Social tolerance in a despotic primate: co-feeding between consortship partners in rhesus macaques

Food sharing among nonkin-one of the most fascinating cooperative behaviors in humans-is not widespread in nonhuman primates. Over the past few years, a large body of work has investigated the contexts in which primates cooperate and share food with unrelated individuals. This work has successfully demonstrated that species-specific differences in temperament constrain the extent to which food sharing emerges in experimental situations, with despotic species being less likely to share food than tolerant ones. However, little experimental work has examined the contexts that promote food sharing and cooperation within a species. Here, we examine whether one salient reproductive context-the consortship dyad-can allow the necessary social tolerance for co-feeding to emerge in an extremely despotic species, the rhesus macaque (Macaca mulatta). We gave naturally formed male-female rhesus macaque pairs access to a monopolizable food site in the free-ranging population at Cayo Santiago, Puerto Rico. Using this method, we were able to show that tolerated co-feeding between unrelated adults can take place in this despotic species. Specifically, our results show that consort pairs co-fed at the experimental food site more than nonconsort control pairs, leading females to obtain more food in this context. These results suggest that co-feeding is possible even in the most despotic of primate species, but perhaps only in contexts that specifically promote the necessary social tolerance. Researchers might profit from exploring whether other kinds of within-species contexts could also generate cooperative behaviors.     

Spontaneous use and modification of a feather as a tool in a captive common raven

Here, we report an observation of a zoo‐housed common raven (Corvus corax) modifying and using a raven feather as a tool to access the food cache of her partner. We believe this record is of importance, as it represents one of the first cases of untrained common ravens spontaneously using and modifying a tool, and a rare example of a non‐human animal manufacturing a tool from a body part. This anecdotal observation suggests that tool use and tool modification may be present in the common raven behavioral repertoire in the foraging context; nevertheless, further investigations are needed to assess this possibility in more controlled settings as well as in the wild.     

Protective behavior or ‘true’ tool use? Scrutinizing the tool use behavior of ants

In the genus Aphaenogaster, workers use tools to transport liquid food to the colony. During this behavior, ants place or drop various kinds of debris into liquids or soft food, and then, they carry the food‐soaked tools back to the nest. According to some authors, this behavior is not "true" tool use because it represents two separate processes: a defense response to cover the dangerous liquid and a transport of food. Here, we investigated the debris dropping and retrieving behavior of the ant Aphaenogaster subterranea to establish which of the two hypotheses is more probable by conducting manipulative experiments. We tested the responses of eight colonies (a) to liquid food (honey‐water) and nonfood liquids (water) in different distances from the nest and (b) to nonthreatening liquids previously covered or presented as small droplets. We also tested whether the nutritional condition of colonies (i.e., starved or satiated) would affect the intensity and rate of debris dropping. Our results were consistent with the tool‐using behavior hypothesis. Firstly, ants clearly differentiated between honey‐water and water, and they directed more of their foraging effort toward liquids farther from the nest. Secondly, ants performed object dropping even into liquids that did not pose the danger of drowning or becoming entangled. Lastly, the nutritional condition of colonies had a significant effect on the intensity and rate of object dropping, but in the opposite direction than we expected. Our results suggest that the foraging behavior of A. subterranea is more complex than that predicted by the two‐component behavior hypothesis and deserves to be considered as "true" tool use.     

The use of nonhuman primates in the study of bilirubin metabolism and bile secretion

Close similarities exist in the chemical structure of fetal and adult bile pigments and mechanisms for hepatic bilirubin conjugation and transport in human and nonhuman primates. Newborn monkeys, unlike other animals, develop physiologic hyperbilirubinemia and are ideal animal models in which to investigate this developmental human disorder. Aberrations in bile pigment metabolism and compartmentalization which occur in hemolytic, hepatocellular, and obstructive diseases, closely resemble those reported in counterpart syndromes in man. Similarities also exist in the mechanisms responsible for the secretion of canalicular and ductular/ductal bile and the composition of bile. Nonhuman primates offer distinct advantages for comparative studies concerning bile pigment metabolism and the secretion of bile.     

Individual variation in the rate of use of tree-hole tools among wild orang-utans: implications for hominin evolution

Primate tool use varies among species, populations, and individuals. Individual variation is especially poorly understood. Orang-utans in the Sumatran swamp forest of Suaq Balimbing varied widely in rates of tool use to extract honey, ants or termites from tree holes and in the degree to which they specialized on this tree-hole tool use. We tested whether individual variation was best explained by effects of social dominance, habitat differences, or by opportunities for socially learning the skills during ontogeny. There was no evidence for the first two hypotheses. However, we found a strong relationship between tool use specialization and mean female party size, which was used as a proxy for the opportunities for socially mediated learning in a foraging context during their development. This use was justified because females are rather philopatric and their mean party size remained stable over time, thus reflecting long-term tendencies. The correlation was not an artifact of a direct effect of party size on tool use tendencies, and did not hold for males, the dispersing sex. Thus, variation in the number of opportunities for social learning explains tool use variation within populations, corroborating hypotheses for between-population variation. The emergence of human culture was accompanied by vastly improved mechanisms of social learning. In order for these improvements to be favored by natural selection, the cultural potential must have actually been expressed. Thus, a combination of strong sociability and a reliance on tool-using or other technical skills acquired through social learning must have characterized early hominins.     

The coevolution of innovation and technical intelligence in primates

In birds and primates, the frequency of behavioural innovation has been shown to covary with absolute and relative brain size, leading to the suggestion that large brains allow animals to innovate, and/or that selection for innovativeness, together with social learning, may have driven brain enlargement. We examined the relationship between primate brain size and both technical (i.e. tool using) and non-technical innovation, deploying a combination of phylogenetically informed regression and exploratory causal graph analyses. Regression analyses revealed that absolute and relative brain size correlated positively with technical innovation, and exhibited consistently weaker, but still positive, relationships with non-technical innovation. These findings mirror similar results in birds. Our exploratory causal graph analyses suggested that technical innovation shares strong direct relationships with brain size, body size, social learning rate and social group size, whereas non-technical innovation did not exhibit a direct relationship with brain size. Nonetheless, non-technical innovation was linked to brain size indirectly via diet and life-history variables. Our findings support ‘technical intelligence’ hypotheses in linking technical innovation to encephalization in the restricted set of primate lineages where technical innovation has been reported. Our findings also provide support for a broad co-evolving complex of brain, behaviour, life-history, social and dietary variables, providing secondary support for social and ecological intelligence hypotheses. The ability to gain access to difficult-to-extract, but potentially nutrient-rich, resources through tool use may have conferred on some primates adaptive advantages, leading to selection for brain circuitry that underlies technical proficiency.     

A model for tool-use traditions in primates: implications for the coevolution of culture and cognition

Inspired by the demonstration that tool-use variants among wild chimpanzees and orangutans qualify as traditions (or cultures), we developed a formal model to predict the incidence of these acquired specializations among wild primates and to examine the evolution of their underlying abilities. We assumed that the acquisition of the skill by an individual in a social unit is crucially controlled by three main factors, namely probability of innovation, probability of socially biased learning, and the prevailing social conditions (sociability, or number of potential experts at close proximity). The model reconfirms the restriction of customary tool use in wild primates to the most intelligent radiation, great apes; the greater incidence of tool use in more sociable populations of orangutans and chimpanzees; and tendencies toward tool manufacture among the most sociable monkeys. However, it also indicates that sociable gregariousness is far more likely to produce the maintenance of invented skills in a population than solitary life, where the mother is the only accessible expert. We therefore used the model to explore the evolution of the three key parameters. The most likely evolutionary scenario is that where complex skills contribute to fitness, sociability and/or the capacity for socially biased learning increase, whereas innovative abilities (i.e., intelligence) follow indirectly. We suggest that the evolution of high intelligence will often be a byproduct of selection on abilities for socially biased learning that are needed to acquire important skills, and hence that high intelligence should be most common in sociable rather than solitary organisms. Evidence for increased sociability during hominin evolution is consistent with this new hypothesis.     

Lateral sequence walking in infant Papio cynocephalus: implications for the evolution of diagonal sequence walking in primates

One of the most distinctive aspects of primate quadrupedal walking is the use of diagonal sequence footfalls in combination with diagonal-couplets interlimb timing. Numerous hypotheses have been offered to explain why primates might have evolved this type of gait, yet this important question remains unresolved. Because infant primates use a wider variety of quadrupedal gaits than do adults, they provide a natural experiment with which to test hypotheses about the evolution of unique aspects of primate quadrupedalism. In this study, we present kinematic data on two infant baboons (Papio cynocephalus) in order to test the recent hypothesis that diagonal sequence, diagonal couplets walking might have evolved in primates because their limb positioning provides stability in a small branch environment (Cartmill et al. [2002] Zool J Linn Soc 136:401-420). To assess hindlimb position at the moment of forelimb touchdown, we measured hindlimb angular excursion and ankle position for 84 walking strides, across three different types of gaits (diagonal sequence, diagonal couplets (DSDC); lateral sequence lateral couplets (LSLC); and lateral sequence diagonal couplets (LSDC)). Results indicate that if a forelimb were to contact an unstable substrate, LSLC walking provides as much, and perhaps more, stability when compared to DSDC walking. Therefore, it appears that this moment in a stride was unlikely to be a particularly important selective factor in the evolution of DSDC walking. Further insight into this issue will likely be gained by observations of primate quadrupedalism in natural environments, where the use of lateral sequence gaits might be more common than currently known.     

The enhanced tool‐kit of two groups of wild bearded capuchin monkeys in the Caatinga: tool making,associative use,and secondary tools

The use of stones to crack open encapsulated fruit is widespread among wild bearded capuchin monkeys (Cebus libidinosus) inhabiting savanna‐like environments. Some populations in Serra da Capivara National Park (Piauí, Brazil), though, exhibit a seemingly broader toolkit, using wooden sticks as probes, and employing stone tools for a variety of purposes. Over the course of 701.5 hr of visual contact of two wild capuchin groups we recorded 677 tool use episodes. Five hundred and seventeen of these involved the use of stones, and 160 involved the use of sticks (or other plant parts) as probes to access water, arthropods, or the contents of insects' nests. Stones were mostly used as “hammers”—not only to open fruit or seeds, or smash other food items, but also to break dead wood, conglomerate rock, or cement in search of arthropods, to dislodge bigger stones, and to pulverize embedded quartz pebbles (licking, sniffing, or rubbing the body with the powder produced). Stones also were used in a “hammer‐like” fashion to loosen the soil for digging out roots and arthropods, and sometimes as “hoes” to pull the loosened soil. In a few cases, we observed the re‐utilization of stone tools for different purposes (N=3), or the combined use of two tools—stones and sticks (N=4) or two stones (N=5), as sequential or associative tools. On three occasions, the monkeys used smaller stones to loosen bigger quartz pebbles embedded in conglomerate rock, which were subsequently used as tools. These could be considered the first reports of secondary tool use by wild capuchin monkeys. Am. J. Primatol. 71:242–251, 2009. © 2008 Wiley‐Liss, Inc.     

The use of new world primates for biomedical research: an overview of the last four decades

Animal experimentation contributes significantly to the progression of science. Nonhuman primates play a particularly important role in biomedical research not only because of their anatomical, physiological, biochemical, and behavioral similarities with humans but also because of their close phylogenetic affinities. In order to investigate the use of New World primates (NWP) in biomedical research over the last four decades (1966–2005), we performed a quantitative study of the literature listed in bibliographic databases from the Health Sciences. The survey was performed for each genus of NWP that has been bred in the National Center of Primates in Brazil. The number of articles published was determined for each genus and sorted according to the country from which the studies originated and the general scientific field. The data obtained suggests that Brazil is a leader in generating knowledge with NWP models for translational medicine. Am. J. Primatol. 72:1055–1061, 2010. © 2010 Wiley‐Liss, Inc.     

Chromosome mapping of Miller-Diecker,Smith-Magenis and RARA loci in non-human primates: implications in the evolution of human chromosome 17

Molecular cytogenetics allows to verify chromosomal homologies previously hypothesised on the base of banding pattern comparison in different species. So far only the chromosome painting technique has been extensively used in studies of chromosomal evolution. This technique allows to detect only interchromosomal rearrangements. Human and Great Apes chromosomes basically differ by intrachromosomal rearrangements, in particular inversions; with chromosome painting it has just been possible to confirm the origin by fusion of human chromosome 2 and a reciprocal translocation in Gorilla, involving the homologous of chromosome 5 and 17. In order to verify intrachromosomal rearrangements in human chromosomal evolution, chromosome mapping of human loci in non-human primates is a useful approach. We mapped Miller-Diecker, Smith-Magenis and RARA loci localised on human chromosome 17, in Gorilla gorilla, Pongo pygmaeus, Macaca fascicularis and Cercopithecus aethiops. On the base of the obtained results it was possible to verify chromosomal rearrangements previously identified by banding, to achieve new informations about the controversial evolution of human chromosome 17, and to detect the occurrence of a paracentric inversion in the homologous in Cercopithecus aethiops.     

Habitat characteristics and species interference influence space use and nest‐site occupancy: implications for social variation in two sister species

Nest‐site selection is an important component of species socio‐ecology, being a crucial factor in establishment of group living. Consequently, nest‐site characteristics together with space‐use proxies may reveal the social organization of species, which is critical when direct observation of social interactions is hindered in nature. Importantly, nest‐site choice is expected to be under strong selective pressures and the object of intra‐ and interspecific competition. Although the bulk of research on sociality focuses on its ecological drivers, our study introduces interspecific competition as a potential factor that could influence social evolution. We investigated the influence of habitat and interspecific competition on the social organization of two sister species of the African four striped mouse, Rhabdomys dilectus dilectus and Rhabdomys bechuanae, in a similar macroenvironment. These species diverged in allopatry and occupy distinct environmental niches. We radiotracked 140 adults to identify their nest‐sites, determine nest characteristics and record groups that shared nest‐sites. Group cohesion was estimated from nest‐site fidelity, group association strength, and home range overlap within versus between group members. We compared the two species in sympatry versus parapatry to determine the impact of species interference on sociality. In parapatry, the two species selected distinct nest‐site types, interpreted as different anti‐predator strategies: R. bechuanae selected fewer, spaced, less concealed nest‐sites whereas R. d. dilectus selected clumped and less visible nest‐sites. Rhabdomys bechuanae also showed more cohesive and stable social groups than R. d. dilectus. In sympatry, compared to R. bechuanae, R. d. dilectus occupied similar nest‐sites, however slightly more exposed and clumped, and displayed similar nest‐site fidelity and group association strength. We conclude that although habitat selection may be an important driver of social divergence in Rhabdomys, species interference, by limiting R. d. dilectus movements and forcing nest‐site sharing may induce new ecological pressures that could influence its social evolution.     

Social selection and the evolution of a female weapon in queens of the ant Messor pergandei (Hymenoptera: Formicidae)

The evolution of weaponry occurs less frequently in females than in males and is most often important for protecting ecological resources or offspring rather than winning mates. The purpose of female weapons is often confounded by the presence of similar weapons in males, so cases where only females need weapons provide important tests of our understanding of how and why weapons evolve. In some populations of the ant, Messor pergandei (Mayr), newly mated queens initiate new nests in social groups that subsequently break down when queens engage in battles for control. The incipient social environment differs geographically, so that lethal fighting occurs in some populations but not others. Consistent with the hypothesis that queens in populations where lethal fighting occurs should show selection for weaponry (broad heads and strong mandibles), we found that heads of queens from sites where lethal fighting occurs were broader than those at sites with non‐fighting queens and a site with solitary queens. Evolution of weaponry is specific to queens, because regression results from workers often did not follow this pattern. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 1011–1020.     

Where to catch a fish? The influence of foraging tactics on the ecology of bottlenose dolphins (Tursiops truncatus) in Florida Bay,Florida

Observations of bottlenose dolphins ( Tursiops truncatus ) in Florida Bay, Florida, between 2002 and 2005 revealed the use of three distinct foraging tactics. The goal of this study was to identify ecological correlates with tactic use and describe the impact of foraging specializations on the overall habitat use and distribution patterns of this dolphin population. Foraging tactics showed strong association with contrasting environmental characteristics, primarily depth. Locations of two of these tactic groups were spatially repulsed. Analyses of sighting histories of individual dolphins observed at foraging events determined that dolphins which employed one tactic never employed the other, and vice versa . Although bottlenose dolphins have plastic foraging behaviors, dolphins in Florida Bay appear to specialize in one tactic and subsequently limit their overall distribution patterns to coincide with habitats that facilitate success using that foraging tactic. This study demonstrates how foraging behavior can be an ecological determinant of overall dolphin habitat use patterns and works to create spatial structure within a population due to consistent mapping of tactics onto environmental variation. These foraging specializations potentially impact the social and demographic patterns of this dolphin population. The possible evolutionary mechanisms behind this intraspecific variation, including resource limitation and social learning, are considered.     

Intra-and interpopulational differences in orangutan (Pongo pygmaeus) activity and diet: implications for the invention of tool use

Tool manufacture and use have been described for wild orangutans (Pongo pygmaeus), with appreciable interpopulational differences in tool complexes. The ecological factors that contribute to these differences require investigation. Significant interpopulational differences in diet suggest that ecological factors contribute to variation in tool-based insect foraging. Using 4 years of behavioral data from the Suaq Balimbing Research Station (Sumatra, Indonesia), we tested predictions of two ecological hypotheses for the invention of tool use for insect foraging. We found limited evidence for inter- and intrasexual differences, as well as temporal variation, in activity budget and diet. However, differences did not correspond to variation in either rate of tool use or specialization on tool-based insectivory. Compared to other populations, orangutans at Suaq Balimbing ate significantly more insects. Low temporal variation in insectivory and an abundance of social insects at Suaq Balimbing suggest that insects formed a staple in the diet rather than a fallback food. Our findings do not support the hypothesis that tool use is a response to the low availability of primary food sources. Rather, greater opportunities for invention likely contributed to insect-extraction tool use at Suaq Balimbing.     

Foraging characteristics and intraspecific behaviour of the exotic species Monomorium sydneyense (Hymenoptera: Formicidae) in New Zealand,with implications for its management

Abstract

We attempt to evaluate the biosecurity risk posed by the newly established exotic ant species Monomorium sydneyense Forel, in New Zealand. Aggression was observed between workers from different M. sydneyense nests, indicating that unicoloniality is unlikely. Nests had multiple queens, and nest foundation is apparently via winged queens. The foraging behaviour corresponded to multicoloniality, with workers foraging in close proximity to the nest. In trials during December (2003) and March (2004), workers had a >50% probability of finding food at a distance of 0.8–1 m from their nest, but on cooler study dates (October 2004) our logistic regression model indicated that they would not reach this threshold irrespective of how close the food was to the nest. Although M. sydneyense forage during both night and day, they appeared to be relatively inefficient at locating food. We conclude that under the conditions assessed here, the environmental damage likely to be caused by M. sydneyense is modest compared with other invasive ant species.     

Allometry of facial mobility in anthropoid primates: implications for the evolution of facial expression

Body size may be an important factor influencing the evolution of facial expression in anthropoid primates due to allometric constraints on the perception of facial movements. Given this hypothesis, I tested the prediction that observed facial mobility is positively correlated with body size in a comparative sample of nonhuman anthropoids. Facial mobility, or the variety of facial movements a species can produce, was estimated using a novel application of the Facial Action Coding System (FACS). I used FACS to estimate facial mobility in 12 nonhuman anthropoid species, based on video recordings of facial activity in zoo animals. Body mass data were taken from the literature. I used phylogenetic generalized least squares (PGLS) to perform a multiple regression analysis with facial mobility as the dependent variable and two independent variables: log body mass and dummy-coded infraorder. Together, body mass and infraorder explain 92% of the variance in facial mobility. However, the partial effect of body mass is much stronger than for infraorder. The results of my study suggest that allometry is an important constraint on the evolution of facial mobility, which may limit the complexity of facial expression in smaller species. More work is needed to clarify the perceptual bases of this allometric pattern.