity did not appear to be a motivating factor in patterns of space use. The data presented here represent the longest uninterrupted continuous monitoring of a polar bear cub in the maternal den currently published. Publication of similar data from other institutions would establish more generalizable trends for early infancy development. These data are critical for understanding cub welfare and improving population sustainability and neonate mortality rates.

Impact of alternating overnight housing conditions on welfare measures in a bachelor group of western lowland gorillas (Gorilla gorilla gorilla).

Spatial parameters and design of overnight housing spaces can have significant influences on both nocturnal and diurnal behaviors of western lowland gorillas (Gorilla gorilla gorilla) in captivity. This is especially true for bachelor groups, as adult males have demonstrated a greater tendency to separate from conspecifics overnight. Additionally, previous studies have suggested that the social needs of individuals in bachelor units may shift over time. The bachelor unit at the Detroit Zoo is managed in a unique hybrid strategy in which the group is housed socially for three nights (either indoors or indoors with outdoor access), then separately on the fourth. A 2016 study of this group (n = 3) suggested that individuals had better welfare following social overnight housing as compared to solitary overnight housing. We aimed to reassess how overnight housing conditions affect individual welfare several years later. We revised a previously developed qualitative behavioral assessment tool that included 13 behavioral items spanning both positive and negative indicators of welfare. Animal care staff completed the assessment and collected a fecal sample every day for each gorilla for a period of 3 months. We used Kruskal-Wallis tests to analyze variation in behavioral items and FGMs between conditions. We then used generalized linear mixed models to identify whether overnight housing condition or other potentially confounding variables were driving observed variation in welfare indicators. We found significant variation demonstrating significantly better welfare indicators after being housed separately as compared to being socially housed indoors overnight. Although separate housing appears to be the ideal condition for this group at this point in time, if seasonality permits, social housing with outdoor access may be a feasible alternative to consistent overnight separation for these gorillas.

Behavioral Assessment of Six Reptile Species during a Temporary Zoo Closure and Reopening.

Although reptiles are commonly housed in zoos and aquariums, their welfare is understudied for the diversity of species housed and the taxon's current captive population size. The sensory abilities of reptiles have adapted to the varied ecological niches they inhabit, and these evolutionary adaptations impact how reptiles perceive the stimuli around them-including zoo visitors. This study aimed to assess visitor effects on small groups of six reptile species during a temporary zoo closure due to COVID-19 by measuring behavioral diversity, use of space (measured by a spread of participation index), and select behaviors. The species assessed showed diverse responses. The Catalina Island rattlesnakes (Crotalus catalinensis) demonstrated increased investigation and behavioral diversity after the zoo reopened compared to when the zoo was closed, but the European glass lizards (Pseudopus apodus) showed decreases in the amount of time spent exposed to the observers' view and in their evenness of space use after the zoo was reopened to visitors. The other species, including beaded lizards (Heloderma horridum), Sonoran spiny-tailed iguana (Ctenosaura macrolopha), Arrau turtles (Podocnemis expansa), and dwarf caimans (Paleosuchus palpebrosus), had intermediate changes in their responses to visitor presence.

Evaluation of the Impact of Behavioral Opportunities on Four Zoo-Housed Aardvarks (Orycteropus afer).

Evaluations of enrichment are critical to determine if an enrichment program is meeting stated goals. However, nocturnal species can present a challenge if their active periods do not align with caretakers' schedules. To evaluate enrichment for four aardvarks housed with a natural light cycle, we provided seven different enrichment items aimed at fulfilling two behavioral goals: exploring and foraging. We wanted to understand how the aardvarks used enrichment, if enrichment promoted the defined goals, and how enrichment that achieves its goals affects welfare indicators, including rates of pacing and social behaviors, behavioral diversity, and fecal glucocorticoid metabolites. Twenty-minute observations from video were performed three times a night for a total of 224 observed hours. We found significant differences in how the aardvarks used items from the two enrichment goals throughout the night, with foraging enrichment used more than exploring at first and exploring enrichment used more later. We found that items promoted their defined goals, and aardvarks showed no evidence of habituation throughout the eight-week study. The impact on selected welfare indicators provided evidence of potentially positive changes, including increased affiliative and decreased agonistic interactions accompanying increases in goal behaviors. These results contribute to the current knowledge available on the impact of goal-directed behavioral opportunities on zoo animal welfare.

Personality in Zoo-Hatched Blanding's Turtles Affects Behavior and Survival After Reintroduction Into the Wild.

Reintroduction programs in which captive-bred or reared animals are released into natural habitats are considered a key approach for conservation; however, success rates have generally been low. Accounting for factors that enable individual animals to have a greater chance of survival can not only improve overall conservation outcomes but can also impact the welfare of the individual animals involved. One such factor may be individual personality, and personality research is a growing field. We designed a project to ascertain the presence of personality traits in Blanding's turtles (Emydoidea blandingii), a species of special concern in the state of Michigan, and to assess potential links between traits and post-release success. As hypothesized, the Blanding's turtles in this study displayed behavioral responses to modified open field tests indicative of distinct personality traits: exploration, boldness, and aggression. Additionally, the personality traits were correlated differently with survival and behavior patterns when the turtles were released into the Shiawassee National Wildlife Refuge. More exploratory turtles had higher survival rates, while neither boldness nor aggression was related to survival. Exploratory turtles were also more likely to travel longer distances after release. The use of muskrat dens was related to increased survival, and both bolder and more exploratory turtles made higher use of this feature. Exploratory and aggressive turtles were found basking outside of water more often, while bold turtles were more likely to be found at the water surface. Both these basking behaviors may increase the risk of predation and may be reflective of a trade-off between the risk and behaviors related to physiological health. Understanding how personality affects behavior and survival post-release can be a critical tool for improving reintroduction success. Zoo animal welfare scientists and practitioners can implement approaches that improve the welfare of individuals within the context of conservation initiatives.

Exploratory Investigation of Infrared Thermography for Measuring Gorilla Emotional Responses to Interactions with Familiar Humans.

Interactions between zoo professionals and animals occur regularly and are believed to be enriching for animals. Little empirical information exists on how animals perceive these interactions, and particularly how the interactions affect the emotional states of animals. Infrared thermography (IRT) has shown some promise in the assessment of emotions in a variety of species, but further research is needed to determine if this method is useful in a zoo setting. We conducted a pilot study to determine if IRT is a valid measure of the emotional responses to routine interactions (positive reinforcement training and cognitive tasks, compared to a control condition) with familiar humans on three western lowland gorillas at the Detroit Zoo. We measured nasal temperatures associated with emotional change using IRT. To examine the validity of the IRT data, we collected saliva samples for hormone analysis before and after each condition, in addition to behavioral data during the interactions and control condition. Decreases in nasal temperatures for two gorillas and an increase in the third indicate that arousal changed consistently within individuals following the interactions but not the control condition. Pre-post cortisol levels and oxytocin concentrations decreased for all conditions, but the decreases seen did not differ among the conditions. The gorillas were highly engaged in the interactions, and two produced more grumble vocalizations during the human-animal interactions (HAIs) compared to the control condition. Additionally, the gorillas performed self-directed behaviors more often during the control condition, also suggesting HAIs were not a negative experience. In summary, we were able to measure changes in arousal using IRT, but we were unable to determine the emotional valence of these changes based on the additional indicators employed. Additionally, the inconsistency across these measures precluded firm conclusions about either the validity of IRT for measuring emotion in this context or how the interactions impacted these gorillas. These findings highlight the challenges of using IRT to measure emotional states in non-human animals, and we discuss further steps necessary to apply this method in future studies.

Case Studies of the Impacts of Cataract Surgery on Crested Penguin Welfare.

As nonhuman animals age, geriatric individuals require additional care and veterinary support to ensure their well being. The focus on lifelong care is a relatively newer approach when providing good welfare, and few studies have examined how veterinary care impacts behavior at different ages or how best to accommodate geriatric individuals in zoos. The objectives of this study were to (a) assess both the immediate and long-term (one year later) behavioral impacts of cataract removal for macaroni (Eudyptes chrysolophus) and southern rockhopper (Eudyptes chrysocome) penguins; (b) compare the behavior of penguins following cataract surgery to that of other conspecifics in the same habitat; and (c) monitor the impacts of cataract surgery on swimming behavior using time-depth recorders. Individual responses to cataract removal differed in direction and magnitude, and these mixed results highlight that welfare is experienced and thus measured at the individual level. Positive responses included increased habitat use, increased time spent swimming, and increased rates of affiliative interactions. This study highlights the importance of assessing welfare impacts of veterinary interventions on geriatric individuals.

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.

Behavioral and hormonal responses to the availability of forage material in Western lowland gorillas (Gorilla gorilla gorilla).

We investigated how forage material affects indicators of welfare in three male Western lowland gorillas (Gorilla gorilla gorilla) at the Detroit Zoo. In addition to their maintenance diet and enrichment foods, the gorillas generally received forage material four times a week. From this baseline, we systematically manipulated how much forage material the group received on a weekly basis, with either daily or bi (twice)-weekly presentation of browse (mulberry, Morus sp.) or alfalfa hay. We collected behavioral data (60 hr per gorilla) and measured fecal glucocorticoid metabolites (FGM). Mixed models indicated that the presence of forage material significantly increased time feeding (F2,351 = 9.58, p < 0.001), and decreased rates of noncontact aggression (F2,351 = 3.69, p = 0.03), and regurgitation and reingestion (F2,353 = 4.70, p = 0.01). Regurgitation and reingestion were never observed during the condition when forage material was provided daily. When forage material was provided, time spent feeding was similar across gorillas, compared to a disproportionately greater amount of time spent feeding by the dominant individual when forage material was absent. Providing forage material in addition to the regular diet likely created more opportunities for equitable feeding for the subordinate gorillas. FGM concentrations did not vary based on the presence or type of forage material available and, instead, likely reflected group social dynamics. In general, alfalfa and mulberry had similar impacts on behavior, indicating that alfalfa can be an adequate behavioral substitute during times when browse is less readily available for gorillas housed in seasonally variable climates.

Welfare impacts of the illegal wildlife trade in a cohort of confiscated greater slow lorises, Nycticebus coucang.

Illegal harvesting and trade are major forces behind population declines of wild slow lorises (genus Nycticebus). The impacts of the wildlife trade on individual slow lorises have not been as well described. In this article, we describe quantitatively the consequences of the wildlife trade for 77 greater slow lorises, N. coucang, who were confiscated en masse and brought to Cikananga Wildlife Center in Indonesia. Medical records indicated that in total, 28.6% of the slow lorises died within the first 6 months, mostly due to traumatic injury, and all the infants died. The greatest sources of morbidity were external wounds (33.1% of 166 total medical events) and dental problems (19.3%). Of the surviving individuals, 25.4% displayed abnormal behavior. Behavioral observations indicated that healthy adults (n = 3) spent 48.2% of their active period performing stereotypies. These data illustrate the physical and behavioral impacts of the illegal wildlife trade on the welfare of slow lorises. We suggest that sharing these individual stories may help generate empathy and educate the public about the impacts of the exotic companion-animal (pet) trade on nonhuman animal welfare.

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.

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.

The effectiveness of indigestible markers for identifying individual animal feces and their prevalence of use in North American zoos.

Techniques for analyzing hormone metabolites in animal excreta have created many opportunities for noninvasive monitoring of health, reproduction, and welfare in zoo animals, but can be difficult to implement when individual samples are not readily identifiable in animal groups. A common approach to this problem is to feed animals an indigestible marker that subsequently appears in feces, but there has been little systematic research on the use of such "fecal markers." First, we used an online survey to assess the prevalence of fecal marker use in North American zoological institutions. Second, we conducted a series of experimental tests utilizing commonly employed fecal markers in a variety of typical zoo taxa to determine the: (1) effectiveness of several markers to accurately distinguish samples in a variety of species, (2) minimum quantity of marker needed for detection, and (3) length of time between ingestion and detection in the feces. The majority of the 45 institutions that completed the survey reported using fecal markers with their collections. The survey also revealed that the most frequently used markers are seeds/grains and food colorants, with the former generally used in Carnivora and the latter in Primates. Our experimental data confirmed the success of these taxa/marker combinations and also revealed that food colorants function as markers in a variety of avian, reptilian, and mammalian species. Our data describe successful fecal markers for a wide variety of zoo taxa and should, therefore, be useful for zoological managers and researchers needing to employ fecal markers in future investigations.

Examining deep litter as environmental enrichment for a family group of Wolf's guenons, Cercopithecus wolfi.

Manipulable substrates promote species-typical behavior and decrease abnormal behavior in a variety of primate species. However, the effects of providing litter to arboreal primates are not as well studied, and there is little information specifically concerning enrichment for guenons. To inform the captive management of an under-studied species, we evaluated deep litter substrate as environmental enrichment for a family group of Wolf's guenons, Cercopithecus wolfi. We expected it to promote species-typical behavior and to act as an intervention by reducing aggressive behaviors targeted toward a juvenile group member by his parents. We compared the guenons' behavior during baseline periods in which normal husbandry routines were followed to periods when the entire floor of their enclosure was covered with 30 cm of straw or wood wool. We then evaluated the group's preference between litters by comparing their relative use. The guenons spent more time feeding and were more active during both litter conditions, but relative to their respective baselines, they spent more time examining straw and less time examining wood wool. Straw, but not wood wool, promoted some affiliative behavior as well as greater tolerance of the juvenile's social proximity to others. However, the addition of deep litter did not ameliorate patterns of agonistic behavior among our subjects. Our results suggest that straw conferred greater behavioral benefits than wood wool as a deep litter substrate for this guenon group and may constitute a form of environmental enrichment for this species.