A tough nut to crack? Proficiency in coconut processing of the Nicobar long-tailed macaque Macaca fascicularis umbrosus.

The ability to manipulate objects enables macaques to utilize resources well. Coconut (Cocos nucifera) is one such food that has high energy and nutrient value but requires complex motor skills for extraction. In this study, we examined the proficiency of a single group of Macaca fascicularis umbrosus from Campbell Bay, India, in feeding on different types of coconuts. The group comprised 16 individuals with 3 adult males, 6 adult females, 3 sub-adult males, and 4 infants. We observed individuals feeding on tender, mature, dry, and dry-dehusked coconuts in 90 feeding bouts between August 2013 and December 2015. Their feeding behaviour was divided into four types of behavioural acts: pluck, process, drink, and feed. We prepared an ethogram consisting of 32 behavioural acts associated with feeding on coconuts, and recorded the occurrence of these acts during focal animal sampling. We used NMDS to examine differences among age/sex classes in the occurrence of behavioural acts associated with feeding on coconuts. Although females and males showed no significant separation in these behaviours, adults and young individuals formed distinct groups. However, only 3 out of 32 acts were exclusive to age classes. Using Discrete Time Markov Chain analysis, we found that adults tended to transition back to processing behaviours after drinking and feeding behaviours more often than young individuals. An almost similar repertoire of behaviours among age and sex classes indicates that there is no single model behaviour. Further, this study indicates that among different age/sex classes, adults tend to maximise the nutritional gains during single feeding bouts than younger individuals.

Infant adoptions in wild bonnet macaques (Macaca radiata).

Though uncommon, adoption of orphaned infants has been observed in both wild and captive non-human primates. In two groups of wild bonnet macaques (Macaca radiata), we observed five instances of infants being cared for after they lost their mothers at a pre-weaning age (< 6 months). Orphaned infants had one or more caregivers (juvenile, subadult, and adult female or male) involved in carrying, grooming, hugging, and protecting them. Adoption did not appear to be related to the age/sex class of the infant, or directly to the mother's rank. Although the dominance rank of the mother of an orphaned infant did not have a direct effect on orphan survivorship, it determined the number of caregivers available to the orphaned infant, and infant survivorship was positively related to the number of caregivers of the orphaned infant. Thus, survivorship was likely a function of the mother's sociality. Two other infants born to high-ranking mothers were also adopted by more individuals and survived longer than the infants of low-ranking mothers.

The rhesus macaque as a success story of the Anthropocene.

Of all the non-human primate species studied by researchers, the rhesus macaque (Macaca mulatta) is likely the most widely used across biological disciplines. Rhesus macaques have thrived during the Anthropocene and now have the largest natural range of any non-human primate. They are highly social, exhibit marked genetic diversity, and display remarkable niche flexibility (which allows them to live in a range of habitats and survive on a variety of diets). These characteristics mean that rhesus macaques are well-suited for understanding the links between sociality, health and fitness, and also for investigating intra-specific variation, adaptation and other topics in evolutionary ecology.

Can urbanization accentuate hand use in the foraging activities of primates?

OBJECTIVES: How a species uses its anatomical manipulators is determined by its anatomy, physiology, and ecology. While ecology explains interspecific variation in gripping, grasping, and manipulating objects, its role in intraspecific variation in mouth- and hand-use by animals is less explored. Primates are distinguished by their prehensile capabilities and manual dexterity. In context to the adaptive pressures of urbanization on primates, we examined if mouth and hand use differed across the forest-urban gradient in food retrieval and processing under experimental and naturalistic conditions in cercopithecids, a family comprising several urbanizing primates. MATERIALS AND METHODS: We recorded the acquisition and processing of peanuts under experimental conditions in three groups of bonnet macaques (BM, Macaca radiata) differing in their dietary dependence on packaged food items along a rural-urban gradient. To affirm the pattern obtained in the experiment, we coded food acquisition of three cercopithecid species in similar habitats from video sources. RESULTS: Urban macaques had a disproportionately higher hand use to acquire and process peanuts while rural macaques had higher mouth use. Based on analyses of videos, urban populations of BM, Japanese macaque (M. fuscata) and vervet monkey (Chlorocebus pygerythrus) showed a bias toward hand use during food acquisition. DISCUSSION: The adaptive pressures of urbanization, like the manual constraints of extracting packaged foods and perhaps, the need for visual-haptic exploration of novel objects seem to accentuate hand use in synanthropic groups of primates. Additional research should ascertain similar patterns in other primates and determine specific aspects of urbanization that modulate the observed trend.

Does rank rule? Rank-related grooming patterns in Nicobar long-tailed macaques Macaca fascicularis umbrosus.

Primates maintain social bonds with specific individuals in the group by directing grooming toward them. Social grooming is often targeted toward individuals with whom the most benefits can be exchanged, which are usually the high-ranking individuals. We used the Seyfarth model to investigate whether dominance rank alters the distribution of grooming in a group of Macaca fascicularis umbrosus at Great Nicobar Island. We investigated whether dominance rank predicted grooming rate in both males and females. We used social network analysis to examine whether high-ranking animals maintain a central position in the grooming network. We also investigated whether adult individuals exchange grooming for social tolerance, as indicated by physical proximity. We found that more social grooming was directed toward high-ranking females, but not high-ranking males. Social network analysis suggested that high-ranking animals are not central individuals in the distribution of grooming; rather, middle-ranking animals were major contributors to the distribution of grooming. There was no relation between the grooming rate and proximity in both males and females. Overall, our findings suggest that females prefer to direct grooming toward high-ranking partners, although the dominance hierarchy is less steep than expected for Macaca fascicularis. Thus rank-related grooming patterns may be a relatively conserved trait in this isolated island population.

Do males bond? A study of male-male relationships in Nicobar long-tailed macaques Macaca fascicularis umbrosus.

In primates, males compete for a mate, which is a non-sharable resource. This makes the conditions less conducive for males to have stable relationships. One such special kind of relationship is a bond where the interactions are reciprocated, equitable and differentiated. Bonds in macaque societies are based on the degree of within-group contest competition for mates which is dependent on the synchronization of female fertile phase and reliability of fertility signals. Species of the Fascicularis group, including Nicobar subspecies, show intermediate reliability in the signals with mild peaks, and studies have shown reciprocity but no differentiation. We conducted a study on a group of wild Nicobar long-tailed macaques Macaca fascicularis umbrosus to understand the existing patterns of male-male relationships. We examined whether there is reciprocity in affiliation among the individuals and whether the rate of affiliation is balanced. We also measured the dominance linearity and steepness in the group to understand the monopolizability of females. We used social network analysis to understand whether the relations are differentiated based on hierarchical position and whether the high-ranking individuals are the most central individuals in the distribution of grooming in the group. We found that there is reciprocity among the males although that is not equitable. There was no rankrelated differentiation of affiliation among the males of the group. Instead, the identities of individuals influenced affiliation patterns. Our results correspond to the existent strong relationships but lack of social bond otherwise found in the Fascicularis group of macaques.

Deceased-infant carrying in nonhuman anthropoids: Insights from systematic analysis and case studies of bonnet macaques (Macaca radiata) and lion-tailed macaques (Macaca silenus).

Existing models of attachment do not explain how death of offspring affects maternal behavior. Previous descriptions of maternal responsiveness to dead offspring in nonhuman anthropoids have not expounded the wide variation of deceased-infant carrying (DIC) behavior. Through the current study, we attempt to (a) identify determinants of DIC through a systematic survey across anthropoids, (b) quantitatively assess behavioral changes of mother during DIC, and (c) infer death perception of conspecifics. Firstly, we performed phylogenetic regression using duration of DIC as the dependent variable. Secondly, we undertook case studies of DIC in the bonnet monkey and the lion-tailed monkey through behavioral sampling. Results of phylogenetic Generalized Linear Mixed Model (Nspecies = 18; Ncases = 48) revealed a strong homology (H2 = 0.86). We also obtained a high intraspecific variation in DIC and found DIC to be affected by mother's age, context of death, habitat condition, and degree of arboreality. We found bonnet mothers to carry their deceased offspring for 3.56 ± 4.03 SD days (N = 7) with diminished feeding, enhanced passivity, and social isolation during DIC and progressive decline in protection/attentiveness of corpse and attachment. Following Anderson (2016)'s framework of death perception, we interpreted repeated sensory investigation of corpses by mothers as comprehending causality of death, inanimate handling of corpse and its defense as comprehension of non-functionality, and a progressive disinterest of mothers in them as perceiving irreversibility of death. Lastly, we integrated DIC with mother-infant attachment theories and proposed a conceptual model characterizing DIC with causal determinants. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Extractive foraging and tool-aided behaviors in the wild Nicobar long-tailed macaque (Macaca fascicularis umbrosus).

Macaques possess a repertoire of extractive foraging techniques that range from complex manipulation to tool-aided behaviors, to access food items that increase their foraging efficiency substantially. However, the complexity and composition of such techniques vary considerably between species and even between populations. In the present study, we report seven such complex manipulative behaviors that include six extractive foraging behaviors, and teeth flossing, in a population of Nicobar long-tailed macaques. The apparent purpose of these behaviors was an extraction of encased food, processing food, foraging hidden invertebrates, and dental flossing. Among these behaviors, three behaviors viz. wrapping, wiping, and teeth-flossing were tool-aided behaviors, where macaques used both natural and synthetic materials as tools. Occasionally macaques also modified those tools prior to their use. The substrate use patterns of leaf rubbing and teeth flossing were similar to that observed in other macaques. The spontaneous tool modification to perform wrapping was a first time observation. These observations suggest that Nicobar long-tailed macaques have a high level of sensorimotor intelligence which helps to evolve such innovative foraging solutions.

Behavioural Variability in Macaques and Langurs of the Western Ghats, India.

Studies that compare differences in the behavioural variability across species and genera are rare among south Asian primates. Such studies are important for understanding within-group feeding competition in primates as interindividual difference in frequency of behaviour is a good indicator of feeding competition. We compared the variability in individual activities of lion-tailed macaques, bonnet macaques, Nilgiri langurs, and black-footed grey langurs. Both macaque species showed variability in their activities, with bonnet macaques showing higher variability than lion-tailed macaques. This indicated higher within-group competition in bonnet macaques than in lion-tailed macaques. Folivorous Nilgiri langurs and black-footed grey langurs did not show variability in any behaviour, indicating weak or negligible within-group competition. Except in the bonnet macaque, the interindividual differences in activities in the other species were potentially due to the differences between lactating and non-lactating females. We observed that langurs were less variable than macaques, indicating higher within-group competition in macaques than in langurs. We also observed a higher frequency of aggressive interactions during feeding among macaques than langurs, substantiating higher within-group competition in macaques than in langurs. We further discuss the different possibilities of within-group contest and scramble competition in these species.

Losing its ground: A case study of fast declining populations of a 'least-concern' species, the bonnet macaque (Macaca radiata).

The populations of many species that are widespread and commensal with humans have been drastically declining during the past few decades, but little attention has been paid to their conservation. Here, we report the status of the bonnet macaque, a species that is considered 'least-concern' for conservation. We show that the widely ranging rhesus macaque is expanding its range into the distributional range of the bonnet macaque, a species endemic only to southern India. Bonnet macaques have very low abundance in forests of all types indicating that it is not a typically forest dwelling species. The traditionally preferred habitats of bonnet macaques have been Hindu temples/ tourist spots but our data reveal that nearly 50% population of bonnet macaques has disappeared from such previously occupied spots. Another preferred habitat of bonnet macaques has been roadsides with abundant Ficus trees adjoining croplands. We found that between 2003 and 2015, the roadsides have drastically changed where vegetation has been replaced with barren lands and urbanization. Consequently, the populations of bonnet macaques have declined by more than 65% over the past 25 years, and by more than 50% between 2003 and 2015 alone. We, therefore, conclude that this 'least-concern' species is actually facing serious conservation challenges. We also identify a few places such as small hillocks with natural vegetation and a few temples/tourist spots which are likely to remain stable and thus can serve as 'bonnet macaque conservation reserves'. Since the bonnet macaque shares many traits with several other commensal and 'low-risk' species, it can serve as a model for the development of long-term conservation strategies for most such species.

Demography and reproductive output in langurs of the Western Ghats, India.

Life history traits evolve such that the reproductive output of an organism is maximized. Demographic characteristics, a consequence of life history traits, indicate the reproductive output per individual in group-living species. Both phylogenetic and ecological factors influence demographic traits. In the forests of the Western Ghats, India, we studied the demography of three langur species: Semnopithecus johnii, a wet forest-dwelling species; Semnopithecus hypoleucos, largely a wet forest-dwelling species; and Semnopithecus priam, a primarily dry forest-dwelling species. S. hypoleucos and S. priam are genetically closer to each other than to S. johnii. We sampled a total of 193 groups of the three species of langurs. The group size was smaller in the two wet forest-dwelling species, S. johnii (median = 10) and S. hypoleucos (nine), than in the dry forest-dwelling species, S. priam (18). The number of adult females per group was higher in S. priam (seven) and S. johnii (six) than in S. hypoleucos (four). On the other hand, the adult female:immature ratio, indicating reproductive output and life history, was highest in S. johnii (1:0.33) followed by S. hypoleucos (1:1) and S. priam (1:1.09). Our results suggest that reproductive output is lowest in the arboreal wet forest species and increases as the species become somewhat dry deciduous forest dwellers, or almost facultative dry forest dwellers, and relatively more terrestrial. Some traits, such as group size, appear to be more sensitive to ecological factors, and some other traits such as age-sex ratios and reproductive output appear to be more conservative.

Population Recovery of Nicobar Long-Tailed Macaque Macaca fascicularis umbrosus following a Tsunami in the Nicobar Islands, India.

Natural disasters pose a threat to isolated populations of species with restricted distributions, especially those inhabiting islands. The Nicobar long tailed macaque.Macaca fascicularis umbrosus, is one such species found in the three southernmost islands (viz. Great Nicobar, Little Nicobar and Katchal) of the Andaman and Nicobar archipelago, India. These islands were hit by a massive tsunami (Indian Ocean tsunami, 26 December 2004) after a 9.2 magnitude earthquake. Earlier studies [Umapathy et al. 2003; Sivakumar, 2004] reported a sharp decline in the population of M. f. umbrosus after thetsunami. We studied the distribution and population status of M. f. umbrosus on thethree Nicobar Islands and compared our results with those of the previous studies. We carried out trail surveys on existing paths and trails on three islands to get encounter rate as measure of abundance. We also checked the degree of inundation due to tsunami by using Normalized Difference Water Index (NDWI) on landsat imageries of the study area before and after tsunami. Theencounter rate of groups per kilometre of M. f. umbrosus in Great Nicobar, Little Nicobar and Katchal was 0.30, 0.35 and 0.48 respectively with the mean group size of 39 in Great Nicobar and 43 in Katchal following the tsunami. This was higher than that reported in the two earlier studies conducted before and after the tsunami. Post tsunami, there was a significant change in the proportion of adult males, adult females and immatures, but mean group size did not differ as compared to pre tsunami. The results show that population has recovered from a drastic decline caused by tsunami, but it cannot be ascertained whether it has reached stability because of the altered group structure. This study demonstrates the effect of natural disasters on island occurring species.

Self-organization of laterally asymmetrical movements as a consequence of space-time optimization.

Laterally asymmetrical movements are ubiquitous among organisms. A bilaterally symmetrical organism cannot maneuver through a two- or three-dimensional space unless and until one side of its body leads, because the forces that cause the movements of the body are generated within the body. One question follows: are there any costs or benefits of laterally asymmetrical movements? We test whether directionally consistent laterally asymmetrical movements at different levels of organization of movements (at the individual, and not the population level) can work synergistically. We show-by means of a hypothetical system resembling a humanoid robot-that a laterally asymmetrical movement at a lower level of organization of movements can stimulate laterally asymmetrical movements that are directionally consistent at consecutive higher levels. We show-by comparing two hypothetical systems, incorporating laterally symmetrical and asymmetrical movements, respectively-that the asymmetrical system outperforms the symmetrical system by optimizing space and time and that this space-time advantage increases with the increasing complexity of the task. Together, these results suggest that laterally asymmetrical movements can self-organize as a consequence of space-time optimization.

Pre-Historic and Recent Vicariance Events Shape Genetic Structure and Diversity in Endangered Lion-Tailed Macaque in the Western Ghats: Implications for Conservation.

Genetic isolation of populations is a potent force that helps shape the course of evolution. However, small populations in isolation, especially in fragmented landscapes, are known to lose genetic variability, suffer from inbreeding depression and become genetically differentiated among themselves. In this study, we assessed the genetic diversity of lion-tailed macaques (Macaca silenus) inhabiting the fragmented landscape of Anamalai hills and examined the genetic structure of the species across its distributional range in the Western Ghats. We sequenced around 900 bases of DNA covering two mitochondrial regions-hypervariable region-I and partial mitochondrial cytochrome b-from individuals sampled both from wild and captivity, constructed and dated phylogenetic trees. We found that the lion-tailed macaque troops in the isolated forest patches in Anamalai hills have depleted mitochondrial DNA diversity compared to troops in larger and continuous forests. Our results also revealed an ancient divergence in the lion-tailed macaque into two distinct populations across the Palghat gap, dating to 2.11 million years ago. In light of our findings, we make a few suggestions on the management of wild and captive populations.

Folivory as a Constraint on Social Behaviour of Langurs in South India.

Folivory, being a dietary constraint, can affect the social time of colobines. In the present study, we compared food items and activity budgets of two closely related species of colobines inhabiting South India, i.e. the Hanuman langur (Semnopithecus hypoleucos) and Nilgiri langur (Semnopithecus johnii), to determine whether folivory had an impact on social time in these species. Our study established that Nilgiri langurs were more folivorous than Hanuman langurs. Nilgiri langurs spent much less time on social activities, but more time on resting, although the social organization of S. hypoleucos was similar to that of the Nilgiri langur. The enforced resting time for fermentation of leafy food items may have reduced the time available for social interactions, which in turn affected the social time in Nilgiri langurs. By comparing the data from previous studies on other Hanuman langur species, we found that S. hypoleucos spent a similar amount of time on social activities as Semnopithecus entellus. Hence, the social behaviour of S. entellus and S. hypoleucos is phylogenetically highly conservative.

Division of labor in hand usage is associated with higher hand performance in free-ranging bonnet macaques, Macaca radiate [corrected].

A practical approach to understanding lateral asymmetries in body, brain, and cognition would be to examine the performance advantages/disadvantages associated with the corresponding functions and behavior. In the present study, we examined whether the division of labor in hand usage, marked by the preferential usage of the two hands across manual operations requiring maneuvering in three-dimensional space (e.g., reaching for food, grooming, and hitting an opponent) and those requiring physical strength (e.g., climbing), is associated with higher hand performance in free-ranging bonnet macaques, Macaca radiate [corrected]. We determined the extent to which the macaques exhibit laterality in hand usage in an experimental unimanual and a bimanual food-reaching task, and the extent to which manual laterality is associated with hand performance in an experimental hand-performance-differentiation task. We observed negative relationships between (a) the latency in food extraction by the preferred hand in the hand-performance-differentiation task (wherein, lower latency implies higher performance), the preferred hand determined using the bimanual food-reaching task, and the normalized difference between the performance of the two hands, and (b) the normalized difference between the performance of the two hands and the absolute difference between the laterality in hand usage in the unimanual and the bimanual food-reaching tasks (wherein, lesser difference implies higher manual specialization). Collectively, these observations demonstrate that the division of labor between the two hands is associated with higher hand performance.

Food resources, distribution and seasonal variations in ranging in lion-tailed macaques, Macaca silenus in the Western Ghats, India.

The distribution and availability of food was examined to see how it influenced ranging patterns and sleeping site selection in a group of lion-tailed macaques. The home range and core area were 130.48 ha (95% kernel) and 26.68 ha (50% kernel) respectively. The lion-tailed macaques had a longer day range, had a greater number of sleeping sites and used more core areas in the summer as compared to the monsoon and the post-monsoon seasons. The ranging patterns and sleeping site use were influenced by the major food resources used in a particular season. The ranging was mainly influenced by Artocarpus heterophyllus in monsoon, Cullenia exarillata and Toona ciliata in post- monsoon, and Artocarpus heterophyllus and Ficus amplissima in summer. The distribution of these four plant species is, therefore, critical to ranging, and thus to conservation of the lion-tailed macaque.

A comparative assessment of hand preference in captive red howler monkeys, Alouatta seniculus and yellow-breasted capuchin monkeys, Sapajus xanthosternos.

There are two major theories that attempt to explain hand preference in non-human primates-the 'task complexity' theory and the 'postural origins' theory. In the present study, we proposed a third hypothesis to explain the evolutionary origin of hand preference in non-human primates, stating that it could have evolved owing to structural and functional adaptations to feeding, which we refer to as the 'niche structure' hypothesis. We attempted to explore this hypothesis by comparing hand preference across species that differ in the feeding ecology and niche structure: red howler monkeys, Alouatta seniculus and yellow-breasted capuchin monkeys, Sapajus xanthosternos. The red howler monkeys used the mouth to obtain food more frequently than the yellow-breasted capuchin monkeys. The red howler monkeys almost never reached for food presented on the opposite side of a wire mesh or inside a portable container, whereas the yellow-breasted capuchin monkeys reached for food presented in all four spatial arrangements (scattered, on the opposite side of a wire mesh, inside a suspended container, and inside a portable container). In contrast to the red howler monkeys that almost never acquired bipedal and clinging posture, the yellow-breasted capuchin monkeys acquired all five body postures (sitting, bipedal, tripedal, clinging, and hanging). Although there was no difference between the proportion of the red howler monkeys and the yellow-breasted capuchin monkeys that preferentially used one hand, the yellow-breasted capuchin monkeys exhibited an overall weaker hand preference than the red howler monkeys. Differences in hand preference diminished with the increasing complexity of the reaching-for-food tasks, i.e., the relatively more complex tasks were perceived as equally complex by both the red howler monkeys and the yellow-breasted capuchin monkeys. These findings suggest that species-specific differences in feeding ecology and niche structure can influence the perception of the complexity of the task and, consequently, hand preference.