Elephants as an animal model for self-domestication.

Humans are unique in their sophisticated culture and societal structures, their complex languages, and their extensive tool use. According to the human self-domestication hypothesis, this unique set of traits may be the result of an evolutionary process of self-induced domestication, in which humans evolved to be less aggressive and more cooperative. However, the only other species that has been argued to be self-domesticated besides humans so far is bonobos, resulting in a narrow scope for investigating this theory limited to the primate order. Here, we propose an animal model for studying self-domestication: the elephant. First, we support our hypothesis with an extensive cross-species comparison, which suggests that elephants indeed exhibit many of the features associated with self-domestication (e.g., reduced aggression, increased prosociality, extended juvenile period, increased playfulness, socially regulated cortisol levels, and complex vocal behavior). Next, we present genetic evidence to reinforce our proposal, showing that genes positively selected in elephants are enriched in pathways associated with domestication traits and include several candidate genes previously associated with domestication. We also discuss several explanations for what may have triggered a self-domestication process in the elephant lineage. Our findings support the idea that elephants, like humans and bonobos, may be self-domesticated. Since the most recent common ancestor of humans and elephants is likely the most recent common ancestor of all placental mammals, our findings have important implications for convergent evolution beyond the primate taxa, and constitute an important advance toward understanding how and why self-domestication shaped humans' unique cultural niche.

Cooperating elephants mitigate competition until the stakes get too high.

Cooperation is ubiquitous in the animal kingdom as it aims to maximize benefits through joint action. Selection, however, may also favor competitive behaviors that could violate cooperation. How animals mitigate competition is hotly debated, with particular interest in primates and little attention paid thus far to nonprimates. Using a loose-string pulling apparatus, we explored cooperative and competitive behavior, as well as mitigation of the latter, in semi-wild Asian elephants (Elephas maximus). Our results showed that elephants first maintained a very high cooperation rate (average = 80.8% across 45 sessions). Elephants applied "block," "fight back," "leave," "move side," and "submission" as mitigation strategies and adjusted these strategies according to their affiliation and rank difference with competition initiators. They usually applied a "fight back" mitigation strategy as a sanction when competition initiators were low ranking or when they had a close affiliation, but were submissive if the initiators were high ranking or when they were not closely affiliated. However, when the food reward was limited, the costly competitive behaviors ("monopoly" and "fight") increased significantly, leading to a rapid breakdown in cooperation. The instability of elephant cooperation as a result of benefit reduction mirrors that of human society, suggesting that similar fundamental principles may underlie the evolution of cooperation across species.

Disgust in animals and the application of disease avoidance to wildlife management and conservation.

Disgust is an adaptive system hypothesized to have evolved to reduce the risk of becoming sick. It is associated with behavioural, cognitive and physiological responses tuned to allow animals to avoid and/or get rid of parasites, pathogens and toxins. Little is known about the mechanisms and outcomes of disease avoidance in wild animals. Furthermore, given the escalation of negative human-wildlife interactions, the translation of such knowledge into the design of evolutionarily relevant conservation and wildlife management strategies is becoming urgent. Contemporary methods in animal ecology and related fields, using direct (sensory cues) or indirect (remote sensing technologies and machine learning) means, provide a flexible toolbox for testing and applying disgust at individual and collective levels. In this review/perspective paper, we provide an empirical framework for testing the adaptive function of disgust and its associated disease avoidance behaviours across species, from the least to the most social, in different habitats. We predict various trade-offs to be at play depending on the social system and ecology of the species. We propose five contexts in which disgust-related avoidance behaviours could be applied, including endangered species rehabilitation, invasive species, crop-raiding, urban pests and animal tourism. We highlight some of the perspectives and current challenges of testing disgust in the wild. In particular, we recommend future studies to consider together disease, predation and competition risks. We discuss the ethics associated with disgust experiments in the above contexts. Finally, we promote the creation of a database gathering disease avoidance evidence in animals and its applications.

Le dégoût est un système adaptatif supposé avoir évolué afin de réduire le risque de tomber malade. Il est associé à des réponses comportementales, cognitives et physiologiques adaptées pour permettre aux animaux d'éviter et/ou de se débarrasser des parasites, pathogènes et toxines. On sait peu de choses sur les mécanismes et les conséquences de l'évitement des maladies chez les animaux sauvages. Étant donné l'escalade des interactions négatives entre humains et faune, la traduction de ces connaissances dans la conception de stratégies de conservation et de gestion de la faune - prenant en considération l'évolution des espèces - devient urgente. Les méthodes contemporaines en écologie animale et dans les domaines connexes, utilisant des moyens directs (indices sensoriels) ou indirects (technologies de télédétection et apprentissage automatique), fournissent une boîte à outils flexible pour tester et appliquer le dégoût aux niveaux individuel et collectif. Dans cet article de revue/perspective, nous fournissons un cadre empirique pour tester la fonction adaptative du dégoût et les comportements associés d'évitement des maladies chez différentes espèces - des moins sociales aux plus sociales, et dans différents habitats. Nous prédisons divers compromis en fonction du système social et de l'écologie de l'espèce. Nous proposons cinq contextes dans lesquels les comportements d'évitement liés au dégoût pourraient être appliqués: la réhabilitation d'espèces menacées; les espèces envahissantes; les dommages aux cultures; les nuisibles urbains; et le tourisme animalier. Nous mettons en avant certaines perspectives et défis actuels de l'expérimentation sur le dégoût en milieu naturel. En particulier, nous recommandons la considération de plusieurs risques ensemble: maladie, prédation et compétition. Nous discutons également de l'éthique associée aux expériences sur le dégoût dans les contextes ci-dessus. Enfin, nous promouvons la création d'une base de données rassemblant les stratégies d'évitement des maladies chez les animaux et leurs applications.

Persistence is key: investigating innovative problem solving by Asian elephants using a novel multi-access box.

Innovative problem solving is considered a hallmark measure of behavioral flexibility as it describes behavior by which an animal manipulates its environment in a novel way to reach a goal. Elephants are a highly social taxa that have demonstrated a remarkable capacity for adapting to changing environments. To understand how individual differences in behavior impact expressions of innovation, we used a novel extractive foraging device comprised of three compartments to evaluate innovation in 14 captive Asian elephants. In the first phase of testing, elephants had an opportunity to learn one solution, while the second phase gave them an opportunity to innovate to open two other compartments with different solutions. We measured the behavioral traits of neophilia, persistence, motivation, and exploratory diversity, and hypothesized that higher levels of each would be associated with more success in the second phase. Eight elephants innovated to solve three compartments, three solved two, and two solved only one. Consistent with studies in other species, we found that higher success was associated with greater persistence, but not with any other behavioral traits when analyzed per test session. Greater persistence and, unexpectedly, lower exploratory diversity, were associated with success when analyzed at the level of each individual door. Further work is needed to understand how innovation varies both within and between species, with particular attention to the potential impact of anthropogenic changes in wild environments.

Elephants have a nose for quantity.

Animals often face situations that require making decisions based on quantity. Many species, including humans, rely on an ability to differentiate between more and less to make judgments about social relationships, territories, and food. Habitat-related choices require animals to decide between areas with greater and lesser quantities of food while also weighing relative risk of danger based on group size and predation risk. Such decisions can have a significant impact on survival for an animal and its social group. Many species have demonstrated a capacity for differentiating between two quantities of food and choosing the greater of the two, but they have done so based on information provided primarily in the visual domain. Using an object-choice task, we demonstrate that elephants are able to discriminate between two distinct quantities using their olfactory sense alone. We presented the elephants with choices between two containers of sunflower seeds. The relationship between the amount of seeds within the two containers was represented by 11 different ratios. Overall, the elephants chose the larger quantity of food by smelling for it. The elephants' performance was better when the relative difference between the quantities increased and worse when the ratio between the quantities of food increased, but was not affected by the overall quantity of food presented. These results are consistent with the performance of animals tested in the visual domain. This work has implications for the design of future, cross-phylogenetic cognitive comparisons that ought to account for differences in how animals sense their world.

The use of a human's location and social cues by Asian elephants in an object-choice task.

Asian elephants have previously demonstrated an ability to follow olfactory cues, but not human-provided social cues like pointing and gazing or orienting to find hidden food (Plotnik et al. in PLoS One 8:e61174, 2013; Anim Behav 88:91-98, 2014). In a study conducted with African elephants, however, elephants were able to follow a combination of these social cues to find food, even when the experimenter's position was counter to the location of the food. The authors of the latter study argued that the differences in the two species' performances might have been due to methodological differences in the study designs (Smet and Byrne in Curr Biol 23(20):2033-2037, 2013). To further investigate the reasons for these potential differences, we partially adapted Smet and Byrne (2013)'s design for a group of Asian elephants in Thailand. In a two-object-choice task in which only one of two buckets was baited with food, we found that, as a group, the elephants did not follow cues provided by an experimenter when she was positioned either equidistant between the buckets or closer to the incorrect bucket when providing the cues. The elephants did, however, follow cues when the experimenter was closer to the correct bucket. In addition, there was individual variability in the elephants' performance within and across experimental conditions. This indicates that in general, for Asian elephants, the pointing and/or gazing cues alone may not be salient enough; local enhancement in the form of the experimenter's position in relation to the food reward may represent a crucial, complementary cue. These results suggest that the variability within and between the species in their performance on these tasks could be due to a number of factors, including methodology, the elephants' experiences with their handlers, ecological differences in how Asian and African elephants use non-visual sensory information to find food in the wild, or some combination of the three.

The evolution of self-control.

Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

Elephants know when they need a helping trunk in a cooperative task.

Elephants are widely assumed to be among the most cognitively advanced animals, even though systematic evidence is lacking. This void in knowledge is mainly due to the danger and difficulty of submitting the largest land animal to behavioral experiments. In an attempt to change this situation, a classical 1930s cooperation paradigm commonly tested on monkeys and apes was modified by using a procedure originally designed for chimpanzees (Pan troglodytes) to measure the reactions of Asian elephants (Elephas maximus). This paradigm explores the cognition underlying coordination toward a shared goal. What do animals know or learn about the benefits of cooperation? Can they learn critical elements of a partner's role in cooperation? Whereas observations in nature suggest such understanding in nonhuman primates, experimental results have been mixed, and little evidence exists with regards to nonprimates. Here, we show that elephants can learn to coordinate with a partner in a task requiring two individuals to simultaneously pull two ends of the same rope to obtain a reward. Not only did the elephants act together, they inhibited the pulling response for up to 45 s if the arrival of a partner was delayed. They also grasped that there was no point to pulling if the partner lacked access to the rope. Such results have been interpreted as demonstrating an understanding of cooperation. Through convergent evolution, elephants may have reached a cooperative skill level on a par with that of chimpanzees.

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

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

Day and night camera trap videos are effective for identifying individual wild Asian elephants.

Regular monitoring of wild animal populations through the collection of behavioral and demographic data is critical for the conservation of endangered species. Identifying individual Asian elephants (Elephas maximus), for example, can contribute to our understanding of their social dynamics and foraging behavior, as well as to human-elephant conflict mitigation strategies that account for the behavior of specific individuals involved in the conflict. Wild elephants can be distinguished using a variety of different morphological traits-e.g., variations in ear and tail morphology, body scars and tumors, and tusk presence, shape, and length-with previous studies identifying elephants via direct observation or photographs taken from vehicles. When elephants live in dense forests like in Thailand, remote sensing photography can be a productive approach to capturing anatomical and behavioral information about local elephant populations. While camera trapping has been used previously to identify elephants, here we present a detailed methodology for systematic, experimenter differentiation of individual elephants using data captured from remote sensing video camera traps. In this study, we used day and night video footage collected remotely in the Salakpra Wildlife Sanctuary in Thailand and identified 24 morphological characteristics that can be used to recognize individual elephants. A total of 34 camera traps were installed within the sanctuary as well as crop fields along its periphery, and 107 Asian elephants were identified: 72 adults, 11 sub-adults, 20 juveniles, and four infants. We predicted that camera traps would provide enough information such that classified morphological traits would aid in reliably identifying the adult individuals with a low probability of misidentification. The results indicated that there were low probabilities of misidentification between adult elephants in the population using camera traps, similar to probabilities obtained by other researchers using handheld cameras. This study suggests that the use of day and night video camera trapping can be an important tool for the long-term monitoring of wild Asian elephant behavior, especially in habitats where direct observations may be difficult.

Acknowledging the Relevance of Elephant Sensory Perception to Human-Elephant Conflict Mitigation.

Elephants are well known for their socio-cognitive abilities and capacity for multi-modal sensory perception and communication. Their highly developed olfactory and acoustic senses provide them with a unique non-visual perspective of their physical and social worlds. The use of these complex sensory signals is important not only for communication between conspecifics, but also for decisions about foraging and navigation. These decisions have grown increasingly risky given the exponential increase in unpredictable anthropogenic change in elephants' natural habitats. Risk taking often develops from the overlap of human and elephant habitat in Asian and African range countries, where elephants forage for food in human habitat and crop fields, leading to conflict over high-quality resources. To mitigate this conflict, a better understanding of the elephants' sensory world and its impact on their decision-making process should be considered seriously in the development of long-term strategies for promoting coexistence between humans and elephants. In this review, we explore the elephants' sensory systems for audition and olfaction, their multi-modal capacities for communication, and the anthropogenic changes that are affecting their behavior, as well as the need for greater consideration of elephant behavior in elephant conservation efforts.

Self-recognition in the Asian elephant and future directions for cognitive research with elephants in zoological settings.

The field of animal cognition has grown steadily for nearly four decades, but the primary focus has centered on easily kept lab animals of varying cognitive capacity, including rodents, birds and primates. Elephants (animals not easily kept in a laboratory) are generally thought of as highly social, cooperative, intelligent animals, yet few studies-with the exception of long-term behavioral field studies-have been conducted to directly support this assumption. In fact, there has been remarkably little cognitive research conducted on Asian (Elephas maximus) or African (Loxodonta africana or L. cyclotis) elephants. Here, we discuss the opportunity and rationale for conducting such research on elephants in zoological facilities, and review some of the recent developments in the field of elephant cognition, including our recent study on mirror self-recognition in E. maximus.

Investigating the use of sensory information to detect and track prey by the Sunda pangolin (Manis javanica) with conservation in mind.

Pangolins are of conservation concern as one of the most heavily poached, yet least understood mammals. The Sunda pangolin (Manis javanica) in particular is a critically endangered species. Here, we investigate the behaviour of these pangolins, for the first time, using a battery of cognitive tasks based on a manipulation of available sensory information. In an object-choice task in which only one of two containers was baited with food, the pangolins were able to find the food with olfactory information alone (N = 2), but not with visual or acoustic information alone (N = 1). The single subject tested on all three domains was further tested on how he used smell to find food by providing him with an opportunity to find it from a controlled distance or by using scent trails as a guide. The results suggest that our subject may have the capacity to exploit scent trails left by prey which can be tracked to a final source, though we found no evidence to suggest that he had the ability to initiate hunts based on distant prey odors. Despite the small sample size, this is the first controlled experiment to investigate pangolin foraging behaviour and cognition, which may have implications for the future protection of pangolin habitat based on the location of prey species.

Investigating Indirect and Direct Reputation Formation in Asian Elephants (Elephas maximus).

Reputation is a key component in social interactions of group-living animals and appears to play a role in the establishment of cooperation. Animals can form a reputation of an individual by directly interacting with them or by observing them interact with a third party, i.e., eavesdropping. Elephants are an interesting taxon in which to investigate eavesdropping as they are highly cooperative, large-brained, long-lived terrestrial mammals with a complex social organisation. The aim of this study was to investigate whether captive Asian elephants (Elephas maximus) could form reputations of humans through indirect and/or direct experience in two different paradigms: (1) a cooperative string-pulling task and (2) a scenario requiring begging. Fourteen captive Asian elephants in Thailand participated in an experimental procedure that consisted of three parts: baseline, observation, and testing. In the observation phase, the subject saw a conspecific interact with two people-one cooperative/generous and one non-cooperative/selfish. The observer could then choose which person to approach in the test phase. The elephants were tested in a second session 2-5 days later. We found no support for the hypothesis that elephants can form reputations of humans through indirect or direct experience, but these results may be due to challenges with experimental design rather than a lack of capacity. We discuss how the results may be due to a potential lack of ecological validity in this study and the difficulty of assessing motivation and attentiveness in elephants. Furthermore, we highlight the importance of designing future experiments that account for the elephants' use of multimodal sensory information in their decision-making.

Elephants know when their bodies are obstacles to success in a novel transfer task.

The capacity to recognise oneself as separate from other individuals and objects is difficult to investigate in non-human animals. The hallmark empirical assessment, the mirror self-recognition test, focuses on an animal's ability to recognise itself in a mirror and success has thus far been demonstrated in only a small number of species with a keen interest in their own visual reflection. Adapting a recent study done with children, we designed a new body-awareness paradigm for testing an animal's understanding of its place in its environment. In this task, Asian elephants (Elephas maximus) were required to step onto a mat and pick up a stick attached to it by rope, and then pass the stick forward to an experimenter. In order to do the latter, the elephants had to see their body as an obstacle to success and first remove their weight from the mat before attempting to transfer the stick. The elephants got off the mat in the test significantly more often than in controls, where getting off the mat was unnecessary. This task helps level the playing field for non-visual species tested on cognition tasks and may help better define the continuum on which body- and self-awareness lie.

Asian elephants (Elephas maximus) reassure others in distress.

Contact directed by uninvolved bystanders toward others in distress, often termed consolation, is uncommon in the animal kingdom, thus far only demonstrated in the great apes, canines, and corvids. Whereas the typical agonistic context of such contact is relatively rare within natural elephant families, other causes of distress may trigger similar, other-regarding responses. In a study carried out at an elephant camp in Thailand, we found that elephants affiliated significantly more with other individuals through directed, physical contact and vocal communication following a distress event than in control periods. In addition, bystanders affiliated with each other, and matched the behavior and emotional state of the first distressed individual, suggesting emotional contagion. The initial distress responses were overwhelmingly directed toward ambiguous stimuli, thus making it difficult to determine if bystanders reacted to the distressed individual or showed a delayed response to the same stimulus. Nonetheless, the directionality of the contacts and their nature strongly suggest attention toward the emotional states of conspecifics. The elephants' behavior is therefore best classified with similar consolation responses by apes, possibly based on convergent evolution of empathic capacities.

Exclusion in corvids: the performance of food-caching Eurasian jays (Garrulus glandarius).

Choice by exclusion involves selecting a rewarded stimulus by rejecting alternatives that are unlikely to be rewarded. It has been proposed that in corvids, exclusion is an adaptive specialization for caching that, together with object permanence and observational spatial memory, enhances a bird's ability to keep track of the contents of caches. Thus, caching species are predicted to perform well in tasks requiring exclusion. We tested this prediction by assessing the performance of Eurasian jays (Garrulus glandarius), a highly specialized cacher, in a two-way object choice task in which food was hidden in 1 of 2 cups. Consistent with the corvids' capacity for observational spatial memory, jays were highly accurate when shown the location of the food reward. However, the jays failed to exclude the empty cup when shown its contents. This failure to select the baited cup when shown the empty cup was possibly due to jays attending to the experimenter's movements and erroneously selecting the empty cup by responding to these local enhancement cues. To date, no corvids have been tested in an auditory two-way object choice task. Testing exclusion in the auditory domain requires that a bird use the noise produced when the baited cup is shaken to locate the reward. Although jays chose the baited cup more frequently than predicted by chance, their performance did not differ from trials controlling for the use of conflicting cues provided by the experimenter. Overall, our results provide little support for the hypothesis that caching has shaped exclusion abilities in corvids.

Visual cues given by humans are not sufficient for Asian elephants (Elephas maximus) to find hidden food.

Recent research suggests that domesticated species--due to artificial selection by humans for specific, preferred behavioral traits--are better than wild animals at responding to visual cues given by humans about the location of hidden food. \Although this seems to be supported by studies on a range of domesticated (including dogs, goats and horses) and wild (including wolves and chimpanzees) animals, there is also evidence that exposure to humans positively influences the ability of both wild and domesticated animals to follow these same cues. Here, we test the performance of Asian elephants (Elephas maximus) on an object choice task that provides them with visual-only cues given by humans about the location of hidden food. Captive elephants are interesting candidates for investigating how both domestication and human exposure may impact cue-following as they represent a non-domesticated species with almost constant human interaction. As a group, the elephants (n = 7) in our study were unable to follow pointing, body orientation or a combination of both as honest signals of food location. They were, however, able to follow vocal commands with which they were already familiar in a novel context, suggesting the elephants are able to follow cues if they are sufficiently salient. Although the elephants' inability to follow the visual cues provides partial support for the domestication hypothesis, an alternative explanation is that elephants may rely more heavily on other sensory modalities, specifically olfaction and audition. Further research will be needed to rule out this alternative explanation.

Self-recognition in an Asian elephant.

Considered an indicator of self-awareness, mirror self-recognition (MSR) has long seemed limited to humans and apes. In both phylogeny and human ontogeny, MSR is thought to correlate with higher forms of empathy and altruistic behavior. Apart from humans and apes, dolphins and elephants are also known for such capacities. After the recent discovery of MSR in dolphins (Tursiops truncatus), elephants thus were the next logical candidate species. We exposed three Asian elephants (Elephas maximus) to a large mirror to investigate their responses. Animals that possess MSR typically progress through four stages of behavior when facing a mirror: (i) social responses, (ii) physical inspection (e.g., looking behind the mirror), (iii) repetitive mirror-testing behavior, and (iv) realization of seeing themselves. Visible marks and invisible sham-marks were applied to the elephants' heads to test whether they would pass the litmus "mark test" for MSR in which an individual spontaneously uses a mirror to touch an otherwise imperceptible mark on its own body. Here, we report a successful MSR elephant study and report striking parallels in the progression of responses to mirrors among apes, dolphins, and elephants. These parallels suggest convergent cognitive evolution most likely related to complex sociality and cooperation.