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.

Mammalian empathy: behavioural manifestations and neural basis.

Recent research on empathy in humans and other mammals seeks to dissociate emotional and cognitive empathy. These forms, however, remain interconnected in evolution, across species and at the level of neural mechanisms. New data have facilitated the development of empathy models such as the perception-action model (PAM) and mirror-neuron theories. According to the PAM, the emotional states of others are understood through personal, embodied representations that allow empathy and accuracy to increase based on the observer's past experiences. In this Review, we discuss the latest evidence from studies carried out across a wide range of species, including studies on yawn contagion, consolation, aid-giving and contagious physiological affect, and we summarize neuroscientific data on representations related to another's state.

The phylogenetic roots of human lethal violence.

The psychological, sociological and evolutionary roots of conspecific violence in humans are still debated, despite attracting the attention of intellectuals for over two millennia. Here we propose a conceptual approach towards understanding these roots based on the assumption that aggression in mammals, including humans, has a significant phylogenetic component. By compiling sources of mortality from a comprehensive sample of mammals, we assessed the percentage of deaths due to conspecifics and, using phylogenetic comparative tools, predicted this value for humans. The proportion of human deaths phylogenetically predicted to be caused by interpersonal violence stood at 2%. This value was similar to the one phylogenetically inferred for the evolutionary ancestor of primates and apes, indicating that a certain level of lethal violence arises owing to our position within the phylogeny of mammals. It was also similar to the percentage seen in prehistoric bands and tribes, indicating that we were as lethally violent then as common mammalian evolutionary history would predict. However, the level of lethal violence has changed through human history and can be associated with changes in the socio-political organization of human populations. Our study provides a detailed phylogenetic and historical context against which to compare levels of lethal violence observed throughout our history.

Zoo-housed mammals do not avoid giving birth on weekends.

There is evidence that zoo visitor presence can influence the behaviour and, in some cases, adrenal response of zoo animals, and can sometimes compromise animal welfare. In some laboratory studies, significantly more primate births have been reported on weekends, when fewer people are working there, compared with weekdays when staffing levels are at their highest. Here, we investigate whether there is evidence of a "weekend effect" on births in zoo animals as a result of visitor numbers. Unlike laboratories, zoos are typically busier with visitors on weekends than on weekdays, although staffing levels remain fairly consistent across days of the week. If zoo animal parturition is sensitive to human presence, then fewer births would be expected on weekends compared with weekdays. We tested this using birth data and visitor numbers on the entrance gate from zoo records across 16 species representing artiodactyls, perissodactyls, carnivores and primates at four British zoos, to see whether there is an association between mean daily birth rates and average visitor numbers. We predict that, if there is a visitor effect, daily births should be lower on weekends than weekdays and should correlate with mean daily visitor numbers. Results showed that births for all 16 species were randomly distributed through the week, and there was no significant decline in births on weekends. We conclude that the "weekend effect", if such a thing exists, does not appear to be a feature of zoo births, suggesting that elevated weekend visitor numbers are not sufficiently stressful to trigger delayed parturition.

Empirical assumptions behind the violation of expectation experiments in human and non-human animals.

One of the most widely used procedures applied to non-human animals or pre-linguistic humans is the "violation of expectation paradigm". Curiously there is almost no discussion in the philosophical literature about it. Our objective will be to provide a first approach to the meta-theoretical nature of the assumptions behind the procedure that appeals to the violation of expectation and to extract some consequences. We show that behind them exists an empirical principle that affirms that the violation of the expectation of certain mental rules generates surprise. We then proceeded to discuss the nature of these "mental rules". We show that, as is often the case with theoretical concepts proposed by theories, they do not have a fixed interpretation. This will allow us to show that the usual relationship found in the developmental psychology literature between this experimental paradigm and cognitive approaches (which interpret experimental results in terms of higher-level mental activities) is not necessary. Finally, we relate this experimental design with the mark test and the inequity aversion test and discuss the possible ampliation of the application of the empirical principle of violation of expectation.

Male-mediated prenatal loss: Functions and mechanisms.

Sexually selected infanticide has been the subject of intense empirical and theoretical study for decades; a related phenomenon, male-mediated prenatal loss, has received much less attention in evolutionary studies. Male-mediated prenatal loss occurs when inseminated or pregnant females terminate reproductive effort following exposure to a nonsire male, either through implantation failure or pregnancy termination. Male-mediated prenatal loss encompasses two sub-phenomena: sexually selected feticide and the Bruce effect. In this review, we provide a framework that explains the relationship between feticide and the Bruce effect and describes what is known about the proximate and ultimate mechanisms involved in each. Using a simple model, we demonstrate that male-mediated prenatal loss can provide greater reproductive benefits to males than infanticide. We therefore suggest that, compared to infanticide, male-mediated prenatal loss may be more prevalent in mammalian species and may have played a greater role in their social evolution than has previously been documented.

The neurobiology of parenting: A neural circuit perspective.

Social interactions are essential for animals to reproduce, defend their territory, and raise their young. The conserved nature of social behaviors across animal species suggests that the neural pathways underlying the motivation for, and the execution of, specific social responses are also maintained. Modern tools of neuroscience have offered new opportunities for dissecting the molecular and neural mechanisms controlling specific social responses. We will review here recent insights into the neural circuits underlying a particularly fascinating and important form of social interaction, that of parental care. We will discuss how these findings open new avenues to deconstruct infant-directed behavioral control in males and females, and to help understand the neural basis of parenting in a variety of animal species, including humans. Please also see the video abstract here.

Common and divergent psychobiological mechanisms underlying maternal behaviors in non-human and human mammals.

Maternal interactions with young occupy most of the reproductive period for female mammals and are absolutely essential for offspring survival and development. The hormonal, sensory, reward-related, emotional, cognitive and neurobiological regulators of maternal caregiving behaviors have been well studied in numerous subprimate mammalian species, and some of the importance of this body of work is thought to be its relevance for understanding similar controls in humans. We here review many of the important biopsychological influences on maternal behaviors in the two best studied non-human animals, laboratory rats and sheep, and directly examine how the conceptual framework established by some of the major discoveries in these animal "models" do or do not hold for our understanding of human mothering. We also explore some of the limits for extrapolating from non-human animals to humans. We conclude that there are many similarities between non-human and human mothers in the biological and psychological factors influencing their early maternal behavior and that many of the differences are due to species-characteristic features related to the role of hormones, the relative importance of each sensory system, flexibility in what behaviors are exhibited, the presence or absence of language, and the complexity of cortical function influencing caregiving behaviors.

Correlates of genetic monogamy in socially monogamous mammals: insights from Azara's owl monkeys.

Understanding the evolution of mating systems, a central topic in evolutionary biology for more than 50 years, requires examining the genetic consequences of mating and the relationships between social systems and mating systems. Among pair-living mammals, where genetic monogamy is extremely rare, the extent of extra-group paternity rates has been associated with male participation in infant care, strength of the pair bond and length of the breeding season. This study evaluated the relationship between two of those factors and the genetic mating system of socially monogamous mammals, testing predictions that male care and strength of pair bond would be negatively correlated with rates of extra-pair paternity (EPP). Autosomal microsatellite analyses provide evidence for genetic monogamy in a pair-living primate with bi-parental care, the Azara's owl monkey (Aotus azarae). A phylogenetically corrected generalized least square analysis was used to relate male care and strength of the pair bond to their genetic mating system (i.e. proportions of EPP) in 15 socially monogamous mammalian species. The intensity of male care was correlated with EPP rates in mammals, while strength of pair bond failed to reach statistical significance. Our analyses show that, once social monogamy has evolved, paternal care, and potentially also close bonds, may facilitate the evolution of genetic monogamy.

Marine mammal audibility of selected shallow-water survey sources.

Most attention about the acoustic effects of marine survey sound sources on marine mammals has focused on airgun arrays, with other common sources receiving less scrutiny. Sound levels above hearing threshold (sensation levels) were modeled for six marine mammal species and seven different survey sources in shallow water. The model indicated that odontocetes were most likely to hear sounds from mid-frequency sources (fishery, communication, and hydrographic systems), mysticetes from low-frequency sources (sub-bottom profiler and airguns), and pinnipeds from both mid- and low-frequency sources. High-frequency sources (side-scan and multibeam) generated the lowest estimated sensation levels for all marine mammal species groups.

Mammals responded to reduced road traffic.

COVID-19 restrictions in 2020 reduced traffic worldwide and altered animal movement.

Behavioral responses of terrestrial mammals to COVID-19 lockdowns.

COVID-19 lockdowns in early 2020 reduced human mobility, providing an opportunity to disentangle its effects on animals from those of landscape modifications. Using GPS data, we compared movements and road avoidance of 2300 terrestrial mammals (43 species) during the lockdowns to the same period in 2019. Individual responses were variable with no change in average movements or road avoidance behavior, likely due to variable lockdown conditions. However, under strict lockdowns 10-day 95th percentile displacements increased by 73%, suggesting increased landscape permeability. Animals' 1-hour 95th percentile displacements declined by 12% and animals were 36% closer to roads in areas of high human footprint, indicating reduced avoidance during lockdowns. Overall, lockdowns rapidly altered some spatial behaviors, highlighting variable but substantial impacts of human mobility on wildlife worldwide.

Care for kin: within-group relatedness and allomaternal care are positively correlated and conserved throughout the mammalian phylogeny.

With an increasing amount of data becoming available, comparative analyses have called attention to the associations between cooperative breeding, monogamy and relatedness. We focus here upon the association between allomaternal care and relatedness among females within a social unit. Previous studies found a positive association, but such results date back to before molecular tools were in common use, they considered only a few mammalian orders, neglected phylogenetic clustering and/or did not correct for group sizes. Here, we use molecular data on relatedness from 44 species of mammals to investigate the phylogenetic clustering of, and the association between, allomaternal care and relatedness among females within a social unit. We find (i) a strong phylogenetic signal for allomaternal care and a moderate one for relatedness and group size, and (ii) a positive association between relatedness and allomaternal care, even when correcting for the smaller than average group sizes in species with allomaternal care. We also find that, in species without allomaternal care, adult females often live with unrelated females even when groups are small. We discuss these results in the light of recent evidence for the role of kin selection and the monogamy hypothesis in cooperative breeding.

Psychophysical studies of auditory masking in marine mammals: key concepts and new directions.

Current models of auditory masking in marine mammals oversimplify hearing in realistic environments. Systematic and progressive experiments using psychoacoustic methods will help us move "out of the ideal and in to the real" to gain a more complete view of potential auditory-masking effects in these animals.

Placentophagia in humans and nonhuman mammals: causes and consequences.

Afterbirth ingestion by nonhuman mammalian mothers has a number of benefits: (1) increasing the interaction between the mother and infant; (2) potentiating pregnancy-mediated analgesia in the delivering mother; (3) potentiating maternal brain opioid circuits that facilitate the onset of caretaking behavior; and (4) suppressing postpartum pseudopregnancy. Childbirth is fraught with additional problems for which there are no practical nonhuman animal models: postpartum depression, failure to bond, hostility toward infants. Ingested afterbirth may contain components that ameliorate these problems, but the issue has not been tested empirically. The results of such studies, if positive, will be medically relevant. If negative, speculations and recommendations will persist, as it is not possible to prove the negative. A more challenging anthropological question is "why don't humans engage in placentophagia as a biological imperative?" Is it possible that there is more adaptive advantage in not doing so?

Interaction between ungulates and bruchid beetles and its effect on Acacia trees: modeling the costs and benefits of seed dispersal to plant demography.

Integrative studies of plant-animal interactions that incorporate the multiple effects of interactions are important for discerning the importance of each factor within the population dynamics of a plant species. The low regeneration capacity of many Acacia species in arid savannas is a consequence of a combination of reduction in seed dispersal and high seed predation. Here we studied how ungulates (acting as both seed dispersers and herbivores) and bruchid beetles (post-dispersal seed predators) modulate the population dynamics of A. raddiana, a keystone species in the Middle East. We developed two simulation models of plant demography: the first included seed ingestion by ungulates and seed predation by bruchids, whereas the second model additionally incorporated herbivory by ungulates. We also included the interacting effects of seed removal and body mass, because larger ungulates destroy proportionally fewer seeds and enhance seed germination. Simulations showed that the negative effect of seed predation on acacia population size was compensated for by the positive effect of seed ingestion at 50 and 30% seed removal under scenarios with and without herbivory, respectively. Smaller ungulates (e.g., <35 kg) must necessarily remove tenfold more seeds than larger ungulates (e.g., >250 kg) to compensate for the negative effect of seed predation. Seedling proportion increased with seed removal in the model with herbivory. Managing and restoring acacia seed dispersers is key to conserving acacia populations, because low-to-medium seed removal could quickly restore their regeneration capacity.

Toward a cross-species neuroscientific understanding of the affective mind: do animals have emotional feelings?

Do we need to consider mental processes in our analysis of brain functions in other animals? Obviously we do, if such BrainMind functions exist in the animals we wish to understand. If so, how do we proceed, while still retaining materialistic-mechanistic perspectives? This essay outlines the historical forces that led to emotional feelings in animals being marginalized in behavioristic scientific discussions of why animals behave the way they do, and why mental constructs are generally disregarded in modern neuroscientific analyses. The roots of this problem go back to Cartesian dualism and the attempt of 19th century physician-scientists to ground a new type of medical curriculum on a completely materialistic approach to body functions. Thereby all vitalistic principles were discarded from the lexicon of science, and subjective experience in animals was put in that category and discarded as an invalid approach to animal behavior. This led to forms of rigid operationalism during the era of behaviorism and subsequently ruthless reductionism in brain research, leaving little room for mentalistic concepts such as emotional feelings in animal research. However, modern studies of the brain clearly indicate that artificially induced arousals of emotional networks, as with localized electrical and chemical brain stimulation, can serve as "rewards" and "punishments" in various learning tasks. This strongly indicates that animal brains elaborate various experienced states, with those having affective contents being easiest to study rigorously. However, in approaching emotional feelings empirically we must pay special attention to the difficulties and vagaries of human language and evolutionary levels of control in the brain. We need distinct nomenclatures from primary (unconditioned phenomenal experiences) to tertiary (reflective) levels of mind. The scientific pursuit of affective brain processes in other mammals can now reveal general BrainMind principles that also apply to human feelings, as with neurochemical predictions from preclinical animal models to self-reports of corresponding human experiences. In short, brain research has now repeatedly verified the existence of affective experience-various reward and punishment functions-during artificial arousal of emotional networks in our fellow animals. The implications for new conceptual schema for understanding human/primate affective feelings and how such knowledge can impact scientific advances in biological psychiatry are also addressed.

Rhythm interaction in animal groups: selective attention in communication networks.

Animals communicating interactively with conspecifics often time their broadcasts to avoid overlapping interference, to emit leading, as opposed to following, signals or to synchronize their signalling rhythms. Each of these adjustments becomes more difficult as the number of interactants increases beyond a pair. Among acoustic species, insects and anurans generally deal with the problem of group signalling by means of 'selective attention' in which they focus on several close or conspicuous neighbours and ignore the rest. In these animals, where signalling and receiving are often dictated by sex, the process of selective attention in signallers may have a parallel counterpart in receivers, which also focus on close neighbours. In birds and mammals, local groups tend to be extended families or clans, and group signalling may entail complex timing mechanisms that allow for attention to all individuals. In general, the mechanisms that allow animals to communicate in groups appear to be fully interwoven with the basic process of rhythmic signalling. This article is part of the theme issue 'Synchrony and rhythm interaction: from the brain to behavioural ecology'.

Rhythm in dyadic interactions.

This review paper discusses rhythmic interactions and distinguishes them from non-rhythmic interactions. We report on communicative behaviours in social and sexual contexts, as found in dyads of humans, non-human primates, non-primate mammals, birds, anurans and insects. We discuss observed instances of rhythm in dyadic interactions, identify knowledge gaps and propose suggestions for future research. We find that most studies on rhythmicity in interactive signals mainly focus on one modality (acoustic or visual) and we suggest more work should be performed on multimodal signals. Although the social functions of interactive rhythms have been fairly well described, developmental research on rhythms used to regulate social interactions is still lacking. Future work should also focus on identifying the exact timing mechanisms involved. Rhythmic signalling behaviours are widespread and critical in regulating social interactions across taxa, but many questions remain unexplored. A multidisciplinary, comparative cross-species approach may help provide answers. This article is part of the theme issue 'Synchrony and rhythm interaction: from the brain to behavioural ecology'.

What emotions might be like in other animals.

In this My word, Joseph LeDoux explores what the emotional lives of other mammals might be like. He proposes that better understanding of the brain mechanisms of emotional consciousness in humans might shed light on the kinds of conscious capacities that might be possible in non-human primates and non-primate mammals, given the kinds of brains they possess.