Wild capuchin monkeys anticipate the amount of ripe fruit in natural trees.

Tropical forests have a high diversity of tree species which have very low densities and vary across time in their seasons of peak fruiting and maturation rates. As evidence of the ability of primates to track or anticipate changes in fruit production at individual trees, researchers have used the increased speed of primate groups toward more rewarding food patches. We analyzed the speed of approach to natural trees of wild capuchin monkeys under the effect of scramble competition, after excluding any plausible visual, olfactory and auditory cues. We conducted all-day group follows of three habituated capuchin groups at Iguazú National Park, Argentina, collecting data on ranging behavior and patterns of visits to fruit trees in relation with their location and fruit availability. Travel speed varied according to the expected reward at a feeding tree, increasing as rewards increased from low values, but decreasing again at very high values. Also, travel speed varied with time of day, decreasing from the time of first activity as the monkeys became less hungry, and increasing again toward late afternoon. Measures of unripe fruit cover did not explain variation in travel speed at any distance from a focal tree. Our data imply that, after excluding sensory cues, capuchins appear to anticipate time-varying ripe fruit quantity of natural resources, suggesting that they use memory of tree location and anticipation of fruit maturation. We also confirm that speed is a good measure about expectations of resources, as has been shown in previous studies.

How far do Neotropical primates disperse seeds?

Seed dispersal distance (SDD) is a vital component of vertebrate-mediated seed dispersal process: the average distance at which seeds are deposited away from the parent plant represents the starting template of plant regeneration. We present a simple model to explain and predict observed measures of average dispersal distance and we hypothesize that it is a consequence of how long seeds are retained in the disperser's gut, how rapidly the disperser moves per unit time and how twisted the animal travel path is relative to the straight-line distance moved away from the seed source. We retrieved data on dispersal distances from 26 published studies including nine primate species dispersing up to 112 plant species per study. We used gut transit time (TT) as a proxy for residence time inside the gut, the disperser's travel path per hour as proxy for movement rate, and the daily path length relative to the home range area as a correlate of path twisting (PT). We illustrate this model with comparative data on Neotropical primates. These three variables explained 90% of the variation in the average SDD. Path analysis indicates that additional variables exerted only indirect effects. Our model can be applied to primate populations for which detailed seed dispersal data are missing, and help evaluate conservation priorities for primate species according to the potential service they provide in terms of forest regeneration.

Capuchins, space, time and memory: an experimental test of what-where-when memory in wild monkeys.

There is considerable controversy about the existence, extent and adaptive value of integrated multimodal memory in non-human animals. Building on prior results showing that wild capuchin monkeys in Argentina appear to recall both the location and amount of food at patches they had previously visited, I tested whether they also track and use elapsed time as a basis for decisions about which feeding patches to visit. I presented them with an experimental array of eight feeding sites, at each of which food rewards increased with increasing elapsed time since the previous visit, similar to the pattern of ripe fruit accumulation in natural feeding trees. Over the course of 68 days, comprising two distinct renewal rate treatments, one group repeatedly visited sites in the feeding array, generating 212 valid choices between sites. Comparison of observations against simulated movements and multinomial statistical models shows that the monkeys' choices were most consistent with dynamic memory for elapsed time specific to each of the eight sites. Thus, it appears that capuchin monkeys possess and use integrated memories of prior food patch use, including where the patch is relative to their current location, how productive the patch is and how long it has been since they last visited the patch. Natural selection to use such integrated memories in foraging tasks may provide an ecologically relevant basis for the evolution of complex intelligence in primates.

Death of the (traveling) salesman: primates do not show clear evidence of multi-step route planning.

Several comparative studies have linked larger brain size to a fruit-eating diet in primates and other animals. The general explanation for this correlation is that fruit is a complex resource base, consisting of many discrete patches of many species, each with distinct nutritional traits, the production of which changes predictably both within and between seasons. Using this information to devise optimal spatial foraging strategies is among the most difficult problems to solve in all of mathematics, a version of the famous Traveling Salesman Problem. Several authors have suggested that primates might use their large brains and complex cognition to plan foraging strategies that approximate optimal solutions to this problem. Three empirical studies have examined how captive primates move when confronted with the simplest version of the problem: a spatial array of equally valuable goals. These studies have all concluded that the subjects remember many food source locations and show very efficient travel paths; some authors also inferred that the subjects may plan their movements based on considering combinations of three or more future goals at a time. This analysis re-examines critically the claims of planned movement sequences from the evidence presented. The efficiency of observed travel paths is largely consistent with use of the simplest of foraging rules, such as visiting the nearest unused "known" resource. Detailed movement sequences by test subjects are most consistent with a rule that mentally sums spatial information from all unused resources in a given trial into a single "gravity" measure that guides movements to one destination at a time.

Primate socioecology at the crossroads: past, present, and future.

Attempts to explain differences in the size and structure of primate groups have argued that they are a consequence of variation in the intensity of feeding competition caused by contrasts in food distribution. However, although feeding competition can limit the size of female groups, many other factors affect the costs and the benefits of sociality to females and contribute to differences in group size. Moreover, interspecific differences in social relationships between females, in female philopatry, and in kinship between group members appear to be more closely associated with variation in life-history parameters, reproductive strategies, and phylogeny than with contrasts in food distribution or feeding competition. The mismatch between predictions of socioecological theory and observed variation in primate social behavior has led to protracted arguments about the future of primate socioecology. We argue that future attempts to understand the diversity of primate societies need to be based on an approach that explores separate explanations for different components of social organization, combines ecological and phylogenetic information, and integrates research on primates with similar studies of other groups of mammals.

Anointing variation across wild capuchin populations: a review of material preferences, bout frequency and anointing sociality in Cebus and Sapajus.

The frequency of anointing bouts and the materials used for self- and social anointing vary across capuchin species in captivity, but there is little published data on capuchin anointing in the wild. Here we present previously unpublished data on anointing behaviors from capuchin monkey populations at ten different field sites and incorporate these data into a review of the anointing literature for captive and wild capuchins. Using a comparative phylogenetic framework, we test four hypotheses derived primarily from captive literature for variation in anointing between wild untufted capuchins (Cebus) and tufted capuchins (Sapajus), including that (1) the frequency of anointing is higher in Cebus, (2) Cebus uses a higher proportion of plant species to insect species for anointing compared with Sapajus, (3) anointing material diversity is higher in Cebus, and (4) social indices of anointing are higher in Cebus. We found that wild Cebus anoints more with plant parts, including fruits, whereas wild Sapajus anoints more with ants and other arthropods. Cebus capucinus in particular uses more plant species per site for anointing compared with other capuchins and may specialize in anointing as an activity independent from foraging, whereas most other capuchin species tend to eat the substances they use for anointing. In agreement with captive studies, we found evidence that wild Cebus anoints at a significantly higher frequency than Sapajus. However, contrary to the captive literature, we found no difference in the range of sociality for anointing between Cebus and Sapajus in the wild. We review anointing in the context of other Neotropical primate rubbing behaviors and consider the evidence for anointing as self-medication; as a mechanism for enhanced sociality; and as a behavioral response to chemical stimuli.

Experimental evidence for route integration and strategic planning in wild capuchin monkeys.

Both in captivity and the wild, primates are found to travel mostly to the nearest available resource, but they may skip over the closest resource and travel to more distant resources, which are often found to be more productive. This study examines the tradeoff between distance and reward in the foraging choices of one group of wild capuchin monkeys (Cebus apella nigritus) using feeding platforms in large-scale foraging experiments conducted over four years. Three feeding sites were arrayed in an oblique triangle, such that once the monkey group had chosen one site to feed, they had a choice between two remaining sites, a close one with less food and the other up to 2.3 times as far away but with more food. Sites were provisioned once per day. The capuchins generally chose the closer feeding site, even when the more distant site offered up to 12 times as much food. The distances to, rewards of, or various profitability measures applied to each alternative site individually did not explain the group's choices in ways consistent with foraging theory or principles of operant psychology. The group's site choices were predicted only by comparing efficiency measures of entire foraging pathways: (1) direct travel to the more rewarding distant site, versus (2) the longer 'detour' through the closer site on the way to the more distant one. The group chose the detour more often when the reward was larger and the added detour distance shorter. They appeared to be more sensitive to the absolute increase in detour distance than to the relative increase compared to the straight route. The qualitative and quantitative results agree with a simple rule: do not use the detour unless the energy gain from extra food outweighs the energy cost of extra travel. These results suggest that members of this group integrate information on spatial location, reward, and perhaps potential food competition in their choice of multi-site foraging routes, with important implications for social foraging.

What wild primates know about resources: opening up the black box.

We present the theoretical and practical difficulties of inferring the cognitive processes involved in spatial movement decisions of primates and other animals based on studies of their foraging behavior in the wild. Because the possible cognitive processes involved in foraging are not known a priori for a given species, some observed spatial movements could be consistent with a large number of processes ranging from simple undirected search processes to strategic goal-oriented travel. Two basic approaches can help to reveal the cognitive processes: (1) experiments designed to test specific mechanisms; (2) comparison of observed movements with predicted ones based on models of hypothesized foraging modes (ideally, quantitative ones). We describe how these two approaches have been applied to evidence for spatial knowledge of resources in primates, and for various hypothesized goals of spatial decisions in primates, reviewing what is now established. We conclude with a synthesis emphasizing what kinds of spatial movement data on unmanipulated primate populations in the wild are most useful in deciphering goal-oriented processes from random processes. Basic to all of these is an estimate of the animal's ability to detect resources during search. Given knowledge of the animal's detection ability, there are several observable patterns of resource use incompatible with a pure search process. These patterns include increasing movement speed when approaching versus leaving a resource, increasingly directed movement toward more valuable resources, and directed travel to distant resources from many starting locations. Thus, it should be possible to assess and compare spatial cognition across a variety of primate species and thus trace its ecological and evolutionary correlates.

Integrating information about location and value of resources by white-faced saki monkeys (Pithecia pithecia).

Most studies of spatial memory in primates focus on species that inhabit large home ranges and have dispersed, patchy resources. Researchers assume that primates use memory to minimize distances traveled between resources. We investigated the use of spatial memory in a group of six white-faced sakis (Pithecia pithecia) on 12.8-ha Round Island, Guri Lake, Venezuela during a period of fruit abundance. The sakis' movements were analyzed with logistic regressions, a predictive computer model and a computer model that simulates movements. We considered all the resources available to the sakis and compared observed distances to predicted distances from a computer model for foragers who know nothing about the location of resources. Surprisingly, the observed distances were four times greater than the predicted distances, suggesting that the sakis passed by a majority of the available fruit trees without feeding. The odds of visiting a food tree, however, were significantly increased if the tree had been visited in the previous 3 days and had more than 100 fruit. The sakis' preferred resources were highly productive fruit trees, Capparis trees, and trees with water holes. They traveled efficiently to these sites. The sakis choice of feeding sites indicate that they combined knowledge acquired by repeatedly traveling through their home range with 'what' and 'where' information gained from individual visits to resources. Although the sakis' foraging choices increased the distance they traveled overall, choosing more valued sites allowed the group to minimize intra-group feeding competition, maintain intergroup dominance over important resources, and monitor the state of resources throughout their home range. The sakis' foraging decisions appear to have used spatial memory, elements of episodic-like memory and social and nutritional considerations.

A socioecological perspective on primate cognition, past and present.

The papers in this special issue examine the relationship between social and ecological cognition in primates. We refer to the intersection of these two domains as socioecological cognition. Examples of socioecological cognition include socially learned predator alarm calls and socially sensitive foraging decisions. In this review we consider how primate cognition may have been shaped by the interaction of social and ecological influences in their evolutionary history. The ability to remember distant, out-of-sight locations is an ancient one, shared by many mammals and widespread among primates. It seems some monkeys and apes have evolved the ability to form more complex representations of resources, integrating "what-where-how much" information. This ability allowed anthropoids to live in larger, more cohesive groups by minimizing competition for limited resources between group members. As group size increased, however, competition for resources also increased, selecting for enhanced social skills. Enhanced social skills in turn made a more sophisticated relationship to the environment possible. The interaction of social and ecological influences created a spiraling effect in the evolution of primate intelligence. In contrast, lemurs may not have evolved the ability to form complex representations which would allow them to consider the size and location of resources. This lack in lemur ecological cognition may restrict the size of frugivorous lemur social groups, thereby limiting the complexity of lemur social life. In this special issue, we have brought together two review papers, five field studies, and one laboratory study to investigate the interaction of social and ecological factors in relation to foraging. Our goal is to stimulate research that considers social and ecological factors acting together on cognitive evolution, rather than in isolation. Cross fertilization of experimental and observational studies from captivity and the field is important for increasing our understanding of this relationship.

Pithecia pithecia's behavioral response to decreasing fruit abundance.

In this article we describe the behavioral responses of a group of white-faced sakis' (Pithecia pithecia) to fruit and water scarcity. Six sakis were observed on Round Island in Guri Lake, Venezuela, between March and May 1996. These months are considered the dry season and the beginning of the wet season. Sakis specialize in eating seeds. During the present study only one tree species, Licania discolor (Chrysobalanaceae), fruited in substantial numbers. Licania seeds accounted for 88% of the time the sakis spent eating fruit in March, 87% in April, and 80% in May. We estimate that the sakis' intake of Licania seeds dropped from 2,573 seeds in the 15-day observation period in March to 956 seeds in the 16-day observation period in May. The sakis not only spent less time eating Licania, they ate the seeds at a much slower rate. The drop in the sakis' feeding rate was probably due to increased local search and inspection times. In response to the scarcity of fruit, the sakis ate more young leaves, insects, and flowers. Feeding bouts became more frequent but shorter. Mean distances between feeding bouts fell significantly and the sakis revisited trees less often.

MEASURING EVOLUTIONARY CONSTRAINTS: A MARKOV MODEL FOR PHYLOGENETIC TRANSITIONS AMONG SEED DISPERSAL SYNDROMES.

I introduce a Markov probabilistic model of transitions among discrete morphological states as a method for describing and testing nonrandom patterns of evolutionary change. The Markov model assumes one-generational dependency, i.e., that the future direction of evolutionary change depends on the current morphology of a species, not on any history of changes. This model is very flexible, allowing for any number of discrete states to describe morphology, yet permit rigorous testing of even complex evolutionary hypotheses. I apply this model to changes in seed dispersal mechanisms within 571 genera of Neotropical plants, using cladistic methods to infer the ancestral and derived states within each genus. I then test a series of progressively more complex hypotheses about the constraints that might shape the patterns of observed evolutionary transitions: 1) no transition constraints; 2) all dispersal mechanisms are equally labile evolutionarily; 3) the probability of particular evolutionary transitions among dispersal mechanisms depends on the descendant state but not on the ancestral state; 4) transition probabilities differ among pairs of dispersal mechanisms, but are reciprocal within such pairs. More complex hypotheses matched the data significantly better than did simpler hypotheses. However, only one of the hypotheses (reciprocal transitions) fit the observed data and then only for the most cautious interpretation of the frequencies of transitions within genera. These results suggest that evolutionary transitions among major adaptive syndromes are indeed ordered, and the observed patterns of transitions suggest possible reasons for such macroevolutionary structure.