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.

The energy allocation trade-offs underlying life history traits in hypometabolic strepsirhines and other primates.

Life history, brain size and energy expenditure scale with body mass in mammals but there is little conclusive evidence for a correlated evolution between life history and energy expenditure (either basal/resting or daily) independent of body mass. We addressed this question by examining the relationship between primate free-living daily energy expenditure (DEE) measured by doubly labeled water method (n = 18 species), life history variables (maximum lifespan, gestation and lactation duration, interbirth interval, litter mass, age at first reproduction), resting metabolic rate (RMR) and brain size. We also analyzed whether the hypometabolic primates of Madagascar (lemurs) make distinct energy allocation tradeoffs compared to other primates (monkeys and apes) with different life history traits and ecological constraints. None of the life-history traits correlated with DEE after controlling for body mass and phylogeny. In contrast, a regression model showed that DEE increased with increasing RMR and decreasing reproductive output (i.e., litter mass/interbirth interval) independent of body mass. Despite their low RMR and smaller brains, lemurs had an average DEE remarkably similar to that of haplorhines. The data suggest that lemurs have evolved energy strategies that maximize energy investment to survive in the unusually harsh and unpredictable environments of Madagascar at the expense of reproduction.

The Central Role of Small Vertical Substrates for the Origin of Grasping in Early Primates.

The manual and pedal grasping abilities of primates, characterized by an opposable hallux, flat nails, and elongated digits, constitute a unique combination of features that likely promoted their characteristic use of arboreal habitats. These hand and foot specificities are central for understanding the origins and early evolution of primates and have long been associated with foraging in a fine-branch milieu. However, other arboreal mammals occupy similar niches, and it remains unclear how substrate type may have exerted a selective pressure on the acquisition of nails and a divergent pollex/hallux in primates or in what sequential order these traits evolved. Here, we video-recorded 14,564 grasps during arboreal locomotion in 11 primate species (6 strepsirrhines and 5 platyrrhines) and 11 non-primate arboreal species (1 scandentian, 3 rodents, 3 carnivorans, and 4 marsupials). We quantified our observations with 19 variables to analyze the effect of substrate orientation and diameter on hand and foot postural repertoire. We found that hand and foot postures correlate with phylogeny. Also, primates exhibited high repertoire diversity, with a strong capability for postural adjustment compared to the other studied groups. Surprisingly, nails do not confer an advantage in negotiating small substrates unless the animal is large, but the possession of a grasping pollex and hallux is crucial for climbing small vertical substrates. We propose that the divergent hallux and pollex may have resulted from a frequent use of vertical plants in early primate ecological scenarios, although nails may not have resulted from a fundamental adaptation to arboreal locomotion.

Tube task hand preference in captive hylobatids.

The link between laterality in humans and other primates is still hotly debated. Hylobatids have been rather neglected in this research area, yet they can provide important insights because: (1) they share with humans a complex vocal repertoire, which in humans is thought to be associated with brain hemispheric specialization and lateralized behaviors; (2) their adaptation to arboreality has produced unique postural constraints; (3) the little that is known about laterality in gibbons is contradictory (captive studies have provided conflicting results, while a field study on siamangs reported a population-level left-hand preference). To clarify this, we investigated hand preference in captive hylobatids [n = 42; 22 siamangs (Symphalangus syndactylus) and 20 gibbons (Hylobates sp., Nomascus leucogenys)] in nine Japanese facilities. We had a large sample size, controlled for possible confounds (posture, enclosure limitations) and used a well-established testing protocol (tube task). Handedness indices calculated from raw frequencies and bouts were highly correlated and showed a significant left-hand skew, which is consistent with data from wild siamangs. Major differences between captive and wild siamangs were a larger number of ambiguously handed individuals, and no significant age-related variation in captivity. The use of the index finger elicited a much more strongly lateralized response than the thumb. These results confirmed a left-hand preference in siamangs, but were equivocal in other hylobatids, and suggest selective pressures that may have acted on the highly arboreal hylobatids to favor handedness. Our study also indicates factors that might explain the discrepancy in the literature between handedness studies on captive and wild primate populations.

Offspring loss after male change in wild siamangs: the importance of abrupt weaning and male care.

OBJECTIVES: Infanticide by males is assumed to promote permanent male-female associations, although its importance for social monogamy is still debated. We examined the consequences of male membership change in the largest socially monogamous primate, the siamang (Symphalangus syndactylus), a species that also forms polyandrous groups and where males may provide offspring care. We examine (a) the potential risk of infanticide by documenting changes in female-offspring relationships following male change, expecting abrupt weaning; and (b) the potential importance of male care and polyandry for offspring survival. METHODS: We witnessed four male changes at Way Canguk Field Station (Indonesia) in groups where the youngest offspring was estimated to be about 2 years of age. We quantified aspects of mother-offspring relationships (interindividual distance, body contact, and nipple contact) and estimated the proportion of time being carried during travel (August 2007-April 2009). RESULTS: In the two groups into which new males immigrated, offspring were weaned abruptly, suggesting infanticide by males as a potential risk. Even though no attacks on infants by males were witnessed, both infants disappeared shortly after the male change. Another infant disappeared after its main carrier (a male) emigrated. Conversely, in a group where the resident subordinate male replaced the dominant male, the offspring experienced no change in care and survived the transition. CONCLUSIONS: These findings suggest that male immigration in hylobatids increases mortality risk for infants, emphasize the importance of offspring care, and cast doubts on prior classifications of 2-year-old siamangs as independently traveling individuals.

Watering holes: The use of arboreal sources of drinking water by Old World monkeys and apes.

Water is one of the most important components of an animal's diet, as it is essential for life. Primates, as do most animals, procure water directly from standing or free-flowing sources such as pools, ponds and rivers, or indirectly by the ingestion of certain plant parts. The latter is frequently described as the main source of water for predominantly arboreal species. However, in addition to these, many species are known to drink water accumulated in tree-holes. This has been commonly observed in several arboreal New World primate species, but rarely reported systematically from Old World primates. Here, we report observations of this behaviour from eight great ape and Old World monkey species, namely chimpanzee, orangutan, siamang, western hoolock gibbon, northern pig-tailed macaque, bonnet macaque, rhesus macaque and the central Himalayan langur. We hypothesise three possible reasons why these primates drink water from tree-holes: (1) coping with seasonal or habitat-specific water shortages, (2) predator/human conflict avoidance, and (3) potential medicinal benefits. We also suggest some alternative hypotheses that should be tested in future studies. This behaviour is likely to be more prevalent than currently thought, and may have significant, previously unknown, influences on primate survival and health, warranting further detailed studies.

Dominance relationships among siamang males living in multimale groups.

Intense intolerance among males is considered to be an important mechanism maintaining the uni-male organization traditionally attributed to socially monogamous gibbons. Long-term field work, however, has revealed the existence of stable, socially polyandrous groups in at least two populations, raising questions about the mechanism that allows two adult males to co-reside in the same group. I collected 21 months of behavioral data on 7 two-male groups of wild siamangs (Symphalangus syndactylus) in southern Sumatra (Indonesia) to test the hypothesis that dominance relationships regulate the interactions of adult male siamangs and ultimately facilitate multi-male social groups. A dominant male could clearly be identified in each dyad, based on a consistent direction of agonistic interactions, displacements and the maintenance of an advantageous position in the canopy. Males identified as dominant enjoyed greater social access to the resident female and monopolized copulations. These results suggest that gibbons possess the psycho-social flexibility to regulate intra-sexual aggression and live in multi-male social units under certain social conditions. I discuss the effects that relatedness between males and female choice have in determining this grouping pattern, and the role of male intolerance in the maintenance of primate mating systems.

Clouded leopard predation on a wild juvenile siamang.

I report the first documented case of a wild siamang killed by a clouded leopard. The event, involving a juvenile male (weighing 3.7 kg), occurred at dawn, near a known sleeping tree in a lowland tropical forest in southern Sumatra (Indonesia). Examination of the siamang's body revealed that the first 2 cervical vertebrae were crushed and the face was partially eaten. This attack highlights the potential importance of predation as an evolutionary pressure for hylobatids, and poses some questions about the antipredator adaptations of this population of siamang.