Feeding enrichment and stereotypic behavior in spectacled bears

The effect of feeding enrichment on the behavior of three spectacled bears (Tremarctos ornatus) was investigated in a large, complex zoo exhibit. Feeding enrichment significantly extended the time bears spent foraging, but no delayed effect on other behaviors was found. The frequency of stereotypic behaviors performed by an old female and a young adult male was not influenced outside the morning feeding period. As yet, a young adult female has not developed stereotypic behaviors. In the old female, the frequency of stereotypic behavior was inversely correlated with the frequency of resting. In the male, the frequency of stereotypic behavior was inversely correlated with the frequency of social interactions with either female. Zoo Biol 18:363–371, 1999. © 1999 Wiley‐Liss, Inc.     

Stereotypic behavior and fecal cortisol level in captive giant pandas in relation to environmental enrichment

Stereotypic behavior is exhibited by a wide range of captive animals. Its association with hormones, especially elevated cortisol level and lack of naturalistic stimuli in the environment, has been little studied. This study hypothesizes that stereotypic behavior is caused by stress due to lack of appropriate, naturalistic stimuli in the environment. Using four adult pandas (Ailuropoda melanoleuca) in the Beijing Zoo from March–July in 2003, we tested the following predictions: 1) stereotypic behavior and fecal cortisol level will not change associated with the progress of reproductive state; 2) there is a positive correlation between the occurrence of stereotypic behavior and fecal cortisol level; and 3) environmental enrichment by adding a naturalistic stimulus will reduce both stereotypic behavior and fecal cortisol level. We did not find any significant differences in the occurrence of stereotypic behavior and fecal cortisol level but did find a significant difference in the total time engaged in displaying the stereotypic behavior among the three estrous periods. The level of stereotypic behavior was correlated with elevated fecal cortisol level. Enrichment simply by adding a naturalistic stimulus did not show significant effects on stereotypic behavior, or on fecal cortisol level. Our results supported the second prediction, but did not completely support the first and the third ones perhaps because of the small sample size. Additionally, our results showed that stereotypic behavior might be a response to a heightened level of cortisol. Zoo Biol 0:1–15, 2006. © 2006 Wiley‐Liss, Inc.     

Environmental influences on stereotypy and the activity budget of Indian leopards (Panthera pardus) in four zoos in Southern India

To eliminate abnormal behaviors in leopards (Panthera pardus), such as stereotypic pacing, by utilizing environmental enrichment techniques, a proper understanding of their behavior in captive environments is required. Hence there is a need for animal welfare studies in Indian zoos. The activity budgets of 16 leopards were recorded across four southern Indian zoos: Thiruvananthapuram Zoo, Arignar Anna Zoological Park, Shri Chamarajendra Zoological Gardens, and the Guindy Children's Park. Of the 16 study animals, 14 were studied on‐exhibit on zoo holidays as well as on days with visitors present, and all 16 individuals were studied off‐exhibit on other days with visitors present. The 11 behaviors recorded were categorized into active, resting, and stereotypic behaviors. Leopards exhibited higher levels of activity in the on‐exhibit enclosures on days with no visitors. Feeding time influenced the behavioral repertoire of all 14 leopards studied on‐exhibit. Lower proportions of resting were exhibited during the hours before feeding. The proportion of active behaviors differed significantly across zoos. Stereotypic pacing levels were not influenced by the presence of visitors or by feeding time, but was significantly influenced by enclosure features. Higher levels of stereotypic pacing were exhibited in off‐exhibit than on‐exhibit enclosures. Our study shows that the behavior of captive leopards is influenced by enclosure type, feeding regime, and the presence of visitors. Zoo Biol 21:585–595, 2002. © 2002 Wiley‐Liss, Inc.     

Technology at the Zoo: The Influence of a Touchscreen Computer on Orangutans and Zoo Visitors

A computer‐controlled touchscreen apparatus (hereafter referred to as “touchscreen”) in the orangutan exhibit at Zoo Atlanta provides enrichment to the animals and allows cognitive research to take place on exhibit. This study investigated the impact of the touchscreen on orangutan behavior and visibility, as well as its impact on zoo visitors. Despite previous research suggesting that providing a single computer system may negatively affect orangutan behavior, there was not a significant increase in aggression, stereotypic, or distress‐related behaviors following the activation of the on‐exhibit touchscreen. We also investigated the possibility that zoo visitors may be negatively affected by technology because it deviates from naturalism. However, we did not find a change in stay time or overall experience rating when the computer was turned on. This research was the first to assess visitor attitudes toward technology at the zoo, and we found that visitors report highly positive attitudes about technology for both animals and visitors. If subjects visited the exhibit when the computer was turned on, they more strongly agreed that orangutans benefit from interacting with computerized enrichment. This study is the first investigation of an on‐exhibit touchscreen in group‐housed apes; our findings of no negative effects on the animals or zoo visitors and positive attitudes toward technology suggest a significant value of this practice. Zoo Biol 31:27;–39, 2012. © 2011 Wiley Periodicals, Inc.     

BIAZA statistics guidelines: toward a common application of statistical tests for zoo research

Zoo research presents many statistical challenges, mostly arising from the need to work with small sample sizes. Efforts to overcome these often lead to the misuse of statistics including pseudoreplication, inappropriate pooling, assumption violation or excessive Type II errors because of using tests with low power to avoid assumption violation. To tackle these issues and make some general statistical recommendations for zoo researchers, the Research Group of the British and Irish Association of Zoos and Aquariums (BIAZA) conducted a workshop. Participants included zoo‐based researchers, university academics with zoo interests and three statistical experts. The result was a BIAZA publication Zoo Research Guidelines: Statistics for Typical Zoo Datasets (Plowman [ 2006 ] Zoo research guidelines: statistics for zoo datasets. London: BIAZA), which provides advice for zoo researchers on study design and analysis to ensure appropriate and rigorous use of statistics. The main recommendations are: (1) that many typical zoo investigations should be conducted as single case/small N randomized designs, analyzed with randomization tests, (2) that when comparing complete time budgets across conditions in behavioral studies, G tests and their derivatives are the most appropriate statistical tests and (3) that in studies involving multiple dependent and independent variables there are usually no satisfactory alternatives to traditional parametric tests and, despite some assumption violations, it is better to use these tests with careful interpretation, than to lose information through not testing at all. The BIAZA guidelines were recommended by American Association of Zoos and Aquariums (AZA) researchers at the AZA Annual Conference in Tampa, FL, September 2006, and are free to download from www.biaza.org.uk . Zoo Biol 27:226–233, 2008. © 2008 Wiley‐Liss, Inc.     

Comparison of several types of enrichment for captive felids

Enrichment can increase the complexity of the captive environment and possibly enhance captive animals' well‐being by stimulating active behaviors and reducing stereotypical behaviors commonly seen in zoo felids. In this study, three different enrichment items were added to outdoor enclosures of felids at the Montgomery Zoo to test their effects on activity levels and stereotypic pacing. Bones, frozen fish, and spices (cinnamon, chili powder, and cumin) were presented over a 3‐month period to six species of felids: cheetah, cougar, jaguar, lion, ocelot, and tiger. Proportion of time spent engaging in active behaviors and stereotypic pacing were compared before, during, and after treatments. All treatments resulted in a significant increase in activity level from baseline (bones: +15.59%; frozen fish: +35.7%; spices: +12.38%). Effects of enrichment items on activity levels were not sustained 7 days after removal. Proportion of time spent pacing significantly decreased during presentation of spices (?21.25%) and frozen fish (?26.58%), but not with the addition of bones. However, only the effect of frozen fish on stereotypic behavior was sustained 7 days after removal of the enrichment item. In conclusion, bones, spices, and frozen fish are inexpensive and easy‐to‐administer enrichment items that may be used to increase active behaviors of captive felids. Zoo Biol 26:371–381, 2007. © 2007 Wiley‐Liss, Inc.     

To hunt or not to hunt? A feeding enrichment experiment with captive large felids

It is often difficult to promote the successful performance of feeding behaviors in zoos, especially for carnivores. Feeding enrichment provides these opportunities and often improves behavioral indications of an animal's well‐being and the experience of the zoo visitor. The effectiveness of two different feeding enrichment techniques was evaluated on five subjects in two species of felids: African lions and Sumatran tigers. The activity budgets of each cat were compared before, during, and after enrichment, focusing on activity levels, frequency and variety of feeding behaviors, and occurrence of stereotypic behaviors. The presentation of live fish increased the variety and frequency of feeding behaviors, while presentation of horse leg bones increased the frequency of these behaviors. Fish reduced the tigers' stereotypic behavior from 60% of scans to 30% of scans on the day of presentation, and this change was maintained for 2 days following enrichment. Bone presentation also reduced stereotypic behavior and increased nonstereotypic activity in both species. Both of these techniques appear to have sustained effects on behavior lasting at least 2 days after presentation, which may indicate their ability to alter the animals' underlying activity patterns. Zoo Biol 22:189–198, 2003. © 2003 Wiley‐Liss, Inc.     

狒狒圈舍废弃栖杠的嗅觉丰容对圈养食肉动物行为的影响

单调的饲养环境是导致圈养食肉动物表现刻板行为的主要原因之一。为减少圈养动物刻板行为的发生,探索便于操作、经济且有效的丰容方式是动物饲养管理者面临的一个挑战。本研究以狒狒圈舍废弃栖杠作为嗅觉丰容材料,对北京动物园小型(9种)、中型(4种)和大型(7种)食肉动物进行嗅觉丰容实验。在非投喂时段,采用扫描动物取样和瞬时记录法,分别对28只动物在丰容前后的5种行为进行观察和比较分析。结果显示,小型和中型食肉动物在丰容后对旧设施的使用频次显著下降(小型：P=0.026;中型：P=0.038),而大型食肉动物无显著变化(P> 0.05)。仅小型食肉动物的刻板性走动、休息和观望行为频次显著下降(走动：P=0.023;休息：P=0.023;观望：P=0.017),其他类群的各类行为均无显著变化(P> 0.05)。同时,丰容后小型食肉动物的行为多样性指数显著降低(P=0.008),主要表现为动物花费较多的时间探究新的丰容设施;中型和大型食肉动物的行为多样性指数变化不显著。结果表明,使用带有狒狒身体气味的栖杠进行嗅觉丰容,仅对小型食肉动物有效,对中型和大型食肉动物无效。研究认为,以其他动物圈舍的...     

When zoo visitors “connect” with a zoo animal,what does that mean?

Connection with a zoo animal may increase conservation‐mindedness in zoo visitors, potentially resulting in conservation‐oriented behavior change. No research has attempted to establish what this “connection” actually means. Visitors (N = 85) to Melbourne Zoo were asked to name the animal with which they most connected, the extent to which they connected with it, and to qualitatively describe what it meant to connect with that animal. Many (but not all) participants connected with charismatic megafauna: primate, great ape, large carnivore, or large herbivore. Qualitative analysis revealed five common themes in the meaning of connection: Appreciation, Attribution, Inspires Emotions, Interaction, and Proximity. Overall connection level was significantly correlated with perceptions of conservation caring for the chosen species. Future research should aim to determine what factors affect a zoo visitor's connection level, which could impact attitudes and behaviors toward conservation.     

A comparative study of litter size and sex composition in a large dataset of callitrichine monkeys

In many birds and mammals, the size and sex composition of litters can have important downstream effects for individual offspring. Primates are model organisms for questions of cooperation and conflict, but the factors shaping interactions among same‐age siblings have been less‐studied in primates because most species bear single young. However, callitrichines (marmosets, tamarins, and lion tamarins) frequently bear litters of two or more, thereby providing the opportunity to ask whether variation in the size and sex composition of litters affects development, survival, and reproduction. To investigate these questions, we compiled a large dataset of nine species of callitrichines (n = 27,080 individuals; Callithrix geoffroyi, Callithrix jacchus, Cebuella pygmaea, Saguinus imperator, Saguinus oedipus, Leontopithecus chrysomelas, Leontopithecus chrysopygus, Leontopithecus rosalia, and Callimico goeldii) from zoo and laboratory populations spanning 80 years (1938–2018). Through this comparative approach, we found several lines of evidence that litter size and sex composition may impact fitness. Singletons have higher survivorship than litter‐born peers and they significantly outperform litter‐born individuals on two measures of reproductive performance. Further, for some species, individuals born in a mixed‐sex litter outperform isosexually‐born individuals (i.e., those born in all‐male or all‐female litters), suggesting that same‐sex competition may limit reproductive performance. We also document several interesting demographic trends. All but one species (C. pygmaea) has a male‐biased birth sex ratio with higher survivorship from birth to sexual maturity among females (although this was significant in only two species). Isosexual litters occurred at the expected frequency (with one exception: C. pygmaea), unlike other animals, where isosexual litters are typically overrepresented. Taken together, our results indicate a modest negative effect of same‐age sibling competition on reproductive output in captive callitrichines. This study also serves to illustrate the value of zoo and laboratory records for biological inquiry.     

A work‐for‐food enrichment program increases exploration and decreases stereotypies in four species of bears

Zoo‐housed bears are prone to exhibiting stereotypic behaviors, generally considered indicators of negative welfare. We explored the effects of a variable‐time feeding enrichment schedule on behavioral indicators of welfare in four bear species at Cleveland Metroparks Zoo. We distributed the diets of eight bears in one of five enrichment items, for two consecutive days each, and monitored behavior throughout the day. In Experiment 1, we compared variable‐time to fixed‐time presentation of enrichment over two, 10‐day periods. Overall, bears performed more exploratory behavior when enriched (p < 0.0001). Furthermore, variable‐time enrichment was associated with a greater increase in exploratory behavior than fixed‐time enrichment when compared to baseline (p < 0.001). Both fixed‐time (p_unadjusted <0.05, p_adjusted = 0.07) and variable‐schedule (p_unadjusted <0.05, p_adjusted = 0.09) enrichment were also associated with similar decreases in abnormal behavior compared to baseline. For Experiment 2, we tested habituation to enrichment over 30 days using multiple items and a semi‐variable presentation schedule. Again during the enrichment period, bears exhibited increased exploratory behavior (p < 0.0001) and decreased abnormal behaviors compared to baseline (p_unadjusted = 0.05, p_adjusted = 0.09). We observed no habituation during the 30‐day sustained enrichment period for these behaviors. Collectively, these results suggest that daily, variable‐schedule feeding enrichment, with intermittent presentation of unique enrichment items, increases behavioral indicators of positive welfare and decreases behavioral indicators of negative welfare.     

Assessing the Welfare of Dairy Cattle

This article attempts to determine the effects of environment (captive or wild) and a simple form of environmental enrichment on the behavior and physiology of a nonhuman animal. Specifically, analyses first compared behavioral budgets and stereotypic behavior of captive coyotes (Canis latrans) in kennels and pens to their counterparts in the wild. Second, experiments examined the effect of a simple form of environmental enrichment for captive coyotes (food-filled bones) on behavioral budgets, stereotypies, and corticosteroid levels. Overall, behavioral budgets of captive coyotes in both kennels and pens were similar to those observed in the wild, but coyotes in captivity exhibited significantly more stereotypic behavior. Intermittently providing a bone generally lowered resting and increased foraging behaviors but did not significantly reduce stereotypic behavior or alter corticosteroid levels. Thus, coyote behavior in captivity can be similar to that exhibited in the wild; in addition, although enrichment can affect proportions of elicited behaviors, abnormal behaviors and corticosteroid levels may require more than a simple form of environmental enrichment for their reduction.     

Behavioral effects of environmental enrichment on harbor seals (Phoca vitulina concolor) and gray seals (Halichoerus grypus)

Zoos and aquariums have been incorporating environmental enrichment into their animal care programs for the past 30 years to increase mental stimulation and promote natural behaviors. However, most attempts to document the effects of enrichment on animal behavior have focused on terrestrial mammals. Staff at the National Aquarium in Baltimore conducted an investigation of the behavioral effects of enrichment on the seven harbor seals and two gray seals housed in the aquarium's outdoor seal exhibit. We expected that enrichment would change the amount of time the animals spent engaged in specific behaviors. The behaviors recorded were: resting in water, resting hauled out, maintenance, breeding display, breeding behavior, aggression, pattern swimming, random swimming, exploration, and out of sight. Activity levels (random swimming and exploration) were expected to increase, while stereotypic behaviors (pattern swimming) were expected to decrease. The frequency and duration of behaviors were documented for 90 hr in both the control phase (without enrichment) and the experimental phase (with enrichment). Statistically significant differences (P<0.05) in the time spent in pattern swimming, random swimming, exploration, and out of sight were observed between the two phases. With enrichment, pattern swimming and out of sight decreased, while random swimming and exploration behavior increased. These findings demonstrate that enrichment can promote behaviors (random swimming and exploration) that are likely to be normal for phocids in the wild, and that may contribute to the behavioral complexity of these seals in captivity. Zoo Biol 21:375–387, 2002. © 2002 Wiley‐Liss, Inc.     

Stereotypic behavior in wild marine carnivores?

Stereotypic behavior is observed in many species within zoological institutions. Attempts to reduce such behavior typically involve some form of environmental enrichment that provides opportunities for species appropriate behavior or some degree of control within the environment. However, environmental enrichment has never been completely successful in eliminating stereotypic behavior for an entire group of animals within a zoological facility. In the wild, stereotypic behavior is rarely observed. Documenting the occurrence of stereotypic behavior in the wild, and circumstances in which it occurs, could help provide insight into the causes of such behavior within zoological institutions. The following commentary details the observations of wild lemon sharks (Negaprion brevirostris) engaging in a stereotyped swimming pattern behind a research vessel north of Grand Bahama Island, Bahamas. We consider a possible explanation for the sharks' behavior and hope to stimulate conversation as well as increase examination of animal management routines in zoological facilities. Zoo Biol 30:365–370, 2011. © 2010 Wiley‐Liss, Inc.     

In the deep end: pooling data and other statistical challenges of zoo and aquarium research

Zoo and aquarium research presents many logistic challenges, including extremely small sample sizes and lack of independent data points, which lend themselves to the misuse of statistics. Pseudoreplication and pooling of data are two statistical problems common in research in the biological sciences. Although the prevalence of these and other statistical miscues have been documented in other fields, little attention has been paid to the practice of statistics in the field of zoo biology. A review of articles published in the journal Zoo Biology between 1999–2004 showed that approximately 40% of the 146 articles utilizing inferential statistics during that span contained some evidence of pseudoreplication or pooling of data. Nearly 75% of studies did not provide degrees of freedom for all statistics and approximately 20% did not report test statistic values. Although the level of pseudoreplication in this dataset is not outside the levels found in other branches of biology, it does indicate the challenges of dealing with appropriate data analysis in zoo and aquarium studies. The standardization of statistical techniques to deal with the methodological challenges of zoo and aquarium populations can help advance zoo research by guiding the production and analysis of applied studies. This study recommends techniques for dealing with these issues, including complete disclosure of data manipulation and reporting of statistical values, checking and control for institutional effects in statistical models, and avoidance of pseudoreplicated observations. Additionally, zoo biologists should seek out other models such as hierarchical or factorial models or randomization tests to supplement their repertoire of t‐tests and ANOVA. These suggestions are intended to stimulate conversation and examination of the current use of statistics in zoo biology in an effort to develop more consistent requirements for publication. Zoo Biol 0:1–14, 2006. © 2006 Wiley‐Liss, Inc.     

Thirty years later: enrichment practices for captive mammals

Environmental enrichment of captive mammals has been steadily evolving over the past thirty years. For this process to continue, it is first necessary to define current enrichment practices and then identify the factors that limit enhancing the quality and quantity of enrichment, as well as the evaluation of its effectiveness. With the objective of obtaining this information, an international multi‐institutional questionnaire survey was conducted with individuals working with zoo‐housed mammals. Results of the survey showed that regardless of how important different types of enrichment were perceived to be, if providing them was particularly time‐consuming, they were not made available to captive mammals as frequently as those requiring less staff time and effort. The groups of mammals provided with enrichment most frequently received it on average fewer than four times per day, resulting in less than two hours per day spent by each animal care staff member on tasks related to enrichment. The time required for staff to complete other husbandry tasks was the factor most limiting the implementation and evaluation of enrichment. The majority of survey respondents agreed that they would provide more enrichment and carry out more evaluation of enrichment if it was manageable to do so. The results of this study support the need for greater quantity, variety, frequency, and evaluation of enrichment provided to captive mammals housed in zoos without impinging on available staff time. Zoo Biol 29:303–316, 2010. © 2009 Wiley‐Liss, Inc.     

N‐glycosylation proteomic characterization and cross‐species comparison of milk fat globule membrane proteins from mammals

Glycosylation of proteins has been implicated in various biological functions and has received much attention; however, glycoprotein components and inter‐species complexity have not yet been elucidated fully in milk proteins. N‐linked glycosylation sites and glycoproteins in milk fat globule membrane (MFGM) fractions were investigated by combining N‐glycosylated peptides enrichment and high‐accuracy Q Exactive identification, to map the N‐glycoproteome profiles in Holstein and Jersey cows, buffaloes, yaks, goats, camels, horses, and humans. A total of 399 N‐glycoproteins with 677 glycosylation sites were identified in the MFGM fractions of the studied mammals. Most glycosylation sites in humans were classified as known and those in the other studied mammals as unknown, according to Swiss‐Prot annotations. Functionally, most of the identified glycoproteins were associated with the ‘response to stimulus’ GO category. N‐glycosylated protein components of MFGM fractions from Holstein and Jersey cows, buffaloes, yaks, and goats were more similar to each other compared with those of camels, horses and human. The findings increased the number of known N‐glycosylation sites in the milk from dairy animal species, revealed the complexity of the MFGM glycoproteome, and provided useful information to further explore the mechanism of MFGM glycoproteins biosynthesis among the studied mammals.     

Experimental evaluation of environmental enrichment of sea turtles

Although behavioral studies have been conducted at zoos and aquaria for years, documentation concerning the effectiveness of environmental enrichment has dealt primarily with terrestrial animals and marine mammals. Few enrichment studies have been conducted on reptiles. For this study, behavioral observations were made on four captive sea turtles (three loggerhead, Caretta caretta, and one blind green, Chelonia mydas) with enrichment present and absent. Enrichment devices were modified for the special needs of the blind turtle. Behaviors were classified as Resting, Pattern Swimming, Random Swimming, Focused Behavior, Aggression, Hiding, Orientation, and Noncategorized Behavior. It was hypothesized that, when enrichment was present, a decrease in Resting and stereotypic Pattern Swimming would be seen along with an increase in Random Swimming and Focused Behavior. It was found that, when no enrichment devices were present, 77% of the turtles' time was spent in Resting and Pattern Swimming. When enrichment devices were provided, 88% of their time was spent in Random Swimming and Focused Behavior with only 8% spent in Pattern Swimming and Resting. Statistically, there were significant increases in Random Swimming (three of the four turtles) and Focused Behavior (4/4) and significant decreases in Resting (3/4) and Pattern Swimming (3/4) when enrichment devices were present. These results suggest that environmental enrichment is as effective with marine reptiles as has been found with other animals and should be encouraged for all captive sea turtles. Zoo Biol 26:407–416, 2007. © 2007 Wiley‐Liss, Inc.     

Zoo Playgrounds: A Source of Enrichment or Stress for a Group of Nearby Cockatoos? A Case Study

There is increasing evidence that in some circumstances, zoo visitors may be aversive stimuli to nonhuman animals housed in zoos. Yet, most previous research has focused on primates with little attention given to numerous other species who are housed in zoos. The focus animal of this project was the cockatoo, a species who has received minimal attention in zoo-based research. Furthermore, although the influence of the zoo setting has become increasingly important in visitor effect studies, this is the 1st study to quantify the effect of activity at a children's playground on zoo animals. There was an investigation on the effect of a zoo playground on the behavior of citron-crested and Moluccan cockatoos (Cacatua sulphurea citrinocristata and Cacatua moluccensis), as well as the effect of children standing in front of the birds' aviaries. The results showed that in some circumstances, the Moluccan cockatoos retreated from visitors, while the citron-crested cockatoos did not retreat from visitors and became more social in the presence of visitors. These findings highlight the importance of careful selection of species and individual animals to be housed near zoo playgrounds.