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.

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.

What Is the Future for Zoos and Aquariums?

Animal welfare concerns have plagued the professional zoo and aquarium field for decades. Societal differences remain concerning the well-being of animals, but it appears a shift is emerging. Scientific studies of animal welfare have dramatically increased, establishing that many previous concerns were not misguided public empathy or anthropomorphism. As a result, both zoo and aquarium animal welfare policy and science are now at the center of attention within the world's professional zoos and aquariums. It is now possible to view a future that embraces the well-being of individual captive exotic animals, as well as that of their species, and one in which professional zoos and aquariums are dedicated equally to advancing both. Though the ethics of keeping exotic animals and animals from the wild in captivity are still a contentious subject both outside and even within the profession, this study argues. We argue that this path forward will substantially improve most zoo and aquarium animals' welfare and could significantly reduce societal concerns. If animal welfare science and policy are strongly rooted in compassion and embedded in robust accreditation systems, the basic zoo/aquarium paradigm will move toward a more thoughtful approach to the interface between visitors and animals. It starts with a fundamental commitment to the welfare of individual animals.

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.

AN EVALUATION OF INFRARED THERMOGRAPHY FOR DETECTION OF BUMBLEFOOT (PODODERMATITIS) IN PENGUINS.

The objective of this study was to evaluate infrared thermography as a noninvasive screening tool for detection of pododermatitis during the developing and active stages of disease in three species of penguins: king penguin (Aptenodytes patagonicus) , macaroni penguin (Eudyptes chrysolophus), and rockhopper penguin (Eudyptes chrysocome). In total, 67 penguins were examined every 3 mo over a 15-mo period. At each exam, bumblefoot lesions were characterized and measured, and a timed series of thermal images were collected over a 4-min period. Three different methods were compared for analysis of thermograms. Feet with active lesions that compromise the surface of the foot were compared to feet with inactive lesions and no lesions. The hypothesis was that feet with active lesions would have warmer surface temperatures than the other conditions. Analysis of the data showed that although feet with active bumblefoot lesions are warmer than feet with inactive or no lesions, the variability seen in each individual penguin from one exam day to the next and the overlap seen between temperatures from each condition made thermal imaging an unreliable tool for detection of bumblefoot in the species studied.

Picture object recognition in an American black bear (Ursus americanus).

Many animals have been tested for conceptual discriminations using two-dimensional images as stimuli, and many of these species appear to transfer knowledge from 2D images to analogous real life objects. We tested an American black bear for picture-object recognition using a two alternative forced choice task. She was presented with four unique sets of objects and corresponding pictures. The bear showed generalization from both objects to pictures and pictures to objects; however, her transfer was superior when transferring from real objects to pictures, suggesting that bears can recognize visual features from real objects within photographic images during discriminations.

A Universal Animal Welfare Framework for Zoos.

The Detroit Zoological Society's (DZS) Center for Zoo Animal Welfare (CZAW) was created to advance the science and policy of the welfare of exotic nonhuman animals in captivity. This important part of the DZS mission is achieved through assessments of, and research on, the welfare of animals in zoos; by recognizing extraordinary achievement in the advancement of animal welfare; by widely sharing knowledge through a bibliographic resource center; by conducting professional training for animal care staff; and by convening important discussions in the form of international symposia. This special issue of the Journal of Applied Animal Welfare Science features selected papers from the most recent international CZAW symposium held at the Detroit Zoo in November 2014, as well as a universal framework for zoo animal welfare developed by the DZS.

MICA variant promotes allosensitization after kidney transplantation.

MHC class I-related chain A (MICA) antigens are surface glycoproteins strongly implicated in innate immunity, and the MICA gene is highly polymorphic. Clinical observations suggest a role for donor MICA antigens expressed on transplant endothelial cells in the alloimmune response, but the effect of MICA genotype is not well understood. Here, we investigated the immunologic effect of the A5.1 mutation, related to the common MICA*008 allele. Compared with wild-type endothelial cells (ECs), homozygosity for MICA A5.1 associated with an endothelial phenotype characterized by 7- to 10-fold higher levels of MICA mRNA and MICA proteins at the cell surface, as well as exclusive release in exosomes instead of enzymatic cleavage. Mechanistically, we did not detect quantitative changes in regulatory microRNAs. Functionally, A5.1 ECs enhanced NKG2D interaction and natural killer cell activation, promoting NKG2D-dependent lysis of ECs. In kidney transplant recipients, polyreactive anti-MICA sera bound preferentially to ECs from MICA A5.1 donors, suggesting that MICA*008(A5.1) molecules are the preferential antigenic determinants on ECs of grafts. Furthermore, the incidence of MICA A5.1 mismatch revealed a statistically significant association between donor MICA A5.1 and both anti-MICA sensitization and increased proteinuria in kidney recipients. Taken together, these results identify the A5.1 mutation as an immunodominant factor and a potential risk factor for transplant survival.

Lion, ungulate, and visitor reactions to playbacks of lion roars at Zoo Atlanta.

Felids in captivity are often inactive and elusive in zoos, leading to a frustrating visitor experience. Eight roars were recorded from an adult male lion and played back over speakers as auditory enrichment to benefit the lions while simultaneously enhancing the zoo visitor experience. In addition, ungulates in an adjacent exhibit were observed to ensure that the novel location and increased frequency of roars did not lead to a stress or fear response. The male lion in this study roared more in the playback phase than in the baseline phases while not increasing any behaviors that would indicate compromised welfare. In addition, zoo visitors remained at the lion exhibit longer during playback. The nearby ungulates never exhibited any reactions stronger than orienting to playbacks, identical to their reactions to live roars. Therefore, naturalistic playbacks of lion roars are a potential form of auditory enrichment that leads to more instances of live lion roars and enhances the visitor experience without increasing the stress levels of nearby ungulates or the lion themselves, who might interpret the roar as that of an intruder.