Fermented food consumption in wild nonhuman primates and its ecological drivers.

OBJECTIVES: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits. MATERIALS AND METHODS: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates. RESULTS: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%-3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late-stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures. DISCUSSION: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods.

Synchronization of weaning time with peak fruit availability in squirrel monkeys (Saimiri collinsi) living in Amazonian Brazil.

Many mammals coincide their reproductive activities with factors such as ambient temperature, rainfall, and food availability. In primates that invest immediate food intake into reproduction, the periods of maximum fruit production often coincide with the peak of lactation (to maximize maternal survival) or the occurrence of weaning (to maximize infant survival). This study investigates the relationship between reproductive periods and the availability of ripe fruit in the habitat of a population of wild squirrel monkeys (Saimiri collinsi) in Amazonian Brazil. We combine data from several years (2002-2003; 2011-2015) during which we followed the monkeys and quantified the occurrence of matings, gestations, births, and the number of lactating females. We also collected rainfall and plant phenological data for 24 months. Our results confirm that reproductive events are highly seasonal in S. collinsi. The period of weaning corresponded to the peak in the abundance of ripe fruits consumed by the monkeys. This indicates that the period of infant nutritional independence is optimally timed to coincide with periods of greater food production in this habitat. We suggest that seasonal breeding in these primates does not necessarily reduce maternal energetic stress, but likely improves infant survivorship.

Reproductive status affects the feeding ecology and social association patterns of female squirrel monkeys (Saimiri collinsi) in an Amazonian rainforest.

When making foraging decisions, female primates may follow specific behavioral strategies that reflect their reproductive state. Lactation is considered the most energetically costly phase for females, but we argue that gestation is also energetically expensive for squirrel monkeys. In this study, we examined whether female squirrel monkeys (a seasonally breeding primate) in different reproductive phases showed significant differences in their foraging ecology. We sampled two wild groups of squirrel monkeys (Saimiri collinsi) using the focal animal method, during 12 months (June 2014 to May 2015). During this time, we quantified the effect of reproductive state (mating, gestation, and lactation) and sex (females vs. males) on activity budgets, foraging efficiency, dietary composition, and nearest neighbors. We found significant effects of both sex and reproductive phase on the mean proportion of time spent foraging, resting, traveling, and being social. Females consumed more insects than did males at all times; among females, time spent eating prey and fruit varied according to reproductive state. These data suggest that, due to their life history and seasonal breeding, reproduction is a costly activity for female Saimiri, and not only during lactation. Therefore, adopting the appropriate behavioral strategies is essential to reduce energetic deficits in females.

A novel method for capturing and monitoring a small neotropical primate, the squirrel monkey (Saimiri collinsi).

Squirrel monkeys (genus Saimiri) are agile, arboreal primates that are seldom captured in the wild due to their small body size (<1 kg) and large, non-cohesive social groups (40-50 individuals). However, long-term studies on these primates often require captures and permanent identification of individuals, in order to monitor their behavior and health. Here we report on a novel trapping method successfully used to capture Saimiri collinsi, in Eastern Amazonia, Brazil. Our objective was to capture as many individuals as possible from one social group of approximately 50 individuals, ranging over 150 ha of terra firme forest. Captures occurred in November and December 2013. We habituated animals to feed on a large platform located in a 123.5 m(2) area enclosed by a green net (3 m high). Multiple individuals could freely enter and exit the area via four ropes affixed from surrounding trees to the platform. Once individuals were feeding inside the netted area on selected trapping days, the ropes were dropped remotely, eliminating their escape routes. We successfully trapped 21 different individuals of the social group (14 adults and 7 immatures) with this method. We conclude that this is a conceptually simple, effective method for trapping squirrel monkeys in most habitats, and possibly other small arboreal primates that live in large social groups. The present method was more effective than previous methods utilized to capture squirrel monkeys in the field, and has the advantages of: allowing for safe capture of several individuals simultaneously; enabling re-captures; releasing of animals as a group at the site of capture; use of soft netting which facilitates safe capture of the monkeys.

Effect of biometric variables on two-dimensional echocardiographic measurements in the red-tailed boa (Boa constrictor constrictor).

The effects of body biometrics on cardiac measurements and description of cardiac anatomy were performed in red-tailed boas (Boa constrictor constrictor) (n = 29) using real-time B-mode ultrasonography. Statistical comparison of measured cardiac metrics according to sex and body measurements demonstrated no significant difference between sexes but a highly significant linear increase between body length and mass and all cardiac metrics.

Integration of field and captive studies for understanding the behavioral ecology of the squirrel monkey (Saimiri sp.).

Captive and field studies both provide valuable and complementary information that lead to a better understanding of a species' behavioral ecology. Here, we review studies from wild, captive, and semi-free ranging populations of squirrel monkeys (Saimiri sp.), in order to (a) provide a more current (1985-2010) review of Saimiri behavioral ecology and (b) illustrate that integrating data collected in a variety of settings is an effective approach to addressing ecological questions in primates. Captive environments, such as zoological facilities and research colonies, can be advantageous to researchers by allowing longitudinal studies of behavior and reproduction, as well as providing opportunities for gathering data on life history, because physiological and life history data are known for individual animals. Studies of field populations can provide contextual information regarding the adaptive nature of behaviors that are studied in captivity. Squirrel monkeys are small, neotropical primates that have extensively been used in captive research. As the last in-depth review of Saimiri biology was published in 1985 [Rosenblum & Coe, The squirrel monkey. New York: Academic Press], we review studies since conducted on Saimiri ecology, life history, social behavior, reproduction, and conservation. Our review indicates that there is much variation in socioecology and life history traits between Saimiri species and, surprisingly, also between populations of the same species studied at different locales. In addition, much is known about squirrel monkey reproductive physiology, basic ecology, and vocal communication, but data are still lacking in the fields of life history and some adaptive components and social behavior. In particular, longitudinal studies in the field would be particularly relevant for a genus with a slow life history such as Saimiri. Finally, few data (captive or wild) are available on S. ustus and S. vanzolinii, though at least one of these species is threatened.

Intergenerational transmission of the behavioral consequences of early experience in prairie voles.

We examined intergenerational and epigenetic effects of early handling manipulations on the social behavior of the prairie vole (Microtus ochrogaster), a monogamous rodent. Laboratory-born parents and their newborn pups were assigned to either a MAN0 "zero handling" manipulation (transfer with a cup during weekly cage changes) or a MAN1 "gloved handling" manipulation (transfer with a gloved hand). Previous studies from our laboratory (Bales et al., 2007) showed that MAN0 juvenile males that received this manipulation as pups are less alloparental and that MAN0 adult females that received this manipulation as pups display impaired pair-bonding. In the present study, when MAN0 and MAN1 pups reached adulthood, they were mated in three combinations (MAN1 female x MAN1 male; MAN0 female x MAN1 male; MAN1 female and MAN0 male). Once the pairs produced offspring, we examined their parental behavior towards their own pups. The offspring of these pairings (F2 generation) also were tested as juveniles for alloparental behavior. MAN1 females paired with a MAN0 male displayed higher levels of parenting behaviors. In the F2 generation, juvenile offspring with a MAN0 parent were less alloparental than were offspring from other pairs. These results suggest that early experiences can be transmitted intergenerationally.

Alloparenting experience affects future parental behavior and reproductive success in prairie voles (Microtus ochrogaster).

Various hypotheses have been proposed to explain the function of alloparental behavior in cooperatively breeding species. We examined whether alloparental experience as juveniles enhanced later parental care and reproductive success in the prairie vole (Microtus ochrogaster), a cooperatively breeding rodent. Juveniles cared for one litter of siblings (1EX), two litters of siblings (2EX) or no siblings (0EX). As adults, these individuals were mated to other 0EX, 1EX or 2EX voles, yielding seven different pair combinations, and we recorded measures of parental behaviors, reproductive success, and pup development. As juveniles, individuals caring for siblings for the first time were more alloparental; and as adults, 0EX females paired with 0EX males spent more time in the nest with their pups. Taken together, these results suggest that inexperienced animals spend more time in infant care. As parents, 1EX males spent more time licking their pups than 2EX and 0EX males. Pups with either a 1EX or 2EX parent gained weight faster than pups with 0EX parents during certain developmental periods. While inexperienced animals may spend more time in pup care, long-term benefits of alloparenting may become apparent in the display of certain, particularly important parental behaviors such as licking pups, and in faster weight gain of offspring.

Age and seasonal effects on predator-sensitive foraging in squirrel monkeys (Saimiri sciureus): a field experiment.

A field experiment was conducted to examine the effect of perceived predation risk on the use of foraging areas by juvenile and adult primates under different conditions of local food abundance. Wild squirrel monkeys, Saimiri sciureus, were observed in an experiment conducted during the dry and the wet seasons at a site in Eastern Amazonia, Brazil. Animals were presented with feeding platforms that differed in food quantity and exposure to aerial predators through varying vegetative cover. In the dry season, juveniles and adults chose platforms based solely on food quantity. However, in the wet season, juveniles foraged preferentially on high-reward platforms only if cover level also was high (i.e., potentially offered greater concealment from predators). In contrast, adults showed the same pattern of platform use regardless of season. These results indicate that age and local resource availability based on seasonality affect whether primates forage in a predator-sensitive manner. Juveniles may be more sensitive to predation risk when foraging, and individuals may take fewer risks when resource abundance is high in their environment.

Responses of squirrel monkeys to seasonal changes in food availability in an eastern Amazonian forest.

Tropical forests are characterized by marked temporal and spatial variation in productivity, and many primates face foraging problems associated with seasonal shifts in fruit availability. In this study, I examined seasonal changes in diet and foraging behaviors of two groups of squirrel monkeys (Saimiri sciureus), studied for 12 months in Eastern Brazilian Amazonia, an area characterized by seasonal rainfall. Squirrel monkeys were primarily insectivorous (79% of feeding and foraging time), with fruit consumption highest during the rainy season. Although monkeys fed from 68 plant species, fruit of Attalea maripa palms accounted for 28% of annual fruit-feeding records. Dietary shifts in the dry season were correlated with a decline in ripe A. maripa fruits. Despite pronounced seasonal variation in rainfall and fruit abundance, foraging efficiency, travel time, and distance traveled remained stable between seasons. Instead, squirrel monkeys at this Eastern Amazonian site primarily dealt with the seasonal decline in fruit by showing dietary flexibility. Consumption of insects, flowers, and exudates increased during the dry season. In particular, their foraging behavior at this time strongly resembled that of tamarins (Saguinus sp.) and consisted of heavy use of seed-pod exudates and specialized foraging on large-bodied orthopterans near the forest floor. Comparisons with squirrel monkeys at other locations indicate that, across their geographic range, Saimiri use a variety of behavioral tactics during reduced periods of fruit availability.