Foraging Benefits of Ecological Cognition in Fruit-Eating Primates: Results From Field Experiments and Computer Simulations

I focus on the foraging efficiency (food intake per time) of a hypothetical forager that uses distinct levels of information about a set of discrete renewing resources. The information may be the distance to the resource (D), both distance and maximum productivity of the resource (DP), or distance, productivity, and the elapsed time since the forager last visited each resource (DPT). The expected foraging efficiencies are based on the results of a field experiment on wild capuchin monkeys (Janson, 2016a) that documented the use of integrative memories of resource location, productivity, and elapsed time since the previous visit. Computer simulations of the choice process are used to extend the resource parameter space beyond the field experiment. The goal is to explore to what extent the use of elapsed time in choosing discrete feeding sites is a benefit under various conditions of resource and consumer characteristics. Major findings include that the use of elapsed time generally increases foraging efficiency on renewing resources by 30–35%, without much effect of resource size or variability—indeed, DPT outperforms D or DP choice even when all resources have the same productivity. The relative benefit of DPT increases when the most productive resources are only moderately common (not so rare that they contribute little to food intake, nor so common that choosing the nearest resource is likely to arrive at a highly productive one). The relative benefit of DPT decreases when the forager's gut capacity is small or gut passage time is long because it cannot ingest all of the resource accumulated after long elapsed intervals. I suggest that memory for and use of elapsed intervals since prior visits in foraging choices will prove to be a common feature of diverse foraging animals whenever the presence of a forager depresses food availability in a local area

Long-Term Spatial Memory and Learning Set Formation in Captive Capuchin Monkeys (Cebus libidinosus = Sapajus cay)

Researchers have long suspected that nonhuman primates have long-term spatial memory for locating food. However, few empirical studies have assessed spatial memory for a period longer than 1 day in nonhuman primates in a foraging context.We used a modified version of the radial maze to test long-term memory for periods of 2 days or longer in two groups of Cebus libidinosus = Sapajus cay (N=10; N=6) in captivity (environment completely human constructed) and semicaptivity (relatively natural environment with few human-made structures) at La Plata Zoo and Botanical Park, Buenos Aires, Argentina, between 2007 and 2010. The experimental design included a set of three accessible baited feeders interspersed among three nonaccessible baited feeders. We tested monkeys in one initial exposure period, four periods of longterm memory (2 days, 76 days, 76+2 days, and 4 months of delay), and one period of inversion of the experimental set location. We used the latter to analyze the monkeys’ abilities to develop learning sets. Captive subjects appeared to remember sites with accessible and nonaccessible food for periods of 2 days, 76 days, and 4 months, and used learning sets to reduce relearning times when exposed to a change in the learned locations. Although semicaptive subjects also appeared to remember sites with accessible and nonaccessible food, their performance was less accurate. We conclude that capuchins used spatial memory to improve their foraging efficiency.Facultad de Ciencias Naturales y Museo (FCNM

Long-Term Spatial Memory and Learning Set Formation in Captive Capuchin Monkeys (Cebus libidinosus = Sapajus cay)

Researchers have long suspected that nonhuman primates have long-term spatial memory for locating food. However, few empirical studies have assessed spatial memory for a period longer than 1 day in nonhuman primates in a foraging context.We used a modified version of the radial maze to test long-term memory for periods of 2 days or longer in two groups of Cebus libidinosus = Sapajus cay (N=10; N=6) in captivity (environment completely human constructed) and semicaptivity (relatively natural environment with few human-made structures) at La Plata Zoo and Botanical Park, Buenos Aires, Argentina, between 2007 and 2010. The experimental design included a set of three accessible baited feeders interspersed among three nonaccessible baited feeders. We tested monkeys in one initial exposure period, four periods of longterm memory (2 days, 76 days, 76+2 days, and 4 months of delay), and one period of inversion of the experimental set location. We used the latter to analyze the monkeys’ abilities to develop learning sets. Captive subjects appeared to remember sites with accessible and nonaccessible food for periods of 2 days, 76 days, and 4 months, and used learning sets to reduce relearning times when exposed to a change in the learned locations. Although semicaptive subjects also appeared to remember sites with accessible and nonaccessible food, their performance was less accurate. We conclude that capuchins used spatial memory to improve their foraging efficiency.Facultad de Ciencias Naturales y Museo (FCNM

Long-Term Spatial Memory and Learning Set Formation in Captive Capuchin Monkeys (Cebus libidinosus = Sapajus cay)

Researchers have long suspected that nonhuman primates have long-term spatial memory for locating food. However, few empirical studies have assessed spatial memory for a period longer than 1 day in nonhuman primates in a foraging context.We used a modified version of the radial maze to test long-term memory for periods of 2 days or longer in two groups of Cebus libidinosus = Sapajus cay (N=10; N=6) in captivity (environment completely human constructed) and semicaptivity (relatively natural environment with few human-made structures) at La Plata Zoo and Botanical Park, Buenos Aires, Argentina, between 2007 and 2010. The experimental design included a set of three accessible baited feeders interspersed among three nonaccessible baited feeders. We tested monkeys in one initial exposure period, four periods of longterm memory (2 days, 76 days, 76+2 days, and 4 months of delay), and one period of inversion of the experimental set location. We used the latter to analyze the monkeys’ abilities to develop learning sets. Captive subjects appeared to remember sites with accessible and nonaccessible food for periods of 2 days, 76 days, and 4 months, and used learning sets to reduce relearning times when exposed to a change in the learned locations. Although semicaptive subjects also appeared to remember sites with accessible and nonaccessible food, their performance was less accurate. We conclude that capuchins used spatial memory to improve their foraging efficiency.Facultad de Ciencias Naturales y Museo (FCNM

Hippocampal Gene Expression Analysis Highlights Ly6a/Sca-1 as Candidate Gene for Previously Mapped Novelty Induced Behaviors in Mice

In this study, we show that the covariance between behavior and gene expression in the brain can help further unravel the determinants of neurobehavioral traits. Previously, a QTL for novelty induced motor activity levels was identified on murine chromosome 15 using consomic strains. With the goal of narrowing down the linked region and possibly identifying the gene underlying the quantitative trait, gene expression data from this F2-population was collected and used for expression QTL analysis. While genetic variation in these mice was limited to chromosome 15, eQTL analysis of gene expression showed strong cis-effects as well as trans-effects elsewhere in the genome. Using weighted gene co-expression network analysis, we were able to identify modules of co-expressed genes related to novelty induced motor activity levels. In eQTL analyses, the expression of Ly6a (a.k.a. Sca-1) was found to be cis-regulated by chromosome 15. Ly6a also surfaced in a group of genes resulting from the network analysis that was correlated with behavior. Behavioral analysis of Ly6a knock-out mice revealed reduced novelty induced motor activity levels when compared to wild type controls, confirming functional importance of Ly6a in this behavior, possibly through regulating other genes in a pathway. This study shows that gene expression profiling can be used to narrow down a previously identified behavioral QTL in mice, providing support for Ly6a as a candidate gene for functional involvement in novelty responsiveness

Effects of the Distribution of Female Primates on the Number of Males

The spatiotemporal distribution of females is thought to drive variation in mating systems, and hence plays a central role in understanding animal behavior, ecology and evolution. Previous research has focused on investigating the links between female spatiotemporal distribution and the number of males in haplorhine primates. However, important questions remain concerning the importance of spatial cohesion, the generality of the pattern across haplorhine and strepsirrhine primates, and the consistency of previous findings given phylogenetic uncertainty. To address these issues, we examined how the spatiotemporal distribution of females influences the number of males in primate groups using an expanded comparative dataset and recent advances in Bayesian phylogenetic and statistical methods. Specifically, we investigated the effect of female distributional factors (female number, spatial cohesion, estrous synchrony, breeding season duration and breeding seasonality) on the number of males in primate groups. Using Bayesian approaches to control for uncertainty in phylogeny and the model of trait evolution, we found that the number of females exerted a strong influence on the number of males in primate groups. In a multiple regression model that controlled for female number, we found support for temporal effects, particularly involving female estrous synchrony: the number of males increases when females are more synchronously receptive. Similarly, the number of males increases in species with shorter birth seasons, suggesting that greater breeding seasonality makes defense of females more difficult for male primates. When comparing primate suborders, we found only weak evidence for differences in traits between haplorhines and strepsirrhines, and including suborder in the statistical models did not affect our conclusions or give compelling evidence for different effects in haplorhines and strepsirrhines. Collectively, these results demonstrate that male monopolization is driven primarily by the number of females in groups, and secondarily by synchrony of female reproduction within groups

Trophic structure of a neotropical frugivore community: is there competition between birds and bats?

Dietary overlap and competition between frugivorous birds and bats in the Neotropics have been presumed to be low, but comparative data have been lacking. We determined the diets of volant frugivores in an early successional patch of Costa Rican wet forest over a one month period. Ordination of the diet matrix by Reciprocal Averaging revealed that birds and bats tend to feed on different sets of fruits and that diets differed more among bat species than among bird species. However, there was overlap between Scarlet-rumped Tanagers and three Carollia bat species on fruits of several Piper species which comprised most of the diet of these bats. Day/night exclosure experiments on P. friedrichsthalli treetlets provided evidence that birds deplete the amount of ripe fruit available to bats. These results indicate that distantly related taxa may overlap in diet and compete for fruit, despite the apparent adaptation of animal-dispersed plant species for dispersal by particular animal taxa.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/47779/1/442_2004_Article_BF00384321.pd

Data from: 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

raw data 2008 trimmed

Sequences of visits by one capuchin monkey group (Macuco group) to a set of experimental feeding sites during 2008 field season. Details of the variables are provided in comments in the upper left-hand cell of each of two worksheets