Primate Ecology Research Articles

Understanding Eocene primate palaeobiology using a comprehensive analysis of living primate ecology, biology and behaviour

The comparative method is central to interpretations of Eocene primate palaeobiology. This method rests upon a thorough study of analogous living forms. With a rapidly increasing knowledge of such forms, most notably the Malagasy lemurs, our ability to advance the study of Eocene primate ecology, biology and behaviour far exceeds that of even just a few years ago. Here we present such a comparison. Based on our data collected from both living lemurs and extant lemur skeletal specimens, we are able to make a number of comparisons that provide insight into middle Eocene primate ecology and palaeobiology. At the Beza Mahafaly Special Reserve, Madagascar, omnivorous living ring-tailed lemurs that feed on large, hard and tough fruits display a pattern of frequent post-canine tooth wear laterality (62 %) when compared to sympatric, folivorous Verreaux’s sifaka (4 %). Our results indicate that Notharctus does not display a high frequency of tooth wear laterality (7 %), indicating folivory without processing large, hard fruits with its postcanines. Our data on Notharctus tooth wear also indicate, similar to living ring-tailed lemurs at Beza Mahafaly, that numerous individuals (21 %) survived long enough to experience heavy tooth wear, contrary to the assumption that heavy tooth wear leads to the rapid death of the individual. Finally, our data on trauma and injury from a living lemur population suggest that the reported wrist injury in Darwinius masillae (i.e. “Ida”) did not necessarily lead to her death, as numerous ring-tailed lemurs at Beza Mahafaly survive with similar or even more traumatic injuries and maintain the ability to climb. Thus, our data from living primates provide a broad comparative framework for interpreting the ecology, biology and behaviour of Eocene forms.

What is dental ecology?

Teeth have long been used as indicators of primate ecology. Early work focused on the links between dental morphology, diet, and behavior, with more recent years emphasizing dental wear, microstructure, development, and biogeochemistry, to understand primate ecology. Our study of Lemur catta at the Beza Mahafaly Special Reserve, Madagascar, has revealed an unusual pattern of severe tooth wear and frequent tooth loss, primarily the result of consuming a fallback food for which these primates are not dentally adapted. Interpreting these data was only possible by combining our areas of expertise (dental anatomy [FC] and primate ecology [MS]). By integrating theoretical, methodological, and applied aspects of both areas of research, we adopted the term "dental ecology"-defined as the broad study of how teeth respond to the environment. Specifically, we view dental ecology as an interpretive framework using teeth as a vehicle for understanding an organism's ecology, which builds upon earlier work, but creates a new synthesis of anatomy and ecology that is only possible with detailed knowledge of living primates. This framework includes (1) identifying patterns of dental pathology and tooth use-wear, within the context of feeding ecology, behavior, habitat variation, and anthropogenic change, (2) assessing ways in which dental development and biogeochemical signals can reflect habitat, environmental change and/or stress, and (3) how dental microstructure and macro-morphology are adapted to, and reflect feeding ecology. Here we define dental ecology, provide a short summary of the development of this perspective, and place our new work into this context.

Primate dental ecology: How teeth respond to the environment

Teeth are central for the study of ecology, as teeth are at the direct interface between an organism and its environment. Recent years have witnessed a rapid growth in the use of teeth to understand a broad range of topics in living and fossil primate biology. This in part reflects new techniques for assessing ways in which teeth respond to, and interact with, an organism's environment. Long-term studies of wild primate populations that integrate dental analyses have also provided a new context for understanding primate interactions with their environments. These new techniques and long-term field studies have allowed the development of a new perspective-dental ecology. We define dental ecology as the broad study of how teeth respond to, or interact with, the environment. This includes identifying patterns of dental pathology and tooth use-wear, as they reflect feeding ecology, behavior, and habitat variation, including areas impacted by anthropogenic disturbance, and how dental development can reflect environmental change and/or stress. The dental ecology approach, built on collaboration between dental experts and ecologists, holds the potential to provide an important theoretical and practical framework for inferring ecology and behavior of fossil forms, for assessing environmental change in living populations, and for understanding ways in which habitat impacts primate growth and development. This symposium issue brings together experts on dental morphology, growth and development, tooth wear and health, primate ecology, and paleontology, to explore the broad application of dental ecology to questions of how living and fossil primates interact with their environments.

Stable Isotope Techniques and Applications for Primatologists

Stable isotope biogeochemistry is useful for quantifying the feeding ecology of modern and extinct primates. Over the past three decades, substantial advances have been made in our knowledge of the physiological causes of isotopic patterns as well as effective methodology to prepare samples for isotopic analysis. Despite these advances, the potential of stable isotope biogeochemistry has yet to be fully exploited by primate researchers, perhaps due to the prolific and somewhat daunting nature of the isotopic literature. I here aim to present a cogent overview of stable isotope applications to nonhuman primate feeding ecology. I review the factors that influence ecological patterns in carbon, nitrogen, and oxygen stable isotopes. I present methods for collecting and preparing samples of tooth enamel and bone mineral hydroxyapatite, bone collagen, fur and hair keratin, blood, feces, and urine for isotope analysis. I discuss both the existing and potential applications of these isotopic patterns to primate feeding ecology. Lastly, I point out some of the pitfalls to avoid when interpreting and comparing isotopic results.

Sex differences in the mother–neonate relationship in wild baboons: social, experiential and hormonal correlates

In mammals, maternal care is essential for offspring survival, yet individual differences in this care can dramatically affect offspring growth and development. Few studies have, however, investigated the sources, magnitude and consequences of naturally occurring interindividual variation in maternal care during the neonatal period. In this study, we examine several hormonal and nonhormonal predictors of naturally occurring variation in the mothereneonate relationship during the first 8 weeks of infancy in 34 wild baboon (Papio cynocephalus) mothereinfant dyads in Amboseli, Kenya. We use data on physical contact and suckling patterns to assess the quality of the mothereneonate relationship and to evaluate the extent to which variation in this relationship is predictable from perinatal ovarian steroids (i.e. faecal oestrogen and progesterone metabolites), previous infant care experience, maternal dominance rank and offspring sex. We found that newborn infants of more experienced mothers initiated higher rates of changes in mothereinfant contact than newborns of less experienced mothers. However, at each level of maternal experience, newborn males initiated higher rates of changes in mothereinfant contact than newborn females. Moreover, we found evidence suggesting that variation in suckling activity among daughters (but not sons) was predictable from maternal dominance rank and faecal oestrogen (fE) concentrations before birth. To our knowledge, our study provides the first evidence of (1) the influence of cumulative maternal experience on the mothereinfant relationship and (2) the emergence of sex differences in the mothereinfant relationship during the neonatal period in wild primates. Our results suggest that the well-documented sex differences in life history, behaviour and ecology in primates (and other social mammals) may originate very early in life. 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. For vertebrates, mammalian newborns are unusually dependent on their mothers for nourishment, transport, protection and support (Clutton-Brock 1991). Although offspring eventually transition from complete reliance on their mothers to nutritional, locomotor and social independence, the timing of these events can vary widely across individuals of the same species (Clutton-Brock 1991). Despite the critical importance of the neonatal period in the life of each individual, few studies have investigated the sources, magnitude and consequences of interindividual variation in the mothereoffspring relationship during the neonatal period in wild mammals (Altmann 1980; Bales et al. 2002). In this study, we

The Ranging Costs of a Fallback Food: Liana Consumption Supplements Diet but Increases Foraging Effort in Howler Monkeys

AbstractLianas are important components in the dynamics of tropical forests and represent fallback foods for some primates, yet little is known about their impact on primate ecology, behavior or fitness. Using 2 yr of field data, we investigated liana consumption and foraging effort in four groups of howler monkeys (two in bigger, more conserved forest fragments and two in smaller, less conserved fragments) to assess whether howler monkeys use lianas when and where food availability is scarce, and how liana consumption is related to foraging effort. Howler monkeys in smaller fragments spent more time consuming lianas and liana consumption was negatively related to the consumption of preferred food resources (fruit and Ficus spp.). Further, travel time was positively related to liana feeding time, but not to tree feeding time, and howler monkeys visited a greater number of food patches when feeding from liana leaves than when feeding from tree leaves. Our results suggest that these increases in foraging effort were related to the fact that lianas are mainly a source of leaves, and that liana patch size was probably smaller than tree patch size. While these results were clear when analyzing all four groups combined, however, they were not always significant in each of the groups individually. We suggest that this may be related to the differences in group size, patch size and the availability of resources among groups. Further studies are necessary to assess whether these dietary and behavioral adjustments negatively impact on the fitness and conservation of primates in fragments.

The Influence of Nutrition on Primate Sociality

Copyright: © 2012 Wallner B. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. This editorial is based on two comprehensive reviews about the effects of nutrients on aggressive, respectively, impulsive behavior in comparative primatology [1,2]. The aim of this work is to highlight the importance of feeding ecology in primates either in experimental or in field studies in relation to its modulatory effects on aggression and its impact to sociality and social styles. Aggressive behavior can be generated, stimulated, and modulated through both intrinsic and extrinsic factors, e.g. social and nutritional influences, endocrine, and neurophysiological regulatory mechanisms. Most of these factors are interrelated and seemed to play important roles during evolutionary adaptative processes.

Methods in Primate Nutritional Ecology: A User’s Guide

An important goal of primatology is to identify the ecological factors that affect primate abundance, diversity, demography, and social behavior. Understanding the nutritional needs of primates is central to understanding primate ecology because adequate nutrition is a prerequisite for successful reproduction. Here, we review nutritional methods and provide practical guidelines to measure nutrient intake by primates in field settings. We begin with an assessment of how to estimate food intake by primates using behavioral observations. We then describe how to collect, prepare, and preserve food samples. Finally, we suggest appropriate nutritional assays for estimating diet nutritional quality and point to the merits and limitations of each. We hope this review will inspire primatologists to use nutritional ecology to answer many unresolved questions in primatology.

Intergroup variation in stable isotope ratios reflects anthropogenic impact on the Barbary macaques (Macaca sylvanus) of Gibraltar

Interactions with humans impact many aspects of behavior and ecology in nonhuman primates. Because of the complexities of the human-nonhuman primate interface, methods are needed to quantify the effects of anthropogenic interactions, including their intensity and differential impacts between nonhuman primate groups. Stable isotopes can be used to quickly and economically assess intergroup dietary variation, and provide a framework for the development of specific hypotheses about anthropogenic impact. This study uses stable carbon and nitrogen isotope analysis to examine intraspecific variation in diet between five groups of Barbary macaques, Macaca sylvanus, in the Upper Rock Nature Reserve, Gibraltar. Analysis of hair from 135 macaques showed significant differences in δ(13)C and δ(15)N values between a group with minimal tourist contact and groups that were main tourist attractions. Because we observed no overt physiological or substantial behavioral differences between the groups, feeding ecology is the most likely cause of any differences in stable isotope ratios. Haphazard provisioning by tourists and Gibraltarians is a likely source of dietary variation between groups. Stable isotope analysis and observational data facilitate a deeper understanding of the feeding ecology of the Barbary macaques relevant to the role of an anthropogenic ecology for the species.

Comparative Feeding Ecology of Two Communities of Chimpanzees (Pan troglodytes) in Kibale National Park, Uganda

Several recent studies have documented considerable intraspecific and intrapopulation ecological variation in primates. However, we generally lack an understanding of how such variability may be linked to concomitant demographic variation among groups or populations of the same species, particularly in regard to large-bodied and wide-ranging species with high ecological flexibility, such as chimpanzees (Pan troglodytes). We compared the feeding ecology of chimpanzees inhabiting 2 sites in Kibale National Park, Uganda that differ 3-fold in chimpanzee density and support notably different plant communities. Chimpanzees at Ngogo, a site with the largest known chimpanzee community and unusually high chimpanzee density, spent a significantly lower percentage of time resting (and pregnant and lactating females spent more time feeding), incorporated higher percentages of ripe fruit in their diet, had lower dietary diversity values, and had shorter and less variable average patch residency times than did their counterparts at the nearby Kanyawara site, which supports a relatively low density of chimpanzees. In addition, feeding party size was significantly and positively related to feeding patch size at Ngogo, but not at Kanyawara. Together these findings aid in explaining the noted disparity in chimpanzee community size and density between Ngogo and Kanyawara by suggesting that the diet of Ngogo chimpanzees is of higher overall quality than that of Kanyawara chimpanzees. They also highlight the potentially profound influence of even small-scale habitat heterogeneity on the ecology of primates. Researchers must take such influences into account when attempting to draw conclusions about species- or population-level characteristics.

Digesta Passage Time, Digestibility, and Total Gut Fill in Captive Japanese Macaques (Macaca fuscata): Effects Food Type and Food Intake Level

Digestion is an important process in understanding the feeding ecology of animals. We examined digesta passage time, digestibility, and total gut fill in Japanese macaques (Macaca fuscata; n = 4) under 4 dietary conditions representing the seasonal and regional variations in the diets of wild populations to determine the effects of food type and food intake on these digestive features. Food type is associated with mean retention time (MRT), digestibility, and total gut fill. Dry matter intake (DMI) of food correlates positively with total gut fill but not with MRT or digestibility. Conversely, indigestible DMI affected MRT negatively. Thus, when Japanese macaques consume high-fiber foods, MRT becomes shorter and digestibility is lower than when eating low-fiber foods. Moreover, macaques experience increases in total gut fill when they consume high-fiber diets or a large amount of food. Japanese macaques may excrete difficult-to-digest food components quickly; they nevertheless buffer an increase in food intake by an increase in gut fill. Our study offers new insights into the relationship between feeding ecology and nutritional physiology in primates by simultaneously examining the effects of food type and intake level on MRT and digestibility.

Figs Are More Than Fallback Foods: The Relationship betweenFicusandCebusin a Tropical Dry Forest

In many studies on primate feeding ecology, figs (Ficusspp.) are characterized as fallback foods, utilized only when preferred sources of food are unavailable. However, for white-faced capuchin monkeys (Cebus capucinus) living in northwestern Costa Rica, figs are a consistently important resource and may increase groupwide energy intake. We investigated whether visits to figs affect ranging and behavioural patterns of capuchins. Although daily range length and average travel speed do not differ on days when fig trees are visited, capuchins spend more time in directed travel and more time stationary on “fig days”. Capuchins also increase time spent foraging for fruit and decrease time spent foraging for invertebrates on days when figs trees are visited. Capuchins experience higher energy intake and lower energy output on “fig” days. Thus, the patterns of foraging for figs support an energy-maximization strategy and constitute an important nutritional resource for capuchins.

Identifying Sykes’ monkeys’, Cercopithecus albogularis erythrarchus, axes of fear through patch use

We used experimental food patches to test how habitat factors affect predation risk for Sykes’ monkeys. We created food patches to reveal monkeys’ foraging cost of predation. We measured the monkeys’ variation in predation costs with patches stratified by height and arrayed horizontally. We expected the monkeys to harvest the most from patches with the least substrate/most food, and to harvest the least from patches with the most substrate/least food. Furthermore, we predicted that giving-up densities (GUDs) would (1) decrease with greater height (2) increase on the ground when sightlines were blocked, and (3) in a landscape grid, decrease in patches near trees and increase in patches near shrubs. Monkeys harvested the most from the richest patches and the least from the poorest patches. Along a vertical axis, GUDs decreased by 15% from 0.1 m to 2 m, and by 10% from 2 m to 5 m. Along a horizontal axis, GUDs were affected by curtain-blocked sightlines (4.7% higher with curtains), but not by distances to vegetation. We demonstrated that the vertical landscape gradient is more meaningful to Sykes’ monkeys than the terrestrial horizontal. We conclude that experiments with giving-up densities in depletable food patches provide effective means for studying primate ecology.

Bioenergetic Constraints on Primate Abundance

Explaining variation in primate population densities is central to understanding primate ecology, evolution, and conservation. Yet no researchers to date have successfully explained variation in primate population density across dietary class and phylogeny. Most previous work has focused on measures of food availability, as access to food energy likely constrains the number of individuals supported in a given area. However, energy output may provide a measure of energy constraints on population density that does not require detailed data on food availability for a given taxon. Across mammals, many studies have shown that population densities generally scale with body mass−0.75. Because individual energy expenditures scale with body mass0.75, population energy use (the product of population density and individual energy use) does not change with body mass, which suggests the existence of energy constraints on population density across body sizes, i.e., taxa are limited to a given amount of energy use, constraining larger taxa to lower densities. We examined population energy use and individual energy expenditure in primates and tested this energy equivalence across body mass. We also used a residual analysis to remove the effects of body mass on primate population densities and energy expenditures using basal metabolic rates (BMR; kcal/d) as a proxy for total daily energy expenditure. After taking into account phylogeny, population energy use did not significantly correlate with body mass. Larger primates, which use more energy per day, live at lower population densities than smaller primates. In addition, we found a significant negative correlation between residuals of BMR from body mass and residuals of population density from body mass after taking phylogeny into account. Thus, energy costs constrain population density across a diverse sample of primates at a given body mass, and primate species that have relatively low BMRs exist at relatively high densities. A better understanding of the determinants of primate energy costs across geography and phylogeny will ultimately help us explain and predict primate population densities.

Measuring salivary analytes from free-ranging monkeys

Studies of large free-ranging mammals have been revolutionized by non-invasive methods for assessing physiology, which usually involve the measurement of fecal or urinary biomarkers. However, such techniques are limited by numerous factors. To expand the range of physiological variables measurable non-invasively from free-ranging primates, we developed techniques for sampling monkey saliva by offering monkeys ropes with oral swabs sewn on the ends. We evaluated different attractants for encouraging individuals to offer samples, and proportions of individuals in different age/sex categories willing to give samples. We tested the saliva samples we obtained in three commercially available assays: cortisol, salivary alpha amylase, and secretory immunoglobulin A. We show that habituated free-ranging rhesus macaques will give saliva samples voluntarily without training, with 100% of infants, and over 50% of adults willing to chew on collection devices. Our field methods are robust even for analytes that show poor recovery from cotton, and/or that have concentrations dependent on salivary flow rate. We validated the cortisol and SAA assays for use in rhesus macaques by showing aspects of analytical validation, such as that samples dilute linearly and in parallel to assay standards. We also found that values measured correlated with biologically meaningful characteristics of sampled individuals (age and dominance rank). The SIgA assay tested did not react to samples. Given the wide range of analytes measurable in saliva but not in feces or urine, our methods considerably improve our ability to study physiological aspects of the behavior and ecology of free-ranging primates, and are also potentially adaptable to other mammalian taxa.

Seasonal Variations in the Diet and Feeding Effort of Two Groups of Howlers in Different Sized Forest Fragments

Little is known about how resource limitation affects the feeding ecology of primates in forest fragments. Here, we describe seasonal variation in the diet and feeding effort of 2 groups (RH and RC3) of howlers (Alouatta palliata mexicana) living in different sized forest fragments in Los Tuxtlas, Mexico. The RH group, which lived in a larger and more preserved forest fragment, with a higher availability of fruit and Ficus trees, had a higher and more constant consumption of fruit throughout the study year. Moreover, this group fed from larger food sources, i.e., trees, lianas, and shrubs, and spent more time feeding from each food source. The feeding effort, defined as the time spent feeding and traveling divided by time spent resting, of the RH group was also significantly lower and more stable than that of the RC3 group throughout the study year. As feeding effort has been positively related to stress in primates, such increases in feeding effort could have negative consequences for howlers in small or degraded forest fragments. Our study suggests that habitat characteristics interact with plant seasonality to determine the diet and feeding effort of howlers in forest fragments and that groups living in small and degraded forest fragments may be particularly vulnerable to years of low fruit production.

Use of Mineral Licks by White-Bellied Spider Monkeys (Ateles belzebuth) and Red Howler Monkeys (Alouatta seniculus) in Eastern Ecuador

Geophagy occurs in all primate groups and is particularly common in species that consume greater quantities of plant material, i.e., leaves, fruit. The function of geophagy is not fully understood and likely varies over space and time, perhaps in connection with changes in diet. Central to a better understanding of geophagy in primate ecology is knowledge of the occurrence of such behavior among different species and seasons. We used camera traps triggered by heat and motion to document the use of mineral licks by primates over a 3-yr period at a lowland forest site in eastern Ecuador (Tiputini Biodiversity Station). Such mineral licks can be important sources of minerals, nutrients, and other compounds for a wide range of species in Amazonian forests. Although 10 species of primates are known from the study site, we obtained photographs of only 2 species, Ateles belzebuth (white-bellied spider monkey) and Alouatta seniculus (red howler) at 2 of 4 saladeros surveyed. From late December 2004 through early January 2008, we recorded 192 photographs with a total of 318 Ateles belzebuth representing ≥66 separate visits. Comparable numbers for Alouatta seniculus were 80, 121, and 37. We recorded both species visiting a mineral lick at the same time on ≥7 occasions. Use of mineral licks varied across months; we recorded more visits from November through February, the drier period at Tiputini. Visits also varied by hour, with no visits before 0830 or after 1630; Ateles belzebuth showed a stronger mid-day peak in visits. Average visit length (calculated as the time between the first and last photographs of a given visit) was similar between the 2 species but median visit length was more than twice as long for Ateles belzebuth (15 min) as for Alouatta seniculus (6 min). Results indicate that mineral licks are important in the ecology of these species, but further studies are needed to determine the precise benefit(s) obtained and how benefits may vary with diet and other factors.

Beyond competition and predation: Infectious disease as a selective force in primate behavior, ecology, and evolution

Beyond competition and predation: Infectious disease as a selective force in primate behavior, ecology, and evolution

Community ecology of the Middle Miocene primates of La Venta, Colombia: the relationship between ecological diversity, divergence time, and phylogenetic richness

It has been suggested that the degree of ecological diversity that characterizes a primate community correlates positively with both its phylogenetic richness and the time since the members of that community diverged (Fleagle and Reed in Primate communities. Cambridge University Press, New York, pp 92-115, 1999). It is therefore questionable whether or not a community with a relatively recent divergence time but high phylogenetic richness would be as ecologically variable as a community with similar phylogenetic richness but a more distant divergence time. To address this question, the ecological diversity of a fossil primate community from La Venta, Colombia, a Middle Miocene platyrrhine community with phylogenetic diversity comparable with extant platyrrhine communities but a relatively short time since divergence, was compared with that of modern Neotropical primate communities. Shearing quotients and molar lengths, which together are reliable indicators of diet, for both fossil and extant species were plotted against each other to describe the dietary ''ecospace'' occupied by each community. Community diversity was calculated as the area of the minimum convex polygon encompassing all community members. The diversity of the fossil community was then compared with that of extant communities to test whether the fossil community was less diverse than extant communities while taking phylogenetic richness into account. Results indicate that the La Ventan community was not significantly less ecologically diverse than modern communities, supporting the idea that ecological diversification occurred along with phylogenetic diversification early in platyrrhine evolution.

A rod cell marker of nocturnal ancestry

In a recent Cell article, Solovei et al. (2009) have shown that the rod cell nuclei of nocturnal and diurnal mammals (including primates) are organized in distinct patterns, and that the nocturnal-associated pattern likely facilitates efficient photon capture by the photoreceptors. Their research underscores the exceptional selective pressures placed on the visual system in low light environments and provides a new marker of nocturnal ancestry. This marker can be used to advance our understanding of activity pattern evolution, potentially including the behavioral ecology of ancestral primates.