Use of passive radio frequency identification technologies to monitor nest usage in the northern carmine bee-eater (Merops n. nubicus).

The use of radio frequency identification (RFID) technology is common in animal-monitoring applications in the wild and in zoological and agricultural settings. RFID is used to track animals and to collect information about movements and other behaviors, as well as to automate or improve husbandry. Disney's Animal Kingdom® uses passive RFID technology to monitor nest usage by a breeding colony of northern carmine bee-eaters. We implemented RFID technologies in various equipment configurations, initially deploying low-frequency (LF) 125 kHz RFID and later changing to high-frequency (HF) 13.56 MHz RFID technology, to monitor breeding behavior in the flock. We installed antennas connected to RFID readers at the entrances of nest tunnels to detect RFID transponders attached to leg bands as birds entered and exited tunnels. Both LF-RFID and HF-RFID systems allowed the characterization of nest visitation, including the timing of nest activity, breeding pair formation, identification of egg-laying females, participation by nonresidents, and detection of nest disruptions. However, we collected a substantially larger volume of data using the increased bandwidth and polling speed inherent with HF-RFID, which permitted tag capture of multiple birds simultaneously and resulted in fewer missed nest visits in comparison to LF-RFID. Herein, we describe the evolution of the RFID setups used to monitor nest usage for more than 7 years, the types of data that can be gained using RFID at nests, and how we used these data to gain insights into carmine bee-eater breeding behavior and improve husbandry.

Seasonal dynamics of agonistic behavior and hormones in an ex situ all-male colony of large flying foxes.

Large flying foxes (Pteropus vampyrus) are a socially complex species. In situ colonies typically comprise thousands of individuals in small harems of one male to many females. In ex situ environments, all-male colonies are becoming more common due to a surplus of males in the population. There is limited information describing the hormonal and behavioral patterns of all-male colonies during the breeding season. We assessed seasonal changes in hormones and behavior in an all-male colony of 12 large flying foxes at Disney's Animal Kingdom® . We validated hormone assays using morning urine and fecal samples to assess seasonal changes in excreted immunoreactive testosterone and glucocorticoid metabolites. We collected behavior data using an all-occurrence method, recording agonistic behaviors related to territorial defense (hooking, biting, wing flexing, vocalizing, and wrestling), and sexual behavior (mounting and frontal grabbing). Results indicated that (i) we could reliably measure testosterone and glucocorticoid metabolites concentrations from fecal and urine samples collected from individual bats; (ii) there were distinct relationships between changes in levels of agonism and hormone concentrations throughout the year; and (iii) three agonistic behaviors (chasing, wrestling, and open-mouth threat) peaked prior to the increase in testosterone and glucocorticoid hormones measured during the breeding season. These three behaviors could potentially be used as early indicators to signal the onset of the breeding season and allow time to implement ex situ management changes to reduce the incidence of agonism between individuals.

Applying behavior-analytic methodology to the science and practice of environmental enrichment in zoos and aquariums.

Environmental enrichment in zoos and aquariums is often evaluated at two overlapping levels: published research and day-to-day institutional record keeping. Several authors have discussed ongoing challenges with small sample sizes in between-groups zoological research and have cautioned against the inappropriate use of inferential statistics (Shepherdson, , International Zoo Yearbook, 38, 118-124; Shepherdson, Lewis, Carlstead, Bauman, & Perrin, Applied Animal Behaviour Science, 147, 298-277; Swaisgood, , Applied Animal Behaviour Science, 102, 139-162; Swaisgood & Shepherdson, , Zoo Biology, 24, 499-518). Multi-institutional studies are the typically-prescribed solution, but these are expensive and difficult to carry out. Kuhar ( Zoo Biology, 25, 339-352) provided a reminder that inferential statistics are only necessary when one wishes to draw general conclusions at the population level. Because welfare is assessed at the level of the individual animal, we argue that evaluations of enrichment efficacy are often instances in which inferential statistics may be neither necessary nor appropriate. In recent years, there have been calls for the application of behavior-analytic techniques to zoo animal behavior management, including environmental enrichment (e.g., Bloomsmith, Marr, & Maple, , Applied Animal Behaviour Science, 102, 205-222; Tarou & Bashaw, , Applied Animal Behaviour Science, 102, 189-204). Single-subject (also called single-case, or small-n) designs provide a means of designing evaluations of enrichment efficacy based on an individual's behavior. We discuss how these designs might apply to research and practice goals at zoos and aquariums, contrast them with standard practices in the field, and give examples of how each could be successfully applied in a zoo or aquarium setting.

A turtle cognition research demonstration enhances visitor engagement and keeper-animal relationships.

Environmental enrichment techniques present animals with cognitive challenges while providing them opportunities to make choices and exert control over their environment. In this way, cognitive research and training is enriching to animals and can be used as a form of enrichment in zoos and aquariums. Cognitive research demonstrations also provide an opportunity to enhance visitor experience, as well as foster interactions between animals and keepers. We investigated how cognitive research sessions involving eastern box turtles (Terrapene carolina carolina) at Disney's Animal Kingdom® impacted both the rate of visitors coming to the exhibit and the amount of time they spent engaged. Further, we used a questionnaire to assess the impact of keeper participation in these sessions on their relationships with and perceptions of the turtles. While visitation rate to the exhibit was not impacted, cognitive research sessions held visitor attention for longer than keeper interpretation or at times during which no keepers or researchers were present. We also found that keepers that had worked with the turtles for longer and keepers that regularly participated in cognitive research sessions reported stronger bonds with the turtles. Our research suggests that use of cognitive research and training demonstrations for guest viewing in zoos and aquariums may enhance visitor learning opportunities by increasing the amount of time they spend at the exhibit. Our study also provides evidence that participation in such demonstrations by zoo and aquarium professionals can be related to improved keeper-animal bonds, potentially resulting in better husbandry and enhanced animal welfare.

Plumage variation and social partner choice in the greater flamingo (Phoenicopterus roseus).

There is evidence that plumage coloration is related to mate choice in several different bird species. However, the relationship between plumage coloration to mate or other social partner choice has rarely been investigated in flamingos. This is important to study because we know plumage coloration can be an indicator of welfare. We assessed plumage color score in relation to sex, age, and social partner choice over a 9-month period in a flock of 34 adult greater flamingos (Phoenicopterus roseus) living at Disney's Animal Kingdom® . When looking at primary social partners, redder males were more likely to have primary social partners compared to less red males. In addition, primary social partners tended to have similar color scores to each other. These findings provide insight into one factor that might influence social partner choice in greater flamingos living in ex situ situations. Future studies should investigate how these results relate to reproductive success as part of ex situ management. Zoo Biol. 35:409-414, 2016. © 2016 Wiley Periodicals, Inc.

The Days and Nights of Zoo Elephants: Using Epidemiology to Better Understand Stereotypic Behavior of African Elephants (Loxodonta africana) and Asian Elephants (Elephas maximus) in North American Zoos.

Stereotypic behavior is an important indicator of compromised welfare. Zoo elephants are documented to perform stereotypic behavior, but the factors that contribute to performance have not been systematically assessed. We collected behavioral data on 89 elephants (47 African [Loxodonta africana], 42 Asian [Elephas maximus]) at 39 North American zoos during the summer and winter. Elephants were videoed for a median of 12 daytime hours per season. A subset of 32 elephants (19 African, 13 Asian) was also observed live for a median of 10.5 nighttime hours. Percentages of visible behavior scans were calculated from five minute instantaneous samples. Stereotypic behavior was the second most commonly performed behavior (after feeding), making up 15.5% of observations during the daytime and 24.8% at nighttime. Negative binomial regression models fitted with generalized estimating equations were used to determine which social, housing, management, life history, and demographic variables were associated with daytime and nighttime stereotypic behavior rates. Species was a significant risk factor in both models, with Asian elephants at greater risk (daytime: p<0.001, Risk Ratio = 4.087; nighttime: p<0.001, Risk Ratio = 8.015). For both species, spending time housed separately (p<0.001, Risk Ratio = 1.009), and having experienced inter-zoo transfers (p<0.001, Risk Ratio = 1.175), increased the risk of performing higher rates of stereotypy during the day, while spending more time with juvenile elephants (p<0.001, Risk Ratio = 0.985), and engaging with zoo staff reduced this risk (p = 0.018, Risk Ratio = 0.988). At night, spending more time in environments with both indoor and outdoor areas (p = 0.013, Risk Ratio = 0.987) and in larger social groups (p = 0.039, Risk Ratio = 0.752) corresponded with reduced risk of performing higher rates of stereotypy, while having experienced inter-zoo transfers (p = 0.033, Risk Ratio = 1.115) increased this risk. Overall, our results indicate that factors related to the social environment are most influential in predicting elephant stereotypic behavior rates.

Application of video recording technology to improve husbandry and reproduction in the carmine bee-eater (Merops n. nubicus).

Incorporating technology with research is becoming increasingly important to enhance animal welfare in zoological settings. Video technology is used in the management of avian populations to facilitate efficient information collection on aspects of avian reproduction that are impractical or impossible to obtain through direct observation. Disney's Animal Kingdom(®) maintains a successful breeding colony of Northern carmine bee-eaters. This African species is a cavity nester, making their nesting behavior difficult to study and manage in an ex situ setting. After initial research focused on developing a suitable nesting environment, our goal was to continue developing methods to improve reproductive success and increase likelihood of chicks fledging. We installed infrared bullet cameras in five nest boxes and connected them to a digital video recording system, with data recorded continuously through the breeding season. We then scored and summarized nesting behaviors. Using remote video methods of observation provided much insight into the behavior of the birds in the colony's nest boxes. We observed aggression between birds during the egg-laying period, and therefore immediately removed all of the eggs for artificial incubation which completely eliminated egg breakage. We also used observations of adult feeding behavior to refine chick hand-rearing diet and practices. Although many video recording configurations have been summarized and evaluated in various reviews, we found success with the digital video recorder and infrared cameras described here. Applying emerging technologies to cavity nesting avian species is a necessary addition to improving management in and sustainability of zoo avian populations.

Reproductive and parental behavior in Taveta golden weavers (Ploceus castaneiceps).

Taveta golden weavers are popular in zoos, but little has been published on their reproduction, social behavior, or other aspects of their management. At Disney's Animal Kingdom® , we have had great success with our breeding program and house a large flock in our mixed-species walk-through Africa aviary and smaller groups in the off-exhibit Avian Research Center. We conducted observations on both groups in order to document behavioral differences between the groups living under differing management conditions. Data on which individuals were inside, on or near focal nests were collected using a 30-s scan samples. Scan data were analyzed using a two-factor ANOVA, with aviary location and nest contents as the factors. We found that, in both aviary locations, females spent more time inside and on the nests than males did. As expected, females spent more time inside the nests containing eggs and more time on the nests containing chicks, likely due to incubation and chick-feeding demands, respectively. Interestingly, we found that females spent significantly more time inside their nests and males spent more time near their nests in the Africa aviary than in ARC. Despite Africa aviary's higher nest attendance, a higher proportion of nests fledged chicks in ARC (72% vs. 41%). These data are consistent with findings in wild sociable weavers [Spottiswoode, 2007. Oecologia 154: 589-600]. Future work with zoo-housed populations of weavers could help shed light on this phenomenon, which is not yet well understood. A better understanding of the consequences of different group sizes and housing conditions could have important implications for how Taveta weavers are managed.

Impact of visual context on public perceptions of non-human primate performers.

Prior research has shown that the use of apes, specifically chimpanzees, as performers in the media negatively impacts public attitudes of their conservation status and desirability as a pet, yet it is unclear whether these findings generalize to other non-human primates (specifically non-ape species). We evaluated the impact of viewing an image of a monkey or prosimian in an anthropomorphic or naturalistic setting, either in contact with or in the absence of a human. Viewing the primate in an anthropomorphic setting while in contact with a person significantly increased their desirability as a pet, which also correlated with increased likelihood of believing the animal was not endangered. The majority of viewers felt that the primates in all tested images were "nervous." When shown in contact with a human, viewers felt they were "sad" and "scared", while also being less "funny." Our findings highlight the potential broader implications of the use of non-human primate performers by the entertainment industry.

The effect of changes in group composition on social dynamics in marabou storks (Leptoptilos crumeniferus).

The reduction of aggressive behaviors can be a concern whenever animals are socially housed, but for some species, such as marabou storks, zoos are still unsure of the best management strategies. To learn more about marabou behavior and how dynamics change as group composition changes, we monitored a total of 3.5 marabous as individuals were added and removed over 2 years. We found that, in mixed-sex groups, males were more likely to be the initiators of displacements and females were more likely to be the recipients. Most contact aggression was intra-sexual, and females engaged in contact aggression more often than males. The highest levels of aggression were seen in our all-female groups, which was unexpected given the high number of male attacks on females reported in zoos. Because females were being added and removed but our males remained the same throughout the study, we are unsure whether this was due to a higher level of instability among females or a true sex difference; regardless, these data highlight the need to monitor aggression even within all female stork groups. Overall, we observed low levels of inter-sexual aggression, suggesting that some fatal attacks may be due, in part, to non-social factors, such as enclosure design. Social birds like marabous may benefit from the same type of group management approach that is commonly utilized with other social taxa. A two-pronged approach of observation and management of marabou social dynamics and some modification of their enclosure structure may limit injurious aggression in the future.

The use of visual barriers to reduce aggression among a group of marabou storks (Leptoptilos crumeniferus).

Marabou storks are one of the most commonly held birds in zoos, but the captive population faces challenges related to high mortality. One of the most common causes of death among captive marabou storks is conspecific aggression. There is a pressing need to better understand how to manage this aggression. One method that has been used successfully to reduce aggression in other species is the addition of visual barriers to the enclosure, though there are no published studies on their effect on storks. We studied the behavioral changes in a group of 2.2 marabou storks following the addition of two shade cloth barriers to their enclosure; we documented all occurrences of aggressive behavior, as well as time spent proximate to the barriers (or the space between barrier posts, when the shade cloth was removed) and time spent using the barriers to block the view of other storks. The presence of the shade cloth did not change the amount of time storks spent proximate to the barriers, nor did they spend more than 2% of their time using the barriers to block other storks, but the presence of the barriers significantly reduced displacement activity. Barriers may afford captive marabou storks an important means of escaping conflict, as flight-restriction and housing in an enclosure can limit their opportunities to give a signal of retreat or submission.

Identifying parentage using molecular markers: improving accuracy of studbook records for a captive flock of marabou storks (Leptoptilos crumeniferus).

Extra-pair copulations (EPCs) leading to extra-pair fertilization (EPF) are common in avian mating systems, despite the prevalence of observed social monogamy in many species. Colonially breeding birds are interesting species to investigate the prevalence of EPCs and EPF because they show nesting habits including close proximity of nest sites and sexual partners, which are proposed to promote alternative reproductive tactics. Endemic to Africa, the colonial marabou stork (Leptoptilos crumeniferus) is one of the most commonly held avian species in North American zoos. The aims of this study were to use genetic information to verify parentage in a population of marabou stork housed at Disney's Animal Kingdom® based on five microsatellite loci and to investigate reproductive behavior. We compared genetic analyses of parents and offspring to studbook data collected through behavioral observations of parental behavior at the nest. Using genetic analyses to reconstruct the pedigree of the marabou stork flock using the program COLONY led to improvement of studbook records by determining parentage of an individual that had previously unknown parentage, and identified one individual that had a sire that differed genetically from studbook records. An important contribution of our analyses was the identification and verification of the most likely parents for offspring hatched in this colony and improving incorrect or undocumented parentage in the studbook. Additionally, the colonial nature of this species makes it difficult to observe and understand reproductive behavior. Gaining better understanding of the mating system of a species is essential for successful breeding and captive management.

Behavioral analysis of tiger night housing practices.

The systematic evaluation of changes in animal management practices is critical to ensuring the best possible welfare. Here, we examined the behavioral impacts of intermittently housing our six adult female tigers, who have been housed socially for much of their lives, individually overnight to allow for specialized care required by their advancing age. We looked for behavioral changes indicative of both positive and negative changes in welfare by monitoring time spent asleep, sleeping position, body position while awake, as well as pacing, door pounding, self-grooming, roaring, and chuffing while housed socially as compared to individually overnight. Housing condition did not affect time spent asleep, sleeping positions assumed or the more preferred body positions while awake. Further, pacing, door-pounding, and roaring were infrequent and not altered by housing condition. Self-grooming did increase when housed individually but no evidence of over-grooming was present and chuffing, a close proximity social vocalization, was more likely to occur when socially housed. Taken together, these findings support the notion that transitioning to individual housing as needed is a viable option for managing cats accustomed to being maintained in a social group.

Relational responding by eastern box turtles (Terrapene carolina) in a series of color discrimination tasks.

Prior work with chelonians has demonstrated their capacity for successful performance in cognitive tasks, including those requiring color discrimination. Here, we sought to expand on historical research and determine whether eastern box turtles (Terrapene carolina) are capable of not only making simple color discriminations but also whether they can demonstrate abstract concept formation evidenced by using a relational response rule in their discrimination performance. Two eastern box turtles were rapidly and successfully trained on a black-and-white two-choice discrimination task using painted paddles and food reinforcement. After mastery, a medium gray paddle was added as a choice stimulus and turtle "Flippy" was reinforced for selecting the darker of the 2 stimuli presented in each trial, and turtle "Mario" was reinforced for selecting the lighter of the paddles presented. Nonreinforced probe trials incorporating light and dark gray stimuli paired with all other color options were then added to each session to test the turtles' ability to use the relationship between choice stimuli to guide responding. The turtles successfully selected the paddles corresponding to their assigned relational response rule of "darker" or "lighter" at a level significantly above that predicted by chance. The turtles then demonstrated immediate generalization of their relational rule in testing with a novel array of blue paddles. Finally, the turtles continued to use their relational rule when presented with a novel array of green paddles in a traditional transposition task. Together, these findings support the capacity for higher order cognitive functioning in chelonians beyond that previously described.

Attempted integration of multiple species of turaco into a mixed-species aviary.

Mixed-species exhibits offer a variety of benefits but can be challenging to maintain due to difficulty in managing interspecific interactions. This is particularly true when little has been documented on the behavior of the species being mixed. This was the case when we attempted to house three species of turaco (family: Musophagidae) together with other species in a walk-through aviary. To learn more about the behavior of great blue turacos, violaceous turacos, and white-bellied gray go-away birds, we supplemented opportunistic keeper observations with systematic data collection on their behavior, location, distance from other birds, and visibility to visitors. Keepers reported high levels of aggression among turacos, usually initiated by a go-away bird or a violaceous turaco. Most aggression occurred during feedings or when pairs were defending nest sites. Attempts to reduce aggression by temporarily removing birds to holding areas and reintroducing them days later were ineffective. Systematic data collection revealed increased social behavior, including aggression, during breeding season in the violaceous turacos, as well as greater location fidelity. These behavioral cues may be useful in predicting breeding behavior in the future. Ultimately, we were only able to house three species of turaco together for a short time, and prohibitively high levels of conflict occurred when pairs were breeding. We conclude that mixing these three turaco species is challenging and may not be the most appropriate housing situation for them, particularly during breeding season. However, changes in turaco species composition, sex composition, or exhibit design may result in more compatible mixed-turaco species groups.

Hand-rearing and sex determination tool for the Taveta golden weaver (Ploceus castaneiceps).

Improvements in the ability to hand-rear birds in captivity have aided zoological institutions in the sustainable management of these species, and have provided opportunities to examine their physical growth in varying conditions. Monitoring the weight gain and development of chicks is an important aspect of developing a hand-rearing protocol. In this paper we provide the institutional history for a colonial species of passerine, the Taveta golden weaver, at Disney's Animal Kingdom®, in order to demonstrate the methods of establishing a successful breeding program which largely incorporates hand-rearing in management of the population. We also tested if we could accurately predict sex of chicks using weights collected on Day 14 during the hand-rearing process. Using this tool, we were able to correctly determine sex before fledging in more than 83% of chicks. Early sex determination is important in captive species for genetic management and husbandry purposes. While genetic sexing can be expensive, we found that using growth curves to determine sex can be a reliable and cost-effective tool for population management of a colonial passerine.

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.

Novel survey method finds dramatic decline of wild cotton-top tamarin population.

The cotton-top tamarin (Saguinus oedipus) is a critically endangered primate, endemic to the tropical forests of Colombia. Population monitoring is essential to evaluate the success of conservation efforts, yet standard survey methods are ineffective because animals flee silently before they are seen. We developed a novel technique that combines the use of playbacks of territorial vocalizations with traditional transect surveys. We used remote sensing to identify potential habitat within the species' historic range, and visited the 27% that we could survey safely. Of this, only 99 km(2) was extant forest, containing an estimated 2,045 animals (95% confidence interval 1,587-2,634). Assuming comparable densities in non-surveyed areas, approximately 7,394 wild cotton-top tamarins remain in Colombia. With 20-30,000 animals exported to the United States in the late 1960s, this must represent a precipitous decline. Habitat destruction and capture for the illegal pet trade are ongoing. Urgent conservation measures are required to prevent extinction in the wild.

GPS assessment of the use of exhibit space and resources by African elephants (Loxodonta africana).

In public discussions of animal rights and welfare, we as members and proponents of zoological institutions often face significant challenges addressing the concerns of our detractors due to an unfortunate deficiency in systematically collected and published data on the animals in our collections. In the case of elephants, there has been a paucity of information describing their use of space within captive environments. Here, using collar-mounted GPS recording devices, we documented the use of exhibit space and resources by a herd of five adult female African elephants (Loxodonta africana) housed at Disney's Animal Kingdom((R)). We found that dominant animals within the herd used a greater percentage of the available space and subordinate females avoided narrow or enclosed regions of the enclosure that we termed "restricted flow areas." In their use of other resources, dominant females demonstrated increased occupation of the watering hole over subordinate females, but all females demonstrated relatively equivalent use of the mud wallow. Overall, our results provide preliminary evidence that position within the dominancy hierarchy impacts the percentage of space occupied in a captive setting and may contribute to resource accessibility. These findings can be applied to future decisions on exhibit design and resource distribution for this species.