The Evolution of Primate Societies - Chapter 3

Compared with other primates, New World monkeys display relatively limited ecological variability. New World monkey anatomy and social systems, however, are extremely diverse. Several unique morphological features (e.g., claws, prehensile tails) and uncommon patterns of social organization (e.g., paternal care, cooperative breeding, female dispersal) have evolved in some platyrrhine species. Social organization and mating patterns include typical harem- like structures where mating is largely polygynous, and large multimale, multifemale groups with promiscuous mating and fi ssion- fusion societies. In addition, some species are socially monogamous and polyandrous. Even closely related species may exhibit strikingly different social organizations, as the example of the squirrel monkeys demonstrates (Mitchell et al. 1991; Boinski et al. 2005b). New World monkey behavior varies within species as well as between them. While the behavior of many species is known from only one study site, intriguing patterns of intraspecific variation are beginning to emerge from observations of populations that sometimes live in close proximity. For example, spider monkeys are often described as showing sex- segregated ranging behavior. Several studies show that males range farther, travel faster, and use larger areas than females, who tend to restrict their habitual ranging to smaller core areas within a group’s large territory (Symington 1988; Chapman 1990; Shimooka 2005). In at least one well- studied population in Yasuní National Park, Ecuador, however, males and females both travel over the entire community home range, and different females within the community show little evidence of occupying distinct core areas (Spehar et al. 2010). Similarly, in most well- studied populations of spider monkeys, females disperse and the resident males within a group are presumed to be close relatives—a suggestion corroborated by genetic data for one local population of spider monkeys in Yasuní. Still, in a different local population, males are not closely related to one another, an unexpected pattern if signifi cant male philopatry were common (Di Fiore 2009; Di Fiore et al. 2009). While the causes of this local variation in group genetic structure are not clear, it may be signifi cant that the groups examined likely had different histories of contact with humans. For longlived animals who occupy relatively small social groups, the loss of even a handful of individuals to hunting, or to any other demographic disturbance, can have a dramatic impact on a group’s genetic structure. Intragroup social relationships, in turn, are likely to be infl uenced by patterns of intragroup relatedness and by the relative availability of social partners of different age or sex class (chapter 21, this volume). Thus, historical and demographic contingencies are likely to create conditions where considerable local, intrapopulation variation in social systems exists. Slight changes in ecological conditions may also contribute to variation in the behavior of individuals living in a single population over time. For example, some authors have hypothesized that howler monkey populations may undergo dramatic fluctuations in size and composition in response to several ecological factors, including resource abundance, parasite and predation pressure, and climate (Milton 1982; Crockett & Eisenberg 1986; Crockett 1996; Milton 1996; Rudran & Fernandez- Duque 2003). This variability, not only among populations, but also within populations across time highlights the need for long- term studies. In sum, our understanding of the behavior of New World monkeys has increased dramatically over the past 25 years. This understanding highlights how their behavior varies within populations over time and among populations or species across space. As our knowledge of platyrrhine behavior continues to unfold and is enriched via additional long- term studies, a central challenge will be to explain how these variations arise. It will be important to entertain adaptive explanations while acknowledging that some differences may emerge via stochastic changes in demography (Struhsaker 2008) or nongenetic, relatively short- term, nonadaptive responses to sudden ecological change

Increasing biomass in Amazonian forest plots

A previous study by Phillips et al. of changes in the biomass of permanent sample plots in Amazonian forests was used to infer the presence of a regional carbon sink. However, these results generated a vigorous debate about sampling and methodological issues. Therefore we present a new analysis of biomass change in old-growth Amazonian forest plots using updated inventory data. We find that across 59 sites, the above-ground dry biomass in trees that are more than 10 cm in diameter (AGB) has increased since plot establishment by 1.22 ± 0.43 Mg per hectare per year (ha-1 yr-1), where 1 ha = 104 m2), or 0.98 ± 0.38 Mg ha-1 yr-1 if individual plot values are weighted by the number of hectare years of monitoring. This significant increase is neither confounded by spatial or temporal variation in wood specific gravity, nor dependent on the allometric equation used to estimate AGB. The conclusion is also robust to uncertainty about diameter measurements for problematic trees: for 34 plots in western Amazon forests a significant increase in AGB is found even with a conservative assumption of zero growth for all trees where diameter measurements were made using optical methods and/or growth rates needed to be estimated following fieldwork. Overall, our results suggest a slightly greater rate of net stand-level change than was reported by Phillips et al. Considering the spatial and temporal scale of sampling and associated studies showing increases in forest growth and stem turnover, the results presented here suggest that the total biomass of these plots has on average increased and that there has been a regional-scale carbon sink in old-growth Amazonian forests during the previous two decades

Increasing dominance of large lianas in Amazonian forests

Ecological orthodoxy suggests that old-growth forests should be close to dynamic equilibrium, but this view has been challenged by recent findings that neotropical forests are accumulating carbon and biomass, possibly in response to the increasing atmospheric concentrations of carbon dioxide. However, it is unclear whether the recent increase in tree biomass has been accompanied by a shift in community composition. Such changes could reduce or enhance the carbon storage potential of old-growth forests in the long term. Here we show that non-fragmented Amazon forests are experiencing a concerted increase in the density, basal area and mean size of woody climbing plants (lianas). Over the last two decades of the twentieth century the dominance of large lianas relative to trees has increased by 1.7–4.6% a year. Lianas enhance tree mortality and suppress tree growth, so their rapid increase implies that the tropical terrestrial carbon sink may shut down sooner than current models suggest. Predictions of future tropical carbon fluxes will need to account for the changing composition and dynamics of supposedly undisturbed forests

Dieta, Forrajeo y Presupuesto de Tiempo en Cotoncillos (Callicebus discolor) del Parque Nacional Yasuní en la Amazonia Ecuatoriana

La subfamilia Callicebinae se encuentra representada por el género Callicebus, conocidos en Ecuador como cotoncillos o songo-songos (Tirira, 1999). La sistemática del género ha recibido importantes revisiones últimamente luego que Hershkovitz (1990) realizara una revisión taxonómica en la que llevó el número de especies de tres a 13 (Kinzey, 1981; de la Torre, 1998; Van Roosmalen et al., 2002). Actualmente, sólo dos especies del género se encuentran en Ecuador (C. lucifer y C. discolor, Van Roosmalen et al., 2002) y las mismas habitan el bosque lluvioso tropical amazónico (Extracto de la Introducción, el trabajo no tiene resumen)Fil: Carrillo Bilbao, Gabriel. Universidad Central del Ecuador; EcuadorFil: Di Fiore, Anthony. University of Texas at Austin; Estados UnidosFil: Fernandez Duque, Eduardo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Centro de Ecología Aplicada del Litoral. Universidad Nacional del Nordeste. Centro de Ecología Aplicada del Litoral; Argentina. University of Pennsylvania; Estados Unido

Quantifying uncertainty due to fission-fusion dynamics as a component of social complexity.

Groups of animals (including humans) may show flexible grouping patterns, in which temporary aggregations or subgroups come together and split, changing composition over short temporal scales, (i.e. fission and fusion). A high degree of fission-fusion dynamics may constrain the regulation of social relationships, introducing uncertainty in interactions between group members. Here we use Shannon's entropy to quantify the predictability of subgroup composition for three species known to differ in the way their subgroups come together and split over time: spider monkeys (Ateles geoffroyi), chimpanzees (Pan troglodytes) and geladas (Theropithecus gelada). We formulate a random expectation of entropy that considers subgroup size variation and sample size, against which the observed entropy in subgroup composition can be compared. Using the theory of set partitioning, we also develop a method to estimate the number of subgroups that the group is likely to be divided into, based on the composition and size of single focal subgroups. Our results indicate that Shannon's entropy and the estimated number of subgroups present at a given time provide quantitative metrics of uncertainty in the social environment (within which social relationships must be regulated) for groups with different degrees of fission-fusion dynamics. These metrics also represent an indirect quantification of the cognitive challenges posed by socially dynamic environments. Overall, our novel methodological approach provides new insight for understanding the evolution of social complexity and the mechanisms to cope with the uncertainty that results from fission-fusion dynamics

Fission-fusion dynamics: New research frameworks

Renewed interest in fission-fusion dynamics is due to the recognition that such dynamics may create unique challenges for social interaction and distinctive selective pressures acting on underlying communicative and cognitive abilities. New frameworks for integrating current knowledge on fission-fusion dynamics emerge from a fundamental rethinking of the term "fission-fusion" away from its current general use as a label for a particular modal type of social system (i.e., "fission-fusion societies"). Specifically, because the degree of spatial and temporal cohesion of group members varies both within and across taxa, any social system can be described in terms of the extent to which it expresses fission-fusion dynamics. This perspective has implications for socioecology, communication, cognitive demands, and human social evolution

Metagenomic analyses reveal previously unrecognized variation in the diets of sympatric Old World monkey species

Insectivory, or the consumption of insects and other arthropods, is a significant yet cryptic component of omnivorous primate diets. Here, we used high-throughput DNA sequencing to identify arthropods from fecal DNA and assess variation in insectivory by closely-related sympatric primates. We identified arthropod prey taxa and tested the hypothesis that variation in insectivory facilitates niche differentiation and coexistence among closely-related species with high dietary overlap. We collected 233 fecal samples from redtail (Cercopithecus ascanius; n = 118) and blue monkeys (C. mitis; n = 115) and used a CO1 metabarcoding approach to identify arthropod DNA in each fecal sample. Arthropod DNA was detected in 99% of samples (N = 223 samples), and a total of 68 families (15 orders) were identified. Redtails consumed arthropods from 54 families, of which 12 (21.8%) were absent from blue monkey samples. Blue monkeys consumed arthropods from 56 families, of which 14 (24.6%) were absent from redtail samples. For both species, &gt;97% of taxa present belonged to four orders (Araneae, Diptera, Hymenoptera, Lepidoptera). Redtail samples contained more Lepidoptera taxa (p&lt;0.05), while blue monkey samples contained more Araneae (p&lt;0.05). Blue monkeys consumed a greater diversity of arthropod taxa than redtail monkeys (p&lt;0.05); however, the average number of arthropod families present per fecal sample was greater in the redtail monkey samples (p&lt;0.05). These results indicate that while overlap exists in the arthropod portion of their diets, 20-25% of taxa consumed are unique to each group. Our findings suggest that variation in arthropod intake may help decrease dietary niche overlap and hence facilitate coexistence of closely-related primate species.</p

A note on comonotonicity and positivity of the control components of decoupled quadratic FBSDE

In this small note we are concerned with the solution of Forward-Backward Stochastic Differential Equations (FBSDE) with drivers that grow quadratically in the control component (quadratic growth FBSDE or qgFBSDE). The main theorem is a comparison result that allows comparing componentwise the signs of the control processes of two different qgFBSDE. As a byproduct one obtains conditions that allow establishing the positivity of the control process.Comment: accepted for publicatio

Double effort: parental behavior of wild Azara's owl monkeys in the face of twins

In species of mammals that habitually bear single offspring, like most anthropoid primates, the occurrence of twins is expected to impose considerable energetic costs on the caretakers. The question then arises of how caregivers cope with the potentially increased costs of raising twins. These increased costs should lead to differing developmental rates in twins when compared to singletons, and/or to changes in the caregivers' behavior. Likewise, time budgets of parents of singletons are expected to differ from those of adults without offspring. Additionally, if twinning was an adaptive response to favorable ecological conditions, it should be more likely in years with high food abundance. Following the birth in 2011 of two sets of twins in a wild population of pair-living Azara's owl monkeys (Aotus azarae) in Northern Argentina, we used long-term demographic, behavioral, and phenological data to compare a) the proportion of time that singleton and twin infants were carried by either parent, b) adult time-budgets and ranging behavior in groups with zero, one, or two infants, and c) the availability of food in 2011 with food availability in other years. Twins, like singletons, were carried nearly exclusively by the male, and they were carried slightly more than singletons, suggesting a relatively inflexible pattern of infant care in the species. Time budgets showed that twin parents foraged more and moved less than singleton parents or groups without infants, despite the fact that phenological data indicate that fruit availability in 2011 was not substantially higher than in some of the other years. Overall, twinning thus presumably increased costs to breeders, especially males, but its effect on animals’ long-term reproductive success remains unclear.National Science Foundation (BCS-1219368); National Geographic Society (9053-11); German Science Foundation (HU1746-2 & 3); het Vreedefonds; Stichting Fundatie van de Vrijvrouwe van Renswoude te‘s-Gravenhage; Stichting Jo Kolk Studiefonds; de Stichting dr.Hendrik Muller's VaderlandschFonds; Wenner-Gren Foundation; L.S.B. Leakey Foundation; National Science Foundation (BCS- 0621020); the University of Pennsylvania Research Foundation; Zoological Society of San Dieg

Variation in stem mortality rates determines patterns of above-ground biomass in Amazonian forests: implications for dynamic global vegetation models

Understanding the processes that determine above-ground biomass (AGB) in Amazonian forests is important for predicting the sensitivity of these ecosystems to environmental change and for designing and evaluating dynamic global vegetation models (DGVMs). AGB is determined by inputs from woody productivity [woody net primary productivity (NPP)] and the rate at which carbon is lost through tree mortality. Here, we test whether two direct metrics of tree mortality (the absolute rate of woody biomass loss and the rate of stem mortality) and/or woody NPP, control variation in AGB among 167 plots in intact forest across Amazonia. We then compare these relationships and the observed variation in AGB and woody NPP with the predictions of four DGVMs. The observations show that stem mortality rates, rather than absolute rates of woody biomass loss, are the most important predictor of AGB, which is consistent with the importance of stand size structure for determining spatial variation in AGB. The relationship between stem mortality rates and AGB varies among different regions of Amazonia, indicating that variation in wood density and height/diameter relationships also influences AGB. In contrast to previous findings, we find that woody NPP is not correlated with stem mortality rates and is weakly positively correlated with AGB. Across the four models, basin-wide average AGB is similar to the mean of the observations. However, the models consistently overestimate woody NPP and poorly represent the spatial patterns of both AGB and woody NPP estimated using plot data. In marked contrast to the observations, DGVMs typically show strong positive relationships between woody NPP and AGB. Resolving these differences will require incorporating forest size structure, mechanistic models of stem mortality and variation in functional composition in DGVMs