A transdisciplinary view on curiosity beyond linguistic humans: animals, infants, and artificial intelligence.

Curiosity is a core driver for life-long learning, problem-solving and decision-making. In a broad sense, curiosity is defined as the intrinsically motivated acquisition of novel information. Despite a decades-long history of curiosity research and the earliest human theories arising from studies of laboratory rodents, curiosity has mainly been considered in two camps: 'linguistic human' and 'other'. This is despite psychology being heritable, and there are many continuities in cognitive capacities across the animal kingdom. Boundary-pushing cross-disciplinary debates on curiosity are lacking, and the relative exclusion of pre-linguistic infants and non-human animals has led to a scientific impasse which more broadly impedes the development of artificially intelligent systems modelled on curiosity in natural agents. In this review, we synthesize literature across multiple disciplines that have studied curiosity in non-verbal systems. By highlighting how similar findings have been produced across the separate disciplines of animal behaviour, developmental psychology, neuroscience, and computational cognition, we discuss how this can be used to advance our understanding of curiosity. We propose, for the first time, how features of curiosity could be quantified and therefore studied more operationally across systems: across different species, developmental stages, and natural or artificial agents.

The endangered brain: actively preserving ex-situ animal behaviour and cognition will benefit in-situ conservation.

Endangered species have small, unsustainable population sizes that are geographically or genetically restricted. Ex-situ conservation programmes are therefore faced with the challenge of breeding sufficiently sized, genetically diverse populations earmarked for reintroduction that have the behavioural skills to survive and breed in the wild. Yet, maintaining historically beneficial behaviours may be insufficient, as research continues to suggest that certain cognitive-behavioural skills and flexibility are necessary to cope with human-induced rapid environmental change (HIREC). This paper begins by reviewing interdisciplinary studies on the 'captivity effect' in laboratory, farmed, domesticated and feral vertebrates and finds that captivity imposes rapid yet often reversible changes to the brain, cognition and behaviour. However, research on this effect in ex-situ conservation sites is lacking. This paper reveals an apparent mismatch between ex-situ enrichment aims and the cognitive-behavioural skills possessed by animals currently coping with HIREC. After synthesizing literature across neuroscience, behavioural biology, comparative cognition and field conservation, it seems that ex-situ endangered species deemed for reintroduction may have better chances of coping with HIREC if their natural cognition and behavioural repertoires are actively preserved. Evaluating the effects of environmental challenges rather than captivity per se is recommended, in addition to using targeted cognitive enrichment.

Material and food exploration by zoo-housed animals can inform cognition and enrichment apparatus design.

To robustly study zoo animal cognition and provide effective enrichment, we must provide animals with carefully designed apparatus made from appropriate (safe, attractive, practical) materials. However, all too often, this design phase is overlooked or omitted from the literature. We evaluated how a troop of 12 ring-tailed lemurs (Lemur catta) explored a range of novel materials and whole foods during outdoor social testing. These items were not intended to test cognition or be enriching; rather we viewed them as the potential "building blocks" from which to build our future apparatus. Lemurs preferred to explore wooden surfaces, but had no preference for manipulanda made from different materials. Large amounts of metal and untreated wood should be avoided in the future; metal produced too much heat and glare, and wood was damaged by biting/chewing. Lemurs used one or two hands to explore manipulanda, and simple touching was more common than twisting or pulling. However, lemurs were most likely to explore by smell than touch or by mouth. Social testing preserved "normal" conditions for the lemurs, including natural food stealing and scrounging in high- and low-ranking individuals, respectively. Our findings culminated in the development of a static, low-level cognitive task apparatus, constructed from modular plastic units. We encourage other researchers to report how they develop cognitive and enrichment apparatuses and consider a similar preference-testing approach.

From Soundwave to Soundscape: A Guide to Acoustic Research in Captive Animal Environments.

Sound is a complex feature of all environments, but captive animals' soundscapes (acoustic scenes) have been studied far less than those of wild animals. Furthermore, research across farms, laboratories, pet shelters, and zoos tends to focus on just one aspect of environmental sound measurement: its pressure level or intensity (in decibels). We review the state of the art of captive animal acoustic research and contrast this to the wild, highlighting new opportunities for the former to learn from the latter. We begin with a primer on sound, aimed at captive researchers and animal caregivers with an interest (rather than specific expertise) in acoustics. Then, we summarize animal acoustic research broadly split into measuring sound from animals, or their environment. We guide readers from soundwave to soundscape and through the burgeoning field of conservation technology, which offers new methods to capture multiple features of complex, gestalt soundscapes. Our review ends with suggestions for future research, and a practical guide to sound measurement in captive environments.

Evaluating Cognitive Enrichment for Zoo-Housed Gorillas Using Facial Recognition.

The use of computer technology within zoos is becoming increasingly popular to help achieve high animal welfare standards. However, despite its various positive applications to wildlife in recent years, there has been little uptake of machine learning in zoo animal care. In this paper, we describe how a facial recognition system, developed using machine learning, was embedded within a cognitive enrichment device (a vertical, modular finger maze) for a troop of seven Western lowland gorillas (Gorilla gorilla gorilla) at Bristol Zoo Gardens, UK. We explored whether machine learning could automatically identify individual gorillas through facial recognition, and automate the collection of device-use data including the order, frequency and duration of use by the troop. Concurrent traditional video recording and behavioral coding by eye was undertaken for comparison. The facial recognition system was very effective at identifying individual gorillas (97% mean average precision) and could automate specific downstream tasks (for example, duration of engagement). However, its development was a heavy investment, requiring specialized hardware and interdisciplinary expertise. Therefore, we suggest a system like this is only appropriate for long-term projects. Additionally, researcher input was still required to visually identify which maze modules were being used by gorillas and how. This highlights the need for additional technology, such as infrared sensors, to fully automate cognitive enrichment evaluation. To end, we describe a future system that combines machine learning and sensor technology which could automate the collection of data in real-time for use by researchers and animal care staff.

Bridging pure cognitive research and cognitive enrichment.

Cognitive enrichment is a growing subset of environmental enrichment for captive animals. However, it has been difficult for practitioners to design, implement, and evaluate relevant and appropriate cognitive challenges. Even though pure comparative cognition researchers focus on fundamental evolutionary questions, their knowledge and expertise can also shape the future of cognitive enrichment. This paper describes the motive, means, and opportunity to do so. Taxon-specific summaries of animal cognition (including inter-individual variation in skill and effects of motivation), and experimental designs (including the task itself, training, and reward) need to be accessible to practitioners in applied settings, such as farms, zoos, and sanctuaries. Furthermore, I invite pure researchers to directly evaluate their cognitive research program as enrichment and thus bridge the disciplines of animal cognition and welfare.

Increasing animal cognition research in zoos.

Animal cognition covers various mental processes including perception, learning, decision-making and memory, and animal behavior is often used as a proxy for measuring cognition. Animal cognition/behavior research has multiple benefits; it provides fundamental knowledge of animal biology and evolution but can also have applied conservation and welfare applications. Zoos provide an excellent yet relatively untapped resource for animal cognition research, because they house a wide variety of species-many of which are under threat-and allow close observation and relatively high experimental control compared to the wild. Multi-zoo collaboration leads to increased sample size and species representation, which in turn leads to more robust science. However, there are salient challenges associated with zoo-based cognitive research, which are animal-based (e.g., small sample sizes at single zoos, untrained/unhabituated subjects, side effects) and human-based (e.g., time restrictions, safety concerns, and perceptions of animals interacting with unnatural technology or apparatus). We aim to increase the understanding and subsequent uptake of animal cognition research in zoos, by transparently outlining the main benefits and challenges. Importantly, we use our own research (1) a study on novelty responses in hornbills, and (2) a multi-site collaboration called the "ManyBirds" Project to demonstrate how challenges may be overcome. These potential options include using "drop and go" apparatuses that require no training, close human contact or animal separation. This study is aimed at zoo animal care and research staff, as well as external researchers interested in zoo-based studies.

High-Tech and Tactile: Cognitive Enrichment for Zoo-Housed Gorillas.

The field of environmental enrichment for zoo animals, particularly great apes, has been revived by technological advancements such as touchscreen interfaces and motion sensors. However, direct animal-computer interaction (ACI) is impractical or undesirable for many zoos. We developed a modular cuboid puzzle maze for the troop of six Western lowland gorillas (Gorilla gorilla gorilla) at Bristol Zoo Gardens, United Kingdom. The gorillas could use their fingers or tools to interact with interconnected modules and remove food rewards. Twelve modules could be interchanged within the frame to create novel iterations with every trial. We took a screen-free approach to enrichment: substituting ACI for tactile, physically complex device components, in addition to hidden automatic sensors, and cameras to log device use. The current study evaluated the gorillas' behavioral responses to the device, and evaluated it as a form of "cognitive enrichment." Five out of six gorillas used the device, during monthly trials of 1 h duration, over a 6 month period. All users were female including two infants, and there were significant individual differences in duration of device use. The successful extraction of food rewards was only performed by the three tool-using gorillas. Device use did not diminish over time, and gorillas took turns to use the device alone or as one mother-infant dyad. Our results suggest that the device was a form of cognitive enrichment for the study troop because it allowed gorillas to solve novel challenges, and device use was not associated with behavioral indicators of stress or frustration. However, device exposure had no significant effects on gorilla activity budgets. The device has the potential to be a sustainable enrichment method in the long-term, tailored to individual gorilla skill levels and motivations. Our study represents a technological advancement for gorilla enrichment, an area which had been particularly overlooked until now. We wholly encourage the continued development of this physical maze system for other great apes under human care, with or without computer logging technology.

Advances in Applied Zoo Animal Welfare Science.

Nonhuman animal welfare science is the scientific study of the welfare state of animals that attempts to make inferences about how animals feel from their behavior, endocrine function, and/or signs of physical health. These welfare measurements are applicable within zoos yet inherently more complex than in farms and laboratories. This complexity is due to the vast number of species housed, lack of fundamental biological information, and relatively lower sample sizes and levels of experimental control. This article summarizes the invited presentations on the topic of "Advances in Applied Animal Welfare Science," given at the Fourth Global Animal Welfare Congress held jointly by the Detroit Zoological Society and the World Association of Zoos and Aquariums in 2017. The article focuses on current trends in research on zoo animal welfare under the following themes: (a) human-animal interactions and relationships, (b) anticipatory behavior, (c) cognitive enrichment, (d) behavioral biology, and (e) reproductive and population management. It highlights areas in which further advancements in zoo animal welfare science are needed and the challenges that may be faced in doing so.

Optimal marine mammal welfare under human care: Current efforts and future directions.

Marine mammals include cetaceans, pinnipeds, sirenians, sea otters and polar bears, many of which are charismatic and popular species commonly kept under human care in zoos and aquaria. However, in comparison with their fully terrestrial counterparts their welfare has been less intensively studied, and their partial or full reliance on the aquatic environment leads to unique welfare challenges. In this paper we attempt to collate and review the research undertaken thus far on marine mammal welfare, and identify the most important gaps in knowledge. We use 'best practice case studies' to highlight examples of research promoting optimal welfare, include suggestions for future directions of research efforts, and make recommendations to strive for optimal welfare, where it is currently lacking, above and beyond minimum legislation and guidelines. Our review of the current literature shows that recently there have been positive forward strides in marine mammal welfare assessment, but fundamental research is still required to validate positive and negative indicators of welfare in marine mammals. Across all marine mammals, more research is required on the dimensions and complexity of pools and land areas necessary for optimal welfare, and the impact of staff absence for most of the 24-h day, as standard working hours are usually between 0900 and 1700.

Cognitive enrichment for bottlenose dolphins (Tursiops truncatus): evaluation of a novel underwater maze device.

Cognitive enrichment is gaining popularity as a tool to enhance captive animal well-being, but research on captive cetaceans is lacking. Dolphin cognition has been studied intensively since the 1950s, and several hundred bottlenose dolphins are housed in major zoos and aquaria worldwide, but most dolphin enrichment consists of simple floating objects. The aim of this study was to investigate whether a novel, underwater maze device (UMD) was cognitively enriching for one group of male and one group of female dolphins at Six Flags Discovery Kingdom, CA. The dolphin's task was to navigate a rubber ball through a maze of pipes, towards an exit pipe. We also tested a modification where an edible gelatine ball fell into the pool once the UMD was solved. The UMD was provided to each group between 8 and 11 times over a 4-week period. Male dolphins used the UMD without prior training, whereas females did not use the UMD at all. Two male dolphins solved the UMD 17 times, using a variety of problem-solving strategies. The UMD had no significant effect on circular (repetitive) swimming patterns, but males spent significantly more time underwater when the UMD was present. Males used the UMD significantly more when it contained the rubber ball, but the gelatine ball stimulated social play. The UMD is a safe and practical device for captive dolphins. It now requires further testing on other dolphins, particularly females, to in order to examine whether the sex differences we observed are a general phenomenon.

Effect of a cognitive challenge device containing food and non-food rewards on chimpanzee well-being.

Exploration and problem-solving are highly motivated behaviors in non-human primates, but little research has focused on whether cognitively challenging tasks can enhance primates' psychological well-being, particularly in the absence of food rewards. We evaluated whether a novel cognitive challenge device (CCD) consisting of a maze of opaque tubes enhanced the well-being of a group of six adult chimpanzees housed at ZSL Whipsnade Zoo, UK, over a two-month period. Chimpanzees had the opportunity to interact with two versions of the CCD: the first contained tokens which fell into a transparent chamber when extracted from the CCD and could not be eaten. The second contained unshelled Brazil nuts, which could be extracted and eaten. CCD-use was low over the study, occupying on average 2.5% of observation time. However, compared to baseline levels, chimpanzees exhibited more problem-solving behaviors (directed toward the CCD) and spent significantly more time engaged in social play when the CCD was present. Cage exploration was rare whether the CCD was present or not. Chimpanzees used the CCD (including tool-use) significantly more when it contained tokens. The relationship between the presence of the CCD and self-directed behavior (rough-scratching) was difficult to interpret. Although rough-scratching was significantly higher in the cage when the CCD was present and 18% of these scratching events occurred within one arm's length from the CCD, rough-scratching decreased when device use increased. This study provides a preliminary investigation of the CCD and two reward types, and suggests how the design could be modified to enhance its effects.

Relationship between behavior, adrenal activity, and environment in zoo-housed western lowland gorillas (Gorilla gorilla gorilla).

Monitoring adrenal activity through noninvasive fecal hormone sampling is rapidly gaining popularity as a tool to assess zoo animal welfare. However, few studies have sought to investigate the interrelationships between behavior, adrenal activity, and environment, and ask whether both behavioral and adrenal monitoring strategies are required to assess welfare sufficiently. We present the findings of a 9-month study of a small group (one male, two females) of Western lowland gorillas, Gorilla gorilla gorilla. First, we examined the effect of environmental variables on gorilla behavior. Second, we examined the effect of environmental variables on the concentration of fecal glucocorticoid metabolites (FGC) and the relationship between behavior and FGC. Environmental variables had similar effects on all three gorillas. Negative vigilance of visitors (NVV; staring, posturing, and charging at visitors) significantly increased in all subjects as environmental noise levels increased, and food-related behavior significantly decreased in all subjects as crowd size increased. Exhibit modifications had a number of positive effects on behavior. Notably, when privacy screens were used, NVV significantly decreased in two subjects. We found no significant effects of environmental variables on FGC. However, we did find significant relationships between behavior and FGC in one female. Specifically, her NVV was significantly higher one day before, and on the same day as, raised FGC. Also, hair plucking significantly increased in the two days following raised FGC. Overall, this study demonstrates how concurrent noninvasive fecal and behavioral monitoring can be used for gorilla welfare assessment.

Environmental enrichment for a mixed-species nocturnal mammal exhibit.

Environmental enrichment (EE) is an integral aspect of modern zoo animal management but, empirical evaluation of it is biased toward species housed in single-species groups. Nocturnal houses, where several nocturnal species are housed together, are particularly overlooked. This study investigated whether three species (nine-banded armadillos, Dasypus novemcinctus; Senegal bush babies, Galago senegalensis; two-toed sloths, Choloepus didactylus) in the nocturnal house at Paignton Zoo Environmental Park, UK could be enriched using food-based and sensory EE. Subjects were an adult male and female of each species. EE was deemed effective if it promoted target species-typical behaviors, behavioral diversity, and increased use of enriched exhibit zones. Results from generalized linear mixed models demonstrated that food-based EE elicited the most positive behavioral effects across species. One set of food-based EEs (Kong®, termite mound and hanging food) presented together was associated with a significant increase in species-typical behaviors, increased behavioral diversity, and increased use of enriched exhibit zones in armadillos and bush babies. Although one type of sensory EE (scented pine cones) increased overall exhibit use in all species, the other (rainforest sounds) was linked to a significant decrease in species-typical behavior in bush babies and sloths. There were no intra or interspecies conflicts over EE, and commensalism occurred between armadillos and bush babies. Our data demonstrate that simple food-based and sensory EE can promote positive behavioral changes in a mixed-species nocturnal mammal exhibit. We suggest that both food and sensory EE presented concurrently will maximize opportunities for naturalistic activity in all species.

Space to choose: network analysis of social preferences in a captive chimpanzee community, and implications for management.

Social network analysis (SNA) is rapidly gaining popularity in primatology, but its application to the management of zoo-housed primates has been largely overlooked. Here I use SNA techniques to explore the social structure of chimpanzees (Pan troglodytes) housed in the new "Budongo Trail" exhibit at Edinburgh Zoo, UK. Given that individuals have extensive space (2332 m(2)), and access to several interconnected exhibit sections, I test the hypothesis that individuals are able to choose to interact with specific social partners. Spatial association and social interaction data were recorded from 400 focal watches on 11 individuals, and association, affiliative, and agonistic networks were constructed. Matrix correlations showed that individuals who spent time in close proximity were likely to affiliate with one another, but spatial association did not predict the frequency of agonistic encounters. Cluster analysis revealed significantly distinct sub-groups in the affiliative network (but not association or agonistic networks) in line with maternal kinship. Overall my findings support the hypothesis that the Budongo Trail exhibit facilitates the expression of social preferences, and suggests that SNA can be a useful tool to study zoo primates when proximity between individuals is not forced (i.e. in large, modern exhibits). Now that I have validated a set of SNA methods for this community, they can be used to trace changes in social dynamics over a longer time period, and ultimately assist zoo staff in their management decisions.

The dining etiquette of desert baboons: the roles of social bonds, kinship, and dominance in co-feeding networks.

To better understand how individual relationships influence patterns of social foraging in primate groups, we explored networks of co-feeding in wild desert baboons (Papio ursinus). To minimize the risk of aggression and injury associated with contest competition, we expected that individual group members would choose to co-feed with those group-mates that are most likely to show tolerance and a willingness to share food patches. We tested two alternative hypotheses about who those group-mates might be: the "social bonds hypothesis" predicts that preferred foraging partners will be those with whom individuals share strong social bonds, indexed by grooming, whereas the "kinship hypothesis" predicts that preferred foraging partners will be relatives. We also investigated and controlled for the effects of dominance rank, given that competitive ability is known to shape foraging patterns. Social network analyses of over 5,000 foraging events for 14 adults in a single troop revealed that baboon co-feeding was significantly correlated with grooming relationships but not genetic relatedness, and this finding was also true of the female-only co-feeding network. Dominant individuals were also found to be central to the co-feeding network, frequently sharing food patches with multiple group-mates. This polyadic analysis of foraging associations between individuals underlines the importance of dominance and affiliation to patterns of primate social foraging.