Primates' behavioural responses to tourists: evidence for a tradeoff between potential risks and benefits

The presence of, and interactions with tourists can be both risky and beneficial for wild animals. In wildlife tourism settings, animals often experience elevated rates of aggression from conspecifics, and they may also be threatened or physically aggressed by the tourists themselves. However, tourist provisioning of wild animals provides them with highly desirable foods. In situations of conflicting motivations such as this, animals would be expected to respond using behavioural coping mechanisms. In the present study, we investigated how animals respond to tourist pressure, using wild adult Barbary macaques in the Middle Atlas Mountains, Morocco, as a case study. We found evidence that these animals use a range of different behavioural coping mechanisms–physical avoidance, social support, affiliative, aggressive and displacement behaviours–to cope with the stress associated with tourists. The pattern of use of such behaviours appears to depend on a trade-off between perceived risks and potential benefits. We propose a framework to describe how animals respond to conflicting motivational situations, such as the presence of tourists, that present simultaneously risks and benefits

Assessing the Effects of Tourist Provisioning on the Health of Wild Barbary Macaques in Morocco

Feeding wildlife is a very popular tourist activity, largely because it facilitates the close observation of animals in their natural habitat. Such provisioning may benefit animals by improving their survival and reproductive success, especially during periods of natural food shortage. However, provisioning by tourists may also have negative impacts on the health of the animals involved; to date such impacts are poorly understood. Here, we investigated the effects of tourist provisioning on the health of wild adult Barbary macaques, Macaca sylvanus, in Morocco. We compared health measures between a heavily provisioned group and a group that received negligible food from tourists and, in the former group, we also assessed health measures in relation to the intensity of provisioning. We used a broad range of non-invasive health measures relating to birth rate and survival, disease and injury risk, body size and condition, and physiological stress. Our findings indicate that feeding by tourists may overall have negative impacts on the health of Barbary macaques, being linked in particular to larger body size, elevated stress levels and more alopecia. Finally, we propose a framework to help consider the potential costs and benefits of provisioning, which may facilitate future research and management decisions on whether—and how much—provisioning is acceptable

Emotion Evaluation and Response Slowing in a Non-Human Primate: New Directions for Cognitive Bias Measures of Animal Emotion?

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 bias in a non-human primate: husbandry procedures influence cognitive indicators of psychological well-being in captive rhesus macaques

The measurement of 'cognitive bias' has recently emerged as a powerful tool for assessing animal welfare. Cognitive bias was initially, and widely, studied in humans, and describes the way in which particular emotions are associated with biases in information processing. People suffering from clinical levels of anxiety or depression, for example, interpret ambiguous events more negatively than do non-anxious or non-depressed people. Development of methods for use with non-human animals has revealed similar biases in several species of mammals and birds, and one invertebrate. However, cognitive bias has not been previously explored in any species of non-human primate, despite specific concerns raised about the welfare of these animals in captivity. Here, we describe a touchscreen-based cognitive-bias task developed for use with captive rhesus macaques (Macaca mulatta). Monkeys were initially trained on a 'Go/No-Go' operant task, in which they learned to touch one of two lines that differed in size in order to receive a reward (food), and to desist from touching the other line to avoid a mildly aversive stimulus (delay to the next trial and white noise). In testing sessions, the monkeys were presented with lines of intermediate size. We measured whether touchscreen responses to these ambiguous stimuli were affected by husbandry procedures (environmental enrichment, and a statutory health check involving restraint and ketamine hydrochloride injection) presumed to induce positive and negative shifts in affective state, respectively. Monkeys made fewer responses to ambiguous stimuli post health check compared to during the phase of enrichment suggesting greater expectation of negative outcomes following the health check compared to during enrichment. Shifts in affective state following standard husbandry procedures may therefore be associated with changes in information processing similar to those demonstrated in anxious and depressed humans, and in a number of other taxa

Emotion evaluation and response slowing in a non-human primate: New directions for cognitive bias measures of animal welfare

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 byparadigms 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

Implications of Tourist-Macaque Interactions for Disease Transmission

During wildlife tourism, proximity or actual contact between people and animals may lead to a significant risk of anthropozoonotic disease transmission. In this paper, we use social network analysis, disease simulation modelling and data on animal health and behaviour to investigate such risks at a site in Morocco, where tourists come to see wild Barbary macaques (Macaca sylvanus). Measures of individual macaques’ network centrality—an index of the strength and distribution of their social relationships and thus potentially their ability to spread disease—did not show clear and consistent relationships with their time spent in close proximity to, or rate of interacting with, tourists. Disease simulation modelling indicated that while higher-ranked animals had a significantly greater ability to spread disease within the group, in absolute terms there was little difference in the size of outbreaks that different individuals were predicted to cause. We observed a high rate of physical contact and close proximity between humans and macaques, including during three periods when the macaques were coughing and sneezing heavily, highlighting the potential risk of disease transmission. We recommend that general disease prevention strategies, such as those aimed at reducing opportunities for contact between tourists and macaques, should be adopted

Repeatable glucocorticoid expression is associated with behavioural syndromes in males but not females in a wild primate

Behavioural syndromes are a well-established phenomenon in human and non-human animal behavioural ecology. However, the mechanisms that lead to correlations among behaviours and individual consistency in their expression at the apparent expense of behavioural plasticity remain unclear. The ‘state-dependent’ hypothesis posits that inter-individual variation in behaviour arises from inter-individual variation in state and that the relative stability of these states within an individual leads to consistency of behaviour. The endocrine stress response, in part mediated by glucocorticoids (GCs), is a proposed behavioural syndrome-associated state as GC levels are linked to an individual’s behavioural responses to stressors. In this study, in wild Barbary macaques (Macaca sylvanus), consistent inter-individual differences were observed in both sexes for GC activity (faecal glucocorticoid, fGC concentrations), but not GC variation (coefficient of variation in fGC concentrations). The expression of the behavioural syndrome ‘Excitability’ (characterized by the frequencies of brief affiliation or aggressive interactions) was related to GC activity in males but not in females; more ‘excitable’ males had lower GC activity. There was no relationship in females between any of the behavioural syndromes and GC activity, nor in either sex with GC variation. The negative relationship between GC activity and Excitability in males provides some support for GC expression as a behavioural syndrome-generating state under the state-dependent framework. The absence of this relationship in females highlights that state-behavioural syndrome associations may not be generalizable within a species and that broader sex differences in state need to be considered for understanding the emergence and maintenance of behavioural syndromes

Variation in paranasal pneumatisation between Mid-Late Pleistocene hominins

There is considerable variation in mid-late Pleistocene hominin paranasal sinuses, and in some taxa distinctive craniofacial shape has been linked to sinus size. Extreme frontal sinus size has been reported in mid-Pleistocene specimens often classified as Homo heidelbergensis, and Neanderthal sinuses are said to be distinctively large, explaining diagnostic Neanderthal facial shape. Here, the sinuses of fossil hominins attributed to several mid-late Pleistocene taxa were compared to those of recent H. sapiens. The sinuses were investigated to clarify differences in the extent of pneumatisation within this group and the relationship between sinus size and craniofacial variation in hominins from this time period. Frontal and maxillary sinus volumes were measured from CT data, and geometric morphometric methods were used to identify and analyse shape variables associated with sinus volume. Some mid

Does dysfunction of the mirror neuron system contribute to symptoms in amyotrophic lateral sclerosis?

There is growing evidence that mirror neurons, initially discovered over two decades ago in the monkey, are present in the human brain. In the monkey, mirror neurons characteristically fire not only when it is performing an action, such as grasping an object, but also when observing a similar action performed by another agent (human or monkey). In this review we discuss the origin, cortical distribution and possible functions of mirror neurons as a background to exploring their potential relevance in amyotrophic lateral sclerosis (ALS). We have recently proposed that ALS (and the related condition of frontotemporal dementia) may be viewed as a failure of interlinked functional complexes having their origins in key evolutionary adaptations. This can include loss of the direct projections from the corticospinal tract, and this is at least part of the explanation for impaired motor control in ALS. Since, in the monkey, corticospinal neurons also show mirror properties, ALS in humans might also affect the mirror neuron system. We speculate that a defective mirror neuron system might contribute to other ALS deficits affecting motor imagery, gesture, language and empathy