Scott A. Suarez

Route-based travel and shared routes in sympatric spider and woolly monkeys: cognitive and evolutionary implications.

Many wild primates occupy large home ranges and travel long distances each day. Navigating these ranges to find sufficient food presents a substantial cognitive challenge, but we are still far from understanding either how primates represent spatial information mentally or how they use this information to navigate under natural conditions. In the course of a long-term socioecological study, we investigated and compared the travel paths of sympatric spider monkeys (Ateles belzebuth) and woolly monkeys (Lagothrix poeppigii) in Amazonian Ecuador. During several field seasons spanning an 8-year period, we followed focal individuals or groups of both species continuously for periods of multiple days and mapped their travel paths in detail. We found that both primates typically traveled through their home ranges following repeatedly used paths, or “routes”. Many of these routes were common to both species and were stable across study years. Several important routes appeared to be associated with distinct topographic features (e.g., ridgetops), which may constitute easily recognized landmarks useful for spatial navigation. The majority of all location records for both species fell along or near identified routes, as did most of the trees used for fruit feeding. Our results provide strong support for the idea that both woolly and spider monkey use route-based mental maps similar to those proposed by Poucet (Psychol Rev 100:163–182, 1993). We suggest that rather than remembering the specific locations of thousands of individual feeding trees and their phenological schedules, spider and woolly monkeys could nonetheless forage efficiently by committing to memory a series of route segments that, when followed, bring them into contact with many potential feeding sources for monitoring or visitation. Furthermore, because swallowed and defecated seeds are deposited in greater frequency along routes, the repeated use of particular travel paths over generations could profoundly influence the structure and composition of tropical forests, raising the intriguing possibility that these and other primate frugivores are active participants in constructing their own ecological niches. Building upon the insights of Byrne (Q J Exp Psychol 31:147–154, 1979, Normality and pathology in cognitive functions. Academic, London, pp 239–264, 1982) and Milton (The foraging strategy of howler monkeys: a study in primate economics. Columbia University Press, New York, 1980, On the move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 375–417, 2000), our results highlight the likely general importance of route-based travel in the memory and foraging strategies of nonhuman primates.

A Multi-Forest Comparison of Dietary Preferences and Seed Dispersal by Ateles spp.

Investigations of coevolutionary relationships between plants and the animals that disperse their seeds suggest that disperser-plant interactions are likely shaped by diffuse, rather than species-to-species, coevolution. We studied the role of dietary plasticity in shaping the potential for diffuse coevolution by comparing dietary fruit preferences and seed dispersal by 3 species of spider monkeys (Ateles spp.) in 4 moist forests in Colombia, Ecuador, Panama, and Surinam. In all forests, spider monkeys were highly frugivorous and preyed upon seeds of few species. We estimated dietary use of fruiting taxa based on absolute consumption and preference, which accounts for resource availability. Of the 59 genera that comprised the 20 most frequently consumed genera summed in each forest, only 3—Brosimum (Moraceae), Cecropia (Cecropiaceae) and Virola (Myristicaceae)—ranked within the top 20 at every forest. Most genera were within the 20 most frequently consumed at only 1 or 2 forests. Based on preferences, only 4 genera ranked in the 20 most-preferred in all 4 forests: Brosimum, Cecropia, Ficus (Moracae), and Virola. Patterns in fruit consumption and preference at the familial level were similar in that only 2 families—Myristicaceae and Moraceae—were in the 10 most-consumed or most-preferred in all 4 forests. Interforest variation in plant specific composition and abundances and supra-annual fruiting phenologies, combined with dietary flexibility of Ateles spp., may partly explain these patterns. Our results suggest that variation in plant community structure strongly influences dietary preferences, and hence, seed dispersal by spider monkeys. Thus, diffuse coevolution in spider monkey-plant relationships may be limited to few taxa at the generic and familial levels.

Enrichment effects on rhesus monkeys successively housed singly, in pairs, and in groups

Abstract Many studies have examined the short-term effects of inanimate environmental enrichment on the behavior of captive primates. Similarly, numerous studies have examined the behavioral effects of manipulations to the social environment. Few analyses have examined the long-term effects of inanimate environmental enrichment or compared the effects of inanimate and social enhancements. The behavior of control ( n = 49) and enriched ( n = 44) rhesus monkeys ( Macaca mulatta ) was observed from 1–4 years, as subjects spent successive years housed singly, in paris, and then in small groups. Social housing condition and/or age of subject significantly affected time spent inactive, grooming, playing, exploring, and behaving abnormally. Frequency of vocalization was similarly affected. Social housing resulted in more species-typical behavior patterns than did single caging. Subjects were more socially oriented when pair-housed than when living in small groups. Inanimate enrichment did not affect behavior over a 3 year period, although enhancements were well-used by singly-caged yearlings and pair-housed juveniles. Subjects used enrichment less frequently when housed in groups. The data suggest that the presence of a social partner(s) led to more beneficial changes in behavior than did the provision of inanimate enhancements for rhesus monkeys in the studied age range. Therefore, it is concluded that social enrichment should be provided when possible and appropriate. Efforts to enrich the inanimate environment will be most beneficial when focused on socially-restricted primates.

Effects of social and inanimate enrichment on the behavior of yearling rhesus monkeys

Certain types of inanimate environmental enrichment have been shown to positively affect the behavior of laboratory primates, as has housing them in appropriate social conditions. While social housing is generally advocated as an important environmental enhancement, few studies have attempted to measure the influence of social conditions on the effects of inanimate enrichment or to compare the relative merits of social and inanimate enhancements. In the present study, inanimate enrichment (predominately physical and feeding enhancements) resulted in increased species‐typical behavior for socially restricted subjects. However, social enrichment (living in groups) appeared to be more beneficial for young rhesus monkeys, leading to increased species‐typical activities and decreased abnormal activities. The behavior of one cohort of yearling rhesus monkeys (Macaca mulatta) housed in small peer groups was compared with the behavior of four yearling cohorts housed in single cages. Half the animals in each cohort received a three‐phase enrichment program and the rest served as controls. Group‐housed yearlings spent significantly more time feeding and exploring and significantly less time behaving abnormally, self‐grooming, and drinking than did singly housed yearlings. Enriched subjects spent significantly more time playing by themselves, and significantly less time self‐grooming and exploring than did controls. Among group‐housed subjects only, there were no differences between enriched and control monkeys. Captive primates should be housed socially, whenever appropriate, as the first and most important step in an enrichment program, with the provision of inanimate enhancements being considerably less important. Limited resources for inanimate enrichment programs instead should be focused on those individuals who can not be housed socially.

The Impact of Geophagy on Ranging Behaviour in Phayre’s Leaf Monkeys (Trachypithecus phayrei)

Resource use is known to influence the ranging behaviour of primates, and this effect may be pronounced when the resource is uncommon in the environment. Here we investigate the effect of geophagy on the ranging behaviour of Phayre’s leaf monkeys (Trachypithecus phayrei) in the Phu Khieo Wildlife Sanctuary, Thailand. UTM coordinates were collected via GPS from the group centre every 30 min during all-day follows of one study group over a 4-month period. On days during which the group visited a distant saltlick (n = 3), the monkeys travelled significantly further (p < 0.001), significantly faster (p < 0.001) and with fewer stops compared to non-saltlick days (n = 61). Saltlick visits also increased the home range size from 73.7 ha to 93.4 ha. Increased daily path length, increased travel speed and consistent pace are necessary because of the distance from the saltlick to the regularly used portion of the home range, and these reflect the import- ance of soil consumption to the leaf monkeys.

The behavior of singly-caged, yearling rhesus monkeys is affected by the environment outside of the cage

Abstract Numerous studies have demonstrated that the behavior of singly caged laboratory primates can be positively affected by inanimate enrichment within the cage. The environment outside of the cage may also influence the behavior of singly caged rhesus monkeys. To test this, we compared two cohorts of yearling rhesus ( Macaca mulatta ); one that had only limited stimulation in the environment outside of the cage (singly caged in indoor rooms), and one that had considerable naturalistic and social stimulation in the extra-cage environment (singly caged in an outdoor building). Half the animals in each housing condition received a three-phase enrichment program and the rest served as controls. Subjects that had sensory access to social groups of conspecifics spent significantly more time drinking, feeding, and behaving abnormally, and significantly less time inactive and playing than did subjects that only had sensory access to other singly caged rhesus. Enriched subjects in both settings spent significantly more time playing and less time self-grooming than did controls. There was also a significant interaction for time spent in play, with enriched subjects living indoors playing the most. Although subjects that received considerable stimulation from outside of the cage spent more time engaged in abnormal behavior, most was pacing; usually in response to human manipulations of the other monkeys in the colony. Subjects housed indoors, with limited extra-cage stimulation spent less time pacing, but more time in potentially injurious abnormal activities. Among enriched subjects only, those housed indoors spent less time drinking and behaving abnormally and more time playing and using enrichment. Inanimate enrichment within the cage led to consistent positive changes in behavior for singly housed rhesus. Although the environment outside of the cage was shown to influence behavior, it was not clear whether exposure to numerous social and naturalistic stimuli was preferable to more limited stimulation for promoting well-being. Although the increased stimulation associated with a complex extra-cage environment is usually considered beneficial, not all such stimulation is positive. Frequent disturbances to social groups in view of singly caged subjects resulted in increased pacing, but the complex extra-cage environment also provided subjects with more opportunities to express and observe components of the species-typical behavioral repertoire.

Ecological factors predictive of wild spider monkey (Ateles belzebuth) foraging decisions in Yasuní, Ecuador.

Because fruiting trees are uncommon in tropical forests, frugivorous primates experience selective pressure to incorporate knowledge of where to find feeding trees, what to expect when they arrive there, and when they can return after depleting a tree. I investigated these abilities in wild spider monkeys (Ateles belzebuth) in Yasuní, Ecuador, by analyzing the characteristics of feeding trees that drive foraging decisions. Foraging data were derived from four 2‐week follows of focal adult females, conducted between May and December 1999, during which I measured and mapped all trees in which the focal subject fed, feeding bout duration, and the number of conspecifics feeding simultaneously with the focal. Taking into account the order in which feeding trees were visited across each follow, I analyzed each foraging decision from the second week of a follow, treating all previously visited trees as options for visits. I scored each option tree in terms of nine ecological variables, including the distance from the decision to each location tree, DBH, recent feeding time and mean feeding times for the focal and other monkeys present, and the interval in hours between the foraging decision and the most recent visit to each option tree. I then examined the predictive strength of the model using logistic regression analysis, comparing characteristics of selected trees to those not selected. The overall model successfully predicted trees selected by focal monkeys (r2 = 0.27). Monkeys preferentially moved to nearby, large canopy trees, in which previous feeding success was high, and which were visited after an interval of 3.5 days. Interval mattered most for medium and large trees, but did not predict selection for trees <10 cm DBH. Despite the large home range and large numbers of trees, Yasuní spider monkeys appeared to integrate spatial, value, and temporal information when deciding where to feed. Am. J. Primatol. 76:1185–1195, 2014.

A comparison of computer-generated and naturally occurring foraging patterns in route-network-constrained spider monkeys.

The attribution of goal‐directed behavior to observations of primate foraging and ranging requires that simpler explanations for observed behavior patterns be eliminated. Computer‐generated simulations of non‐goal‐directed foraging behavior can be used as null models for higher complexity cognitive foraging, and can provide quantifiable data against which to compare the observed behavioral patterns in wild primates. In this paper, we compare the results of two variations of computer simulated null models with observed foraging behavior of wild spider monkeys (Ateles belzebuth). One model simulates monkeys searching using a modified random‐walk model in which monkeys alternate 100‐m steps with turn angles derived from observed behavior. The second model constrains travel to an observed route system derived from observations of wild spider monkeys. Simulated monkeys in each model searched among increasing densities of feeding trees ranging from 10 to 1,000. We compared travel distance, travel directness, and accuracy of starting direction for each feeding tree discovered for the two models. We then compared these results with those derived from observations of wild spider monkeys. Route‐model monkeys traveled shorter distances and more directly to feeding trees than did randomly foraging monkeys, and discovered trees in the direction they started more often. Observed spider monkeys outperformed simulated monkeys from both models in all variables, allowing us to reject the null hypothesis that observed foraging and ranging behavior could be explained by non‐goal‐directed travel. Am. J. Primatol. 76:460–471, 2014.

Personality assessment and model comparison with behavioral data: A statistical framework and empirical demonstration with bonobos (Pan paniscus)

Interest in quantifying consistent among‐individual variation in primate behavior, also known as personality, has grown rapidly in recent decades. Although behavioral coding is the most frequently utilized method for assessing primate personality, limitations in current statistical practice prevent researchers’ from utilizing the full potential of their coding datasets. These limitations include the use of extensive data aggregation, not modeling biologically relevant sources of individual variance during repeatability estimation, not partitioning between‐individual (co)variance prior to modeling personality structure, the misuse of principal component analysis, and an over‐reliance upon exploratory statistical techniques to compare personality models across populations, species, and data collection methods. In this paper, we propose a statistical framework for primate personality research designed to address these limitations. Our framework synthesizes recently developed mixed‐effects modeling approaches for quantifying behavioral variation with an information‐theoretic model selection paradigm for confirmatory personality research. After detailing a multi‐step analytic procedure for personality assessment and model comparison, we employ this framework to evaluate seven models of personality structure in zoo‐housed bonobos (Pan paniscus). We find that differences between sexes, ages, zoos, time of observation, and social group composition contributed to significant behavioral variance. Independently of these factors, however, personality nonetheless accounted for a moderate to high proportion of variance in average behavior across observational periods. A personality structure derived from past rating research receives the strongest support relative to our model set. This model suggests that personality variation across the measured behavioral traits is best described by two correlated but distinct dimensions reflecting individual differences in affiliation and sociability (Agreeableness) as well as activity level, social play, and neophilia toward non‐threatening stimuli (Openness). These results underscore the utility of our framework for quantifying personality in primates and facilitating greater integration between the behavioral ecological and comparative psychological approaches to personality research.