Ben T. Hirsch

Thieving rodents as substitute dispersers of megafaunal seeds

The Neotropics have many plant species that seem to be adapted for seed dispersal by megafauna that went extinct in the late Pleistocene. Given the crucial importance of seed dispersal for plant persistence, it remains a mystery how these plants have survived more than 10,000 y without their mutualist dispersers. Here we present support for the hypothesis that secondary seed dispersal by scatter-hoarding rodents has facilitated the persistence of these large-seeded species. We used miniature radio transmitters to track the dispersal of reputedly megafaunal seeds by Central American agoutis, which scatter-hoard seeds in shallow caches in the soil throughout the forest. We found that seeds were initially cached at mostly short distances and then quickly dug up again. However, rather than eating the recovered seeds, agoutis continued to move and recache the seeds, up to 36 times. Agoutis dispersed an estimated 35% of seeds for >100 m. An estimated 14% of the cached seeds survived to the next year, when a new fruit crop became available to the rodents. Serial video-monitoring of cached seeds revealed that the stepwise dispersal was caused by agoutis repeatedly stealing and recaching each other’s buried seeds. Although previous studies suggest that rodents are poor dispersers, we demonstrate that communities of rodents can in fact provide highly effective long-distance seed dispersal. Our findings suggest that thieving scatter-hoarding rodents could substitute for extinct megafaunal seed dispersers of tropical large-seeded trees.

Directed seed dispersal towards areas with low conspecific tree density by a scatter-hoarding rodent.

Scatter-hoarding animals spread out cached seeds to reduce density-dependent theft of their food reserves. This behaviour could lead to directed dispersal into areas with lower densities of conspecific trees, where seed and seedling survival are higher, and could profoundly affect the spatial structure of plant communities. We tested this hypothesis with Central American agoutis and Astrocaryum standleyanum palm seeds on Barro Colorado Island, Panama. We radio-tracked seeds as they were cached and re-cached by agoutis, calculated the density of adult Astrocaryum trees surrounding each cache, and tested whether the observed number of trees around seed caches declined more than expected under random dispersal. Seedling establishment success was negatively dependent on seed density, and agoutis carried seeds towards locations with lower conspecific tree densities, thus facilitating the escape of seeds from natural enemies. This behaviour may be a widespread mechanism leading to highly effective seed dispersal by scatter-hoarding animals.

COSTS AND BENEFITS OF WITHIN‐GROUP SPATIAL POSITION: A FEEDING COMPETITION MODEL

An animal’s within‐group spatial position has several important fitness consequences. Risk of predation, time spent engaging in antipredatory behavior, and feeding competition can all vary with respect to spatial position. Previous research has found evidence that feeding rates are higher at the group edge in many species, but these studies have not represented the entire breadth of dietary diversity and ecological situations faced by many animals. In particular, the presence of concentrated, defendable food patches can lead to increased feeding rates by dominants in the center of the group that are able to monopolize or defend these areas. To fully understand the tradeoffs of within‐group spatial position in relation to a variety of factors, it is important to be able to predict where individuals should preferably position themselves in relation to feeding rates and food competition. A qualitative model is presented here to predict how food depletion time, abundance of food patches within a group, and the presence of prior knowledge of feeding sites affect the payoffs of different within‐group spatial positions for dominant and subordinate animals. In general, when feeding on small abundant food items, individuals at the front edge of the group should have higher foraging success. When feeding on slowly depleted, rare food items, dominants will often have the highest feeding rates in the center of the group. Between these two extreme points of a continuum, an individual’s optimal spatial position is predicted to be influenced by an additional combination of factors, such as group size, group spread, satiation rates, and the presence of producer‐scrounger tactics.

Within-group spatial position in ring-tailed coatis: balancing predation, feeding competition, and social competition

A variety of factors can influence an individual’s choice of within-group spatial position. For terrestrial social animals, predation, feeding success, and social competition are thought to be three of the most important variables. The relative importance of these three factors was investigated in groups of ring-tailed coatis (Nasua nasua) in Iguazú, Argentina. Different age/sex classes responded differently to these three variables. Coatis were found in close proximity to their own age/sex class more often than random, and three out of four age/sex classes were found to exhibit within-group spatial position preferences which differed from random. Juveniles were located more often at the front edge and were rarely found at the back of the group. Juveniles appeared to choose spatial locations based on feeding success and not predation avoidance. Since juveniles are the most susceptible to predation and presumably have less prior knowledge of food source location, these results have important implications in relation to predator-sensitive foraging and models of democratic group leadership. Subadults were subordinate to adult females, and their relationships were characterized by high levels of aggression. This aggression was especially common during the first half of the coati year (Nov–April), and subadults were more peripheralized during this time period. Subadults likely chose spatial positions to avoid aggression and were actively excluded from the center of the group by adult females. In the Iguazú coati groups, it appeared that food acquisition and social agonism were the major determinants driving spatial choice, while predation played little or no role. This paper demonstrates that within-group spatial structure can be a complex process shaped by differences in body size and nutritional requirements, food patch size and depletion rate, and social dominance status. How and why these factors interact is important to understanding the costs and benefits of sociality and emergent properties of animal group formation.

Kinship shapes affiliative social networks but not aggression in ring-tailed coatis

Animal groups typically contain individuals with varying degrees of genetic relatedness, and this variation in kinship has a major influence on patterns of aggression and affiliative behaviors. This link between kinship and social behavior underlies socioecological models which have been developed to explain how and why different types of animal societies evolve. We tested if kinship and age-sex class homophily in two groups of ring-tailed coatis (Nasua nasua) predicted the network structure of three different social behaviors: 1) association, 2) grooming, and 3) aggression. Each group was studied during two consecutive years, resulting in four group-years available for analysis (total of 65 individuals). Association patterns were heavily influenced by agonistic interactions which typically occurred during feeding competition. Grooming networks were shaped by mother-offspring bonds, female-female social relationships, and a strong social attraction to adult males. Mother-offspring pairs were more likely to associate and groom each other, but relatedness had no effect on patterns of aggressive behavior. Additionally, kinship had little to no effect on coalitionary support during agonistic interactions. Adult females commonly came to the aid of juveniles during fights with other group members, but females often supported juveniles who were not their offspring (57% of coalitionary interactions). These patterns did not conform to predictions from socioecological models.

Raccoon Social Networks and the Potential for Disease Transmission

Raccoons are an important vector of rabies and other pathogens. The degree to which these pathogens can spread through a raccoon population should be closely linked to association rates between individual raccoons. Most studies of raccoon sociality have found patterns consistent with low levels of social connectivity within populations, thus the likelihood of direct pathogen transmission between raccoons is theoretically low. We used proximity detecting collars and social network metrics to calculate the degree of social connectivity in an urban raccoon population for purposes of estimating potential pathogen spread. In contrast to previous assumptions, raccoon social association networks were highly connected, and all individuals were connected to one large social network during 15 out of 18 months of study. However, these metrics may overestimate the potential for a pathogen to spread through a population, as many of the social connections were based on relatively short contact periods. To more closely reflect varying probabilities of pathogen spread, we censored the raccoon social networks based on the total amount of time spent in close proximity between two individuals per month. As this time criteria for censoring the social networks increased from one to thirty minutes, corresponding measures of network connectivity declined. These findings demonstrate that raccoon populations are much more tightly connected than would have been predicted based on previous studies, but also point out that additional research is needed to calculate more precise transmission probabilities by infected individuals, and determine how disease infection changes normal social behaviors.

Raccoon contact networks predict seasonal susceptibility to rabies outbreaks and limitations of vaccination

Infectious disease transmission often depends on the contact structure of host populations. Although it is often challenging to capture the contact structure in wild animals, new technology has enabled biologists to obtain detailed temporal information on wildlife social contacts. In this study, we investigated the effects of raccoon contact patterns on rabies spread using network modelling. Raccoons (Procyon lotor) play an important role in the maintenance of rabies in the United States. It is crucial to understand how contact patterns influence the spread of rabies in raccoon populations in order to design effective control measures and to prevent transmission to human populations and other animals. We constructed a dynamic system of contact networks based on empirical data from proximity logging collars on a wild suburban raccoon population and then simulated rabies spread across these networks. Our contact networks incorporated the number and duration of raccoon interactions. We included differences in contacts according to sex and season, and both short-term acquaintances and long-term associations. Raccoons may display different behaviours when infectious, including aggression (furious behaviour) and impaired mobility (dumb behaviour); the network model was used to assess the impact of potential behavioural changes in rabid raccoons. We also tested the effectiveness of different vaccination coverage levels. Our results demonstrate that when rabies enters a suburban raccoon population, the likelihood of a disease outbreak affecting the majority of the population is high. Both the magnitude of rabies outbreaks and the speed of rabies spread depend strongly on the time of year that rabies is introduced into the population. When there is a combination of dumb and furious behaviours in the rabid raccoon population, there are similar outbreak sizes and speed of spread to when there are no behavioural changes due to rabies infection. By incorporating detailed data describing the variation in raccoon contact rates into a network modelling approach, we were able to show that suburban raccoon populations are highly susceptible to rabies outbreaks, that the risk of large outbreaks varies seasonally and that current vaccination target levels may be inadequate to prevent the spread of rabies within these populations. Our findings provide new insights into rabies dynamics in raccoon populations and have important implications for disease control.

Seasonal Variation in the Diet of Ring-Tailed Coatis (Nasua nasua) in Iguazu, Argentina

Abstract There is widespread evidence that feeding ecology can lead to differences in mammalian social systems. To understand how diet and ecology affect the social behavior of ring-tailed coatis (Nasua nasua), detailed measures of feeding behavior were recorded from 2 well-studied groups over a 2-year period. The proportion of fruit and invertebrates in the diet of ring-tailed coatis in Iguazu, Argentina, was very similar to that in diets of white-nosed coatis (N. narica) and ring-tailed coatis studied at field sites in Brazil. Consumption of vertebrates in Iguazu was exceptionally rare. The proportion of time spent foraging for invertebrates and fruit generally matched seasonal changes in the abundance these foods in the environment. During the winter, when invertebrate and fruit availability was low, coatis spent a large amount of time feeding on 2 exotic fruit species. The presence of exotic fruits provided coatis with food during the lean winter season and may have influenced the high reproduction and survivorship found in this population. Coatis spent about 44% of their fruit-foraging time exploiting pindo palm (Syagrus romanzoffianum) fruits and it appeared that this fruit species played a major role in shaping the ranging and feeding behavior of coati groups. The time spent foraging at fruit trees and the total number of fruits eaten varied depending on the species of tree. Coati groups spent an average of 2.5–12.5 min feeding on different species of fruit trees, and coati groups ate an average of 2.6–269.8 fruits per tree species. The quick depletion of fruit trees and high density of foraging individuals, especially when feeding on pindo, plays an important role in shaping the social system of coatis.

Familiarity breeds progeny: sociality increases reproductive success in adult male ring‐tailed coatis (Nasua nasua)

The ring‐tailed coati (Nasua nasua) is the only coati species in which social groups contain an adult male year round, although most males live solitarily. We compared reproductive success of group living and solitary adult male coatis to determine the degree to which sociality affects reproductive success. Coati mating is highly seasonal and groups of female coatis come into oestrus during the same 1–2 week period. During the mating season, solitary adult males followed groups and fought with the group living male. This aggression was presumably to gain access to receptive females. We expected that high reproductive synchrony would make it difficult or impossible for the one group living male to monopolize and defend the group of oestrous females. However, we found that group living males sired between 67–91% of the offspring in their groups. This reproductive monopolization is much higher than other species of mammals with comparably short mating seasons. Clearly, living in a group greatly enhanced a male’s reproductive success. At the same time, at least 50% of coati litters contained offspring sired by extra‐group males (usually only one offspring per litter); thus, resident males could not prevent extra‐group matings. The resident male’s reproductive advantage may reflect female preference for a resident male strong enough to fend off competing males.

Evidence for cache surveillance by a scatter-hoarding rodent

The mechanisms by which food-hoarding animals are capable of remembering the locations of numerous cached food items over long time spans has been the focus of intensive research. The ‘memory enhancement hypothesis’ states that hoarders reinforce spatial memory of their caches by repeatedly revisiting cache sites, yet no study has documented this behaviour in wild animals. We investigated whether scatter-hoarding Central American agoutis, Dasyprocta punctata, actively survey their seed caches. We placed remote cameras at sites where seeds were buried by known individuals and at nearby random locations to compare the behaviour and visiting rates between owners and naive individuals. We found that cache owners were almost four times more likely to walk near their cache than to walk past random locations. Moreover, cache owners that passed in front of a cache camera were more than twice as likely to approach their caches than were naive individuals but half as likely to excavate the seed when interacting with the cache. We conclude that agoutis remember the location of cached seeds, are aware of their ownership and actively survey their caches. Surveillance could serve to monitor cache theft and food quality as well as enhance spatial memory of cache locations; thus, this behaviour could have important fitness benefits and may be exhibited by other scatter-hoarding animals.