Cynthia L. Thompson

Within-group social bonds in white-faced saki monkeys (Pithecia pithecia) display male–female pair preference

White‐faced saki monkeys (Pithecia pithecia) lack most of the behavioral and physical traits typical of primate monogamy [Fuentes, 1999 ]. In order to determine if social bonds in this species reflect patterns displayed by pair‐bonded groups or larger multimale–multifemale groups, we draw on 17 months of data collected on wild white‐faced sakis at Brownsberg Nature Park, Suriname. We analyzed within‐group social bonds for three habituated groups (one two‐adult and two multiadult groups) by measuring grooming, proximity, and approach/leave patterns between adult and subadult group members. We found that both two‐adult and multiadult groups showed significantly stronger social bonds between a single male–female dyad within each group (deemed “primary dyads”). In all three groups, primary dyads were composed of the oldest adult male and a breeding female. These pairs had significantly higher levels of grooming than other within‐group dyads and were also in close proximity (<1 m) more often than nonprimary dyads. Grooming in primary dyads was nonreciprocal, and consistently biased toward female investment. Grooming patterns in nonprimary dyads varied, but were often more reciprocal. Grooming and proximity of the primary dyad also changed in relation to infant development. Our results suggest that while white‐faced sakis do not show behavioral and physical traits typical of monogamy or pair‐bonding, social bonds are strongest between a single male–female pair. Pitheciine social systems range from small group monogamy in Callicebus to large multimale–multifemale groups in Chiropotes and Cacajao. As the middle taxon in this platyrrhine radiation, behavioral strategies of white‐faced sakis provide a model for how social bonds and affiliation could be influenced by and affect the evolution of larger group size in primates. Am. J. Primatol. 73:1051–1061, 2011.

Telemetry System for Assessing Jaw-Muscle Function in Free-ranging Primates

In vivo laboratory-based studies describing jaw-muscle activity and mandibular bone strain during mastication provide the empirical basis for most evolutionary hypotheses linking primate masticatory apparatus form to diet. However, the laboratory data pose a potential problem for testing predictions of these hypotheses because estimates of masticatory function and performance recorded in the laboratory may lack the appropriate ecological context for understanding adaptation and evolution. For example, in laboratory studies researchers elicit rhythmic chewing using foods that may differ significantly from the diets of wild primates. Because the textural and mechanical properties of foods influence jaw-muscle activity and the resulting strains, chewing behaviors studied in the laboratory may not adequately reflect chewing behaviors of primates feeding in their natural habitats. To circumvent this limitation of laboratory-based studies of primate mastication, we developed a system for recording jaw-muscle electromyograms (EMGs) from free-ranging primates so that researchers can conduct studies of primate jaw-muscle function in vivo in the field. We used the system to record jaw-muscle EMGs from mantled howlers (Alouatta palliata) at Hacienda La Pacifica, Costa Rica. These are the first EMGs recorded from a noncaptive primate feeding in its natural habitat. Further refinements of the system will allow long-term EMG data collection so that researchers can correlate jaw-muscle function with food mechanical properties and behavioral observations. In addition to furthering understanding of primate feeding biology, our work will foster improved adaptive hypotheses explaining the evolution of primate jaw form.

Non-Monogamous Copulations and Potential Within-Group Mating Competition in White-Faced Saki Monkeys (Pithecia pithecia)

Many primates display within‐species variation in social organization and mating system. Individuals of these species may be confronted with both the challenges of between‐group competition to exclude same‐sex competitors as well as within‐group competition for mating opportunities. Free‐ranging white‐faced saki monkeys (Pithecia pithecia) live in both male–female pairs and small multi‐male, multi‐female groups. Despite commonly held views that this species is monogamous, there are currently no published accounts of mating patterns in the genus Pithecia. I recorded copulations and sexual behavior from three free‐ranging groups of white‐faced sakis at Brownsberg Naturepark, Suriname over a period of 17 months. Groups displayed both monogamous and polygynandrous mating. Individuals in polygynandrous groups were not observed to mate more frequently with certain partners. Copulation harassment occurred in 8.6% of copulations (total N = 81) and was performed by both sexes. This harassment successfully prevented ejaculation in six out of seven instances and harassment by males resulted in male–male aggression on four occasions. Two cases of female‐directed sexual aggression by males were also observed, which may indicate that males use sexual coercion to influence female mating behavior. Although based on a small number of groups, these data show that white‐faced sakis display variability in mating system and that this variability is not directly dictated by social organization. Furthermore, groups with promiscuous copulations exhibit behaviors indicative of within‐group mating competition. Am. J. Primatol. 75:817–824, 2013.

Why fight? Selective forces favoring between-group aggression in a variably pair-living primate, the white-faced saki (Pithecia pithecia)

Between-group aggression is a common feature of many group-living animals. Yet aggressive behaviors are often costly, involving risk of injury, increased energy expenditure and the potential to reduce feeding time. For aggression to be evolutionarily advantageous these costs must be outweighed by the benefits gained from exclusive access to resources and/or mates, or through committing infanticide. However, the dynamics favoring aggression in species living in small groups may differ from those in larger groups since mating exclusivity is higher and the potential to numerically dominate opponents is lower. We examined the selective factors influencing between-group aggression in a primate that lives in both pairs and small groups, the white-faced saki monkey (Pithecia pithecia). Data were collected on three free-ranging groups at Brownsberg Naturepark (Suriname) over 17 months. Intergroup encounter frequency and intensity of aggression during encounters were compared to temporal changes in diet, variation in ovarian hormones, frequency of copulations and the presence of dependent infants. Participation in between-group aggression was heavily male-biased and the presence of cycling females was a significant predictor of aggression frequency. Percentage of mesocarp in the diet also had a significant effect on the frequency and the intensity of aggression, with high mesocarp consumption corresponding to increased aggression. Presence of dependent infants did not affect between-group aggression. Our results support both the male mate defense and male resource defense hypotheses, suggesting that male reproductive interests are the principle selective pressures acting on between-group aggression in white-faced sakis. White-faced sakis’ rigid conformity to traditional expectations of male intrasexual intolerance appears to be unique among primates living in small groups with variable mating systems.

Terrestrial Activity in Pitheciins (Cacajao, Chiropotes, and Pithecia)

Neotropical monkeys of the genera Cacajao, Chiropotes, and Pithecia (Pitheciidae) are considered to be highly arboreal, spending most of their time feeding and traveling in the upper canopy. Until now, the use of terrestrial substrates has not been analyzed in detail in this group. Here, we review the frequency of terrestrial use among pitheciin taxa to determine the ecological and social conditions that might lead to such behavior. We collated published and unpublished data from 14 taxa in the three genera. Data were gleaned from 53 published studies (including five on multiple pitheciin genera) and personal communications of unpublished data distributed across 31 localities. Terrestrial activity was reported in 61% of Pithecia field studies (11 of 18), in 34% of Chiropotes studies (10 of 29), and 36% of Cacajao studies (4 of 11). Within Pithecia, terrestrial behavior was more frequently reported in smaller species (e.g. P. pithecia) that are vertical clingers and leapers and make extensive use of the understory than in in the larger bodied canopy dwellers of the western Amazon (e.g. P. irrorata). Terrestrial behavior in Pithecia also occurred more frequently and lasted longer than in Cacajao or Chiropotes. An apparent association was found between flooded habitats and terrestrial activity and there is evidence of the development of a “local pattern” of terrestrial use in some populations. Seasonal fruit availability also may stimulate terrestrial behavior. Individuals also descended to the ground when visiting mineral licks, escaping predators, and responding to accidents such as a dropped infant. Overall, the results of this review emphasize that terrestrial use is rare among the pitheciins in general and is usually associated with the exploitation of specific resources or habitat types. Am. J. Primatol. 74:1106‐1127, 2012.

The influence of experimental manipulations on chewing speed during in vivo laboratory research in tufted capuchins (Cebus apella)

Even though in vivo studies of mastication in living primates are often used to test functional and adaptive hypotheses explaining primate masticatory behavior, we currently have little data addressing how experimental procedures performed in the laboratory influence mastication. The obvious logistical issue in assessing how animal manipulation impacts feeding physiology reflects the difficulty in quantifying mechanical parameters without handling the animal. In this study, we measured chewing cycle duration as a mechanical variable that can be collected remotely to: 1) assess how experimental manipulations affect chewing speed in Cebus apella, 2) compare captive chewing cycle durations to that of wild conspecifics, and 3) document sources of variation (beyond experimental manipulation) impacting captive chewing cycle durations. We find that experimental manipulations do increase chewing cycle durations in C. apella by as much as 152 milliseconds (ms) on average. These slower chewing speeds are mainly an effect of anesthesia (and/or restraint), rather than electrode implantation or more invasive surgical procedures. Comparison of captive and wild C. apella suggest there is no novel effect of captivity on chewing speed, although this cannot unequivocally demonstrate that masticatory mechanics are similar in captive and wild individuals. Furthermore, we document significant differences in cycle durations due to inter-individual variation and food type, although duration did not always significantly correlate with mechanical properties of foods. We advocate that the significant reduction in chewing speed be considered as an appropriate qualification when applying the results of laboratory-based feeding studies to adaptive explanations of primate feeding behaviors.

Spatial Distribution and Exploitation of Trees Gouged by Common Marmosets (Callithrix jacchus)

Resource distribution shapes many aspects of primate behavioral ecology. Though the spatial patterning of fruits, leaves, and insects has been explored among primate foods, comparatively less is known about exudate distributions. Tree exudates are a renewable resource, provide long-term evidence of exploitation, and may be selectively exploited to manipulate spatial distribution. We assessed the spatial patterning of trees gouged by common marmosets (Callithrix jacchus) to determine if they exhibit a uniform, random, or clumped distribution. We also asked whether marmosets selectively gouge trees in home range centers, which may afford them exclusive access to exudates. We explored whether spatial or physical characteristics of trees predict how intensely gouged trees were exploited. The mean nearest neighbor distance of gouged trees was significantly closer than expected for a random distribution and Ripley’s K-function showed that gouged trees were clumped across all spatial scales in our study area. Clumping may enable marmosets to reduce day and home ranges and facilitate repeated gouging of trees. Gouged trees were not closer to marmosets’ home range centers than peripheries, nor were centrally located trees more intensely gouged. Increased gouging intensity was associated with larger tree circumferences, although this effect was primarily driven by interspecific differences in circumference. Although marmosets may benefit from exploiting clumped exudates, they do not concentrate gouging in areas where they are more likely to gain exclusive access. Species-specific tree characteristics such as exudate quality and/or bark properties may play a larger role in determining gouging patterns than intergroup feeding competition.

To Pair or Not To Pair: Sources of Social Variability with White-Faced Saki Monkeys (Pithecia Pithecia) As a Case Study

Intraspecific variability in social systems is gaining increased recognition in primatology. Many primate species display variability in pair‐living social organizations through incorporating extra adults into the group. While numerous models exist to explain primate pair‐living, our tools to assess how and why variation in this trait occurs are currently limited. Here I outline an approach which: (i) utilizes conceptual models to identify the selective forces driving pair‐living; (ii) outlines novel possible causes for variability in social organization; and (iii) conducts a holistic species‐level analysis of social behavior to determine the factors contributing to variation in pair‐living. A case study on white‐faced sakis (Pithecia pithecia) is used to exemplify this approach. This species lives in either male‐female pairs or groups incorporating “extra” adult males and/or females. Various conceptual models of pair‐living suggest that high same‐sex aggression toward extra‐group individuals is a key component of the white‐faced saki social system. Variable pair‐living in white‐faced sakis likely represents alternative strategies to achieve competency in this competition, in which animals experience conflicting selection pressures between achieving successful group defense and maintaining sole reproductive access to mates. Additionally, independent decisions by individuals may generate social variation by preventing other animals from adopting a social organization that maximizes fitness. White‐faced saki inter‐individual relationships and demographic patterns also lend conciliatory support to this conclusion. By utilizing both model‐level and species‐level approaches, with a consideration for potential sources of variation, researchers can gain insight into the factors generating variation in pair‐living social organizations. Am. J. Primatol. 78:561–572, 2016.

Observations of hand preference in wild groups of white-faced sakis (Pithecia pithecia) in Suriname.

Hand preference is well observed in humans and some primates. Unlike many other primates, however, humans show a consistent hand preference across a variety of tasks, and a distinct right‐handed skew at the population level. Although there are a moderate number of published studies, primate hand preference literature is unbalanced by the large number of studies on only a few species. No previous studies have addressed hand preference in white‐faced sakis (WFS; Pithecia pithecia). We followed three habituated groups of wild WFS in Suriname and recorded individual hand preference for six different manual behaviors. There was no consistent hand preference across a range of uni‐manual behaviors for any individual. Likewise, there were significantly more ambidextrous individuals in the population than expected (χ2(df = 2) = 11.2, P = 0.004) and thus, no population level hand preference. Our findings contribute baseline data to the debate of primate hand lateralization, and support the notion that lateralization of hand function does not characterize all species. Am. J. Primatol. 73:655–664, 2011.

Geographic comparison of plant genera used in frugivory among the pitheciids Cacajao, Callicebus, Chiropotes, and Pithecia.

Pitheciids are known for their frugivorous diets, but there has been no broad‐scale comparison of fruit genera used by these primates that range across five geographic regions in South America. We compiled 31 fruit lists from data collected from 18 species (three Cacajao, six Callicebus, five Chiropotes, and four Pithecia) at 26 study sites in six countries. Together, these lists contained 455 plant genera from 96 families. We predicted that 1) closely related Chiropotes and Cacajao would demonstrate the greatest similarity in fruit lists; 2) pitheciids living in closer geographic proximity would have greater similarities in fruit lists; and 3) fruit genus richness would be lower in lists from forest fragments than continuous forests. Fruit genus richness was greatest for the composite Chiropotes list, even though Pithecia had the greatest overall sampling effort. We also found that the Callicebus composite fruit list had lower similarity scores in comparison with the composite food lists of the other three genera (both within and between geographic areas). Chiropotes and Pithecia showed strongest similarities in fruit lists, followed by sister taxa Chiropotes and Cacajao. Overall, pitheciids in closer proximity had more similarities in their fruit list, and this pattern was evident in the fruit lists for both Callicebus and Chiropotes. There was no difference in the number of fruit genera used by pitheciids in habitat fragments and continuous forest. Our findings demonstrate that pitheciids use a variety of fruit genera, but phylogenetic and geographic patterns in fruit use are not consistent across all pitheciid genera. This study represents the most extensive examination of pitheciid fruit consumption to date, but future research is needed to investigate the extent to which the trends in fruit genus richness noted here are attributable to habitat differences among study sites, differences in feeding ecology, or a combination of both. Am. J. Primatol. 78:493–506, 2016.