Genetic, spatial, and social relationships among adults in a group of howler monkeys (Alouatta palliata) from Barro Colorado Island, Panama.

Kinship plays an important role in the social behavior of many primate species, including patterns of intra-group affiliation and cooperation. Within social groups, kinship is strongly affected by dispersal patterns, with the degree of relatedness among group-mates expected to decrease as the tendency to disperse increases. In primate species characterized by bisexual dispersal, relatedness among adult group-mates is predicted to be low, with social interactions shaped largely by factors other than kinship. To date, however, few studies have examined the role of kinship in social interactions in bisexually dispersing species. Accordingly, we collected genetic, spatial and behavioral data on all adult members (three males, six females) in a group of free-ranging mantled howler monkeys (Alouatta palliata)--a bisexually dispersing species of atelid primate--from Barro Colorado Island (BCI), Panama. Analyses of microsatellite variation revealed that relatedness was greater among adult males in this group (mean pairwise relatedness = 0.32 for males versus 0.09 for females). Relatedness among individuals, however, was not associated with either spatial proximity or frequency of social interactions. Instead, sex was a better predictor of both of these aspects of social behavior. While relatedness among adults had no discernible effect on the intra-group social interactions documented in this study, we postulate that kinship may facilitate affiliative and cooperative behaviors among male group-mates when interacting competitively with neighboring howler groups over access to food or potential mates.

Differential effects of unusual climatic stress on capuchin (Cebus capucinus) and howler monkey (Alouatta palliata) populations on Barro Colorado Island, Panama.

Though the harmful effects anthropogenic disturbances pose to wild primates are well appreciated, comparatively little is known about the effects of natural disturbances. From December 2010 to January 2011, different mortality patterns were observed for two primate species, capuchins and howler monkeys, on Barro Colorado Island (BCI), Panama. Unusually high rainfall in 2010 was associated with census and cadaver data indicating the rapid loss of >70% of the capuchin population in late 2010 to early 2011. In contrast, over this same period, no decline was documented for howler monkeys and cadaver data for howlers was unexceptional. The high mortality experienced by the capuchin population was unexpected and its extent was not fully appreciated until the event was largely over. Explanations proposed for it included effects of hypothermia, disease or a shortage of some essential nutrient(s). Of these, the dietary explanation seems most probable. BCI capuchins depend most heavily on arthropod foods in December, when few higher quality ripe fruits are available. The unprecedented high rainfall in December 2010 is hypothesized to have largely eliminated the arthropod peak expected on BCI each December. A lack of protein-rich arthropods, when coupled with the climatic and nutritional stress capuchins generally experience at this time of year, appears to have precipitated the rapid die-off of most of the island's capuchin population. As howler monkeys obtain dietary protein primarily from leaves, a shortage of edible arthropods would not affect howler numbers. Comparison of our 2010 data with similar data on earlier primate/mammalian mortality events reported for BCI and for Corcovado, Costa Rica indicates that our understanding of the effects of natural disturbances on wild primate populations is not profound. We suggest that more research be devoted to this increasingly timely topic, so important to conservation policy.

Estrogenic plant consumption predicts red colobus monkey (Procolobus rufomitratus) hormonal state and behavior.

Numerous studies have examined the effects of anthropogenic endocrine disrupting compounds; however, very little is known about the effects of naturally occurring plant-produced estrogenic compounds (i.e., phytoestrogens) on vertebrates. To examine the seasonal pattern of phytoestrogen consumption and its relationship to hormone levels (407 fecal samples analyzed for estradiol and cortisol) and social behavior (aggression, mating, and grooming) in a primate, we conducted an 11-month field study of red colobus (Procolobus rufomitratus) in Kibale National Park, Uganda. The percent of diet from estrogenic plants averaged 10.7% (n=45 weeks; range: 0.7-32.4%). Red colobus fed more heavily on estrogenic Millettia dura young leaves during weeks of higher rainfall, and the consumption of this estrogenic item was positively correlated to both their fecal estradiol and cortisol levels. Social behaviors were related to estradiol and cortisol levels, as well as the consumption of estrogenic plants and rainfall. The more the red colobus consumed estrogenic plants the higher their rates of aggression and copulation and the lower their time spent grooming. Our results suggest that the consumption of estrogenic plants has important implications for primate health and fitness through interactions with the endocrine system and changes in hormone levels and social behaviors.

Estrogenic plant foods of red colobus monkeys and mountain gorillas in Uganda.

Phytoestrogens, or naturally occurring estrogen-mimicking compounds, are found in many human plant foods, such as soybeans (Glycine max) and other legumes. Because the consumption of phytoestrogens may result in both health benefits of protecting against estrogen-dependent cancers and reproductive costs of disrupting the developing endocrine system, considerable biomedical research has been focused on the physiological and behavioral effects of these compounds. Despite this interest, little is known about the occurrence of phytoestrogens in the diets of wild primates, nor their likely evolutionary importance. We investigated the prevalence of estrogenic plant foods in the diets of two folivorous primate species, the red colobus monkey (Procolobus rufomitratus) of Kibale National Park and mountain gorilla (Gorilla beringei) of Bwindi Impenetrable National Park, both in Uganda. To examine plant foods for estrogenic activity, we screened 44 plant items (species and part) comprising 78.4% of the diet of red colobus monkeys and 53 plant items comprising 85.2% of the diet of mountain gorillas using transient transfection assays. At least 10.6% of the red colobus diet and 8.8% of the gorilla diet had estrogenic activity. This was mainly the result of the red colobus eating three estrogenic staple foods and the gorillas eating one estrogenic staple food. All estrogenic plants exhibited estrogen receptor (ER) subtype selectivity, as their phytoestrogens activated ERß, but not ERα. These results demonstrate that estrogenic plant foods are routinely consumed by two folivorous primate species. Phytoestrogens in the wild plant foods of these two species and many other wild primates may have important implications for understanding primate reproductive ecology.

Ferment in the family tree: does a frugivorous dietary heritage influence contemporary patterns of human ethanol use?

Humans and apes are placed together in the superfamily Hominoidea. The evolutionary trajectory of hominoids is intimately bound up with the exploitation of ripe, fleshy fruits. Fermentation of fruit sugars by yeasts produces a number of alcohols, particularly ethanol. Because of their pre-human frugivorous dietary heritage, it has been hypothesized that humans may show pre-existing sensory biases associating ethanol with nutritional rewards. This factor, in turn, could influence contemporary patterns of human ethanol use. At present, there seems little evidence to support a view of selection specifically for ethanol detection or its utilization over the course of hominoid evolution. Ethanol concentration in wild fruits consumed by monkeys and apes is predicted to be low. Wild monkeys and apes avoid consumption of over-ripe fruits, the class showing notable ethanol concentrations, and for this reason, ethanol plumes may act as deterrents rather than attractants. Any energetic benefits to wild primates from ingested ethanol appear negligible, at best. Mice and rats show patterns of ethanol self-administration similar to humans, indicating that a frugivorous dietary heritage is not necessary for such behaviors. In the natural environment, ethanol is predicted to be just one of many alcohols, esters and related compounds routinely encountered by frugivorous primates and of no particular significance. The strong attraction ethanol holds for some individuals could be due to a broad range of genetic and environmental factors. In some humans, the appetite for ethanol appears related to the appetite for sugar. The predisposition some individuals display toward excessive ethanol consumption could involve features of their genetics and biochemical similarities of ethanol and carbohydrate. Regular low ethanol intake is hypothesized to lower the incidence of cardiovascular disease in humans, perhaps through its effects on body fat distribution. Such a benefit, if confirmed, would appear to relate to features of the contemporary human rather than pre-human diet.

The critical role played by animal source foods in human (Homo) evolution.

Wild primates take most of the daily diet from plant sources, eating moderate to small amounts of animal source foods (ASF). Plant materials make up from 87% to >99% of the annual diet of great apes, the closest living relatives of modern humans (Homo sapiens sapiens). Reflecting their close genetic relationship, gut form and nutrient requirements of apes and humans (Hominoidea) are very similar, as is their pattern of digestive kinetics-one predicated on a relatively slow turnover of ingesta. In plant-eating mammals, in contrast to carnivorous mammals, greater body size is associated with lower dietary quality. Turning to ASF as a routine rather than occasional dietary component would have permitted the evolving human lineage to evade the nutritional constraints placed on body size increases in apes. Without routine access to ASF, it is highly unlikely that evolving humans could have achieved their unusually large and complex brain while simultaneously continuing their evolutionary trajectory as large, active and highly social primates. As human evolution progressed, young children in particular, with their rapidly expanding large brain and high metabolic and nutritional demands relative to adults would have benefited from volumetrically concentrated, high quality foods such as meat. Today, many humans, particularly those in high income nations, have a variety of high quality, non-ASF dietary alternatives, but such foods were not generally available to paleolithic human ancestors nor to many people today in low income nations.

Micronutrient intakes of wild primates: are humans different?

Low micronutrient intake is implicated in a diversity of human health problems, ranging from problems associated with food insufficiency to those associated with food over-consumption. Humans are members of the order primates, suborder anthropoidea, and are most closely related to the great apes. Humans and apes are remarkably similar biologically. In the wild, apes and monkeys consume diets composed largely of plant foods, primarily the fruits and leaves of tropical forest trees and vines. Considerable evidence indicates that the ancestral line giving rise to humans (Homo spp.) was likewise strongly herbivorous (plant-eating). The wild plant parts consumed by apes and monkeys show moderate to high levels of many minerals and vitamins. The estimated daily intake of specific minerals, vitamin C and some other vitamins by wild primates is often quite high in comparison to intake levels of these same micronutrients recommended for humans. Are the high micronutrient intakes of wild primates simply a non-functional, unavoidable by-product of their strongly plant-based diets or might they actually be serving important as yet undetermined immunological or other beneficial functions? A better understanding of the basis for this apparent difference between humans and wild primates could help to clarify the range and proportions of micronutrients best suited for optimal human development, health and longevity.

Natural selection on molar size in a wild population of howler monkeys (Alouatta palliata).

Dental traits have long been assumed to be under selection in mammals, based on the macroevolutionary correlation between dental morphology and feeding behaviour. However, natural selection acting on dental morphology has rarely, if ever, been documented in wild populations. We investigated the possibility of microevolutionary selection on dental traits by measuring molar breadth in a sample of Alouatta palliata (mantled howler monkey) crania from Barro Colorado Island (BCI), Panama. The age at death of the monkeys is an indicator of their fitness, since they were all found dead of natural causes. Howlers with small molars have significantly decreased fitness as they die, on average, at an earlier age (well before sexual maturity) than those with larger molars. This documents the existence of phenotypic viability selection on molar tooth size in the BCI howlers, regardless of causality or heritability. The selection is further shown to occur during the weaning phase of A. palliata life history, establishing a link between this period of increased mortality and selection on a specific morphological feature. These results provide initial empirical support for the long-held assumption that primate molar size is under natural selection.

Features of meat digestion by captive chimpanzees (Pan troglodytes).

The pronounced carnivory of many human populations contrasts sharply with feeding habits of other Hominoidea. Of extant great apes, only chimpanzees (Pan spp.) actively seek out vertebrate prey, but meat is only a minor portion of their diet. Some accounts suggest that wild chimpanzees digest prey inefficiently. To investigate the capacity of chimpanzees to digest meat, feeding trials were carried out on three captive chimpanzees (Pan troglodytes) using a fixed amount of nonpurified diet with and without a predetermined amount of boned cooked chicken. The results showed no significant differences in the rate of passage of digesta and digestion of diets with and without chicken. Meat ingestion did not change the nitrogen (N) concentration of feces or the total amount of N defecated. Visual inspection of fecal matter showed no evidence of undigested meat. Taken together, the results indicate that chimpanzees are able to digest meat of the type and quantity consumed during these trials.

Evidence for insectivory in two primate species (Callicebus torquatus lugens and Lagothrix lagothricha lagothricha) from northwestern Amazonia.

Insects were recovered and identified from stomach contents of two Callicebus torquatus lugens and one Lagothrix lagothricha lagothricha collected in a remote area of northwestern Amazonia. Both C. torquatus lugens showed little insect matter in stomach contents. Conversely, a minimum of 133 individual insects were recovered from stomach contents of the L. lagothricha lagothricha. These included various larger, rapid forms (Cicadellidae) unlikely to have been inadvertently consumed while the animal was eating fruit.

Aspects of dietary quality, nutrient assimilation and water balance in wild howler monkeys (Alouatta palliata).

Wild howler monkeys were fed natural fruit and leaf diets in order to determine their ability to assimilate minerals (Ca, P, Mg, Si, Sr, Ba, Fe, Al, Mn, B, Cu, Li, V), and to assess their water and electrolyte budgets by the balance method. Results were extrapolated to the field situation so that the nutritional status of free-living monkeys could be examined in relation to their diet. The figs and young leaves of Ficus insipida and F. yoponensis trees (the most important foods in the dry season) provide adequate amounts of most required minerals, and an abundance of water. However, the copper requirement would not be met by this diet, which also provides only marginal amounts of sodium and phosphorus. These deficiencies may be corrected by consuming other available food items that are rich in Cu, Na or P. These results help explain the diversity that has been observed in the diet of wild howler monkeys, and suggest that these herbivores should feed selectively in order to obtain a nutritionally adequate diet.