The current state of carnivore cognition.

The field of animal cognition has advanced rapidly in the last 25 years. Through careful and creative studies of animals in captivity and in the wild, we have gained critical insights into the evolution of intelligence, the cognitive capacities of a diverse array of taxa, and the importance of ecological and social environments, as well as individual variation, in the expression of cognitive abilities. The field of animal cognition, however, is still being influenced by some historical tendencies. For example, primates and birds are still the majority of study species in the field of animal cognition. Studies of diverse taxa improve the generalizability of our results, are critical for testing evolutionary hypotheses, and open new paths for understanding cognition in species with vastly different morphologies. In this paper, we review the current state of knowledge of cognition in mammalian carnivores. We discuss the advantages of studying cognition in Carnivorans and the immense progress that has been made across many cognitive domains in both lab and field studies of carnivores. We also discuss the current constraints that are associated with studying carnivores. Finally, we explore new directions for future research in studies of carnivore cognition.

Environmental, individual and social traits of free-ranging raccoons influence performance in cognitive testing.

Cognitive abilities, such as learning and flexibility, are hypothesized to aid behavioral adaptation to urbanization. Although growing evidence suggests that cognition may indeed facilitate persistence in urban environments, we currently lack knowledge of the cognitive abilities of many urban taxa. Recent methodological advances, including radio frequency identification (RFID), have extended automated cognitive testing into the field but have yet to be applied to a diversity of taxa. Here, we used an RFID-enabled operant conditioning device to assess the habituation, learning and cognitive flexibility of a wild population of raccoons (Procyon lotor). We examined how several biological and behavioral traits influenced participation and performance in testing. We then compared the cognitive performance of wild raccoons tested in natural conditions with that of wild-caught raccoons tested in captivity from a previous study. In natural conditions, juvenile raccoons were more likely to habituate to the testing device, but performed worse in serial reversal learning, compared with adults. We also found that docile raccoons were more likely to learn how to operate the device in natural conditions, which suggests a relationship between emotional reactivity and cognitive ability in raccoons. Although raccoons in both captive and natural conditions demonstrated rapid associative learning and flexibility, raccoons in captive conditions generally performed better, likely owing to the heightened vigilance and social interference experienced by raccoons in natural conditions. Our results have important implications for future research on urban carnivores and cognition in field settings, as well as our understanding of behavioral adaptation to urbanization and coexistence with urban wildlife.

Links between personality traits and problem-solving performance in zebra finches (Taeniopygia guttata).

Consistent individual differences in behaviour across time or contexts (i.e. personality types) have been found in many species and have implications for fitness. Likewise, individual variation in cognitive abilities has been shown to impact fitness. Cognition and personality are complex, multidimensional traits. However, previous work has generally examined the connection between a single personality trait and a single cognitive ability, yielding equivocal results. Links between personality and cognitive ability suggest that behavioural traits coevolved and highlight their nuanced connections. Here we examined individuals' performance on multiple personality tests and repeated problem-solving tests (each measuring innovative performance). We assessed behavioural traits (dominance, boldness, activity, risk-taking, aggressiveness and obstinacy) in 41 captive zebra finches. Birds' scores for boldness and obstinacy were consistent over two years. We also examined whether personality correlated with problem-solving performance on repeated tests. Our results indicate that neophobia, dominance and obstinacy were related to successful solving, and less dominant, more obstinate birds solved the tasks quicker on average. Our results indicate the importance of examining multiple measures over a long period. Future work that identifies links between personality and innovation in non-model organisms may elucidate the coevolution of these two forms of individual differences.

Multiple assessments of personality and problem-solving performance in captive Asian elephants (Elephas maximus) and African savanna elephants (Loxodonta africana).

Animal personality has been shown to predict many behavioral responses across taxa, but the relationship between personality and performance on cognitive tasks remains unclear. To address this gap, we investigated whether personality predicted problem-solving performance and learning in captive Asian and African savanna elephants. We leveraged 3 novel problem-solving tasks to assess success rate, latency to touch the apparatus, exploratory diversity (the number of different behaviors exhibited toward the task), work time (the proportion of time working on the tasks), and latency to solve. To measure multiple different personality traits, such as boldness, activity, aggressiveness, curiosity, and sociability, across contexts, we carried out novel object presentations, behavioral coding through observations, and trait rating through surveys with zookeepers. We found evidence of personality through behavioral observations and surveys, but not through novel object testing. Aggressiveness and activity were important predictors of problem solving, but this was task-dependent, and the traits we measured did not significantly predict learning. Elephants solved 2 out of 3 tasks faster over time, but they did not vary their latency to touch, exploratory diversity, or work time. We discuss our results in terms of task difficulty and previous work on personality in elephants. Results from this study lay the foundation for future work connecting individual variation in personality to cognitive performance in elephants. In addition, for zoo-housed animals, individual differences research could inform enrichment and welfare decisions as well as conservation strategies. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Cytoarchitectural characteristics associated with cognitive flexibility in raccoons.

With rates of psychiatric illnesses such as depression continuing to rise, additional preclinical models are needed to facilitate translational neuroscience research. In the current study, the raccoon (Procyon lotor) was investigated due to its similarities with primate brains, including comparable proportional neuronal densities, cortical magnification of the forepaw area, and cortical gyrification. Specifically, we report on the cytoarchitectural characteristics of raccoons profiled as high, intermediate, or low solvers in a multiaccess problem-solving task. Isotropic fractionation indicated that high-solvers had significantly more cells in the hippocampus (HC) than the other solving groups; further, a nonsignificant trend suggested that this increase in cell profile density was due to increased nonneuronal (e.g., glial) cells. Group differences were not observed in the cellular density of the somatosensory cortex. Thionin-based staining confirmed the presence of von Economo neurons (VENs) in the frontoinsular cortex, although no impact of solving ability on VEN cell profile density levels was observed. Elongated fusiform cells were quantified in the HC dentate gyrus where high-solvers were observed to have higher levels of this cell type than the other solving groups. In sum, the current findings suggest that varying cytoarchitectural phenotypes contribute to cognitive flexibility. Additional research is necessary to determine the translational value of cytoarchitectural distribution patterns on adaptive behavioral outcomes associated with cognitive performance and mental health.

Variation in reversal learning by three generalist mesocarnivores.

Urbanization imposes novel challenges for wildlife, but also provides new opportunities for exploitation. Generalist species are commonly found in urban habitats, but the cognitive mechanisms facilitating their successful behavioral adaptations and exploitations are largely under-investigated. Cognitive flexibility is thought to enable generalists to be more plastic in their behavior, thereby increasing their adaptability to a variety of environments, including urban habitats. Yet direct measures of cognitive flexibility across urban wildlife are lacking. We used a classic reversal-learning paradigm to investigate the cognitive flexibility of three generalist mesocarnivores commonly found in urban habitats: striped skunks (Mephitis mephitis), raccoons (Procyon lotor), and coyotes (Canis latrans). We developed an automated device and testing protocol that allowed us to administer tests of reversal learning in captivity without extensive training or experimenter involvement. Although most subjects were able to rapidly form and reverse learned associations, we found moderate variation in performance and behavior during trials. Most notably, we observed heightened neophobia and a lack of habituation expressed by coyotes. We discuss the implications of such differences among generalists with regard to urban adaptation and we identify goals for future research. This study is an important step in investigating the relationships between cognition, generalism, and urban adaptation.

Behavioral flexibility of a generalist carnivore.

Innovative problem solving, repeated innovation, learning, and inhibitory control are cognitive abilities commonly regarded as important components of behaviorally flexible species. Animals exhibiting these cognitive abilities may be more likely to adapt to the unique demands of living in novel and rapidly changing environments, such as urbanized landscapes. Raccoons (Procyon lotor) are an abundant, generalist species frequently found in urban habitats, and are capable of innovative problem solving, which makes them an ideal species to assess their behavioral flexibility. We gave 20 captive raccoons a multi-access puzzle box to investigate which behavioral and cognitive mechanisms enable the generation of innovative and flexible behaviors in this species. Over two-thirds of raccoons tested were not only capable of innovative problem solving, but displayed repeated innovation by solving more than one solution on the multi-access puzzle box and demonstrated that they learned multiple solutions to a novel problem. Although we found no relationship between our measure of inhibitory control and a raccoon's ability to exhibit repeated innovations, we did find a positive relationship between the diversity of behaviors that an individual exhibited when interacting with the problem and the number of solution types that they solved. We identified other predictors of problem-solving performance, including neophobia and persistence. Finally, we examine the implications of our results in the context of the cognitive-buffer hypothesis and consider whether the widespread success of an adaptive generalist carnivore could be due in part to having these cognitive and behavioral traits.

Adaptation of the Aesop's Fable paradigm for use with raccoons (Procyon lotor): considerations for future application in non-avian and non-primate species.

To gain a better understanding of the evolution of animal cognition, it is necessary to test and compare the cognitive abilities of a broad array of taxa. Meaningful inter-species comparisons are best achieved by employing universal paradigms that standardize testing among species. Many cognitive paradigms, however, have been tested in only a few taxa, mostly birds and primates. One such example, known as the Aesop's Fable paradigm, is designed to assess causal understanding in animals using water displacement. To evaluate the universal effectiveness of the Aesop's Fable paradigm, we applied this paradigm to a previously untested taxon, the raccoon (Procyon lotor). We first trained captive raccoons to drop stones into a tube of water to retrieve a floating food reward. Next, we presented successful raccoons with objects that differed in the amount of water they displaced to determine whether raccoons could select the most functional option. Raccoons performed differently than corvids and human children did in previous studies of Aesop's Fable, and we found raccoons to be innovative in many aspects of this task. We suggest that raccoon performance in this paradigm reflected differences in tangential factors, such as behavior, morphology, and testing procedures, rather than cognitive deficiencies. We also present insight into previously undocumented challenges that should better inform future Aesop's Fable studies incorporating more diverse taxa.

The evolution of intelligence in mammalian carnivores.

Although intelligence should theoretically evolve to help animals solve specific types of problems posed by the environment, it is unclear which environmental challenges favour enhanced cognition, or how general intelligence evolves along with domain-specific cognitive abilities. The social intelligence hypothesis posits that big brains and great intelligence have evolved to cope with the labile behaviour of group mates. We have exploited the remarkable convergence in social complexity between cercopithecine primates and spotted hyaenas to test predictions of the social intelligence hypothesis in regard to both cognition and brain size. Behavioural data indicate that there has been considerable convergence between primates and hyaenas with respect to their social cognitive abilities. Moreover, compared with other hyaena species, spotted hyaenas have larger brains and expanded frontal cortex, as predicted by the social intelligence hypothesis. However, broader comparative study suggests that domain-general intelligence in carnivores probably did not evolve in response to selection pressures imposed specifically in the social domain. The cognitive buffer hypothesis, which suggests that general intelligence evolves to help animals cope with novel or changing environments, appears to offer a more robust explanation for general intelligence in carnivores than any hypothesis invoking selection pressures imposed strictly by sociality or foraging demands.

Numerical assessment in the wild: insights from social carnivores.

Playback experiments have proved to be a useful tool to investigate the extent to which wild animals understand numerical concepts and the factors that play into their decisions to respond to different numbers of vocalizing conspecifics. In particular, playback experiments have broadened our understanding of the cognitive abilities of historically understudied species that are challenging to test in the traditional laboratory, such as members of the Order Carnivora. Additionally, playback experiments allow us to assess the importance of numerical information versus other ecologically important variables when animals are making adaptive decisions in their natural habitats. Here, we begin by reviewing what we know about quantity discrimination in carnivores from studies conducted in captivity. We then review a series of playback experiments conducted with wild social carnivores, including African lions, spotted hyenas and wolves, which demonstrate that these animals can assess the number of conspecifics calling and respond based on numerical advantage. We discuss how the wild studies complement those conducted in captivity and allow us to gain insights into why wild animals may not always respond based solely on differences in quantity. We then consider the key roles that individual discrimination and cross-modal recognition play in the ability of animals to assess the number of conspecifics vocalizing nearby. Finally, we explore new directions for future research in this area, highlighting in particular the need for further work on the cognitive basis of numerical assessment skills and experimental paradigms that can be effective in both captive and wild settings.This article is part of a discussion meeting issue 'The origins of numerical abilities'.

Sex and pairing status impact how zebra finches use social information in foraging.

Many factors, including the demonstrator's sex, status, and familiarity, shape the nature and magnitude of social learning. Given the important role of pair bonds in socially-monogamous animals, we predicted that these intimate relationships would promote the use of social information, and tested this hypothesis in zebra finches (Taeniopygia guttata). Observer birds witnessed either their mate or another familiar, opposite-sex bird eat from one, but not a second novel food source, before being allowed to feed from both food sources themselves. Birds used social information to make foraging decisions, but not all individuals used this information in the same way. While most individuals copied the foraging choice of the demonstrator as predicted, paired males did not, instead avoiding the feeder demonstrated by their mate. Our findings reveal that sex and pairing status interact to influence the use of social information and suggest that paired males might use social information to avoid competing with their mate.

Brain size predicts problem-solving ability in mammalian carnivores.

Despite considerable interest in the forces shaping the relationship between brain size and cognitive abilities, it remains controversial whether larger-brained animals are, indeed, better problem-solvers. Recently, several comparative studies have revealed correlations between brain size and traits thought to require advanced cognitive abilities, such as innovation, behavioral flexibility, invasion success, and self-control. However, the general assumption that animals with larger brains have superior cognitive abilities has been heavily criticized, primarily because of the lack of experimental support for it. Here, we designed an experiment to inquire whether specific neuroanatomical or socioecological measures predict success at solving a novel technical problem among species in the mammalian order Carnivora. We presented puzzle boxes, baited with food and scaled to accommodate body size, to members of 39 carnivore species from nine families housed in multiple North American zoos. We found that species with larger brains relative to their body mass were more successful at opening the boxes. In a subset of species, we also used virtual brain endocasts to measure volumes of four gross brain regions and show that some of these regions improve model prediction of success at opening the boxes when included with total brain size and body mass. Socioecological variables, including measures of social complexity and manual dexterity, failed to predict success at opening the boxes. Our results, thus, fail to support the social brain hypothesis but provide important empirical support for the relationship between relative brain size and the ability to solve this novel technical problem.

Brains, brawn and sociality: a hyaena's tale.

Theoretically intelligence should evolve to help animals solve specific types of problems posed by the environment, but it remains unclear how environmental complexity or novelty facilitates the evolutionary enhancement of cognitive abilities, or whether domain-general intelligence can evolve in response to domain-specific selection pressures. The social complexity hypothesis, which posits that intelligence evolved to cope with the labile behaviour of conspecific group-mates, has been strongly supported by work on the sociocognitive abilities of primates and other animals. Here we review the remarkable convergence in social complexity between cercopithecine primates and spotted hyaenas, and describe our tests of predictions of the social complexity hypothesis in regard to both cognition and brain size in hyaenas. Behavioural data indicate that there has been remarkable convergence between primates and hyaenas with respect to their abilities in the domain of social cognition. Furthermore, within the family Hyaenidae, our data suggest that social complexity might have contributed to enlargement of the frontal cortex. However, social complexity failed to predict either brain volume or frontal cortex volume in a larger array of mammalian carnivores. To address the question of whether or not social complexity might be able to explain the evolution of domain-general intelligence as well as social cognition in particular, we presented simple puzzle boxes, baited with food and scaled to accommodate body size, to members of 39 carnivore species housed in zoos and found that species with larger brains relative to their body mass were more innovative and more successful at opening the boxes. However, social complexity failed to predict success in solving this problem. Overall our work suggests that, although social complexity enhances social cognition, there are no unambiguous causal links between social complexity and either brain size or performance in problem-solving tasks outside the social domain in mammalian carnivores.

Limited social learning of a novel technical problem by spotted hyenas.

Social learning can have profound evolutionary consequences because it drives the diffusion of novel behaviours among individuals and promotes the maintenance of traditions within populations. We inquired whether spotted hyenas (Crocuta crocuta), generalist carnivores living in complex, primate-like societies, acquire information from conspecifics about a novel problem-solving task. Previously, we presented wild hyenas with a food-access puzzle and found that social learning opportunities did not affect problem-solving success among observers, but did reduce observers' neophobia. However, we had little control over which individuals observed conspecifics solve the problem, and few wild hyenas were successful. Therefore, we conducted an experiment in captivity where we controlled observer access to two demonstration styles. Again, social learning opportunities did not affect problem-solving success, but tended to reduce neophobia among captive observers. Social learning opportunities also influenced problem-solving style. Captive hyenas showed limited evidence for directed social learning; low-ranking individuals paid closer attention to demonstrators than high-ranking individuals, although this greater attention did not result in greater success. We conclude that wild and captive hyenas exploit social learning opportunities similarly, and that the limited social learning shown by hyenas on this task is likely based on localized stimulus enhancement.

Innovative problem solving by wild spotted hyenas.

Innovative animals are those able to solve novel problems or invent novel solutions to existing problems. Despite the important ecological and evolutionary consequences of innovation, we still know very little about the traits that vary among individuals within a species to make them more or less innovative. Here we examine innovative problem solving by spotted hyenas (Crocuta crocuta) in their natural habitat, and demonstrate for the first time in a non-human animal that those individuals exhibiting a greater diversity of initial exploratory behaviours are more successful problem solvers. Additionally, as in earlier work, we found that neophobia was a critical inhibitor of problem-solving success. Interestingly, although juveniles and adults were equally successful in solving the problem, juveniles were significantly more diverse in their initial exploratory behaviours, more persistent and less neophobic than were adults. We found no significant effects of social rank or sex on success, the diversity of initial exploratory behaviours, behavioural persistence or neophobia. Our results suggest that the diversity of initial exploratory behaviours, akin to some measures of human creativity, is an important, but largely overlooked, determinant of problem-solving success in non-human animals.