Spot the odd one out: do snake pictures capture macaques' attention more than other predators?

Detecting and identifying predators quickly is key to survival. According to the Snake Detection Theory (SDT), snakes have been a substantive threat to primates for millions of years, so that dedicated visual skills were tuned to detect snakes in early primates. Past experiments confronted the SDT by measuring how fast primate subjects detected snake pictures among non-dangerous distractors (e.g., flowers), but did not include pictures of primates' other predators, such as carnivorans, raptors, and crocodilians. Here, we examined the detection abilities of N = 19 Tonkean macaques (Macaca tonkeana) and N = 6 rhesus macaques (Macaca mulatta) to spot different predators. By implementing an oddity task protocol, we recorded success rates and reaction times to locate a deviant picture among four pictures over more than 400,000 test trials. Pictures depicted a predator, a non-predator animal, or a simple geometric shape. The first task consisted of detecting a deviant picture among identical distractor pictures (discrimination) and the second task was designed to evaluate detection abilities of a deviant picture among different distractor pictures (categorization). The macaques detected pictures of geometric shapes better and faster than pictures of animals, and were better and faster at discriminating than categorizing. The macaques did not detect snakes better or faster than other animal categories. Overall, these results suggest that pictures of snakes do not capture visual attention more than other predators, questioning previous findings in favor of the SDT.

New mitogenomic lineages in Papio baboons and their phylogeographic implications.

OBJECTIVES: Incomplete and/or biased sampling either on a taxonomic or geographic level can lead to delusive phylogenetic and phylogeographic inferences. However, a complete taxonomic and geographical sampling is often and for various reasons impossible, particularly for widespread taxa such as baboons (Papio spp.). Previous studies on baboon phylogeography identified several sampling gaps, some of which we fill by investigating additional material including samples from museum specimens. MATERIALS AND METHODS: We generated 10 new mitochondrial genomes either via conventional PCR and subsequent Sanger sequencing from two blood samples or via high-throughput shotgun sequencing from degraded DNA extracted from eight museum specimens. Phylogenetic relationships and divergence times among baboon lineages were determined using maximum-likelihood and Bayesian inferences. RESULTS: We identified new mitochondrial lineages in baboons from Central Africa (Chad, the Central African Republic), from the Mahale, and the Udzungwa Mountains (Tanzania), with the latter likely representing a case of mitochondrial capture from sympatric kipunjis (Rungwecebus kipunji). We also found that the mitochondrial clades of olive baboons found in Ivory Coast and Tanzania extend into Niger and the Democratic Republic of Congo, respectively. Moreover, an olive baboon from Sierra Leone carries a mitochondrial haplotype usually found in Guinea baboons, suggesting gene flow between these two species. DISCUSSION: The extension of the geographic sampling by including samples from areas difficult to visit or from populations that are most likely extirpated has improved the geographic and temporal resolution of the mitochondrial phylogeny of baboons considerably. Our study also shows the great value of museum material for genetic analyses even when DNA is highly degraded.

Survival is linked with reaction time and spatial memory in African striped mice.

Studying the association between fitness and cognition in free-living animals is a fundamental step in the elucidation of the evolution of cognition. We assessed whether survival until the onset of the breeding season was related to reaction time or spatial memory in the African striped mouse Rhabdomys pumilio, a rodent that has to survive summer drought before breeding. We tested a total of 90 individuals at the beginning of summer. Female survival was related to a faster response to predation stimuli. Male survival increased with greater spatial memory, possibly because it is important for males to remember the configuration of the environment during dispersal. This study revealed that individual variation in reaction time and spatial memory can be related to survival probability, which is important for understanding the selection pressures acting on basic cognitive traits.

Seasonal variation in attention and spatial performance in a wild population of the African striped mouse (Rhabdomys pumilio).

Cognitive flexibility describes the reversible changes of cognition in response to environmental changes. Although various environmental factors such as temperature, photoperiod and rainfall change seasonally, seasonal variation in cognitive performance has been reported in merely a few birds and mammals. We assessed whether cognitive performance in a wild population of African striped mice Rhabdomys pumilio, from the Succulent Karoo semidesert of South Africa, differed between summer and winter. In order to measure cognitive performance, striped mice were trapped in the field, tested under laboratory conditions at our research station and returned to the field within 5 h. We measured attention and spatial memory using the standardized orientation response test and the Barnes maze test. Males tested during summer oriented faster toward a predator-stimulus but made more errors and took longer to locate a shelter than males tested during winter. In contrast, females' performance did not differ between the two seasons. We discuss how the faster orientation in males during winter might be the consequence of lower temperatures and/or prolonged food restriction. We suggest that the enhancement of spatial performance during winter might be due to a greater motivation for future dispersal in male striped mice, as spring represents the breeding season.

Manual laterality and strategy use for a coordinated bimanual task requiring precise and power grip in guenons and mangabeys.

Bimanual tasks have been repeatedly shown to elicit manual asymmetries supposed to reflect hemispheric specialization. And yet, a coordinated bimanual task, the BOX task, appears to be inefficient in detecting biases of hand preferences. The BOX task involves two sequential actions requiring a precise grip, lift the lid of a box and grasp a small item inside the box (while holding the lid). In the present study, we compared manual laterality exhibited for the classic bimanual BOX task and for a unimanual BOX task in 11 De Brazza's monkeys (Cercopithecus neglectus) and 19 red-capped mangabeys (Cercocebus torquatus). In addition, we assessed strategy use for solving the bimanual BOX task. We found that left-hand use for grasping the item was higher in the BOX-bimanual task than in the BOX-unimanual task. We propose that this increase in left-hand use for grasping the item results from both a hemispheric specialization for lifting the lid and an advantage in using a skillful strategy. Indeed, we revealed (1) group-level right biases for lifting the lid and (2) a complete differentiation between the roles of the two hands in subjects showing a left-hand preference for grasping the item. Finally, the bimanual BOX task showed age differences in the two species, either in manual laterality for grasping the item or in strategy use. This study provides additional evidence that manual laterality might be sensitive to maturational factors and characteristics of the bimanual tasks such as the order and the features of sequential actions.

Hand preference and its flexibility according to the position of the object: a study in cercopithecines examining spontaneous behaviour and an experimental task (the Bishop QHP task).

The extant literature on manual laterality in non-human primates is inconclusive, plagued by inconsistent or contradictory findings and by disturbing methodological issues (e.g. uncontrolled influential factors, comparability issues). The present study examined hand preference and its flexibility in 15 red-capped mangabeys (C. t. torquatus) and 13 Campbell's monkeys (C. c. campbelli), two species that differ in their degree of arboreality. We investigated the influence of the spatial position of the object on hand preference for reaching. We considered spontaneous behaviour (reaching for food during daily feeding) and an experimental task: the QHP task. The QHP is a task that is used in humans. This is a simple reaching task that involves high spatial constraints on hand use. In our study, the subject had to reach for items that were placed on a semi-circle in front of it on five positions, including in the centre position, in the ipsilateral space and in the contralateral space. We assessed hand preference for reaching in front (baseline condition), and we examined how this preference changed when reaching in lateral positions. For reaching in front, about half of the subjects were lateralized and no group-level bias occurred, for both spontaneous and experimental conditions. When considering reaching in the lateral positions, we observed that the position of the object influenced hand use: individuals used the hand that was closest to the object. The results are discussed in relation to previous findings in humans and in non-human primates and regarding theories on handedness and flexibility of hand preference.

Response of Bolivian gray titi monkeys (Plecturocebus donacophilus) to an anthropogenic noise gradient: behavioral and hormonal correlates.

Worldwide urban expansion and deforestation have caused a rapid decline of non-human primates in recent decades. Yet, little is known to what extent these animals can tolerate anthropogenic noise arising from roadway traffic and human presence in their habitat. We studied six family groups of titis residing at increasing distances from a busy highway, in a park promoting ecotourism near Santa Cruz de la Sierra, Bolivia. We mapped group movements, sampled the titis' behavior, collected fecal samples from each study group and conducted experiments in which we used a mannequin simulating a human intrusion in their home range. We hypothesized that groups of titi monkeys exposed to higher levels of anthropogenic noise and human presence would react weakly to the mannequin and show higher concentrations of fecal cortisol compared with groups in least perturbed areas. Sound pressure measurements and systematic monitoring of soundscape inside the titis' home ranges confirmed the presence of a noise gradient, best characterized by the root-mean-square (RMS) and median amplitude (M) acoustic indices; importantly, both anthropogenic noise and human presence co-varied. Study groups resided in small, overlapping home ranges and they spent most of their time resting and preferentially used the lower forest stratum for traveling and the higher levels for foraging. Focal sampling analysis revealed that the time spent moving by adult pairs was inversely correlated with noise, the behavioral change occurring within a gradient of minimum sound pressures ranging from 44 dB(A) to 52 dB(A). Validated enzyme-immunoassays of fecal samples however detected surprisingly low cortisol concentrations, unrelated to the changes observed in the RMS and M indices. Finally, titis' response to the mannequin varied according to our expectation, with alarm calling being greater in distant groups relative to highway. Our study thus indicates reduced alarm calling through habituation to human presence and suggests a titis' resilience to anthropogenic noise with little evidence of physiological stress.

Orangutans' Comprehension of Zoo Keepers' Communicative Signals.

Zoological institutions often encourage cooperative interactions between keepers and animals so as to promote animals' welfare. One useful technique has been conditioning training, whereby animals learn to respond to keepers' requests, which facilitates a number of, otherwise sensitive, daily routines. As various media have been used to convey keepers' instructions, the question remains of which modality is best to promote mutual understanding. Here, we explored this question with two captive female orangutans. In the first experiment, we compared orangutans' understanding of previously acquired instructions when those were performed with verbal signals only, gazes only, gestures only, and when all those modalities were combined. Our results showed that gestures were sufficient for successful comprehension by these two apes. In the second experiment, we asked whether this preference could be driven by the non-arbitrary relationship that gestures bear to what they refer to, through iconicity or pointing. Our results revealed that neither iconicity nor pointing helped the subjects comprehend the keepers' instructions. Our results indicate a preference for instructions given through gestural signals in two captive female orangutans, although its cause remains elusive. Future practice may encourage the use of gestures in communication between keepers and orangutans in general or potentially other animals.

Ecophysiology of cognition: How do environmentally induced changes in physiology affect cognitive performance?

Cognitive performance is based on brain functions, which have energetic demands and are modulated by physiological parameters such as metabolic hormones. As both environmental demands and environmental energy availability change seasonally, we propose that cognitive performance in free-living animals might also change seasonally due to phenotypic plasticity. This is part of an emerging research field, the 'ecophysiology of cognition': environmentally induced changes in physiological traits, such as blood glucose and hormone levels, are predicted to influence cognitive performance in free-living animals. Energy availability for the brain might change, and as such cognition, with changing energetic demands (e.g. reproduction) and changes of energy availability in the environment (e.g. winter, drought). Individuals spending more energy than they can currently obtain from their environment (allostatic overload type I) are expected to trade off energy investment between cognition and other life-sustaining processes or even reproduction. Environmental changes reducing energy availability might thus impair cognition. However, selection pressures such as predation risk, mate choice or social demands may act on the trade-off between energy saving and cognition. We assume that different environmental conditions can lead to three different trade-off outcomes: cognitive impairment, resilience or enhancement. Currently we cannot understand these trade-offs, because we lack information about changes in cognitive performance due to seasonal changes in energy availability and both the resulting changes in homeostasis (for example, blood glucose levels) and the associated changes in the mechanisms of allostasis (for example, hormone levels). Additionally, so far we know little about the fitness consequences of individual variation in cognitive performance. General cognitive abilities, such as attention and associative learning, might be more important in determining fitness than complex and specialized cognitive abilities, and easier to use for comparative study in a large number of species. We propose to study seasonal changes in cognitive performance depending on energy availability in populations facing different predation risks, and the resulting fitness consequences.

Does a nonprimate mammal, the northern tree shrew (Tupaia belangeri), exhibit paw preference in two forms of a grasping task?

Tree shrews represent a relevant model to study the evolution of primate manual laterality as they are phylogenetically close to primates, they are able to grasp despite having a nonopposable thumb, and they possess a well-developed visual system. In this study, we examined the paw laterality and grasping success rate of 30 Tupaia belangeri (15 males, 15 females) in 2 forced-food grasping tasks (i.e., in a forced-food grasping experiment, the animal has to use paws instead of mouth for food retrieval). We also attempted to determine whether paw usage would be affected by the availability of visual cues using both a visual task (transparent tube) and a nonvisual task (identical but opaque tube). In both tasks, tree shrews showed paw preferences at an individual but not at a population level. Paw laterality (direction and strength) did not differ between tasks. Moreover, in the specific task that we used, grasping success rate was not affected by an absence of visual cues, indicating that tree shrews did not rely on visual guidance to direct their grasps in this forced-food grasping experiment. Our findings suggest that, in contrast to primates, paw usage in tree shrews may result from a modification of a fixed motor pattern in which the preferred direction may be learned. This basic motor organization might be a first step in the evolution of manual laterality, which eventually became controlled by vision in the primate lineage.

Which are the features of the TUBE task that make it so efficient in detecting manual asymmetries? An investigation in two Cercopithecine species (Cercopithecus neglectus and Cercocebus torquatus).

In the last decade, the TUBE task has been repeatedly shown to be highly efficient in detecting manual asymmetries that are strong hand preferences reflecting hemispheric specialization, in non human primates. The TUBE task was thus classified as a high-level task, presumably because it involves bimanual coordination. However, this task also requires a precise action made by digit(s), which may also be a crucial feature in eliciting manual asymmetries. In the present study, we compared hand preferences for a new TUBE-unimanual task and the classic TUBE-bimanual task, both performed mostly by using the forefinger, in 12 guenons (De Brazza's monkey: Cercopithecus neglectus) and 18 mangabeys (red-capped mangabey: Cercocebus torquatus). We found a relationship between hand preferences exhibited for the two tasks, suggesting that precise use of the forefinger may induce the activation of a specialized hemisphere in both the TUBE-unimanual and the TUBE-bimanual task. However, we showed that the strength of manual laterality was higher in the TUBE-bimanual task than in the TUBE-unimanual task, indicating that bimanual coordination may enhance the expression of hand preferences. We propose that the TUBE-bimanual task is highly efficient in detecting hemispheric specialization because bimanual role differentiation would make precise digit use highly skillful. Finally, we revealed species differences in hand use, especially in females: the most arboreal species, De Brazza's monkeys, increased left-hand use from the TUBE-unimanual to the TUBE-bimanual task whereas the most terrestrial species, red-capped mangabeys, increased right-hand use.

To beg, or not to beg? That is the question: mangabeys modify their production of requesting gestures in response to human's attentional states.

BACKGROUND: Although gestural communication is widespread in primates, few studies focused on the cognitive processes underlying gestures produced by monkeys. METHODOLOGY/PRINCIPAL FINDINGS: The present study asked whether red-capped mangabeys (Cercocebus torquatus) trained to produce visually based requesting gestures modify their gestural behavior in response to human's attentional states. The experimenter held a food item and displayed five different attentional states that differed on the basis of body, head and gaze orientation; mangabeys had to request food by extending an arm toward the food item (begging gesture). Mangabeys were sensitive, at least to some extent, to the human's attentional state. They reacted to some postural cues of a human recipient: they gestured more and faster when both the body and the head of the experimenter were oriented toward them than when they were oriented away. However, they did not seem to use gaze cues to recognize an attentive human: monkeys begged at similar levels regardless of the experimenter's eyes state. CONCLUSIONS/SIGNIFICANCE: These results indicate that mangabeys lowered their production of begging gestures when these could not be perceived by the human who had to respond to it. This finding provides important evidence that acquired begging gestures of monkeys might be used intentionally.