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A review of zoo-based cognitive research using touchscreen interfaces
Abstract
In the past few decades, there has been an increase in the number of zoo-based touchscreen studies of animal cognition around the world. Such studies have contributed to the field of comparative cognition despite the fact research has only been performed at a relatively small number of institutions and with a narrow range of species. Nonetheless, zoo-based touchscreen studies are increasingly recognized as both having the potential to be enriching for captive animals by providing them with opportunities for choice, as well as potentially being a tool with which to measure changes in welfare. Zoo-based touchscreen research on public display also has the potential to impact zoo visitors; encouraging them not only learn more about the cognitive abilities of animals, but also potentially promoting increased respect for these species. Given the lack of a comprehensive review of this scope of specialized research, and the broad potential impacts on animals and programs, here we discuss the history, implementation, and potential outcomes of touchscreen research in zoo settings. K E Y W O R D S comparative cognition, touch panel, touchscreens, welfare, zoos
... In addition to scientific advancements, researchs in recent years have encouraged the introction of cognitive enrichment into zoological ttings in which animals are challenged to probm solve during the enrichment session (Clark, 17;Makecha & Highfill, 2018). Such enrichent has included spatial challenges (e.g., Clark & Kuczaj, 2016), solving a puzzle (e.g., de Rosa et al., 2003;Kuczaj et al., 2009;Lauderdale & Miller, 2019), engaging in a cooperative task (e.g., Chalmeau, 1994;Péron et al., 2011;Plotnik et al., 2011;Kuczaj et al., 2015;Matrai et al., 2019), and interacting with computerized systems (Perdue et al., 2012;Kim-McCormack et al., 2016;Perdue, 2016;Egelkamp & Ross, 2018). ...
... The diversity of games and stimuli that a computer system can present allows for various cognitive abilities to be tested and presents many opportunities to create variability with such a system in terms of type of gameplay as well as type of reinforcement administered (e.g., Washburn & Hopkins, 1994). Touchscreen interfaces have been used with success in zoological facilities (see Egelkamp & Ross, 2018, for review) but have been generally limited to terrestrial species, primarily primates. For species with anatomical differences that make using such a hand/finger driven controller challenging, researchers have been forced to construct large apparatuses to achieve similar findings (e.g., Schusterman & Kastak, 1993;Reichmuth Kastak & Schusterman, 2002b). ...
... Similarly, human infants seem to enjoy observing their own reflections prior to understanding that they are the human in the reflection (see Rochat, 2001). Observations of the reinforcing nature of choice have been reported elsewhere in animals (Tarou et al., 2004;Egelkamp & Ross, 2018), and control has been noted as one of the Four Cs of psychological well-being in primates and is an important facet of enrichment (Washburn, 2015). Such results warrant further investigation in sea lions. ...
The use of technology in laboratory and zoological settings has provided opportunities for advancement of cognition research as well as cognitive enrichment in a variety of species. Such systems have been successfully created for nonhuman primates and introduced to other anatomically and physiologically diverse species such as bears and tortoises. However, such systems have yet to be used with frequency in aquatic species given the challenge of incorporating accessible technology in such a setting. Herein, we report the successful creation and implementation of a novel manipulatable computerized system with California sea lions (Zalophus californianus) housed in outdoor sea pens. The Enclosure Video Enrichment (EVE) system was created and provided to three adult male sea lions living at the U.S. Navy’s Marine Mammal Program. The interface was modified from those used with other species to accommodate the anatomical and physiological differences of the study subjects. Training procedures were adapted from those successfully used with nonhuman primates to emphasize successive learning approximations. Each of the sea lions introduced to EVE successfully learned to engage with the system at differing rates over the course of a year and a half. While each showed significant differences in interaction style (e.g., number of button presses), all were able to achieve the same criterion for acquisition. This system is the first recorded success in providing a technological means to test cognition in California sea lions through an animal-manipulated interface and has the potential to function as a form of cognitive enrichment in this species.
... Traditionally, primates are given access to computer enrichment systems to undertake cognition tasks [10]. These tasks motivate animals in zoos to exhibit comparable physical and cognitive processes and behaviours to their wild counterparts [34]. ...
... Computers developed for enrichment purposes for primates are typically screen devices designed to be used by humans, often making them inadequate both in terms of usability and function for primates. These devices are typically touch screens [10,34,67], tablet devices like iPads [4,16] and computer screens [2,3]. Screen devices are used for husbandry purposes [24] and to gain insight into a primate's mood, personality, social skills and food preferences [10]. ...
... These devices are typically touch screens [10,34,67], tablet devices like iPads [4,16] and computer screens [2,3]. Screen devices are used for husbandry purposes [24] and to gain insight into a primate's mood, personality, social skills and food preferences [10]. ...
... Although the use of technology in environmental enrichment was originally criticized for being artificial (Hosey et al., 2009), it has recently been more positively acknowledged because such technology-based enrichment can provide animals with "functionally natural" activities (Egelkamp & Ross, 2019;Martin & Shumaker, 2018) that would not be possible without the assistance of technology. The living environment of wild animals offers various stimuli that are not obtainable in a captive environment. ...
... In zoo environments, the use of movies, or more generally visually complex stimuli, is still limited, but touchscreen-based tasks have often been used for both research and enrichment purposes (Hopper, 2017). The value of implementing touchscreen-based tasks for animal welfare and visitor education has been previously described (Egelkamp & Ross, 2019;Herrelko et al., 2012). However, most of the touchscreen-based tasks use food rewards, and the contribution of visual stimuli to maintaining the motivation of animals may be limited. ...
... This study poses the question of defining what "natural" behavior is. Our approach induced more dynamic behaviors than previous approaches that used touch screen or joystick devices (Egelkamp & Ross, 2019;Tarou et al., 2004), such as in the study that used interactive projections of zoo-housed orangutans (Carter et al., 2021). Some traditional enrichment also uses artificial materials, such as buoys and burlap sacks, facilitating naturalistic actions. ...
Environmental enrichment is essential for the well-being of zoo animals. Recent advances in sensor and video technologies may contribute to improvements in enrichment in terms of their flexibilities and time constraints. The purpose of this study was to investigate whether interactive movie art can be used as a form of environmental enrichment. We implemented interactive movies designed by a professional artist, a visual art aiming to reflect naturalistic forest habitat, in an indoor chimpanzee enclosure at Kyoto City Zoo in Japan. Motion-tracking sensors embedded in buoys were installed at several locations around the indoor enclosure; the chimpanzees could change the movie contents by physically interacting with these objects. We recorded behaviors by observing entire troop of chimpanzees (six) between March 16 and 20, 2020 (control condition), then recorded behaviors when the interactive movie was presented (experimental condition) between March 21 and 29, 2020. Behaviors were recorded via direct observations and video recordings to examine any changes after the installation of interactive art. The chimpanzees spent more time in the indoor enclosures during the experimental condition than during the control condition. Activity budgets did not change substantially during the study period. There was no evidence of habituation to the movie during the study period. Three chimpanzees, including two young chimpanzees, interacted with the movie more frequently than the others; these young chimpanzees occasionally showed playful expressions when interacting with the movie and exhibited different reactivities to the movie scenes. These results demonstrate, first, that the interactive art did not negatively affect chimpanzee behavior, and second, that some of the chimpanzees indeed showed positive responses to the art. This study, therefore, introduces a novel possibility for environmental enrichment in zoos, involving a collaboration between science and art.
... Digital technologies are increasingly used with and for nonhuman animals (hereafter, animals) to track behavior (Nelson & Shih, 2017), support welfare (French et al., 2018), facilitate human-animal interaction (Kleinberger et al., 2020), and study comparative cognition (Egelkamp & Ross, 2019). Such technologies are rapidly evolving and offer creative scope for a vast array of specific uses with both animals and humans. ...
... In several modern zoos, interactive digital technologies have been provided to apes for cognitive research as well as enrichment. These initiatives are often seen as opportunities for public engagement and education, by allowing zoo visitors to learn about the animals' cognitive abilities and motivate their interest in species conservation (Egelkamp & Ross, 2019;Shumaker, 2018). At Zoo Atlanta, for instance, the 'Learning Tree' presented orangutans with a touchscreen housed in a large artificial tree for cognitive testing and enrichment. ...
... Similarly, great apes at zoo-based research centers such as the Smithsonian's Think Tank exhibit and Indianapolis Zoo's Simon Skjodt International Orangutan Center participate in cognition research using touch-sensitive computers (Egelkamp & Ross, 2019) in front of audiences (Shumaker, 2018). In computer-based testing paradigms, food rewards help train apes to use devices correctly and reinforce correct responses to cognitive tests. ...
This paper examines how digital technologies might be used to improve ethical attitudes towards nonhuman animals, by exploring the case study of nonhuman apes kept in modern zoos. The paper describes and employs a socio-ethical framework for undermining anti-ape prejudice advanced by philosopher Edouard Machery which draws on classic anti-racism strategies from the social sciences. We also discuss how digital technologies might be designed and deployed to enable and enhance rather than impede the three anti-prejudice strategies of contact and interaction, enlightenment, and individualization. In doing so, the paper illuminates the broad potential and limitations of digital technology to both harm and benefit animals via its effects on human ethical attitudes. This examination provides guidance for future projects and empirical work on using digital technologies to promote moral respect for a range of nonhuman animals in different settings.
... A second type of cognitive challenge that is becoming increasingly prevalent for terrestrial animals are virtual puzzles or games presented on a computer interface (see reviews in, e.g., [120,121]). Although thus far many of these animal computer systems have been implemented for the purpose of conducting cognitive research rather than for providing enrichment, there is evidence that such cognitive tasks do in fact provide enrichment [120][121][122], and such tools could easily lend themselves to presenting appropriate cognitive challenges even outside of a specific research study. ...
... A second type of cognitive challenge that is becoming increasingly prevalent for terrestrial animals are virtual puzzles or games presented on a computer interface (see reviews in, e.g., [120,121]). Although thus far many of these animal computer systems have been implemented for the purpose of conducting cognitive research rather than for providing enrichment, there is evidence that such cognitive tasks do in fact provide enrichment [120][121][122], and such tools could easily lend themselves to presenting appropriate cognitive challenges even outside of a specific research study. As with physical puzzles, the key for virtual puzzles is that they must include something for the animal to figure out. ...
Simple Summary
Over the past several decades, the attention paid to the physical needs of marine mammals in zoos and aquariums has led to steady improvements in their physical well-being. Up until now, however, we haven’t paid as much attention to their cognitive needs. Studies have suggested that providing animals with puzzles and games that engage their thinking skills can improve their welfare. To help marine mammal managers and trainers achieve this for the animals in their care, this paper discusses different ways of creating such puzzles and thinking games, along with the pros and cons of each.
Abstract
The past several decades have witnessed significant improvement in the physical welfare of marine mammals in zoos and aquariums. Over that same time period, research has revealed complex cognitive abilities in at least some of these species, yet there has been comparatively little attention paid to addressing their cognitive welfare per se. Studies primarily conducted with terrestrial animals have suggested that providing appropriate cognitive challenges in managed care settings can improve animal well-being. As a step toward facilitating this practice with marine mammals, this paper discusses factors relevant for creating appropriate cognitive challenges, outlines the three major categories of cognitive challenge that have been utilized with marine mammals, along with the logistical pros and cons of each, and calls on organizations that care for marine mammals to cultivate a bias for action with respect to providing cognitive care.
... Unfortunately, comparative studies often suffer from low sample sizes due to the limited access to individuals and the major efforts and resources that are necessary to conduct noninvasive studies with animals. Indeed, a recent overview of touchscreen-based studies with great apes in zoos shows an average VAN BERLO, BIONDA, AND KRET 10 sample size of four (Egelkamp & Ross, 2019). Nevertheless, the findings are still valuable for improving our understanding of our evolutionary roots and great apes' sociocognitive competencies (similar to how findings in one or two patients with unique brain lesions have been crucial for understanding the neuroscientific foundations of emotion recognition [e.g., Adolphs et al., 1994]). ...
... We acknowledge that our sample size is limited compared to studies with humans. Nevertheless, it is in line with touchscreen-based experiments involving apes, which have an average sample size of fourEgelkamp & Ross, 2019). Despite this limitation, we argue that comparative studies such as ours have scientific merit and provide crucial insights into the cognitive abilities of animals. ...
Why can humans be intolerant of, yet also be empathic toward strangers? This cardinal question can be tackled by studying emotions in our closest living relatives, bonobos. Their striking xenophilic tendencies make them an interesting model for reconstructing the socioemotional capacities of the last common ancestor of hominids. Within two dot-probe studies, we compared bonobos’ and humans’ attention toward scenes depicting familiar (kith and kin) or unfamiliar individuals with emotional or neutral expressions. Results show that the attention of bonobos is biased toward emotional scenes depicting unfamiliar bonobos, but not toward emotional groupmates (Study 1). In contrast, Study 2 shows that human attention is biased toward emotional rather than neutral expressions of family and friends, but not toward unfamiliar others. On the one hand, our results show that an attentional bias toward emotions is a shared phenomenon between humans and bonobos, but on the other, both species have their own unique evolutionarily informed biases. These findings support previously proposed adaptive explanations for xenophilia in bonobos that potentially biases them toward emotional expressions of unfamiliar conspecifics, and parochialism in humans, which makes them sensitive to the emotional expressions of close others.
... While restricting the movement of subjects has practical benefits, there are several scientists beginning to experiment with less restrictive data collection methods, for example cage-based cognitive testing in animal housing environments such as touchscreen "kiosk" stations [93]. Just to give one example, we have developed touchscreen kiosks for our monkeys, and allow them to perform gambling tasks; we find that the data generated in these contexts is just as good (indeed, may be more externally valid) than data generated using conventional chaired techniques [94]. While these kiosks have scientific benefits, such as improved ecological validity (because tasks allow for unrestrained species-typical behaviors) and reduced manpower (because the animal does not need to be handled), they also improve welfare by allowing for more free movement in the world, which animals typically find rewarding. ...
... Indeed, in-cage touchscreens have been shown to be a form of cognitive enrichment and also allow for autonomy, provision of choice (e.g., the choice of which task to engage in, at what time, and for how long), and a sense of agency, which are imperative for psychological well-being [94][95][96]. Handling and transfers to primate chairs are also a source of stress eliminated by home-cage kiosks. Touchscreen kiosks also may allow for a Reduction in the number of animals used in the study as a single animal, with access to a kiosk all day, can work multiple times per day, when it is most motivated (an animal's time preferences may change daily and be difficult to predict by investigators). ...
Recent years have witnessed major advances in the ability of computerized systems to track the positions of animals as they move through large and unconstrained environments. These systems have so far been a great boon in the fields of primatology, psychology, neuroscience, and biomedicine. Here, we discuss the promise of these technologies for animal welfare. Their potential benefits include identifying and reducing pain, suffering, and distress in captive populations, improving laboratory animal welfare within the context of the three Rs of animal research (reduction, refinement, and replacement), and applying our understanding of animal behavior to increase the “natural” behaviors in captive and wild populations facing human impact challenges. We note that these benefits are often incidental to the designed purpose of these tracking systems, a reflection of the fact that animal welfare is not inimical to research progress, but instead, that the aligned interests between basic research and welfare hold great promise for improvements to animal well-being.
... To make flexible virtual environments available to a large number of captive primates, be it for scientific or cognitive enrichment purposes (59), tasks that are easy to set up, easy to learn, and engaging need to be developed. Computerized testing, in particular with touch screen interfaces, has become widespread in cognitive research with nonhuman primates in captive settings (61). In addition, providing naturalistic environments affords the capacity to address a variety of questions that link nonhuman primate behavioral ecology and experimental spatial cognition (2,59). ...
... More generally, virtual environments may be used for studying navigation in any species that can use an input device like a touch screen, eye tracker, or joystick for computerized testing with visual feedback. The list of species that have successfully been trained for computerized testing currently includes all great ape species (Gorilla gorilla, Pan paniscus, Pan troglodytes, and Pongo spp.), capuchins (Sapajus apella), macaques (Macaca spp.), dogs (Canis familiaris), kea (Nestor notabilis), pigeons (Columbidae spp.), and bottlenose dolphins [Tursiops truncatus; see (61,71,(78)(79)(80)]. Moreover, with virtual environments, there is no need to restrict studies to investigating ground navigation; rather, environments could be tailored to the study species, e.g., with flight simulation for avian species. ...
Almost all animals navigate their environment to find food, shelter, and mates. Spatial cognition of nonhuman primates in large-scale environments is notoriously difficult to study. Field research is ecologically valid, but controlling confounding variables can be difficult. Captive research enables experimental control, but space restrictions can limit generalizability. Virtual reality technology combines the best of both worlds by creating large-scale, controllable environments. We presented six chimpanzees with a seminaturalistic virtual environment, using a custom touch screen application. The chimpanzees exhibited signature behaviors reminiscent of real-life navigation: They learned to approach a landmark associated with the presence of fruit, improving efficiency over time; they located this landmark from novel starting locations and approached a different landmark when necessary. We conclude that virtual environments can allow for standardized testing with higher ecological validity than traditional tests in captivity and harbor great potential to contribute to longstanding questions in primate navigation, e.g., the use of landmarks, Euclidean maps, or spatial frames of reference.
... Touchscreen computers in primate cognitive research are described by Perdue et al. [42]. Egelkamp and Ross [43] survey the history and wide international uses of such systems. They suggest that advantages of computer use include the ability to record data while researchers are not present, thus avoiding experimenter bias and improving efficiency. ...
... The intended setting is also important, for example, in public areas where visitor education and possible interaction is intended, or in off-exhibit areas and isolated research settings. Once learned, touchscreen use appears to be enriching to the animal users, with ninety percent of apes and macaques tested at Lincoln Park Zoo voluntarily participating [43] and even sun bears actively participated at Zoo Atlanta [42]. ...
... Previous work has thoroughly reviewed the species involved and methods used in cognitive research in zoos (Hopper, 2017), the range of research in primate sanctuaries (Ross & Leinwand, 2020), and the extent of primate cognition research using touchscreens in zoos (Egelkamp & Ross, 2019). Here, we compare the number of articles published, the diversity of species investigated, and the level of technological sophistication required by each investigation, to place the impact of zoo-based primate cognition research in context with other site types. ...
... It is also important, however, to consider the positive impacts that zoo-based research can have on the primates and institutions themselves. Primate cognition research conducted in zoos can have positive implications such as contributing to animal welfare and enhancing science education(Egelkamp & Ross, 2019). ...
Primate cognition research is reliant on access to members of the study sp ecies and logistical infrastructures to conduct observations and experiments. Historically founded in research centers and private collections, and spreading to modern zoos, sanctuaries, and the field, primate cognition has been investigated in diverse settings, each with benefits and challenges. In our systematic review of 12 primatology, animal behavior, and animal cognition journals over the last 15 years, we turn a spotlight on zoos to quantify their current impact on the field and to highlight their potential as robust contributors to future work. To put zoo-based research in context, we compare zoos to three other site types: university-owned or independent research centers, sanctuaries, and field sites. We assess the contributions of zoos across several critical considerations in primate cognition research, including number of investigations, species diversity, sample size, research topic diversity, and methodology. We identified 1119 publications reporting studies of primate cognition, almost 25% of which report research conducted in zoos. Across publications, zoo-based research has greater species diversity than research centers and covers a diverse range of research topics. Although our review is merely a snapshot of primate cognition research, our findings suggest that zoos may present advantages to researchers regarding species diversity, and lack some of the methodological constraints of field sites, allowing greater ease of access to a diverse range of subjects for cognition investigations. We suggest that zoos have great potential as key contributors for future investigations in primate cognition. Finally, we shed light on the symbiotic relationship that can emerge between researchers and zoos, forming partnerships that bring unique advantages to both parties.
... In some locations, such as the Orangutan Learning Tree exhibit at Zoo Atlanta, members of the public are able to observe live research with animals during their visit. Exposure to animal research suggests that it may improve overall attitudes towards research methods involving animals (Clay et al., 2011;Egelkamp & Ross, 2018;Perdue, Clay, et al., 2012;Shumaker, 2018). This is likely to be important because misperceptions or misunderstandings about the nature of animal research can have broader implications for zoos and policy. ...
... The results showed improved attitudes towards orangutans immediately after the visitors' visit and in the follow-up evaluations when compared to before their visit -indicating lasting effects from their experience observing orangutan cognitive research (Alexander et al., 2017;Shumaker, 2018). Overall, cognitive research involving great apes serves as positive enrichment for the animals and has received positive feedback from the observing public allowing for greater knowledge and interest in conservation issues (Clay et al., 2011;Egelkamp & Ross, 2018;Ross, 2017;Shumaker, 2018;Webber et al., 2017;Whitehouse et al., 2014). ...
Zoos average about 183 million visitors per year, which makes them a major source for educating the public due to the diverse and wide-ranging demographic that visit. Zoos are increasingly a source of scientific research in a variety of subfields, including animal cognition, although much of this research takes place behind the scenes. Bringing this research to the public perspective has the potential to increase engagement of zoo visitors. However, it is not always possible to show live research, but videos have been found to be an effective educational approach in other domains. Here, we presented a brief video illustrating cognitive research involving sun bears at Zoo Atlanta to determine the potential effect on visitors. We measured several aspects of visitor behavior (stay time and actual behaviors in the exhibit), attitudes (towards both animal research and educational technology), and knowledge gained at the exhibit. We also presented a control video that focused on sun bear enrichment to tease out whether potential effects on visitors were related to the research focus of the video, or merely an effect of a video playing in the exhibit space. Visitor behavior, attitudes, and knowledge were determined by observing a randomly selected visitor’s behavior throughout their time in the exhibit space, and then requesting completion of a survey when they exited the exhibit (N = 148). We compared various aspects of behavior, attitudes, and knowledge across the Scientific Video, Enrichment Video, and No Video conditions. There were no differences between the Scientific Video and the Enrichment Video conditions; however, some differences were found between visitors who experienced a video during their visit (scientific or enrichment video) versus those who did not. Attitudes towards technology in the exhibit space were generally positive. There was also a significant correlation between visitor stay time (overall time spent in the exhibit space) and knowledge gained. Visitors learning about research in zoos remains important, but it is unclear if a video is a sufficient means to share that information.
... The use of virtual stimuli has become common in studies of both human psychology and animal cognition [1][2][3][4][5][6][7]. Subjects are sometimes required to respond to virtual stimuli through real-life choices, for example by selecting between real-life objects and agents after observing relevant videos on a screen [8,9]. ...
... To date, there have been no attempts to test whether animals also expect a discontinuity in physical events between the real and virtual worlds, despite the regular use of virtual stimuli and VR in animal testing [3][4][5][6][7], and studies showing that they recognize images of real objects on both photographs and screens [11][12][13][14][15]. It is therefore unclear if animals are naive realists and behave equivalently across VR, mixed and fully real contexts or if, like 19-month-old infants, they perceive a disconnect between events occurring in virtual and real environments. ...
Human psychology and animal cognition have increasingly used virtual stimuli to test cognitive abilities, with the expectation that participants are ‘naive realists’, that is, that they perceive virtual environments as both equivalent and continuous with real-life equivalents. However, there have been no attempts to investigate whether nonhuman subjects in fact behave as if physical processes in the virtual and real worlds are continuous. As kea parrots have previously shown the ability to transfer knowledge between real stimuli and both images on paper and images on touchscreens, here we test whether kea behave as naive realists and so expect physical processes to be continuous between the physical and virtual worlds. We find that, unlike infants, kea do not discriminate between these two contexts, and that they do not exhibit a preference for either. Our findings therefore validate the use of virtual stimuli as a powerful tool for testing the cognition of nonhuman animal species.
... Typically, an animal waits already at the gate of the apartment cage before it is opened by the operator with the gate remaining open for 90-120 min on weekdays daily so that animals can choose whether to engage with the kiosk. This indicates anticipation and motivation to engage with the Kiosk touchscreen and confirms prior reports that Kiosk engagement is a form of cognitive enrichment (Washburn and Rumbaugh, 1992;Bennett et al., 2016;Calapai et al., 2017;Egelkamp and Ross, 2019). There are few exceptions to this behavior. ...
... Previous work with rhesus monkeys in cage-based touchscreen settings showed that these task variations can reliably measure working memory, perceptual classification, or transitive inferences, amongst others (Fagot and Paleressompoulle, 2009;Gazes et al., 2013;Hutsell and Banks, 2015;Calapai et al., 2017;Curry et al., 2017;Fizet et al., 2017;Berger et al., 2018;Sacchetti et al., 2021). Such cognitive testing is not restricted to rhesus monkeys as prior work showed cognitive engagement with touchscreens in multiple species including baboons (Fagot and Paleressompoulle, 2009;Fagot and De Lillo, 2011;Rodriguez et al., 2011;Claidiere et al., 2017), capuchin monkeys (Evans et al., 2008), marmosets (Kangas et al., 2016;Walker et al., 2020), and others (Hopkins et al., 1996;Beran et al., 2005;Egelkamp and Ross, 2019). ...
Nonhuman primates (NHP’s) are self-motivated to perform cognitive tasks on touchscreens in their animal housing setting. To leverage this ability, fully integrated hardware and software solutions are needed that work within housing and husbandry routines while also spanning cognitive task constructs of the Research Domain Criteria (RDoC). Here, we detail such an integrated robust hardware and software solution for running cognitive tasks in cage-housed NHP’s with a cage-mounted Kiosk Station (KS-1). KS-1 consists of a frame for mounting flexibly on housing cages, a touchscreen animal interface with mounts for receptables, reward pumps, and cameras, and a compact computer cabinet with an interface for controlling behavior. Behavioral control is achieved with a Unity3D program that is virtual-reality capable, allowing semi-naturalistic visual tasks to assess multiple cognitive domains.KS-1 is fully integrated into the regular housing routines of monkeys. A single person can operate multiple KS-1’s. Monkeys engage with KS-1 at high motivation and cognitive performance levels at high intra-individual consistency. KS-1 is optimized for flexible mounting onto standard apartment cage systems and provides a new design variation complementing existing cage-mounted touchscreen systems. KS-1 has a robust animal interface with options for gaze/reach monitoring. It has an integrated user interface for controlling multiple cognitive tasks using a common naturalistic object space designed to enhance task engagement. All custom KS-1 components are open-sourced.In summary, KS-1 is a versatile new tool for cognitive profiling and cognitive enrichment of cage-housed monkeys. It reliably measures multiple cognitive domains which promises to advance our understanding of animal cognition, inter-individual differences, and underlying neurobiology in refined, ethologically meaningful behavioral foraging contexts.
... There are also a range of physical interface options that can be adapted for use by animals-even dolphins have been successfully provided with underwater keyboard systems [59]. Much ACI technology uses touchscreen interfaces, which have been used for a long time in zoos to test animals' cognitive capacities as well as provide them with cognitive stimulation to improve their welfare [60]. As an example, Zoo Atlanta successfully implemented a touchscreen in a tree of the orangutan enclosure called the "Learning Tree" (https://zooatlanta.org/orangutan-learning-tree/, (accessed on 10 December 2024)). ...
Recent discussions in animal welfare have emphasised the importance of animal agency—the ability of animals to make choices and exert control over their environment in a way that aligns with their needs and preferences. In this paper, we discuss the importance of animal agency for welfare and examine how use of some types of animal–computer interaction can enable animals to exercise more agency in captive environments through increased choice and control, cognitive challenge, and social interactions; as well as considering some of the potential limitations of such efforts.
... Technology's rapid development and integration into more and more of day-to-day life has given impetus to research investigating how animals engage with screen-based stimuli, and constant evolution in the felds of human-computer interaction (HCI) and animal-computer interaction (ACI) has cultivated frameworks and tools aligned with this aim [14]. We anchored our study in prior work exploring screen-mediated interactions among birds, animal agency, and video calling for animals. ...
... In recent years, many matching-to-sample tasks have been performed using computer-controlled touch panels. There are several advantages in using these devices [1]. First is the intuitive clarity created by the direct relationship between the stimulus projected on the screen and the animal's response to that stimulus. ...
Matching-to-sample tasks have been a useful method in visual cognitive studies on non-human animals. The use of touch panels in matching-to-sample tasks has contributed to cognitive studies on terrestrial animals; however, there has been a difficulty in using these devices underwater, which is one of the factors that has slowed the progress of visual studies on underwater animals. Cetaceans (e.g., dolphins and whales) are highly adapted to underwater environments, and further studies on their cognitive abilities are needed to advance our understanding of the interactions between environmental factors and the evolution of cognitive abilities. In this study, we aimed to develop a new experimental method in which a captive killer whale performed a matching-to-sample task using a monitor shown through an underwater window as if a touch panel were used. In order to confirm the usefulness of this method, one simple experiment on mirror image discrimination was conducted, and the pairs with mirror images were shown to be more difficult to identify than the pairs with other normal images. The advantages of using this method include (1) simplicity in the devices and stimuli used in the experiments, (2) appropriate and rigorous experimental control, (3) the possibility of increasing the number of individuals to be tested and interspecies comparisons, and (4) contributions to animal welfare. The use of this method solves some of the problems in previous visual cognitive studies on cetaceans, and it suggests the further possibility of future comparative cognitive studies. It is also expected to contribute to animal welfare in terms of cognitive enrichment, and it could help with the proposal of new exhibition methods in zoos and aquariums.
... Perhaps captive individuals in group-living species express reduced anxiety when exposed to a photograph of an unknown and smaller conspecific. Some researchers are exploring the use of computer touchscreens for animals in captivity as a form of enrichment (Egelkamp and Ross 2019;Scheer et al. 2019;Webber et al. 2020;Kleiber et al. 2021). In captive Sumatran Orangutans (Pongo abelii), individuals interacting with a touchscreen preferred to view photographs of conspecifics over humans (Adams and MacDonald 2018). ...
Cues to individuality, and the corresponding capacity for individual-level discrimination, can allow individually specific investment by conspecifics into offspring, partners, neighbors or competitors. Here we investigated possible cues to individuality via faces in an ancient avian lineage, the Greylag Goose ( Anser anser ). Konrad Lorenz could famously name each Greylag Goose in ‘his’ flock from a photograph. Confirming this anecdotal observation, we developed facial recognition software that can reliably (~ 97% accuracy) assign a goose face to a goose ID within a database, using bill morphology normalized during photo preparation. To explore conspecific detection of individuality cues, we erected life-size photos of geese and measured subjects’ responses to photos of themselves (unfamiliar goose), their partner, and another flock mate. Geese displayed significantly greater affiliative response to photos of their partners, providing evidence that geese can use two-dimensional images as cues to determine social category (partner/non-partner) and/or individual-level recognition. Our methods provide novel approaches to automatically detect and monitor geese and to test avian cognition. Our approach may also create new opportunities for species monitoring approaches more generally using photographic images and citizen-science engagement.
... For instance, does manipulation knowledge need to be acquired before being able to use increasingly sensorimotor decoupled MTTA, or does the latter even allow for tool use with less derived cognitive and manual prerequisites? On the one hand, primates are quite able to use human touchscreens (Egelkamp and Ross, 2019), e.g., to navigate an avatar through three-dimensional space (Allritz et al., 2022). On the other hand, young children have difficulties in transferring tool use strategies learned from 2D screen media to real-life (Moser et al., 2015;Hipp et al., 2017). ...
Tools have coined human life, living conditions, and culture. Recognizing the cognitive architecture underlying tool use would allow us to comprehend its evolution, development, and physiological basis. However, the cognitive underpinnings of tool mastering remain little understood in spite of long-time research in neuroscientific, psychological, behavioral and technological fields. Moreover, the recent transition of tool use to the digital domain poses new challenges for explaining the underlying processes. In this interdisciplinary review, we propose three building blocks of tool mastering: (A) perceptual and motor abilities integrate to tool manipulation knowledge, (B) perceptual and cognitive abilities to functional tool knowledge, and (C) motor and cognitive abilities to means-end knowledge about tool use. This framework allows for integrating and structuring research findings and theoretical assumptions regarding the functional architecture of tool mastering via behavior in humans and non-human primates, brain networks, as well as computational and robotic models. An interdisciplinary perspective also helps to identify open questions and to inspire innovative research approaches. The framework can be applied to studies on the transition from classical to modern, non-mechanical tools and from analogue to digital user-tool interactions in virtual reality, which come with increased functional opacity and sensorimotor decoupling between tool user, tool, and target. By working towards an integrative theory on the cognitive architecture of the use of tools and technological assistants, this review aims at stimulating future interdisciplinary research avenues.
... Touchscreens have been successfully used for experiments in life enrichment [4,10,17] and in Comparative Psychology [6], with individuals from various nonhuman species. Could digital Life Enrichment techniques allows the replication of Al Aïn et al. [1]'s results at a lower cost, but with a better precision, and with less potential experimental bias? ...
Ain et al. [1] measured three African Grey (Psittacus Erithacus)
parrots’ discrimination abilities between discrete and continuous
quantities. Some features of their experimental protocol make it
difficult to apply to other subjects and/or species without intro-
ducing a risk for some bias, as subjects could read cues from the
experimenter (even though the study’s subjects probably did not).
Can digital life enrichment techniques permit us to replicate their
results with other species with less risk for experimental bias, with
a better precision, and at lower cost? Inspired by previous informal
digital life enrichment experiments with parrots, we designed and
tested a web application to digitally replicate and extend Ain et
al.’s experimental setup. We were able to obtain similar results
to theirs for two individuals from a distinct species of parrots,
Monk Parakeets (Myiopsitta Monachus), with increased guaran-
tees against potential experimental biases, in a way which allows
the replication of such experiments at larger scale and at a much
lower cost.
... Implementing cognitive challenges for animals in professional care has recently become a focus of research and management efforts to improve welfare and enrichment programs [1][2][3]. Modern research on animal cognition has shifted focus to emotional welfare but investigation of cognitive needs is still lacking [4,5]. Animals are naturally highly motivated to explore and acquire resources in various conditions [6,7] (p. ...
Cognitive enrichment for professionally managed species has become more prevalent in recent years in both zoological and research settings and has been encouraged as a means of welfare enhancement. However, the task’s difficulty must be specifically tailored as it can impact the successful nature of the sessions, as tasks that are too simple or difficult may not be perceived as enriching by the animals. While pinnipeds are common in zoos, aquariums, and research facilities, few studies have explored the use of cognitively challenging enrichment in this species, and the level of difficulty and presence of failure on animal success and engagement in this type of session has not been assessed. In this study, gameplay strategies during computerized enrichment sessions were evaluated before and after a game that introduced failure, or the loss of opportunity to complete a level for a reward after an incorrect movement. Interest in participation during the session, measured as the latency without contact, was also tested as a proxy for this enrichment’s effect on welfare. When incorrect movements resulted in a short pause and removed the opportunity to finish individual levels for a reward, all three sea lions tested significantly reduced the amount of time spent on each of several strategies they employed, but significantly increased the number of button presses per strategy, suggesting the animals focused on more precise movements as their proficiency improved. Two sea lions also showed a significant decline in latency without contact following the introduction of failure in the form of a single opportunity to complete a task for a reward after previously having unlimited opportunities, while one maintained a low latency without contact across both test conditions. The results suggest that more cognitively challenging tasks incorporating failure did not cause a reduction in gameplay performance and session interest in sea lions. Individual variation was also noted in strategy use, emphasizing the importance of evaluating the individual in terms of enrichment provision.
... Although comparative study of nonhuman primates is by no means a new endeavor, the scope of species involved has been relatively limited. Most studies of NHP cognition evaluate members of the catarhines (Cercopithecoidea; Egelkamp et al., 2018;Joly et al., 2014;Munger et al., 2017;Nagahara et al., 2010;Ryan et al., 2019;Rodriguez et al., 2011;Taffe & Taffe, 2011;Vogel et al., 2009;Weed et al., 2008;Zurcher et al., 2010) or the great apes (Hominidae; Beran et al., 2016;Call, 2001Call, , 2010Cronin et al., 2017;Damerius et al., 2019;Hopper et al., 2019Hopper et al., , 2021Inoue & Matsuzawa, 2007;Kanngiesser & Call, 2010;Köhler, 1925;Morimura & Matsuzawa, 2001;Osvath & Martin-Ordas, 2014;Rumbaugh & Rice, 1962;Vonk, 2013;Vonk et al., 2013;Vonk & MacDonald, 2004;Vonk & Rastogi, 2019;Wagner et al., 2016;Wobber et al., 2014;Yerkes & Yerkes, 1929). Despite certain species of hylobatid (e.g., Hylobates lar) being commonly housed in captivity, most studies exclude gibbons and siamangs (Abordo, 1976;Andrieu et al., 2020;Caspar et al., 2018;Cunningham et al., 2006;Sánchez-Amaro, 2021), which occupy a phylogenetic position between the two more-commonly studied groups (Hopper, 2017). ...
Studies of nonhuman primate cognition have traditionally employed subjects from the monkey (Cercopithecoidea) and ape (Hominidae) lineages, with relatively much less examination of the phylogenetically intermediate gibbons (Hylobatidae). To begin to rectify this gap in our understanding of primate cognition, we used a short-term training and testing method to preliminarily evaluate siamang gibbon (Symphalangus syndactylus) performance on a battery of standardized cognitive tasks, using Monkey CANTAB cognition testing software (Lafayette-Campden Neuroscience) and a computer touchscreen apparatus. Five different operant tasks examining distinct perceptual and cognitive functions were used to train and test each subject over a period of five weeks. Over 1900 cognitive testing trials were completed with three subjects. Despite limited training and testing opportunity, all siamangs achieved proficiency scores well above chance (> 65%) in both Concurrent Discrimination and Spatial Working Memory tasks. Over the limited training opportunities available, our subjects did not achieve proficiency in Delayed Match-to-Sample, Paired Associates Learning, or Conditional Visual Discrimination tasks; however, subjects did exhibit (to varying degrees) improved performance in these tasks, suggesting that additional training may lead to higher proficiency and that siamangs demonstrate effective, task-based learning capabilities. We present one of the first successful tests of a hylobatid ape using touchscreen cognitive testing methods and demonstrate that hylobatids can be evaluated using the same methods now commonly employed in tests of other nonhuman primates. Further, our testing regime proved to be behaviorally rewarding for our subjects, suggesting that hylobatids may benefit from advanced forms of interactive cognitive enrichment.
... Computerized testing allows us to control the level, timing, and duration of challenge and record the participants' behavioral and physiological responses at the same time. There are already two decades of digitized Flow research on humans to build upon , and computerized testing has already been used to investigate the cognitive abilities of a range of species (Egelkamp & Ross, 2019;Kangas & Bergman, 2017;Seitz et al., 202;Washburn et al., 2017). Despite the popularity of computerized testing, it requires captive animals under at least moderately high control, so sample sizes and generalizability to an entire species are restricted. ...
Flow is an altered state of feeling ‘in the zone’ when fully absorbed in a challenge and is associated with positive affective state (feelings). Despite almost five decades of research, Flow has not yet been recognized in non- human animals, despite repeated suggestions from animal researchers it could exist. Recent advancements in behavioral and neurophysiological indicators of experience in humans and animals make it more possible than ever to detect Flow in other species. In this article, I propose a framework for comparative Flow research on humans and great apes. I conserve the original nine-component definition of human Flow developed by Csikszentmihalyi and its three conditional components, but re-structure the six experiential components into three dimensions: Focus, Motivation, and Affect. I evaluate the evidence for each dimension and component in great apes, and how current human Flow methods may translate to great apes. If Flow state exists beyond our species, this has major implications. It would provide insight into the evolution of internally derived happiness and ignite more comparative research in the field of positive psychology. Second, knowledge of Flow or a Flow-like state in other species would inform the design of more effective enrichment and therefore promote higher captive animal welfare. I hope to spark new discussions among human positive psychologists, comparative psychologists, and animal cognition and welfare scientists, so that we may begin to conceptualize and recognize non-human Flow.
... Most computer-enabled systems for enrichment have been used with great apes and involve tasks on screens [8,30]. The interfaces have typically taken the form of touchscreens [2,15,44,50,54] or joysticks [34] but have also involved balls [48], brain-teaser puzzles [14] and projected screens [5]. ...
... Touchscreens have been used in captivity to examine cognitive processes including memory, decision making, associative and reversal learning, and collaboration (Egelkamp & Ross, 2019). There are already many examples of cognitive testing using touchscreens in captive primates (Martin et al., 2022). ...
Touchscreen technology has provided researchers with opportunities to conduct well‐controlled cognitive tests with captive animals, allowing researchers to isolate individuals, select participants based on specific traits, and control aspects of the environment.
In this study, we aimed to investigate the potential utility of touchscreen technology for the study of cognition in wild vervet monkeys. We assessed the viability of touchscreen testing by comparing rates of participation between wild and sanctuary‐housed vervets. Additionally, we compared performance on a simple associative learning task in order to verify that wild participants are able to engage meaningfully with a touchscreen task presented in their natural environment.
We presented eight groups of vervet monkeys (four wild and four sanctuary groups, totalling 240 individuals) with a portable touchscreen device. The touchscreen displayed tasks in which food rewards could be gained by touching a stimulus displayed on the screen. We assessed individuals' likelihood of interacting with the touchscreen, their frequency of participation, and their performance on a simple associative learning task.
We found that sanctuary‐housed monkeys were more likely to interact with the touchscreen. Participation in wild vervet monkeys was influenced by sex and age. However, monkeys in the two contexts (sanctuary vs. wild) did not differ in their performance on a simple associative learning task.
This study demonstrates that touchscreen technology can be successfully deployed in a population of wild primates. This gives us a starting point to test animal cognition under natural conditions that include varying group composition, environmental challenges and ongoing activities such as foraging, which are challenging to recreate in captivity. While rates of participation were lower than those found in captivity, reasonable sample sizes can be achieved, and wild primates can successfully learn touchscreen tasks in a manner comparable to their captive counterparts.
... In these systems, rather than moving the animal to a different testing area, the testing apparatus itself can be moved to the familiar environment in which the primate is housed (e.g., Crofts et al., 1999;Prescott et al., 2010). In nontraditional research venues, such as zoos and sanctuaries, where specialized research areas may not be present, such home-cage testing paradigms may be especially relevant (Egelkamp & Ross, 2019;Ross & Leinwand, 2020). For protocols where transport or restraint is still deemed necessary, a number of refinements have been adopted to reduce the welfare burden on primate subjects. ...
Researchers have studied non-human primate cognition along different paths, including social cognition, planning and causal knowledge, spatial cognition and memory, and gestural communication, as well as comparative studies with humans. This volume describes how primate cognition is studied in labs, zoos, sanctuaries, and in the field, bringing together researchers examining similar issues in all of these settings and showing how each benefits from the others. Readers will discover how lab-based concepts play out in the real world of free primates. This book tackles pressing issues such as replicability, research ethics, and open science. With contributors from a broad range of comparative, cognitive, neuroscience, developmental, ecological, and ethological perspectives, the volume provides a state-of-the-art review pointing to new avenues for integrative research.
... For an overview of monitoring systems (such as accelerometers to measure vibrations, GPS to determine location, bioacoustics to measure natural sounds, thermography to determine temperature, and individual identification using RFID), see [54]. Touch-screen computers, some accessible to the apes 24/7, in primate cognitive research has been found to be enriching [55][56][57]. Simple computers can allow both pre-programmed and remote operation of such devices as gates, feeders, touch screens, climate controls, and other enrichment features, as well as surveillance, security, and alarm systems, all accessible by smart phone from nearly anywhere in the world. Such systems have potential for use with primates and are already being used with elephants at the Dublin Zoo (G. ...
This review commentary focuses on traditional management practices and facility design with suggested improvements in non-public primate management areas, often called “back-of-house”, (henceforth BOH) in zoos, sanctuaries, and research facilities. Progress has been made toward improving animal quality of life in larger, more naturalistic, and enriched indoor and outdoor display areas. However, the quality of life in BOH areas has improved little in comparison. Basic management, regulatory, structural, and spatial BOH environments are lagging, especially in the developing world, and animals may be confined in less enriching spaces for substantial periods of the 24 h day. We reviewed traditional management policy and practice, as well as newer training, enrichment, and welfare policies and actions, and suggested alternatives for structural environments and spatial environments. The suggestions included using more animal-friendly construction materials and animal–computer interaction, providing greater control of the ambient environment and choice of access to multiple areas by the animals themselves, and designing for optimal animal wellbeing at all times, including when caregivers are no longer present. Case studies focused on primates were included. We concluded by suggesting a new, integrated design model based not upon rote standards and old models but building on empirical foundations while embracing empathy and innovation.
... Operant training was used to shape animal behavior and teach animals how to play the games (42). In cognitive research programs, primates and other animals have long used technologies such as joystick-controlled computers and touchscreen interfaces (43,44), and there are claims that this type of activity can be enriching for animals (44). In recent years, researchers have explored the potential of using sensor-based technologies to provide animals with greater variety, and more opportunities for active interaction and agency in their environment (45)(46)(47)(48) and to offer substitutes for natural behaviors, such as hunting live prey (49). ...
Digital technologies offer new ways to ensure that animals can lead a good life in managed settings. As interactive enrichment and smart environments appear in zoos, farms, shelters, kennels and vet facilities, it is essential that the design of such technologies be guided by clear, scientifically-grounded understandings of what animals need and want, to be successful in improving their wellbeing. The field of Animal-Computer Interaction proposes that this can be achieved by centering animals as stakeholders in technology design, but there remains a need for robust methods to support interdisciplinary teams in placing animals' interests at the heart of design projects. Responding to this gap, we present the Welfare through Competence framework, which is grounded in contemporary animal welfare science, established technology design practices and applied expertise in animal-centered design. The framework brings together the “Five Domains of Animal Welfare” model and the “Coe Individual Competence” model, and provides a structured approach to defining animal-centric objectives and refining them through the course of a design project. In this paper, we demonstrate how design teams can use this framework to promote positive animal welfare in a range of managed settings. These much-needed methodological advances contribute a new theoretical foundation to debates around the possibility of animal-centered design, and offer a practical agenda for creating technologies that support a good life for animals.
... Comparative research is most productive if different species can be tested with ecologically relevant problems presented to them in a comparable way (133)(134)(135). Recent advances in eye tracking (111,121,136,137) and touchscreen technology (66,138,139) render such an approach both feasible and simple to implement in a noninvasive setting. For example, eye tracking studies suggest that apes may be able to perform highlevel theory of mind assessments, such as understanding false belief, at an implicit level (136,140,141), and these implicit responses may also extend to Old World monkeys (142). ...
Languages tend to encode events from the perspective of agents, placing them first and in simpler forms than patients. This agent bias is mirrored by cognition: Agents are more quickly recognized than patients and generally attract more attention. This leads to the hypothesis that key aspects of language structure are fundamentally rooted in a cognition that decomposes events into agents, actions, and patients, privileging agents. Although this type of event representation is almost certainly universal across languages, it remains unclear whether the underlying cognition is uniquely human or more widespread in animals. Here, we review a range of evidence from primates and other animals, which suggests that agent-based event decomposition is phylogenetically older than humans. We propose a research program to test this hypothesis in great apes and human infants, with the goal to resolve one of the major questions in the evolution of language, the origins of syntax.
... Touchscreens have been successfully used for experiments in life enrichment [4,11,20] and in Comparative Psychology [7], with individuals from various nonhuman species. Could digital life enrichment techniques allow to replicate Al Aïn et al. [1]'s results at a lower cost, but with a better precision, and less potential experimental bias? ...
Ain et al. measured three African Grey (Psittacus erithacus) parrot's discrimination abilities between discreet and continuous quantities. Some features of their experimental protocol make it difficult to apply to other subjects and/or species without introducing a risk for some bias, as subjects could read cues from the experimenter (even though the study's subjects probably did not). Can digital life enrichment techniques permit us to replicate their results with other species with less risk for experimental bias, with a better precision, and at lower cost? Inspired by previous informal digital life enrichment experiments with parrots, we designed and tested a web application to digitally replicate and extend Ain et al.'s experimental setup. We were able to obtain similar results to theirs for two individuals from a distinct species, Monk Parakeets (Myiopsitta Monachus), with increased guarantees against potential experimental biases, in a way which should allow to replicate such experiments at larger scale and at a much lower cost.
... Indeed, in-cage touchscreens have been shown to be a form of cognitive enrichment and also allow for autonomy and provision of choice (e.g. the choice of which task to engage in, at what time, and for how long), which are imperative for psychological well being (Egelkamp et. al. 2016;Egelkamp & Ross 2019). Handling and transfers to primate chairs are also a source of stress eliminated by home-cage kiosks. ...
Recent years have witnessed major advances in the ability of computerized systems to track the positions of animals as they move through large and unconstrained environments. These systems have so far been a great boon in the fields of primatology, psychology, neuroscience, and biomedicine. Here, we discuss the promise of these technologies for animal welfare. Their potential benefits include identifying and reducing pain, suffering, and distress in captive populations, improving laboratory animal welfare within the context of the three Rs of animal research (reduction, refinement, and replacement), and applying our understanding of animal behavior to increase the natural behaviors in captive and wild populations facing human impact challenges. We note that these benefits are often incidental to the designed purpose of these tracking systems, a reflection of the fact that animal welfare is not inimical to research progress, but instead, that the aligned interests between basic research and welfare hold great promise for improvements to animal well-being.
... Digital interfaces can augment how cognitive challenges are provided to animals in their enclosure (e.g., the contrast between a tangible and digital maze, for example), and furthermore, provide more novel and repeatable experiences across time (13). Technology also creates opportunities for instant feedback and to automate processes such as food reward presentation (13)(14)(15). For the focus of this paper, however, we are interested in the use of technology to automatically log an animal's response to a cognitive enrichment device, foremost to save researcher time and effort, but also to prevent human observation from influencing animal behavior. ...
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.
... In zoo settings, automated touch-panel tasks can provide a platform for cognitive research, enrichment, and education (Egelkamp and Ross 2019). Major efforts to provide zoo-housed chimpanzees with touch panel tasks include the Lincoln Park Zoo (Egelkamp et al. 2016) and Kyoto City Zoo, Japan. ...
... cognition studies(Egelkamp & Ross, 2019). Nevertheless, single-subject studies have been key373 in animal cognition research(Pepperberg, 2009;Premack & Premack, 1983), including zoo 374 research(Slocombe & Zuberbühler, 2005), as they provide evidence that the trait under study is375 within the range of the species' cognitive abilities. ...
Social learning is of universal importance to animal life, and communication is likely to foster it. How do animals recognize when others produce actions that lead to relevant new information? To address this, we exposed 4 chimpanzees to an arbitrary learning task, a 2-choice visual discrimination paradigm presented on a touch screen that led to food reward. In each trial, images were paired with 1 of 4 acoustic treatments: (a) relevant or (b) irrelevant chimpanzee calls ("rough grunts" to food; "pant grunts" to a dominant conspecific), (c) a mechanical noise (hammer knocking sounds) and (d) silence. As we were interested in the effect of food calls on learning speed as compared to control stimuli, each chimpanzee was tested with the food call treatment, and 1 of the 3 control stimuli (either the pant grunt, mechanical noise, or silence condition). We found that learning was significantly enhanced in the contextually correct "rough grunt" condition, suggesting that food calls may play a role in the cultural transmission of food preferences, by priming individuals about a learning opportunity. We discuss these findings and propose that, at least in chimpanzees, the enhancing effect of these vocalizations may be related to the way they affect receivers' motivational/emotional and/or attentional systems. (PsycInfo Database Record (c) 2021 APA, all rights reserved).
... Public-facing cognitive research is becoming more present in zoos (Egelkamp and Ross, 2019;Hopper, 2017) and offers a myriad of opportunities to answer theoretical questions about animal behavior and cognition (e.g., Barnard et al., 2013;Vonk et al., 2020), to provide enrichment to participating animals (Clark, 2017;Hopper et al., 2016), to assess and enhance animal welfare (Cronin et al., 2018;Ross, 2010), and to educate the public (e.g., Bowler et al., 2012;Price et al., 2015;Webber et al., 2017). While not all zoo-based cognitive research is conducted in view of visitors, in cases where the public can view research sessions (especially when actively interpreted to aid public understanding of research), the research set up may require animals to spend time in close proximity to visitors and/or the research may attract larger numbers of people. ...
The influence of visitors on zoo-housed primate behavior and welfare is relatively well-studied but less is known about the possible impact of zoo visitor presence on primates’ cognition. The Japanese macaques (Macaca fuscata) at Lincoln Park Zoo, USA, participate in voluntary cognitive research sessions in two touchscreen testing booths adjacent to their home enclosure, which are in view of the public. As other anthropogenic influences, such as loud noise levels, have been shown to induce attention bias effects in zoo primates, we wanted to determine if visitors also created cognitive bias effects for these macaques. Therefore, we sought to evaluate if and how the macaques’ testing participation and performance changed in response to the presence and number of visitors, and what any changes might mean for their welfare. Taking advantage of the zoo’s closure in response to COVID-19, we conducted 10 test sessions when the zoo was closed and 10 test sessions after reopening. Across all 20 test sessions, we recorded ambient sound levels (dB) and, when visitors were present, we also recorded visitor numbers and their location near the exhibit. Between when the zoo was closed and open, we did not find a difference in the macaques’ participation rates (p = 0.45) or task accuracy (p = 0.62) in an identity match-to-sample paradigm. However, we found the macaques’ response latencies were significantly faster when the zoo re-opened (p < 0.001) and with visitors present, but that the macaques did not avoid the testing booth that was closer to visitors. Considering the number of visitors, we found that the macaques completed most of their trials when small crowds were present (1–20 visitors) – the most common crowd size we recorded – but the macaques’ task accuracy did not differ across crowd size categories. Based on our findings, we found no clear evidence that these macaques were impacted by the return of zoo visitors and remain confident that such voluntary touchscreen opportunities can be an engaging aspect of animal lives in zoo settings.
... an animal husbandry principle that seeks to enhance the quality of captive animal care by identifying and providing the environmental stimuli necessary for optimal psychological and physiological well-being" [17] (p. 1). To meet the demands of these high cognitive skills, ape environmental enrichment must be varied, challenging, and flexible [18]. ...
The conservation status of great apes (chimpanzees Pan troglodytes, gorillas Gorilla sp., orangutans Pongo sp., and bonobos Pan paniscus) is grave and zoological institutions are vital for maintaining numbers of these species and educating the public about their importance. Technology provides tools that can assist zoos in meeting these objectives. However, the extant research on technology use in zoos is potentially constrained by small sample sizes and there is no framework detailing the methodologies necessary for the successful incorporation of technology into great ape management. Therefore, this study aimed to determine current technology use in the management of captive great apes and whether technology-directed behaviour differs between ape genera. Primary carers of great apes in zoos were surveyed using a 43-question, online questionnaire. The purpose of integrating interactive technology into captive ape management was primarily for enrichment (53% of respondents), followed by research (20% of respondents). However, only 25% of respondents had apes directly engaged with technology. There were no differences in technology-directed behaviours between ape genera. By identifying differences in practice, this research marks the initial stage in developing a best practice framework for using technology.
Whole food diets in zoos have the potential to reduce microbial contamination and keeper preparation time, whilst also reducing food nutrient breakdown. Given these benefits, it is important to determine whether there is any value in chopping up food. Lemurs (Family Lemuridae) are common in zoos, with over 7500 individuals housed globally. Given their regular occurrence in collections, plus the high incidence of frugivory, lemurs are an excellent taxon to investigate food presentation effects on behavior. A study was undertaken at Beale Wildlife Park on a group of four black-and-white ruffed lemurs (Varecia variegata) to investigate food presentation and preference. Animal behavior was recorded using instantaneous focal sampling at 60 s intervals to record state behaviors and continuous focal sampling to record event behaviors in 1-h sessions. Food preference was done by recording the first three food items consumed by individual lemurs. Overall, food manipulation was significantly increased during whole food presentation allowing the lemurs to display species-specific behaviors. Feeding and foraging were highest during very chopped food condition and inactivity was lowest in very chopped food presentation. When looking at aggressive interactions, there was an increase in stealing and locomotion with food during whole food presentation, whereas biting and startle were lower. Proving high-value food items chopped and low-value food items whole could reduce aggression while reduce aggression seen over high-value food items. For food preference, sweet potato was consistently in the top three food items for all lemurs, with beetroot being the second most-picked food item. This suggests that these individuals have a strong preference for food items high in carbohydrates. Keeper preparation time was significantly reduced during whole food preparation. Further research assessing a wider range of zoo-housed species would be beneficial to assess the effects of food presentation on behavior.
When conversing, humans instantaneously predict meaning from fragmentary and ambiguous mspeech, long before utterance completion. They do this by integrating priors (initial assumptions about the world) with contextual evidence to rapidly decide on the most likely meaning. One powerful prior is attentional preference for agents, which biases sentence processing but universally so only if agents are animate. Here, we investigate the evolutionary origins of this preference, by allowing chimpanzees, gorillas, orangutans, human children, and adults to freely choose between agents and patients in still images, following video clips depicting their dyadic interaction. All participants preferred animate (and occasionally inanimate) agents, although the effect was attenuated if patients were also animate. The findings suggest that a preference for animate agents evolved before language and is not reducible to simple perceptual biases. To conclude, both humans and great apes prefer animate agents in decision tasks, echoing a universal prior in human language processing.
Animals under human care are exposed to a potentially large range of both familiar and unfamiliar humans. Human-animal interactions vary across settings, and individuals, with the nature of the interaction being affected by a suite of different intrinsic and extrinsic factors. These interactions can be described as positive, negative or neutral. Across some industries, there has been a move towards the development of technologies to support or replace human interactions with animals. Whilst this has many benefits, there can also be challenges associated with increased technology use. A day-long Animal Welfare Research Network workshop was hosted at Harper Adams University, UK, with the aim of bringing together stakeholders and researchers (n = 38) from the companion, farm and zoo animal fields, to discuss benefits, challenges and limitations of human-animal interactions and machine-animal interactions for animals under human care and create a list of future research priorities. The workshop consisted of four talks from experts within these areas, followed by break-out room discussions. This work is the outcome of that workshop. The key recommendations are that approaches to advancing the scientific discipline of machine-animal interactions in animals under human care should focus on: (1) interdisciplinary collaboration; (2) development of validated methods; (3) incorporation of an animal-centred perspective; (4) a focus on promotion of positive animal welfare states (not just avoidance of negative states); and (5) an exploration of ways that machines can support a reduction in the exposure of animals to negative human-animal interactions to reduce negative, and increase positive, experiences for animals.
Experiments are widely used to investigate the behaviour and cognition of animals. While the automation of experiments to avoid potential experimenter bias is sometimes possible, not all experiments can be conducted without human presence. This is particularly true for large animals in captivity, which are often managed by professional handlers. For the safety of the animals and experimenters, a handler must be present during behavioural studies with certain species. It is not always clear to what extent cues provided by handlers affect the animals, and therefore the experimental results. In this study, we investigate handler interventions during the training process for a behavioural experiment with Asian elephants (Elephas maximus) in Nepal. We show that elephant handlers (mahouts) intervened to guide elephants in performing the learning task using vocal and behavioural cues, despite experimenters requesting minimal intervention. We found that although the frequency of mahout interventions did not decrease as the training progressed, the nature of their interventions changed. We also found more non-verbal than verbal cues across the training. Our results suggest that guidance from handlers may be common in behavioural studies, and continued consideration should be put into experimental design to reduce or account for cues that animals may receive from humans. This study also emphasises the need to take into account the presence of humans in interpreting the results of animal behavioural experiments, which not only presents challenges to behavioural research, but also represents opportunities for further study.
We report on the development and testing of a portable touchscreen apparatus and accompanying software program for primate enrichment, cognitive research, and husbandry applications. For zoos considering using technology to bolster scientific efforts or enhance the welfare of primates in their care, touchscreen activities offer a solution that has a long and proven record of primate use in laboratory settings as well as a history of usage in the zoo world. We review the options that are available for zoos to build their own touchscreen systems and we offer as an alternative our pre-built apparatus, Apex, and primate software suite, ApeTouch, both of which are tailored for use in a zoo setting. The efficacy and utility of these tools are demonstrated in a training study with four macaque groups of different species that were previously naïve to touchscreens. All of the groups in the study learned to use the device and displayed a consistent engagement with the touchscreen tasks over 95 daily sessions of exposure. In the final stage of the training, two of the four groups displayed an above-chance level performance on a numerical sequencing task.
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.
Primatological research in zoos is increasing globally. Such research allows scientists to study primate biology, behavior, and cognition while helping to advance the welfare of captive primates. Moreover, zoos welcome millions of visitors annually, which creates unique opportunities for public engagement with this research. Reflecting the importance of zoos in the field of primatology, the articles in this special issue showcase the range of primatological research currently being conducted in zoos around the world. With this special issue, I have chosen to focus on research examining primate behavior and cognition, addressing both basic and applied questions. The articles included in this special issue also highlight the array of technologies and methods being used to study zoo‐housed primates. While zoos house a variety of primate species, potentially enabling the testing of under‐studied species or widescale comparative research, great apes are disproportionately represented in current zoo‐based research. Thus, while an interest in conducting research with primates in zoos continues to grow, there are still opportunities to increase the breadth and diversity of this study. Primatological research in zoos is increasing globally. Such research allows scientists to study primate biology, behavior, and cognition. This research helps to advance the welfare of captive primates. While zoos house many primate species, apes are disproportionately represented in current zoo research. Primatological research in zoos is increasing globally. Such research allows scientists to study primate biology, behavior, and cognition. This research helps to advance the welfare of captive primates. While zoos house many primate species, apes are disproportionately represented in current zoo research.
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.
The emotional Stroop task is a paradigm commonly applied in human studies to investigate how emotionally laden stimuli interfere with cognitive processes. Recent modifications of this task have enabled researchers to study similar Stroop effects in zoo-housed primates. Across three experiments using a pictorial emotional Stroop task, we investigated if the attention of bonobos was influenced by social (facial expressions during play, conflict, and neutral events) and nonsocial stimuli (a preferred food item, predator, and flower). Four bonobos successfully learned to complete the task on a touchscreen. First, we tested the bonobos on a standard color-interference Stroop task and found that they made more errors in color-congruent trials. Second, we included facial expressions of unknown conspecifics and found that it took the bonobos longer to select targets with play facial expressions compared to neutral expressions. Last, we included objects and found that the negative, positive and neutral objects altered performance. Our findings show that the cognitive processes of bonobos are influenced by both relevant social and nonsocial stimuli. Specifically, play faces interfered with the bonobos' attention suggesting that these facial expressions form a salient stimulus within bonobo society. Nonsocial stimuli also altered accuracy and reaction times during the task which may be explained by their evolutionary relevance. Our results help us to better understand the (socio-)emotional competencies of bonobos and how they respond to external stimuli. Future studies can further examine how a wider range of biologically relevant stimuli interfere with attentional processes in bonobos.
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 on 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 subject-based (e.g., small sample sizes at single zoos, untrained/unhabituated subjects, site 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-zoo 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 article is aimed at zoo animal care and research staff, as well as external researchers interested in zoo-based studies.
RESEARCH HIGHLIGHTS
Zoos are an excellent yet relatively untapped resource for animal cognition research.
Zoo cognition research has historically been challenging, and traditional laboratory paradigms often do not translate well to the majority of zoos.
Salient challenges of zoo-based cognitive research can be overcome by using less restrictive test apparatuses, limiting animal training and isolation, and subscribing to multi-zoo collaborative programs.
In Experiment 1, we wished to determine whether a singly-housed adult male captive chimpanzee could discriminate the behavioral categories of sex and aggression. He was reinforced for selecting sexual rather than aggressive images on a touch-screen computer in a two-choice discrimination paradigm. He showed no discrimination after 24 sessions with non-human photos, but immediately selected human sexual images at above-chance levels. To explore whether this differential discrimination was due to a preference for human sexual images, he was presented with images of humans versus non-humans under non-differential reinforcement in Experiment 2. He preferred human photos if the images depicted sex, but not if the images depicted aggression. To further explore these preferences in Experiment 3 the chimpanzee was presented with images of genitalia of non-humans versus humans, genitalia versus eyes, and finally female versus male genitalia of both non-humans and humans, using non-differential reinforcement. The chimpanzee preferred human to non-human genitalia, and eyes to genitalia, but did not prefer female to male genitalia. This chimpanzee’s unusual social environment may have interfered with species-typical social preferences.
To understand the evolutionary development of cognition, comparing the cognitive capacities of different animal species is essential. However, getting access to various species with sufficiently large sample sizes can be very challenging. Zoos, housing large ranges of animal taxa, would offer ideal research environments, but zoo-based studies on cognition are still rare. The use of touchscreen computers to explore the cognitive abilities of nonhuman animals has been shown to be highly applicable, and simultaneously offers new enrichment possibilities for captive animals. To facilitate zoo-based research, the assembly and usage of newly developed touchscreen computer systems (Zoo-based Animal-Computer Interaction System, ZACI) are illustrated, which can be used in various zoo environments, and importantly, with different taxa (e.g. primates, birds). The developed setups are portable, can be attached to various mesh sizes, and do not need any external power supply while being used. To evaluate the usability of the ZACI, they were tested with experimentally naïve subjects of three great ape species (orang-utans, chimpanzees, gorillas) housed at Zoo Heidelberg, Germany, demonstrating ZACI to be animal-proof, easy to handle, and of great interest to the animals. Animals could be tested within their social group, as each subject had access to its own device during testing. To support the implementation of touchscreen setups at other facilities, the training procedure is also illustrated and first data on the apes' performance in a simple object discrimination task are presented. Portable touchscreen setups offer the great possibility to enhance collaboration between zoos and researchers, allow a standardisation of methods, and improve data collection.
Training nonhuman primates (NHPs) to perform cognitive tasks is essential for many neuroscientific investigations, yet laboratory training is a time-consuming process with inherent limitations. Habituating NHPs to the laboratory staff and experimental equipment can take months before NHPs are ready to proceed to the primary tasks. Laboratory training also necessarily separates NHPs from their home-room social group and typically involves some form of restraint or limited mobility, and data collection is often limited to a few hours per day so that multiple NHPs can be trained on the same equipment. Consequently, it can often take a year to train NHPs on complex cognitive tasks. To overcome these issues, we developed a low-cost, open-source, wireless touchscreen training system that can be installed in the home-room environment. The automated device can run continuously all day, including over weekends, without experimenter intervention. The system utilizes real-time facial recognition to initiate subject-specific tasks and provide accurate data logging, without the need for implanted microchips or separation of the NHPs. The system allows NHPs to select their preferred reward on each trial and to work when and for as long as they desire, and it can analyze task performance in real time and adapt the task parameters in order to expedite training. We demonstrate that NHPs consistently use this system on a daily basis to quickly learn complex behavioral tasks. The system therefore addresses many of the welfare and experimental limitations of laboratory-based training of NHPs and provides a platform for wireless electrophysiological investigations in more naturalistic, freely moving environments.
Digital devices, including tablet computers and other touchscreens, can potentially serve as flexible and convenient means for providing behavioral enrichment activities to captive primates. Despite increased interest in incorporating technology into enrichment programs, no direct quantitative comparison has previously been made between the effectiveness of typical tactile enrichment activities and enrichment activities on digital devices. One way in which these activities differ is in the degree of controllability afforded the animals in interacting with the enrichment objects, since digital devices will be limiting to varying degrees based on the particulars of software and the interface format. This study compared the effects of painting with brush on paper to those of a painting application on a digital tablet device (iPad™) in eight group‐living chimpanzees at the Honolulu Zoo. Observations were analyzed across baseline, enrichment, and post‐enrichment periods to measure significant differences in the reduction of displacement and stereotypic behaviors. We found that the digital tablet device running an application that permits production of semi‐automated visualizations, was as effective as painting with brush on paper in reducing some stereotypic and displacement behaviors, including yawning and self‐picking. However, the digital tablet was not as effective in reducing other displacement behaviors, nor was it as effective in retaining the chimpanzee's attention. These results confirm a useful role for digital devices in enrichment programs but suggest a need to assess individual device applications in their capacity to promote greater controllability and sensory breadth of the enrichment experience.
Typically, animals’ food preferences are tested manually, which can be both time-consuming and vulnerable to experimenter biases. Given the utility of ascertaining animals’ food preferences for research and husbandry protocols, developing a quick, reliable, and flexible paradigm would be valuable for expediting many research protocols. Therefore, we evaluated the efficacy of using a touchscreen interface to test nonhuman primates’ food preferences and valuations, adapting previously validated manual methods. We tested a nonhuman primate subject with four foods (carrot, cucumber, grape, and turnip). Preference testing followed a pairwise forced choice protocol with pairs of food images presented on a touchscreen: The subject was rewarded with whichever food was selected. All six possible pairwise combinations were presented, with 90 trials per pairing. Second, we measured how hard the subject was willing to work to obtain each of the four foods, allowing us to generate demand curves. For this phase, a single image of a food item was presented on the touchscreen that the subject had to select in order to receive the food, and the number of selections required increased following a quarter-log scale, with ten trials per cost level (1, 2, 3, 6, 10, and 18). These methods allowed us to ascertain the subject’s relative preferences and valuations of the four foods. The success of this touchscreen protocol for testing the subject’s food preferences, from both a practical and a theoretical standpoint, suggests that the protocol should be further validated with other foods with this subject, with other subjects, and with other test items.
s
To understand the evolutionary development of cognition, comparing the cognitive capacities of different animal species is essential. However, getting access to various species with sufficient sample sizes can be very challenging. Zoos, housing large ranges of animal taxa, would offer ideal research environments, but zoo-based studies on cognition are still rare. The use of touchscreen-computers to explore the cognitive abilities of nonhuman animals has shown to be highly applicable, and simultaneously offers new enrichment possibilities for captive animals. To facilitate zoo-based research, I here illustrate the assembly and usage of newly developed touchscreen-computer-systems ( Z oo-based A nimal- C omputer- I nteraction System, ZACI ), which can be used in various zoo environments and, importantly, with different taxa (e.g. primates, birds). The developed setups are portable, can be attached to various mesh sizes, and do not need any external power supply while being used. To evaluate the usability of the ZACI, they have been tested with experimentally naïve subjects of three great ape species (orang-utans, chimpanzees, gorillas) housed at Zoo Heidelberg, Germany, demonstrating to be easy to handle, animal-proof, and of great interest to the animals. Animals could be tested within their social group, as each subject had access to its own device during testing. To support the implementation of touchscreen-setups at other facilities, I also illustrate the training procedure and present first data on the apes’ performance in a simple object discrimination task. Portable touchscreen-setups offer the great possibility to enhance collaboration between zoos and researchers, allow a standardisation of methods, and improve data collection.
The spatial-numerical association of response codes (SNARC) effect is the tendency for humans to respond faster to relatively larger numbers on the left or right (or with the left or right hand) and faster to relatively smaller numbers on the other side. This effect seems to occur due to a spatial representation of magnitude either in occurrence with a number line (wherein participants respond to relatively larger numbers faster on the right), other representations such as clock faces (responses are reversed from number lines), or culturally specific reading directions, begging the question as to whether the effect may be limited to humans. Given that a SNARC effect has emerged via a quantity judgement task in Western lowland gorillas and orangutans (Gazes et al., Cog 168:312–319, 2017), we examined patterns of response on a quantity discrimination task in American black bears, Western lowland gorillas, and humans for evidence of a SNARC effect. We found limited evidence for SNARC effect in American black bears and Western lowland gorillas. Furthermore, humans were inconsistent in direction and strength of effects, emphasizing the importance of standardizing methodology and analyses when comparing SNARC effects between species. These data reveal the importance of collecting data with humans in analogous procedures when testing nonhumans for effects assumed to bepresent in humans.
In the zoo environment, anthropogenic noise is common as sound levels fluctuate due to visitors, construction, habitat design, and special events. In this study, changes in the mood of three species of zoo-housed primates in response to a loud annual event were evaluated with the response-slowing paradigm. In this paradigm, animals experiencing anxiety slow responses on simple cognitive tasks when emotional content is displayed. Following a previously validated approach, we measured latencies to touch potentially threatening (conspecific faces with directed gaze) and non-threatening (conspecific faces with averted gaze) images overlaid on a grey square, relative to neutral control images (grey squares only) on a touchscreen. In Experiment 1, four Japanese macaques (Macaca fuscata) were tested in two conditions: during a baseline (non-stressful) period and opportunistically during three days during which loud jets frequently flew overhead. Results indicated a significant effect of condition, with an increase in latency to touch images of conspecific faces relative to control images during the days of the loud event. In Experiment 2, chimpanzees (Pan troglodytes, n = 4) and western lowland gorillas (Gorilla gorilla gorilla, n = 2) were tested during the same loud event following a similar methodology. The results revealed subtle changes across conditions; however, this was likely driven by the apes increasing their response speed to face stimuli relative to control stimuli over time (habituation). These findings suggest that the macaques, but not the apes, underwent detectable affective changes during the loud event. With additional development, this relatively simple paradigm may be an effective and feasible way to evaluate real-time changes in the mood of zoo-housed animals.
We presented two American black bears (Ursus americanus) with a serial list learning memory task, and one of the bears with a matching-to-sample task. After extended training, both bears demonstrated some success with the memory task but failed to generalize the overarching rule of the task to novel stimuli. Matching to sample proved even more difficult for our bear to learn. We conclude that, despite previous success in training bears to respond to natural categories, quantity discriminations, and other related tasks, that bears may possess a cognitive limitation with regards to learning abstract rules. Future tests using different procedures are necessary to determine whether this is a limit of bears’ cognitive capacities, or a limitation of the current tasks as presented. Future tests should present a larger number of varying stimuli. Ideally, bears of various species should be tested on these tasks to demonstrate species as well as individual differences.
In order to assess mood state in three male western lowland gorillas housed in a bachelor group, we developed a novel version of a cognitive bias task. The background color of a touchscreen presented a conditional ‘if, then…” rule relating to outcomes involving differential amounts of food rewards. The gorillas struggled to reach a criterion of 80% responding required for testing. In follow-up experiments, we assessed whether the gorillas did in fact prefer three pieces of food to one piece of food when presented with images of food quantities and actual food quantities. Gorillas did not learn to select the stimulus that indicated three food items over one food item when we used images of actual quantities of the rewarded food but they did prefer three actual pieces of food. Thus, like other primates, gorillas may respond differently to quantities of edible and inedible items. In addition, they may struggle with learning conditional discriminations when cues to differential responses and outcomes are arbitrary rather than intuitively connected. These studies highlight the importance of methodology when devising tests to assess cognition or affect in nonhuman primates.
Modern zoos and aquariums aspire to contribute significantly to biodiversity conservation and research. For example, conservation research is a key accreditation criterion of the Association of Zoos and Aquariums (AZA). However, no studies to date have quantified this contribution. We assessed the research productivity of 228 AZA members using scientific publications indexed in the ISI Web of Science (WoS) database between 1993 and 2013 (inclusive). AZA members published 5175 peer-reviewed manuscripts over this period, with publication output increasing over time. Most publications were in the zoology and veterinary science subject areas, and articles classified as “biodiversity conservation” by WoS averaged 7% of total publications annually. From regression analyses, AZA organizations with larger financial assets generally published more, but research-affiliated mission statements were also associated with increased publication output. A strong publication record indicates expertise and expands scientific knowledge, enhancing organizational credibility. Institutions aspiring for higher research productivity likely require a dedicated research focus and adequate institutional support through research funding and staffing. We recommend future work build on our results by exploring links between zoo and aquarium research productivity and conservation outcomes or uptake.
Aged dogs suffer from reduced mobility and activity levels, which can affect their daily lives. It is quite typical for owners of older dogs to reduce all activities such as walking, playing and training, since their dog may appear to no longer need them. Previous studies have shown that ageing can be slowed by mental and physical stimulation, and thus stopping these activities might actually lead to faster ageing in dogs, which can result in a reduction in the quality of life of the animal, and may even decrease the strength of the dog-owner bond. In this paper, we describe in detail a touchscreen apparatus, software and training method that we have used to facilitate dog computer interaction (DCI). We propose that DCI has the potential to improve the welfare of older dogs in particular through cognitive enrichment. We provide hypotheses for future studies to examine the possible effects of touchscreen use on physiological, behavioural and cognitive measures of dogs' positive affect and well-being, and any impact on the dog-owner bond. In the future, collaborations between researchers in animal-computer interaction, dog trainers, and cognitive scientists are essential to develop the hardware and software necessary to realise the full potential of this training and enrichment tool.
Cognitive bias tests are frequently used to assess affective state in nonhumans. We adapted the ambiguous-cue paradigm to assess affective states and to compare learning of reward associations in two distantly related species, an American black bear and three Western lowland gorillas. Subjects were presented with three training stimuli: one that was always rewarded (P), one that was never rewarded (N) and one that was ambiguous (A) because its reward association depended on whether it had been paired with P (PA pairing) or N (NA pairing). Differential learning of NA and PA pairs provided insight into affective state as the bear and one gorilla learned NA pairs more readily, indicating that they focused on cues of reinforcement more than cues of non-reinforcement, whereas the opposite was true of one gorilla. A third gorilla did not learn either pairings at above chance levels. Although all subjects experienced difficulty learning the pairings, we were able to assess responses to A during probe trials in the bear and one gorilla. Both responded optimistically, but it was difficult to determine whether their responses were a true reflection of affective state or were due to preferences for specific stimuli.
Background
Studying animal cognition in a social setting is associated with practical and statistical challenges. However, conducting cognitive research without disturbing species-typical social groups can increase ecological validity, minimize distress, and improve animal welfare. Here, we review the existing literature on cognitive research run with primates in a social setting in order to determine how widespread such testing is and highlight approaches that may guide future research planning.
Survey Methodology
Using Google Scholar to search the terms “primate” “cognition” “experiment” and “social group,” we conducted a systematic literature search covering 16 years (2000–2015 inclusive). We then conducted two supplemental searches within each journal that contained a publication meeting our criteria in the original search, using the terms “primate” and “playback” in one search and the terms “primate” “cognition” and “social group” in the second. The results were used to assess how frequently nonhuman primate cognition has been studied in a social setting (>3 individuals), to gain perspective on the species and topics that have been studied, and to extract successful approaches for social testing.
Results
Our search revealed 248 unique publications in 43 journals encompassing 71 species. The absolute number of publications has increased over years, suggesting viable strategies for studying cognition in social settings. While a wide range of species were studied they were not equally represented, with 19% of the publications reporting data for chimpanzees. Field sites were the most common environment for experiments run in social groups of primates, accounting for more than half of the results. Approaches to mitigating the practical and statistical challenges were identified.
Discussion
This analysis has revealed that the study of primate cognition in a social setting is increasing and taking place across a range of environments. This literature review calls attention to examples that may provide valuable models for researchers wishing to overcome potential practical and statistical challenges to studying cognition in a social setting, ultimately increasing validity and improving the welfare of the primates we study.
Exploration (interacting with objects to gain information) and neophobia (avoiding novelty) are considered independent traits shaped by the socio-ecology of a given species. However, in the literature it is often assumed that neophobia inhibits exploration. Here, we investigate how different approaches to novelty (fast or slow) determine the time at which exploration is likely to occur across a number of species. We presented four corvid and five parrot species with a touchscreen discrimination task in which novel stimuli were occasionally interspersed within the familiar training stimuli. We investigated the likelihood that an animal would choose novelty at different stages of its training and found evidence for a shift in the pattern of exploration, depending on neotic style. The findings suggest that faster approaching individuals explored earlier, whilst animals with long initial approach latencies showed similar amounts of exploration but did so later in training. Age rather than species might have influenced the amount of total exploration, with juveniles exploring more than adults. Neotic style varied consistently only for one species and seems to involve a strong individual component, rather than being a purely species-specific trait. This suggests that variation in behavioural phenotypes within a species may be adaptive.
Human intellect is characterized by intercorrelated psychological domains, including intelligence, academic performance and personality. Higher openness is associated with higher intelligence and better academic performance, yet high performance among individuals is itself attributable to intelligence, not openness. High conscientiousness individuals, although not necessarily more intelligent, are better performers. Work with other species is not as extensive, yet animals display similar relationships between exploration-and persistence-related personality traits and performance on cognitive tasks. However, previous studies linking cognition and personality have not tracked learning, performance and dropout over time—three crucial elements of cognitive performance. We conducted three participatory experiments with touchscreen cognitive tasks among 19 zoo-housed chimpanzees, whose personalities were assessed 3 years prior to the study. Performance and participation were recorded across experiments. High conscientiousness chimpanzees participated more, dropped out less and performed better, but their performance could be explained by their experience with the task. High openness chimpanzees tended to be more interested, perform better and continue to participate when not rewarded with food. Our results demonstrate that chimpanzees, like humans, possess broad intellectual capacities that are affected by their personalities.
Many facilities that house captive primates play music for animal enrichment or for caregiver enjoyment. However, the impact on primates is unknown as previous studies have been inconclusive. We conducted three studies with zoo-housed chimpanzees (Pan troglodytes) and one with group-housed chimpanzees at the National Centre for Chimpanzee Care to investigate the effects of classical and pop/rock music on various variables that may be indicative of increased welfare. Study one compared the behaviour and use of space of 18 animals when silence, classical or pop/rock music was played into one of several indoor areas. Overall, chimpanzees did not actively avoid the area when music was playing but were more likely to exit the area when songs with higher beats per minute were broadcast. Chimpanzees showed significantly fewer active social behaviours when music, rather than silence, was playing. They also tended to be more active and engage in less abnormal behaviour during the music but there was no change to either self-grooming or aggression between music and silent conditions. The genre of music had no differential effects on the chimpanzees’ use of space and behaviour. In the second study, continuous focal observations were carried out on three individuals with relatively high levels of abnormal behaviour. No differences in behaviour between music and silence periods were found in any of the individuals. The final two studies used devices that allowed chimpanzees to choose if they wanted to listen to music of various types or silence. Both studies showed that there were no persistent preferences for any type of music or silence. When taken together, our results do not suggest music is enriching for group-housed captive chimpanzees, but they also do not suggest that music has a negative effect on welfare.
“Cognitive enrichment” is a subset of enrichment that has gained interest from researchers over the past decade, particularly those working in zoos. This review explores the forms of cognitive enrichment that have been attempted for laboratory, farmed and zoo animals with a focus on the latter, including various definitions, aims, and approaches. This review reveals the fundamental theoretical and practical problems associated with cognitive enrichment, leading to recommendations for further research in this field. Critically, more research is needed to elucidate what makes challenges appropriate for certain taxa, acknowledging that individual differences exist. Going forward, we should be prepared to incorporate more computer technology into cognitive tasks, and examine novel welfare indicators such as flow, competence, and agency.
Zoo-housed animals are provided with many temporary elements in their exhibit, such as environmental enrichment devices (EEDs), which may not match the aesthetic of their exhibit. Some zoos object to the use of artificial EEDs in naturalistic exhibits, but there has been little research into whether the appearance of these temporary elements influences visitors' perceptions. Therefore, we investigated visitors' opinions about a naturalistic chimpanzee exhibit at Lincoln Park Zoo when EEDs were provided to the chimpanzees (Pan troglodytes). We wished to determine whether exhibit naturalism was important to visitors; what their perceptions were of the chimpanzees' behaviour and emotions; what their thoughts were about the suitability of chimpanzees as pets; and whether these beliefs were affected by the type of EED in the chimpanzees' exhibit. Eight EEDS were chosen for this study: four that were naturalistic in appearance and four that were designed to elicit similar species-typical behaviours, but were artificial in appearance. Visitors' responses to the survey revealed that they generally believed that exhibit naturalism was important, and that the chimpanzee exhibit was naturalistic in appearance; they viewed the chimpanzees' behaviour and feelings positively; and they did not think chimpanzees made good pets. Visitors' responses to the survey questions did not differ whether artificial or naturalistic EEDs were provided in the exhibit. These results support previous research that zoo visitors are not affected by EED aesthetic in a naturalistic exhibit, perhaps because the naturalism of the exhibit supersedes any effect or because the EEDs represent such small elements within the exhibit.
Comparing the cognitive capacities of different animal species is essential to understand the evolutionary origins of cognition, but getting access to various species can be very challenging. Zoos, housing large ranges of animal taxa, would offer ideal research environments, but zoo-based studies on cognition are still very rare. To facilitate zoo-based research, I am currently developing and validating portable touchscreen computer systems, working with great apes (orangutans, chimpanzees, gorillas) at Zoo Heidelberg, Germany. Methodological variations in experimental conditions can strongly influence animals’ performances in cognitive tests, and the use of touchscreen computers to explore the cognitive abilities of nonhuman animals has shown to be highly applicable. The newly developed setups can be used in various zoo environments and, importantly, with different species (e.g. primates, birds), offering the unique opportunity to conduct comparative studies on different animal species and taxa. In addition, zoos profit from the welfare aspect of scientific studies, as cognitive challenges can enhance the lives of zoo animals, known as cognitive enrichment. To examine the influence of the touchscreen studies on animal wellbeing, behavioural observations are conducted. I present first results and discuss how increasing zoo-based research can facilitate cognitive studies and enhance animal welfare.
Annually, over 180 million people visit zoos accredited by the Association of Zoos and Aquariums (AZA), giving them the chance to see a variety of primate species and to learn about their behavior and ecology. In the past decade, some zoos have also become increasingly involved in conducting high-quality cognitive research that not only contributes to the academic literature, but also increases our knowledge of captive primate care. Using technology such as touchscreen computers, scientists are able to explore a range of primate cognitive abilities through different types of computer tasks. In 2004, Lincoln Park Zoo scientists began a comparative touchscreen research program with resident Western-lowland gorillas (Gorilla gorilla gorilla) and chimpanzees (Pan troglodytes). In 2015, this research program was expanded to include Japanese macaques (Macaca fuscata). This applied and comparative research is exploring several facets of primate cognition: serial learning, prosociality, affective states, and individual preferences. The purpose of this research is threefold: to learn more about primates’ cognitive abilities; to develop new ways to assess and positively impact primate welfare; and to facilitate public engagement with science. Both the macaque and ape facilities at Lincoln Park Zoo were designed specifically to accommodate touchscreen research that could be conducted in view of zoo guests while the primates remain in their social group during voluntary testing sessions. The cognitive research demonstrations are interpreted by zoo educators every weekday, where guests can observe the primates working on the touchscreens, and ask questions about the research. This zoo-based cognitive research program offers benefits to scientists, zoo visitors as well as to the animals themselves, as the research strives to improve the care and management of program participants.
Annually, over 180 million people visit zoos accredited by the Association of Zoos and Aquariums (AZA), giving them the chance to see a variety of primate species and to learn about their behavior and ecology. In the past decade, some zoos have also become increasingly involved in conducting high-quality cognitive research that not only contributes to the academic literature, but also increases our knowledge of captive primate care. Using technology such as touchscreen computers, scientists are able to explore a range of primate cognitive abilities through different types of computer tasks. In 2004, Lincoln Park Zoo scientists began a comparative touchscreen research program with resident Western-lowland gorillas (Gorilla gorilla gorilla) and chimpanzees (Pan troglodytes). In 2015, this research program was expanded to include Japanese macaques (Macaca fuscata). This applied and comparative research is exploring several facets of primate cognition: serial learning, prosociality, affective states, and individual preferences. The purpose of this research is threefold: to learn more about primates’ cognitive abilities; to develop new ways to assess and positively impact primate welfare; and to facilitate public engagement with science. Both the macaque and ape facilities at Lincoln Park Zoo were designed specifically to accommodate touchscreen research that could be conducted in view of zoo guests while the primates remain in their social group during voluntary testing sessions. The cognitive research demonstrations are interpreted by zoo educators every weekday, where guests can observe the primates working on the touchscreens, and ask questions about the research. This zoo-based cognitive research program offers benefits to scientists, zoo visitors as well as to the animals themselves, as the research strives to improve the care and management of program participants.
The field of comparative cognition investigates species' differences and similarities in cognitive abilities, and sheds light on the evolutionary origins of such capacities. Cognitive testing has been carried out in a variety of species; however, there are some taxa that are underrepresented in this field. The current work follows on a recent increase in cognitive research in the order Carnivora with a specific focus on sun bears. Sun bears are the smallest existing bear species and live in tropical regions of Southeast Asia. They have an omnivorous diet and use their tongues to forage for insects and sap. Little is known about sun bear cognition, although much like other bear species, anecdotes suggest a high level of intelligence. The current work explored training sun bears to use a touchscreen computer. This effort allows for insight into cognitive abilities as well as providing a complex source of enrichment for the bears. The bears use their tongues to respond to a touchscreen computer, and the effects on stereotypic behaviors on exhibit and preference for this over other forms of enrichment were examined. Overall, bears performed well on the task and showed a preference for the computer.
Music is commonly employed as auditory enrichment in non-human primate (NHP) facilities under the
assumption that music is as enriching for NHPs as it is for humans (Hinds et al. 2007; Lutz and Novak
2005). The purpose of this study was to assess the utility of music as NHP enrichment by exploring
musical preference and discriminative ability in three Sumatran orangutans. In Experiment 1, orangutan
preference for music vs silence was tested. Following exposure to a sample of music belonging to
one of seven musical genres, orangutans were given the choice via touchscreen to continue to listen
to the music sample previously played or to listen to silence instead. Results indicated that all three
orangutans either preferred silence to music or were indifferent. No preference for any one of the
musical genres tested over others was found. In Experiment 2, orangutans’ ability to discriminate
music from scrambled music was assessed using a touchscreen delivered standard delayed matchingto-
sample (DMTS) task. Results indicated that none of the three orangutans could reliably discriminate
“music” from “scrambled music”. Taken together, results strongly suggest that these orangutans did
not experience the musical stimuli as reinforcing and that use of music as enrichment in captive NHP
facilities may be more aversive than enriching for some species.
There is widespread acceptance that facial expressions are useful in social interactions, but empirical demonstration of their adaptive function has remained elusive. Here, we investigated whether macaques can use the facial expressions of others to predict the future outcomes of social interaction. Crested macaques (Macacanigra) were shown an approach between two unknown individuals on a touchscreen and were required to choose between one of two potential social outcomes. The facial expressions of the actors were manipulated in the last frame of the video. One subject reached the experimental stage and accurately predicted different social outcomes depending on which facial expressions the actors displayed. The bared-teeth display (homologue of the human smile) was most strongly associated with predicted friendly outcomes. Contrary to our predictions, screams and threat faces were not associated more with conflict outcomes. Overall, therefore, the presence of any facial expression (compared to neutral) caused the subject to choose friendly outcomes more than negative outcomes. Facial expression in general, therefore, indicated a reduced likelihood of social conflict. The findings dispute traditional theories that view expressions only as indicators of present emotion and instead suggest that expressions form part of complex social interactions where individuals think beyond the present.
Electronic supplementary material
The online version of this article (doi:10.1007/s10071-016-0992-3) contains supplementary material, which is available to authorized users.
With its roots firmly planted in behaviorist and animal learning traditions, lab-based research is an enduring and pervasive characteristic of comparative cognition. In this review, we discuss progress in comparative cognition research in other experimental settings such as zoos, captive animal parks, and wild settings. Zoos provide access to a large array of species housed in seminatural environments that allow a reasonable degree of experimental control. Thanks to the advent of computer technology, a wide range of complex cognitive processes is increasingly being successfully studied in zoo environments. Further, cognitive research provides enrichment for captive animal participants, reducing anxiety and promoting psychological well-being. The results of cognitive research also benefit the welfare of captive animals through preference assessment, species-specific exhibit design, and behavioral management. Field settings also offer unique advantages and have allowed researchers to systematically study such diverse topics as spatial cognition, cultural transmission, problem solving, and preference. Not only does field research expand our understanding of the evolutionary and ecological drivers of animal cognition, but it also can directly inform conservation efforts. Although venturing out of the lab presents tangible challenges, including the restriction of testable hypotheses and conclusions that can be inferred from results, the benefits to be gained outweigh the costs.
Significance
Applying well-established psychological paradigms to our closest relatives represents a promising approach for providing insight into similarities and differences between humans and apes. Numerous articles have been published on the dot-probe task, showing that humans have an attentional bias toward emotions, especially when threatening. For social species like primates, efficiently responding to others’ emotions has great survival value. Observational research has shown that, compared with humans and chimpanzees, bonobos excel in regulating their own and others’ emotions, thereby preventing conflicts from escalating. The present study is an initial effort to apply a psychological test to the bonobo, and demonstrates that they, like humans, have heightened attention to emotional—compared with neutral—conspecifics, but are mostly drawn toward protective and affiliative emotions.
Self-directed behaviors (SDBs) are a commonly used behavioral indicator of arousal in nonhuman primates. Experimental manipulations, designed to increase arousal and uncertainty, have been used to elicit SDB production in primates. Beyond measuring rates of SDB production, researchers have also recorded their lateralized production by primates, thought to reflect laterality of hemispheric brain control and response to emotion. Although a handful of such studies exist, all have been conducted with chimpanzees. Expanding on this line of inquiry, we tested both chimpanzees (N = 3) and gorillas (N = 3) in a serial learning task presented on a touchscreen interface that incorporated both EASY (two-item list) and HARD (four-item list) versions of the task. Although SDB production by the apes did not differ across the two levels of task complexity, both species produced higher rates of SDB when they made an error, regardless of task difficulty. Furthermore, the apes made more SDB with the left hand-directed to the right side of their body (contralateral SDB) and left side of their body (ipsilateral SDB)-when they made an incorrect response. There was no difference in the rate of SDB produced with the right hand across correct compared to incorrect trials. The apes' responses reflect previous reports that show humans are quicker at selecting negative emotional stimuli when using their left, compared to their right, hand (the reverse is true for positive stimuli). However, previous work has shown that chimpanzees are more likely to produce (contralateral) SDB with their right hand when aroused and so we discuss our results in relation to these findings and consider how they relate to the 'right hemisphere' and 'valence' models of emotional processing in apes.
The cognitive bias model of animal welfare assessment is informed by studies with humans demonstrating that the interaction between emotion and cognition can be detected using laboratory tasks. A limitation of cognitive bias tasks is the amount of training required by animals prior to testing. A potential solution is to use biologically relevant stimuli that trigger innate emotional responses. Here; we develop a new method to assess emotion in rhesus macaques; informed by paradigms used with humans: emotional Stroop; visual cueing and; in particular; response slowing. In humans; performance on a simple cognitive task can become impaired when emotional distractor content is displayed. Importantly; responses become slower in anxious individuals in the presence of mild threat; a pattern not seen in non-anxious individuals; who are able to effectively process and disengage from the distractor. Here; we present a proof-of-concept study; demonstrating that rhesus macaques show slowing of responses in a simple touch-screen task when emotional content is introduced; but only when they had recently experienced a presumably stressful veterinary inspection. Our results indicate the presence of a subtle "cognitive freeze" response; the measurement of which may provide a means of identifying negative shifts in emotion in animals.
Cognitive testing programs are being implemented more frequently in zoo settings due to the benefits these programs can provide for the animals, researchers and zoo visitors. However, the impact that
cognitive studies have on the welfare of captive animals, particularly for primates in a social group, is debated. Although cognitive testing can be mentally enriching, the provision of monopolisable apparatuses to a primate social group can elicit competition and potentially contribute to negative welfare. We sought to investigate how behaviours changed when a group of 12 Japanese macaques had access to two touchscreen devices. We assessed rates of affiliative behaviours, anxiety-related behaviours, general activity, and aggression over 15 months at matched time periods on days when cognitive testing was available and when it was not. Rates of affiliative behaviours, anxiety-related behaviours, and general activity were not significantly different between conditions. Rates of contact and noncontact aggression were significantly higher during cognitive testing compared to times without cognitive testing (p < 0.05 for both). To further explore this result, we used social network analysis to visualize the aggressive interactions between individual macaques. We found that juveniles were receiving the most aggression. However, because the overall rates of aggression were low and did not deter the macaques from participating in cognitive research, we do not think these results should broadly discourage the implementation of cognitive testing programs. Instead, we intend this study to inform how cognitive testing programs are executed. We also discuss how social interactions and the corresponding welfare implications may differ in closely related macaque species based on species-typical sociality.
Cognitive research in the United States spans approximately 100 years. Most studies have occurred in primate centers, fewer at universities, and for a brief period, in home-based projects focused on enculturation. Historically, great apes living in zoos have been under represented. A shift has occurred that affects the future of the field. Studies at primate centers have significantly decreased, all university based projects have ended, and work in zoos is increasing. The Simon Skjodt International Orangutan Center at the Indianapolis Zoo provides an example of one stable, longitudinally based project. The primary areas of study at the Center are symbolic representation, numerical competency, social learning, memory, and strategic reasoning. All data collection sessions are conducted with visitors present. Cognitive studies in a zoo environment promote great ape welfare, offer a platform for transformational public education, and provide an effective means to advance support for in situ conservation of great apes.
Innovations in apparatus technology come about for a variety of reasons such as the need to use the same methodology with various species, the opportunity to present dynamic and carefully controlled stimuli, the goal of using automation to make data collection more precise or efficient, and the need to control for and/or eliminate the presence of experimenters in the testing context. At the Language Research Center (LRC) of Georgia State University, a computer-based system has been developed and used extensively with nonhuman primate species. This system involves the animal working in an enclosure that provides visual access to a computer screen, access to a joystick to control a cursor on the screen, and access to a food dish where pellets are delivered for correct responses. Here we will describe the history and development of this system as well as some considerations that might be applied to expanding this apparatus to a new environment, including the mobility of test stations, equipment needs, training protocols, and the cost and considerations for initial set up of such a system. A variety of computer based programs have been developed for use with this system. These programs have allowed insight into many nonhuman primate cognitive abilities and we highlight some that have been the focus of study at the LRC such as metacognition, numerical cognition, inhibitory processes, prospective memory, attention, and cognitive control. In addition, this cognitive testing apparatus has been shown to create a stimulating and enriching environment for the animals. We advocate that the computerized testing apparatus is useful for advancing our understanding of nonhuman animal cognition and may be uniquely suited to optimizing animal welfare. This area of research is already rapidly expanding in zoos, and we hope to offer some insight from one journey of designing, implementing and adapting a computerized testing paradigm.
Given the difficulties of conducting regular endocrine and veterinary assessments of animals, behavioural observations are often the most commonly used tool to assess the welfare of animals in human care. Behavioural measures, inexpensive and convenient to collect, also have their challenges, such as ensuring the behaviours of interest are reliable indicators of an animal's internal state. Welfare assessments include both positive and negative indicators, and a commonly used indicator of negative welfare is self-directed behaviour (SDB). SDB has been described as a behavioural indicator of stress through observation and experimentation; however, this pattern is not universal despite assumptions otherwise. The purpose of this study was to experimentally evaluate the use of SDB as an indicator of negative welfare in mandrills (Mandrillus sphinx) with the goal of understanding the function of SDB in relation to stress. Using a touchscreen-mediated cognitive task, the mandrills were observed to self-scratch significantly more often during incorrect than correct trials; however, rates of SDB did not vary between increasingly difficult testing conditions. The mandrills had individual variation in their use of body-shakes and yawns under negative and positive conditions that mirror similar variation observed in other primates. This study provides experimental evidence that self-scratching in mandrills can be used as a behavioural indicator of anxiety and that welfare assessments for animals in human care need to account not only for species' differences, but also for individual differences.
Environmental enrichment plays an integral role in the everyday life of a captive non-human animal. The introduction of technology, as a form of enrichment to captive animals, has opened a new method for their improved welfare. Two captive Siamang (Symphalangus syndactylus) were introduced to digital enrichment through tablet computers. Their behaviors were observed during their interactions with the tablet applications to ensure they were active participants in demonstrating their preferences regarding long-term choices. This provided them with their own freedom of choice not only in interacting with the tablets but, also in selecting their enrichment activities. The goal is to increase their observed well-being, provide cognitive stimulation, and install a permanent technology area for them to safely access and use when they choose.
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.
Many zoos are committed to conservation efforts and answering applied questions about veterinary care and welfare. It is less common, however, for basic science to be conducted in zoos. Comparative cognitive research run in zoos is gaining momentum, with more zoos becoming involved and a greater diversity of species being studied. The majority of cognitive research in zoos is conducted with primates, bears, and elephants. There is less cognitive research run with other species, in particular birds, reptiles and insects, or with zoo visitors. Given the number and variety of animals they house, zoos offer a unique forum to expand the taxonomic focus of cognitive research, especially via multi-institutional collaborations, whilst creating an opportunity to foster public engagement with research.
Animal conservation organisations occasionally harness depictions of animals using digital technology to inspire interest in, and concern for animals. To better understand the forms of empathy experienced by people observing animal-computer interaction, we designed and studied an interactive installation for orangutans at a zoo. Through collaborative design we established an understanding of zoos' objectives and strategies related to empathy in the zoo context. We deployed a prototype installation, and observed and interviewed visitors who watched orangutans use the installation. Analysis of observations and interviews revealed that visitors responded with cognitive, affective and motor empathy for the animals. We propose that these empathetic responses are prompted by the visibility of orangutans' bodily movements, by the 'anthropic frame' provided by digital technology, and by prompting reflection on animals' cognitive processes and affective states. This paper contributes new evidence and understanding of people's empathetic responses to observing animal-computer interaction and confirms the value of designing for empathy in its various forms.
Apes understand false beliefs
We humans tend to believe that our cognitive skills are unique, not only in degree, but also in kind. The more closely we look at other species, however, the clearer it becomes that the difference is one of degree. Krupenye et al. show that three different species of apes are able to anticipate that others may have mistaken beliefs about a situation (see the Perspective by de Waal). The apes appear to understand that individuals have different perceptions about the world, thus overturning the human-only paradigm of the theory of mind.
Science , this issue p. 110 ; see also p. 39
Many animals have been tested for conceptual discriminations using two-dimensional images as stimuli, and many of these species appear to transfer knowledge from 2D images to analogous real life objects. We tested an American black bear for picture-object recognition using a two alternative forced choice task. She was presented with four unique sets of objects and corresponding pictures. The bear showed generalization from both objects to pictures and pictures to objects; however, her transfer was superior when transferring from real objects to pictures, suggesting that bears can recognize visual features from real objects within photographic images during discriminations.
Kyoto City Zoo has collaborated with the Wildlife Research Center of Kyoto University according to the partnership agreement on research and education in wildlife conservation since 2008. As a result of this collaboration, Kyoto City Zoo has established a new section, the "Center for Research and Education of Wildlife," to further promote research and education in the zoo. We have continued to run the "Exhibition of Intelligence" for more than seven years, with four species of primates: chimpanzees, western gorillas, white-handed gibbons, and mandrills. We have also observed various types of behaviors in giraffes, red pandas, Brazilian tapirs, and Humboldt penguins to understand the behaviors in each species. In November 2014, four Asian elephants were given to our zoo by Lao P. D. R. We have used this great opportunity to start various types of research on the elephants, collaborating with many university researchers. We also promote environmental education using this theme. I introduce the activities of research and education in the zoo from the perspective of the "four roles of modern zoos."
In this study, we evaluated the potential for a behavioral research study, designed to evaluate chimpanzee decision-making behavior, to also encourage increased activity in a group of zoo-housed chimpanzees. For the behavioral study, the chimpanzees had to carry tokens to different locations such that they always had to travel farther to obtain a more-preferred reward. We recorded the distance travelled by each subject in each of the three phases of the 15-month study. By the final phase, the chimpanzees' rate of travel during test sessions was significantly higher compared to their baseline activity. Importantly, the chimpanzees' increase in locomotion was not dependent on their participation in the study; rate of travel was not correlated with number of tokens exchanged. However, the chimpanzees' activity returned to baseline within 2 hr of the 30-min test sessions. This study emphasizes the role that research can have in providing enrichment, the importance for long-term enrichment plans, and the essential need to evaluate the impact of research on animal participants, just as we evaluate the efficacy of enrichment strategies. Zoo Biol. XX:1-5, 2016. © 2016 Wiley Periodicals, Inc.
In this paper we investigate social dimensions of technology use in human-animal interactions, through a study of interactive systems at the zoo.