Feeding on Phytoestrogens: Implications of Estrogenic Plants for Primate Ecology

As most primates depend heavily on plant foods, the chemical composition of edible plant parts, both nutritional and detrimental, are of key importance in understanding primate ecology and evolution. One class of plant compounds of strong current interest due to their potential ability to alter the fertility, fecundity, and survival of both males and females are phytoestrogens. These plant compounds mimic the activity of vertebrate estrogens mainly through binding with the estrogen receptors, which results in altered physiology and behavior. Considerable evidence of interactions between phytoestrogens and the vertebrate endocrine system comes from research conducted on the potential health benefits and reproductive costs of phytoestrogens in human foods, especially soybeans (Glycine max) and other legumes. Despite this interest, little is known about the occurrence of estrogenic plants in the diets of wild primates. If wild primates do consume phytoestrogens, then the physiological and behavioral effects documented in captive and laboratory studies may promote differential survival and reproduction of individuals in a natural setting. Consequently, estrogenic plants would have an important, thus far neglected, role in primate ecology and evolution./nTo examine the occurrence of estrogenic plants in the diets of wild primates, I screened plant foods for estrogenic activity in two strongly 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 if the consumption of phytoestrogens relates to physiological changes in a wild primate, I determined the seasonal pattern of estrogenic plant consumption and its relationship to hormone levels of the red colobus in Kibale during an 11-month field study. I screened 44 plant items 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 bound to and activated ERβ, but not ERα. Climatic factors were important for understanding variation in the proportion of diet coming from estrogenic plants for the red colobus, particularly for the consumption of Millettia dura young leaves. Although red colobus did not feed more heavily on M. dura young leaves when they were more available, they did feed more heavily on them during months of higher rainfall. Both fecal estradiol and fecal cortisol levels were positively related to the percent of diet from estrogenic M. dura young leaves. Thus, it appears that climatic factors may influence the intake of estrogenic plant foods by red colobus and that the consumption of estrogenic plant foods influences the hormone levels of these monkeys. These results show that phytoestrogens occur in the wild plant foods of at least two Ugandan primate species and suggest that consumption of estrogenic plants by red colobus monkeys may have important implications for their health and fitness through interactions with the endocrine system. Future studies should build upon these results by examining the prevalence of estrogenic plants in the diets of other primate species, especially frugivores, and by determining if the hormonal changes documented here translate into important physiological and behavioral changes that affect reproduction and survival. Phytoestrogens in the diets of wild primates may have important implications for understanding primate ecology and may provide insight into both non-human and human evolution.

Advisor: Milton, Katharine