Cyril C. Grueter

Evolution of Multilevel Social Systems in Nonhuman Primates and Humans

Multilevel (or modular) societies are a distinct type of primate social system whose key features are single-male–multifemale, core units nested within larger social bands. They are not equivalent to fission–fusion societies, with the latter referring to routine variability in associations, either on an individual or subunit level. The purpose of this review is to characterize and operationalize multilevel societies and to outline their putative evolutionary origins. Multilevel societies are prevalent in three primate clades: papionins, Asian colobines, and hominins. For each clade, we portray the most parsimonious phylogenetic pathway leading to a modular system and then review and discuss likely socioecological conditions promoting the establishment and maintenance of these societies. The multilevel system in colobines (most notably Rhinopithecus and Nasalis) has likely evolved as single-male harem systems coalesced, whereas the multilevel system of papionins (Papio hamadryas, Theropithecus gelada) and hominins most likely arose as multimale–multifemale groups split into smaller units. We hypothesize that, although ecological conditions acted as preconditions for the origin of multilevel systems in all three clades, a potentially important catalyst was intraspecific social threat, predominantly bachelor threat in colobines and female coercion/infanticide in papionins and humans. We emphasize that female transfers within bands or genetic relationships among leader males help to maintain modular societies by facilitating interunit tolerance. We still lack a good or even basic understanding of many facets of multilevel sociality. Key remaining questions are how the genetic structure of a multilevel society matches the observed social effort of its members, to what degree cooperation of males of different units is manifest and contributes to band cohesion, and how group coordination, communication, and decision making are achieved. Affiliative and cooperative interunit relations are a hallmark of human societies, and studying the precursors of intergroup pacification in other multilevel primates may provide insights into the evolution of human uniqueness.

Feeding strategies of primates in temperate and alpine forests: comparison of Asian macaques and colobines

We analyzed regional variation in the diets of two primate clades, Asian macaques and colobines, whose distributions include temperate–alpine forests. We addressed feeding strategies that enabled them to adapt to harsh environments characterized by relatively low mean temperatures and strong seasonality in both temperature and food availability. Macaques in tropical–lowland forests feed mainly on fruit and animal matter whereas populations in temperate–alpine forests feed more on foliage and on such items as bark and fungi. In comparison, colobines in tropical–lowland forests feed more on fruit and foliage whereas populations in temperate–alpine forests feed less on flowers and more on lichens. Annual precipitation and mean temperature, both of which reflect primary production, had the most significant effects on the feeding behavior of the macaques, whereas only mean temperature had a significant effect on that of colobines. We found two behavioral strategies used by both clades to cope with severe environmental conditions in temperate–alpine forests—shifting to other food items and adjusting feeding plasticity for fruit and foliage. Macaques responded to latitudinal changes by use of both strategies whereas the colobines adapted by using the latter only. By contrast, changes in altitude resulted in the macaques’ using the latter strategy and colobines’ using both. The different current distributions of Asian macaques and colobines could be attributed to differences in their feeding strategies originating in their digestive systems.

Dietary Profile of Rhinopithecus bieti and Its Socioecological Implications

To enhance our understanding of dietary adaptations and socioecological correlates in colobines, we conducted a 20-mo study of a wild group of Rhinopithecus bieti (Yunnan snub-nosed monkeys) in the montane Samage Forest. This forest supports a patchwork of evergreen broadleaved, evergreen coniferous, and mixed deciduous broadleaved/coniferous forest assemblages with a total of 80 tree species in 23 families. The most common plant families by basal area are the predominantly evergreen Pinaceae and Fagaceae, comprising 69% of the total tree biomass. Previous work has shown that lichens formed a consistent component in the monkeys’ diet year-round (67%), seasonally complemented with fruits and young leaves. Our study showed that although the majority of the diet was provided by 6 plant genera (Acanthopanax, Sorbus, Acer, Fargesia, Pterocarya, and Cornus), the monkeys fed on 94 plant species and on 150 specific food items. The subjects expressed high selectivity for uncommon angiosperm tree species. The average number of plant species used per month was 16. Dietary diversity varied seasonally, being lowest during the winter and rising dramatically in the spring. The monkeys consumed bamboo shoots in the summer and bamboo leaves throughout the year. The monkeys also foraged on terrestrial herbs and mushrooms, dug up tubers, and consumed the flesh of a mammal (flying squirrel). We also provide a preliminary evaluation of feeding competition in Rhinopithecus bieti and find that the high selectivity for uncommon seasonal plant food items distributed in clumped patches might create the potential for food competition. The finding is corroborated by observations that the subjects occasionally depleted leafy food patches and stayed at a greater distance from neighboring conspecifics while feeding than while resting. Key findings of this work are that Yunnan snub-nosed monkeys have a much more species-rich plant diet than was previously believed and are probably subject to moderate feeding competition.

Choice of analytical method can have dramatic effects on primate home range estimates

Primate home range sizes can vary tremendously as a consequence of the analytical technique chosen to estimate home range. This is exemplified by a recent dataset on free ranging snub-nosed monkeys (Rhinopithecus bieti) in Northwest Yunnan, China. Our findings show that the grid cell method cannot substitute for the minimum convex polygon (MCP) method and vice versa. MCP-based estimates are far too large, especially when the form of the home range is irregular due to forays into peripheral areas. Here, we propose an adjusted polygon method, whereby unsuitable and never visited areas are clipped out from the polygon, thus producing more accurate results. Compared to the grid cell method, the adjusted MCP is much more robust when the number of group relocations is limited; MCP turned out to be the method of choice for calculation of monthly and seasonal home ranges. The grid cell method on the other hand yielded the most precise estimates for total or annual home ranges. The style of ranging exhibited by a given primate taxon or population determines which analytical procedures should be applied to estimate home range size, and we would stress the need for thorough evaluation of the pros and cons of home range estimators before conducting field work and analysing data.

Socioecological correlates of energy balance using urinary C-peptide measurements in wild female mountain gorillas

Maintaining a balanced energy budget is important for survival and reproduction, but measuring energy balance in wild animals has been fraught with difficulties. Female mountain gorillas are interesting subjects to examine environmental correlates of energy balance because their diet is primarily herbaceous vegetation, their food supply shows little seasonal variation and is abundant, yet they live in cooler, high-altitude habitats that may bring about energetic challenges. Social and reproductive parameters may also influence energy balance. Urinary C-peptide (UCP) has emerged as a valuable non-invasive biomarker of energy balance in primates. Here we use this method to investigate factors influencing energy balance in mountain gorillas of the Virunga Volcanoes, Rwanda. We examined a range of socioecological variables on energy balance in adult females in three groups monitored by the Karisoke Research Center over nine months. Three variables had significant effects on UCP levels: habitat (highest levels in the bamboo zone), season (highest levels in November during peak of the bamboo shoot availability) and day time (gradually increasing from early morning to early afternoon). There was no significant effect of reproductive state and dominance rank. Our study indicates that even in species that inhabit an area with a seemingly steady food supply, ecological variability can have pronounced effects on female energy balance.

Males collectively defend their one-male units against bachelor males in a multi-level primate society

Group‐level male–male co‐operation, which has been documented in several primate and non‐primate societies, may be mutualistically advantageous to the participants when confronted with threats such as takeovers and cuckoldry by external males. Co‐operation among members of distinct social units—while universal among humans—is extremely rare in non‐human primates. We present the first observations of collective action or co‐operation among males of different one‐male units (OMU) in a multi‐level society of Rhinopithecus roxellana. A total of 59 instances of male co‐operation were recorded. Male co‐operation included coordinated chasing, joint vigilance, and patrolling behavior directed at lone adult males trying to enter an OMU. Male co‐operation was significantly more frequent during the mating season when the risk of incursions and extra‐group paternity was higher. Paternity of infants born in the subsequent birth season and kin relationships among resident males were identified using microsatellite genotype. All infants were sired by OMU males, which we interpret as possible evidence for their success at thwarting mating attempts by satellite males. OMU males were principally unrelated suggesting that male co‐operation is best understood in terms of the mutual direct benefits individuals obtain through collective action. Our findings lend support to the bachelor threat hypothesis in which the cooperative behavior of several individuals is more effective than the lone action of a single individual in providing mate defense. Our research has implications for understanding male bonding, higher‐level collective action, and the evolution of social co‐operation in human societies. Am. J. Primatol. 76:609–617, 2014.

Multilevel Societies in Primates and Other Mammals: Introduction to the Special Issue.

Murdoch (1981) remarked that nowhere on Earth do people live regularly in isolated families. The habitual formation of superfamily level groupings is one of the unmistakable universals of human sociality. Males and females within these higher level groupings are connected via kinship and affinity ties, and affiliative and cooperative bonds reach far beyond the nuclear family unit (Rodseth et al. 1991; Wiessner 1977). Although interunit encounters are usually circumvented or characterized by animosity because of mating or resource competition in many nonhuman primates (Cheney 1987; Fashing 2001), some primates such as hamadryas baboons (Papio hamadryas), geladas (Theropithecus gelada), snub-nosed monkeys (Rhinopithecus spp.), and proboscis monkeys (Nasalis larvatus) (for an exhaustive list, see Grueter et al. 2012) exhibit a social arrangement in which regular or constant proximity as well as coordinated activity among subunits is the norm. This type of social organization has been termed multilevel, nested, or modular. The phenomenon of social modularity is not restricted to the primate order. Similarly structured societies can be observed in other mammals, most notably African elephants (Loxodonta africana: de Silva and Wittemyer 2012; Moss and Poole 1983; Wittemyer et al. 2005), Asian elephants (Elephas maximus: de Silva and Wittemyer 2012), plains zebras (Equus burchelli: Rubenstein and Hack 2004), khulans (Equus hemionus: Feh et al. 2001), prairie dogs (Cynomys ludovicianus: Hoogland 1995), sperm whales (Physeter macrocephalus: Whitehead et al. 1991, 2012), and killer whales (Orcinus orca: Baird 2000).

Sexual size dimorphism in Asian colobines revisited

Asian colobines exhibit a wide range of sexual dimorphism in body mass. Some species are monomorphic, whereas others are strongly dimorphic. Strong sexual dimorphism is generally viewed as the consequence of intense male contest competition over access to mates, but this idea appears not to explain variation in sexual dimorphism in Asian colobines. Our results show that modular colobines, i.e. species in which social units aggregate into higher‐level bands or often associate, have significantly higher levels of sexual dimorphism in body mass than the nonmodular ones. This finding was corroborated by means of phylogenetically controlled methods and multiple regression analyses. The results suggest that living in a modular society intensifies the contest competition among males, which is further exacerbated by the continuous presence of all‐male units. Am. J. Primatol. 71:609–616, 2009.

Long-term temporal and spatial dynamics of food availability for endangered mountain gorillas in Volcanoes National Park, Rwanda.

Monitoring temporal and spatial changes in the resource availability of endangered species contributes to their conservation. The number of critically endangered mountain gorillas (Gorilla beringei beringei) in the Virunga Volcano population has doubled over the past three decades, but no studies have examined how food availability has changed during that period. First, we assessed if the plant species consumed by the gorillas have changed in abundance and distribution during the past two decades. In 2009–2010, we replicated a study conducted in 1988–1989 by measuring the frequency, density, and biomass of plant species consumed by the gorillas in 496 plots (ca. 6 km2) in the Karisoke study area in Volcanoes National Park, Rwanda. We expected to observe a decreased presence of major gorilla food plants as a likely result of density‐dependent overharvesting by gorillas. Among the five most frequently consumed species (composing approximately 70% of the gorillas diet, excluding bamboo), two have decreased in availability and abundance, while three have increased. Some species have undergone shifts in their altitudinal distribution, possibly due to regional climatic changes. Second, we made baseline measurements of food availability in a larger area currently utilized by the gorillas. In the extended sampling (n = 473 plots) area (ca. 25 km2), of the five most frequently consumed species, two were not significantly different in frequency from the re‐sampled area, while two occurred significantly less frequently, and one occurred significantly more frequently. We discuss the potential impact of gorilla‐induced herbivory on changes of vegetation abundance. The changes in the species most commonly consumed by the gorillas could affect their nutrient intake and stresses the importance of monitoring the interrelation among plant population dynamics, species density, and resource use. Am. J. Primatol. 75:267‐280, 2013.

Behavioral variation in gorillas: Evidence of potential cultural traits

The question of whether any species except humans exhibits culture has generated much debate, partially due to the difficulty of providing conclusive evidence from observational studies in the wild. A starting point for demonstrating the existence of culture that has been used for many species including chimpanzees and orangutans is to show that there is geographic variation in the occurrence of particular behavioral traits inferred to be a result of social learning and not ecological or genetic influences. Gorillas live in a wide variety of habitats across Africa and they exhibit flexibility in diet, behavior, and social structure. Here we apply the ‘method of exclusion’ to look for the presence/absence of behaviors that could be considered potential cultural traits in well-habituated groups from five study sites of the two species of gorillas. Of the 41 behaviors considered, 23 met the criteria of potential cultural traits, of which one was foraging related, nine were environment related, seven involved social interactions, five were gestures, and one was communication related. There was a strong positive correlation between behavioral dissimilarity and geographic distance among gorilla study sites. Roughly half of all variation in potential cultural traits was intraspecific differences (i.e. variability among sites within a species) and the other 50% of potential cultural traits were differences between western and eastern gorillas. Further research is needed to investigate if the occurrence of these traits is influenced by social learning. These findings emphasize the importance of investigating cultural traits in African apes and other species to shed light on the origin of human culture.