Keeper effect: Animals are more active in the presence of their caretakers.

Zookeepers are the primary caretakers of animals, providing daily care through frequent and close interactions. From the animal's perspective, most of these daily interactions are likely to have positive outcomes. With consistent and reliable interactions, a human-animal relationship is expected to develop. Our aim of this study was to investigate if the presence of the primary keeper in the public viewing area of zoo exhibits impacts the behavior of animals. We observed the behavior of 15 individuals of six species in the presence and absence of their primary keeper. Overall, we observed animals being more active in their keeper's presence than when the keeper was not present. When we considered if the keeper was nearby around times of offered opportunities to animals (e.g., feeding, enrichment, and training), our results showed that animals were equally as active when the keeper was present before an opportunity and when no opportunity was offered. These equal activity levels imply that the keeper is a cue for a forthcoming event to the animals, which reflects anticipatory behavior. Overall, we demonstrate that keeper presence is an environmental context in which animals behave differently than in keeper absence.

Quantifying animals' perception of environmental predictability using anticipatory behavior.

Animals under human care often experience predictable daily husbandry events, which can promote the development of anticipatory behavior. Previous research suggests even short delays in the arrival of a predictable, desired outcome can lead to negative welfare outcomes for animals. As such, providing reliable information to animals regarding the onset of important events may be a simple but useful method to support positive welfare. Here we evaluated the quantitative characteristics of anticipatory behavior of a California sea lion at the San Francisco Zoo in three situations (1) when the animal had accurate information about the occurrence of the event (temporally predictable training sessions), (2) when the information was semi-reliable (unscheduled training session), and (3) when a reliable signal was offered before unscheduled sessions. Results showed that providing a reliable cue resulted in a stronger temporal correlation of anticipation before the beginning of the unscheduled session, similar to the temporally predictable training session. However, providing a reliable cue did not reduce the intensity of the anticipatory behavior. We propose to take into account two aspects of the quantitative characteristics of anticipatory behavior: correlation with time until a desired event (correlation) and intensity, where the correlation indicates the ability of an individual animal to predict the occurrence of an event, and the intensity indicates the degree of sensitivity of the animal to reward. We discuss the implications for animal welfare and husbandry.

A Quantitative Approach for Using Anticipatory Behavior as a Graded Welfare Assessment.

To perform quick assessments, welfare practitioners may focus on specific behavioral indicators of welfare, which can lead to challenges in interpretation. Anticipatory behavior has been suggested as a potentially graded indicator of well-being in animals. However, there are difficulties in assessing variations in this class of behavior quantitatively. Here, we propose an analytical approach for identifying and comparing the intensity of anticipatory behavior across different conditions. We evaluated the changes in the behavior of a sea lion at the San Francisco Zoo before and after daily training sessions, the start time of which had differing degrees of predictability. We show that anticipatory behavior is a complex suite of behaviors that can show multi-directional changes prior to an anticipated event. Additionally, we show that the methods utilized here can distinguish among differing intensities of anticipation directed toward daily husbandry events. We suggest that this approach may be broadly applicable for applying measures of anticipatory behavior as a graded welfare indicator.

Dither: A unifying model of the effects of visitor numbers on zoo animal behavior.

Interest in the impact of human presence on the behavior and well-being of zoo and aquarium animals is increasing. Previous work has conceptualized the presence of zoo visitors as having one of three impacts on the behavior of animals in zoos: positive, negative, or neutral. Research suggests the same species may exhibit all three responses under different conditions, calling into question whether the positive/negative/neutral framework is the most useful way of considering visitor impact on animal behavior. Here we present a model of visitor effects that unifies these three predictions. Our model suggests that zoo-goers may provide a "dither effect" for some animals living in zoos. We posit animals may show nonlinear behavioral responses over a range of visitor densities, effectively exhibiting changes in both comfortable and anxiety-like behaviors under different levels of human presence. We tested this model during two COVID-19 related closures at the San Francisco Zoo, studying seven species for evidence of nonlinear relationships between visitor numbers and animal behavior. Our results support the dither effect acting in several species observed.

Space, time, and context drive anticipatory behavior: Considerations for understanding the behavior of animals in human care.

Animal-based measures reflecting the welfare state of individuals are critical for ensuring the well-being of animals under human care. Anticipatory behavior is one potential animal-based measure that has gained traction in recent years, as it is theorized to relate to animals' reward sensitivity. It is of particular interest as an assessment for animals living under human care, as the predictability of the captive environment lends itself to the development of this class of behaviors. Animals are likely to exhibit anticipation in locations related to the anticipated event, often in temporally predictable time frames, and before specific contexts they experience in their day-to-day management. In this sense and under certain circumstances, anticipatory behaviors are likely to drive observed behavioral or space use patterns of animals under human care. Drawing conclusions from such data without identifying anticipation may result in misleading conclusions. Here we discuss how space, time, and context are related to patterns of anticipatory behaviors in animals under human care, how unidentified anticipation may alter conclusions regarding animal behavior or welfare under certain circumstances.

Behavioral changes in senescent giant Pacific octopus (Enteroctopus dofleini) are associated with peripheral neural degeneration and loss of epithelial tissue.

Most species of octopus experience extreme physical decline after a single reproductive bout which extends over a period of days, weeks, or months before eventual death. Although outward indicators of senescence are widely recognized, comparatively little is known about physiological and neural changes accompanying terminal decline in octopuses. Here, we measured changes in behavioral response to nociceptive stimuli across the lifespan in giant Pacific octopus (GPO), Enteroctopus dofleini, held in public aquariums in the USA. Post-euthanasia, tissue was collected from arm tips, and neural and epithelial cell degeneration was quantified and compared with biopsies of arm tips from healthy, pre-reproductive GPOs. Behavioral assays showed significant changes both in low threshold mechanosensory responses and nociceptive behavioral responses beginning early in senescence and extending until euthanasia. Histology data showed that while the ratio of apoptotic cells to total cell number stayed constant between healthy and senescent GPOs, overall neural and epithelial cell density was significantly lower in terminally senescent octopuses compared with healthy controls. Our data provide new insight into the time-course and causes of sensory dysfunction in senescent cephalopods and suggest proactive welfare management should begin early in the senescence phase, well before animals enter terminal decline.

Assessing and Enhancing the Welfare of Animals with Equivocal and Reliable Cues.

The actions of human caretakers strongly influence animals living under human care. Here, we consider how intentional and unintentional signals provided by caretakers can inform our assessment of animals' well-being as well as help to support it. Our aim is to assist in further developing techniques to learn animals' affective state from their behavior and to provide simple suggestions for how animal caretakers' behavior can support animal welfare. We suggest that anticipatory behavior towards expected rewards is related to decision-making behavior as viewed through the cognitive bias lens. By considering the predictions of the theories associated with anticipatory behavior and cognitive bias, we propose to use specific cues to probe the cumulative affective state of animals. Additionally, our commentary draws on the logic of reward sensitivity and judgement bias theories to develop a framework that suggests how reliable and equivocal signals may influence animals' affective states. Application of this framework may be useful in supporting the welfare of animals in human care.

Managing Aged Animals in Zoos to Promote Positive Welfare: A Review and Future Directions.

Improvements in veterinary care, nutrition, and husbandry of animals living in zoos have led to an increase in the longevity of these animals over the past 30 years. In this same time period, the focus of animal welfare science has shifted from concerns over mitigating negative welfare impacts to promoting positive welfare experiences for animals. For instance, providing opportunities for animals to exert agency, solve problems, or acquire rewards are all associated with positive welfare outcomes. Many common age-related changes result in limitations to opportunities for positive welfare experiences, either due to pain or other physical, cognitive, or behavioral limitations. This review aggregates information regarding common age-related physical and behavioral changes across species, discusses how age-related changes may limit positive welfare opportunities of aged animals in human care, and suggests potential management methods to help promote positive welfare for animals at all life stages in zoos and aquariums.

Applying Behavioral Conditioning to Identify Anticipatory Behaviors.

The ability to predict regular events can be adaptive for nonhuman animals living in an otherwise unpredictable environment. Animals may exhibit behavioral changes preceding a predictable event; such changes reflect anticipatory behavior. Anticipatory behavior is broadly defined as a goal-directed increase in activity preceding a predictable event and can be useful for assessing well being in animals in captivity. Anticipation may look different in different animals, however, necessitating methods to generate and study anticipatory behaviors across species. This article includes a proposed method for generating and describing anticipatory behavior in zoos using behavioral conditioning. The article also includes discussion of case studies of the proposed method with 2 animals at the San Francisco Zoo: a silverback gorilla (Gorilla gorilla gorilla) and a red panda (Ailurus fulgens). The study evidence supports anticipation in both animals. As behavioral conditioning can be used with many animals, the proposed method provides a practical approach for using anticipatory behavior to assess animal well being in zoos.

Crowdfunding Campaigns Help Researchers Launch Projects and Generate Outreach.

Organizers of participatory research (citizen science) projects can generate funds and outreach through crowdfunding. Here we provide insights from three successful science crowdfunding campaigns recently completed on Indiegogo, Experiment, and Kickstarter. Choosing a crowdfunding platform that fits the project is just the beginning; a successful campaign reflects its content, management, and marketing, and some researchers may need to acquire new skills. In addition, the growing trend of crowdfunding for science reinforces the importance of academic engagement with social media.

Searching for behavioral indicators of welfare in zoos: uncovering anticipatory behavior.

A current focus of zoo-based research aims to identify indicators of animal welfare. Reliable behavioral indicators of welfare are highly desirable as behavioral observation is non invasive and requires little in the way of specialized equipment and other costly resources-save for observer time. Anticipatory behavior is an indicator of an animal's sensitivity to reward and as such, it is a real-time indicator of animals' own perceptions of their well-being. In fact, anticipatory behavior may generate a positive affective state and thus be at least a brief manifestation of good welfare itself. The husbandry conditions of most captive animals are such that food acquisition and other positive outcomes are highly scheduled and easily signaled. These conditions promote the development of anticipatory behavior, yet little research has either documented or interpreted this behavior in zoo and aquarium animals. This commentary suggests that anticipatory behavior could be a useful tool for assessing welfare and calls upon zoo and aquarium researchers to begin to develop this tool by describing the behavior and the circumstances that lead to its modulation.

Measuring animal personality for use in population management in zoos: suggested methods and rationale.

The concept that animals have personalities is gaining traction in the scientific community and is well established in zoos and aquariums. Applying knowledge of animal personalities has occurred more slowly and is most often only considered informally. However, animal personalities are likely to affect the welfare animals experience in captivity and thus should be of primary concern to zoo managers. In addition, animal personality likely affects the outcomes of zoo guest experiences and potentially guests' conservation-related behavior. With over 1,000,000 animals in the care of zoos internationally and hundreds of millions of visitors annually, it would be prudent and beneficial to maximize our use of animal personality data in zoos to effect positive conservation outcomes. Understanding how to broaden population planning techniques to include measures of animal personality and the important outcomes of welfare and education value is of prime importance to the zoo industry. In order to succeed, it is necessary to employ techniques that reliably assess animal personalities and provide measures that can easily be used in population planning models. We discuss the outcomes of recent workshops designed to determine the best techniques for measuring animal personalities in the zoo setting with the goal of incorporating personality into population planning.

Note on optimizing environmental enrichment: a study of fennec fox and zoo guests.

Environmental enrichment is widely used to stimulate animal time budgets that seem more natural and diverse than those of unenriched animals. Uncertainty of reward is a suggested means to maintain enrichment's efficacy. Foraging tasks are widely applied in zoo animal enrichment, yet few rely on the logic of optimal foraging theory to help maintain animal motivation. We applied a foraging strategy to zoo housed fennec foxes as enrichment. We varied only the probability of when and where food would occur in the animals' exhibit. Our methods increased behavioral diversity, animal activity, and stimulated guest interest in the exhibit.

Odor-based recognition of familiar and related conspecifics: a first test conducted on captive Humboldt penguins (Spheniscus humboldti).

Studies of kin recognition in birds have largely focused on parent-offspring recognition using auditory or visual discrimination. Recent studies indicate that birds use odors during social and familial interactions and possibly for mate choice, suggesting olfactory cues may mediate kin recognition as well. Here, we show that Humboldt penguins (Spheniscus humboldti), a natally philopatric species with lifetime monogamy, discriminate between familiar and unfamiliar non-kin odors (using prior association) and between unfamiliar kin and non-kin odors (using phenotype matching). Penguins preferred familiar non-kin odors, which may be associated with the recognition of nest mates and colony mates and with locating burrows at night after foraging. In tests of kin recognition, penguins preferred unfamiliar non-kin odors. Penguins may have perceived non-kin odors as novel because they did not match the birds' recognition templates. Phenotype matching is likely the primary mechanism for kin recognition within the colony to avoid inbreeding. To our knowledge this is the first study to provide evidence of odor-based kin discrimination in a bird.

Introduction to the special issue on zoo animal welfare.

In May 2008, the Chicago Zoological Society's Center for the Science of Animal Welfare (CSAW) held a two-day international workshop designed to establish and foster new connections between zoo animal welfare scientists and welfare scientists in other fields, and to take the first step toward the development of a research agenda for zoo animal welfare science. Such a research agenda by its very nature would need to be highly multi-disciplinary and collaborative. In support of this purpose this article serves as an introduction for a collection of invited papers presented at the workshop. Workshop themes included the investigation of welfare metrics currently used and in development, elucidating gaps and determining needs for zoo welfare research, and gaining a deeper understanding of the value that understanding animals in the wild can bring to zoo animal welfare. Here we discuss some of the most relevant points made at the workshop and describe the seven most salient research needs that were suggested in consensus.

Toward a predictive theory for environmental enrichment.

There have been many applications of and successes with environmental enrichment for captive animals. The theoretical spine upon which much enrichment work hangs largely describes why enrichment should work. Yet, there remains no clear understanding of how enrichment should be applied to achieve the most beneficial results. This lack of understanding may stem in part from the assumptions that underlie the application of enrichment by practitioners. These assumptions are derived from an understanding that giving animals choice and control in their environment stimulates their motivation to perform behaviors that may indicate a heightened state of well-being. Learning theory provides a means to question the manner in which these constructs are routinely applied, and converting learning theory's findings to optimality predictions suggests a particularly vexing paradox-that motivation to perform appears to be maintained best when acquiring a payoff for expressing the behavior is uncertain. This effect occurs even when the actual value of the payoff is the same for all schedules of certainty of payoff acquisition. The paradox can be resolved by invoking rewards of an alternative type, such as cognitive rewards, or through an understanding of how the average payoff changes with changes in the probability of reward. This model, with measures of the average change of the payoff, suggests testable scenarios by which practitioners can measure the quality of environmental uncertainty in enrichment programs.

Behavioral monitoring in zoos and aquariums: a tool for guiding husbandry and directing research.

Behavioral monitoring is the scientific collection of animal behavior data to understand normal patterns of behavior and changes in these patterns. This tool is underutilized in the zoo industry although it can be an effective indicator of many potential problems that compromise zoo animal well-being. We suggest that a behavioral monitoring program should be a core component of a zoological institution's care program. We detail the benefits of such a program and describe its components. We provide guidelines for implementing such a program and make recommendations that will help institutions to employ behavioral monitoring programs with reasonable expense. We argue that the benefits of such a program, primarily increased detection of rising or potential problems, far outweigh the minor costs of implementation.