Hideshi Ogawa

Hierarchical steepness and phylogenetic models: phylogenetic signals in Macaca

Phylogenetic models of primate social behaviour posit that core social traits are inherent species characteristics that depend largely on phylogenetic histories of species rather than on adaptation to current socioecological conditions. These models predict that aspects of social structure will vary more between species than within species and that they will display strong phylogenetic signals. We tested these predictions in macaques focusing on dominance gradients, a relatively little studied, yet central, aspect of social structure. We used data from 14 social groups representing nine macaque species living in a variety of conditions. We examined proportions of counteraggression and two recently developed measures of dominance gradients (hierarchical steepness) for phylogenetic signals in nine phylogenetic trees constructed using (1) available genetic data sets and (2) Bayesian Markov Chain Monte Carlo (MCMC) and maximum likelihood algorithms. Hierarchical steepness and counteraggression showed significant variation between species but inconsistent variation within species. Both steepness and counteraggression showed evidence of phylogenetic signals, with results being particularly strong for one steepness measure and for counteraggression. Our results suggest that between-species variation in some core aspects of social structure are shaped by species’ evolutionary relationships, despite differences in living conditions. As such, they provide broad support for the phylogenetic model.

Hierarchical Steepness, Counter-Aggression, and Macaque Social Style Scale

Nonhuman primates show remarkable variation in several aspects of social structure. One way to characterize this variation in the genus Macaca is through the concept of social style, which is based on the observation that several social traits appear to covary with one another in a linear or at least continuous manner. In practice, macaques are more simply characterized as fitting a four‐grade scale in which species range from extremely despotic (grade 1) to extremely tolerant (grade 4). Here, we examine the fit of three core measures of social style—two measures of dominance gradients (hierarchical steepness) and another closely related measure (counter‐aggression)—to this scale, controlling for phylogenetic relationships. Although raw scores for both steepness and counter‐aggression correlated with social scale in predicted directions, the distributions appeared to vary by measure. Counter‐aggression appeared to vary dichotomously with scale, with grade 4 species being distinct from all other grades. Steepness measures appeared more continuous. Species in grades 1 and 4 were distinct from one another on all measures, but those in the intermediate grades varied inconsistently. This confirms previous indications that covariation is more readily observable when comparing species at the extreme ends of the scale than those in intermediate positions. When behavioral measures were mapped onto phylogenetic trees, independent contrasts showed no significant consistent directional changes at nodes below which there were evolutionary changes in scale. Further, contrasts were no greater at these nodes than at neutral nodes. This suggests that correlations with the scale can be attributed largely to species’ phylogenetic relationships. This could be due in turn to a structural linkage of social traits based on adaptation to similar ecological conditions in the distant past, or simply to unlinked phylogenetic closeness. Am. J. Primatol. 74:915‐925, 2012.

Using Biological Markets Principles to Examine Patterns of Grooming Exchange in Macaca thibetana

Biological markets principles offer testable hypotheses to explain variation in grooming exchange patterns among nonhuman primates. They predict that when within‐group contest competition (WGC) is high and dominance hierarchies steep, grooming interchange with other “commodity” behaviors (such as agonistic support) should prevail. In contrast, when WGC is low and gradients shallow, market theory predicts that grooming reciprocity should prevail. We tested these predictions in a wild, provisioned Tibetan macaque (Macaca thibetana) group across six time periods during which the group had been subjected to varying degrees of range restriction. Data on female–female aggression, grooming, and support were collected using all‐occurrences and focal animal sampling techniques, and analyzed using ANCOVA methods and correlation analyses. We found that hierarchical steepness varied significantly across periods, but did not correlate with two indirect indicators of WGC (group size and range restriction) in predicted directions. Contrary to expectations, we found a negative correlation between steepness and group size, perhaps because the responses of group members to external risks (i.e. prolonged and unavoidable exposure to humans) may have overshadowed the effects of WGC. As predicted, grooming reciprocity was significant in each period and negatively correlated with steepness, even after we controlled group size, kinship, rank differences, and proximity. In contrast, there was no evidence for grooming interchange with agonistic support or for a positive relationship between interchange and steepness. We hypothesize that stressful conditions and/or the presence of stable hierarchies during each period may have led to a greater market demand for grooming than support. We suggest that future studies testing these predictions consider more direct measures of WGC and commodities in addition to support, such as feeding tolerance and access to infants. Am. J. Primatol. 73:1269–1279, 2011.

Hierarchical steepness, counter-aggression, and Macaque social style scale

Nonhuman primates show remarkable variation in several aspects of social structure. One way to characterize this variation in the genus Macaca is through the concept of social style, which is based on the observation that several social traits appear to covary with one another in a linear or at least continuous manner. In practice, macaques are more simply characterized as fitting a four‐grade scale in which species range from extremely despotic (grade 1) to extremely tolerant (grade 4). Here, we examine the fit of three core measures of social style—two measures of dominance gradients (hierarchical steepness) and another closely related measure (counter‐aggression)—to this scale, controlling for phylogenetic relationships. Although raw scores for both steepness and counter‐aggression correlated with social scale in predicted directions, the distributions appeared to vary by measure. Counter‐aggression appeared to vary dichotomously with scale, with grade 4 species being distinct from all other grades. Steepness measures appeared more continuous. Species in grades 1 and 4 were distinct from one another on all measures, but those in the intermediate grades varied inconsistently. This confirms previous indications that covariation is more readily observable when comparing species at the extreme ends of the scale than those in intermediate positions. When behavioral measures were mapped onto phylogenetic trees, independent contrasts showed no significant consistent directional changes at nodes below which there were evolutionary changes in scale. Further, contrasts were no greater at these nodes than at neutral nodes. This suggests that correlations with the scale can be attributed largely to species’ phylogenetic relationships. This could be due in turn to a structural linkage of social traits based on adaptation to similar ecological conditions in the distant past, or simply to unlinked phylogenetic closeness. Am. J. Primatol. 74:915‐925, 2012.

Variation in kin bias over time in a group of Tibetan macaques at Huangshan, China: contest competition, time constraints or risk response?

We examine variation in grooming kin bias intensity (KBI) among wild female Tibetan macaques ( Macaca thibetana huangshanensis ) in one group over time. We test three hypotheses based on socioecological theory, time constraints and risk-related responses. Only the time constraints hypothesis was supported. Grooming KBI was higher when the group was larger, but was unrelated to other indicators of within-group competition. Allies were not necessarily frequent grooming partners; thus, support did not depend on maintaining strong grooming relationships. Females groomed similar amounts, regardless of group size, but groomed smaller percentages of available partners when the group was larger, suggesting that they were unable to maintain grooming relationships with all females as the group expanded. Females with several close kin groomed each of them less than females with few. The lowest ranking females tended to groom close kin almost exclusively, as expected if they had less grooming time to spare than other females. Although grooming KBI was higher when stressful external risks (many humans) were present, the correlation was unsustained when group size was controlled. We suggest that kin-focused grooming networks are shaped at least in part by time constraints and may not be linked directly or indirectly to within-group competition.

Triadic Positions of Tibetan Macaques Huddling at a Sleeping Site

We studied huddling of Tibetan macaques (Macaca thibetana) at a sleeping site in Huangshan, China, during the mating and birth seasons. Tibetan macaques in a free-ranging group made physical contact with each other and formed huddling groups on the ledge of a steep cliff at night. We analyzed the size and composition of huddling groups and the frequencies of dyadic huddles—two individuals in physical contact—in the huddling group to determine the social influences on huddling behavior. Affiliated dyads that frequently groomed in the daytime frequently formed dyadic huddles in night-time huddling groups. Female–male dyads formed dyadic huddles less frequently than expected. In addition, Tibetan macaques chose 2 partners with which they initiated contact when they approached a huddling group. The frequencies with which some combinations of 3 individuals contacted each other and formed triangular huddles are not consistent with the expected frequencies. For example, female–male–male triads frequently formed triangular huddles in the birth season but did so infrequently in the mating season because of male competition for estrous females. When all 3 dyads within a certain triad formed dyadic huddles frequently, the triad was more likely to form a triangular huddle. The choices of approaching individuals might make a systematic, rather than random, positioning of individuals in huddling groups at their sleeping site.

Chimpanzees in the Ntakata and Kakungu Areas, Tanzania

Abstract Surveys were carried out for chimpanzees, Pan troglodytes schweinfurthii, in the areas of Ntakata (300 km2 between the Mkamba River and the Lubalisi River, 05°45′–06°15′S, 30°00′–30°15′E), and Kakungu (200 km2 between the Lubalisi River and the sources of the Rubufu River, 05°55′–06°15′S, 30°00′–30°15′E), Tanzania, during the dry seasons of 2001 and 2003. The predominant vegetation was savanna woodland with forest patches (mainly along watercourses and hillsides). Population information was obtained by sightings and sleeping-nest counts. In the Ntakata area, chimpanzees occur in Ntakata, Mlofwezi, Kapalagulu (05°52′S, 30°02′E), and Mpulumuka (5°58′S, 30°11 ′E) and in the Ntakata-Kapalagulu Hills (Fig. 1). No evidence was forthcoming for their existence in Ikubulu, Lunfampa, Kakundu, Kabufisa, and Kamafiga, nor the plains of north of Kapalagulu Hill and the entire Lugufu basin. In the Kakungu area, they occur at Kakungu itself (05°58′S, 30°03′E) and Kalobwa in the Kakungu-Kalobwa Hills. With evidently large home ranges, densities were found to be low in the 500-km2 area between the Ntakata-Kapalagulu Hills and Kakungu-Kalobwa Hills — everywhere less than 0.05(0.048) individuals/km2. Hunting (by immigrant farmers and refugees), besides habitat loss (logging, firewood, and clearing for agriculture) are believed be causing a steady decline of chimpanzee populations in the region.

Gene Flow and Genetic Diversity of Chimpanzees in Tanzanian Habitats

Abstract: Tanzania is located at the southeastern end of the eastern chimpanzee (Pan troglodytes schweinfurthii) distribution. Except for two national parks, their habitats have been degraded due to human activities. To clarify the gene flow and genetic diversity of chimpanzees in Tanzania, we analyzed the mitochondrial sequences of chimpanzees in six sites (Lwazi, Wansisi, Mahale, Karobwa, Ugalla-Masito, and Gombe), some of which are now isolated. The southernmost habitat (Lwazi) was about 150 km away from the nearest habitat but, considering the geographic distance, the genetic distance of the chimpanzees between Lwazi and the other habitats was not high. In contrast, the genetic distance between the chimpanzees in the northernmost habitat (Gombe), and the other habitats was relatively high considering the geographic distance. The results suggest that the Malagarasi River, which runs between Gombe and the southern habitats, limits gene flow. The genetic difference analyses also suggest that the habitats of Wansisi, Mahale, Karobwa, and Ugalla-Masito can be regarded as one population (“Greater Mahale”). The genetic distance between Lwazi and Gombe was lower than that between Gombe and the Greater Mahale habitats. This result suggests that early chimpanzees came to the Greater Mahale habitats through the southern habitats around Lwazi. The nucleotide diversity was not different from that in other countries, probably due to the sequence variety. There were unique haplotypes in several habitats where the number of chimpanzees was estimated to be small, which implies that some haplotypes are probably be at risk of disappearing. These data will be useful for conservation planning.

Consistency of dominance rank order: a comparison of David's Scores with I&SI and Bayesian methods in macaques.

In nonhuman primate social groups, dominance ranks are usually assigned to individuals based on outcomes of dyadic agonistic encounters. Multiple approaches have been used, but currently there is no consensus. One approach, Davids Scores (DS), offers dual advantages of yielding cardinal scores that may in turn be used to compute hierarchical steepness. Here we correlate rank orders yielded by DS with those yielded by both the traditionally used I&SI approach and the recently proposed parametric Bayesian approach. We use six datasets for female macaques (three despotic and three tolerant groups), and 90 artificially generated datasets modeling macaque groups. We also use the artificial datasets to determine the impact of three characteristics (group size, interaction frequency, and directional asymmetry of aggression) on the magnitude of correlation coefficients, and assess the relative utility of two indices used to compute DS: Dij versus Pij. DS‐based rank orders were strongly positively correlated with those yielded by the other two approaches for five out of the six macaque datasets, and for the majority of artificial datasets. Magnitudes of correlation coefficients were unrelated to group size or interaction frequency, but increased with directional asymmetry, suggesting methodological inconsistencies were more likely when dyads had more frequent reversals in directions of aggression. Finally, rank orders calculated using the Dij and Pij indices were similarly consistent with orders from other methods. We conclude that DS offers consistent estimates of rank orders, except perhaps in groups with very low levels of aggression asymmetry. In such “tolerant” groups, we suggest that the relatively greater methodological variability in rank orders may reflect behavioral characteristics of tolerant groups rather than computational inconsistencies between methods. We hypothesize that this quality may be quantified using posterior probability scores of Bayesian rank orders and may also index macaque social styles. Am. J. Primatol. 75:959–971, 2013.

The influence of phylogeny, social style, and sociodemographic factors on macaque social network structure

Among nonhuman primates, the evolutionary underpinnings of variation in social structure remain debated, with both ancestral relationships and adaptation to current conditions hypothesized to play determining roles. Here we assess whether interspecific variation in higher‐order aspects of female macaque (genus: Macaca) dominance and grooming social structure show phylogenetic signals, that is, greater similarity among more closely‐related species. We use a social network approach to describe higher‐order characteristics of social structure, based on both direct interactions and secondary pathways that connect group members. We also ask whether network traits covary with each other, with species‐typical social style grades, and/or with sociodemographic characteristics, specifically group size, sex‐ratio, and current living condition (captive vs. free‐living). We assembled 34–38 datasets of female‐female dyadic aggression and allogrooming among captive and free‐living macaques representing 10 species. We calculated dominance (transitivity, certainty), and grooming (centrality coefficient, Newmans modularity, clustering coefficient) network traits as aspects of social structure. Computations of K statistics and randomization tests on multiple phylogenies revealed moderate‐strong phylogenetic signals in dominance traits, but moderate‐weak signals in grooming traits. GLMMs showed that grooming traits did not covary with dominance traits and/or social style grade. Rather, modularity and clustering coefficient, but not centrality coefficient, were strongly predicted by group size and current living condition. Specifically, larger groups showed more modular networks with sparsely‐connected clusters than smaller groups. Further, this effect was independent of variation in living condition, and/or sampling effort. In summary, our results reveal that female dominance networks were more phylogenetically conserved across macaque species than grooming networks, which were more labile to sociodemographic factors. Such findings narrow down the processes that influence interspecific variation in two core aspects of macaque social structure. Future directions should include using phylogeographic approaches, and addressing challenges in examining the effects of socioecological factors on primate social structure.