Selecting between iron-rich and clay-rich soils: a geophagy field experiment with black-and-white colobus monkeys in the Budongo Forest Reserve, Uganda.

Geophagy, the intentional consumption of soil, has been observed in humans and numerous other animal species. Geophagy has been posited to be adaptive, i.e., consumed soil protects against gastrointestinal distress and/or supplements micronutrients. We conducted a field experiment in the Budongo Forest, Uganda, to investigate geophagic behaviors, including soil preference, the quantity of soil eaten, and competition for access to preferred soils. We placed pairs of artificial tree stumps at two existing geophagy sites. One stump contained soil from the surrounding area, Sonso, that could supplement bioavailable iron. The other stump contained soil from a neighboring community, Waibira, that was richer in clay minerals, which could provide protection from plant secondary compounds. We monitored activity and engagement with the stumps for 10 days using camera traps. After 5 days, we reversed the type of soil that was in the stumps at both sites (i.e., a crossover design). Only Colobus guereza (black-and-white colobus monkeys) interacted with the stumps. These monkeys used visual and olfactory cues to select between the two soils and exclusively ate the clay-rich soil, consuming 9.67 kg of soil over 4.33 h. Our findings lend the greatest plausibility to the protection hypothesis. Additionally, monkeys competed for access to the stumps, and 13% of the videos captured aggression, including pushing, excluding, and chasing other individuals from the experimental stumps. Nine episodes of vigilance and flight behavior were also observed. Given that intentionally ingested soil is a valuable resource that may confer health benefits, geophagy sites should be conserved and protected.

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.

Mating behavior and endocrine profiles of wild black and white Colobus monkeys (Colobus guereza): toward an understanding of their life history and mating system.

Black and white colobus monkeys (Colobus guereza, "guerezas") show no external signs of estrus, and little is known about their mating behavior or reproductive endocrinology. To learn more about the life history characteristics and mating system of guerezas, we documented the mating behavior and ovarian hormone profiles of 10 cycling, lactating, and pregnant females in a wild population. We studied six groups of guerezas in Kibale National Park, Uganda, and collected ad libitum data on their mating behavior. We collected urine samples every 1.9+/-0.2 days from potentially fertile females and quantified conjugated urinary estrogen (E1S) and progesterone (PdG) metabolites using enzyme immunoassay (EIA). Females solicited 50.5% of copulations, and most copulations occurred during the interval starting 5 days before presumptive ovulation and ending 2-3 days later, with the highest copulatory levels occurring close to ovulation. We show that the median ovarian cycle length is 24 days, the median gestation length is approximately 158 days, the length of lactational amenorrhea is at least 7-8 months, and the median interbirth interval for females with surviving infants is approximately 22 months. We also document overlap between females' receptive periods in one-male, two- to three-female groups, which may mean that male transfer into such groups is potentially profitable.

Behavioral and endocrine dynamics associated with infanticide in a black and white colobus monkey (Colobus guereza).

Infanticide has been observed in several colobines, but only one infanticide has previously been documented for black and white colobus monkeys (Colobus guereza). This report describes an infanticide observed in Kibale National Park, Uganda, in the summer of 2001. An adult male from a neighboring group attacked and killed a young infant whose mother subsequently remained in her own group and was observed mating 10 days later. She engaged in two mating periods of several days each, separated by approximately 1 month, during which she copulated frequently with the dominant male within her group. Urinary estrogen (EC) and progesterone metabolite (PdG) excretion patterns demonstrated that the female resumed ovarian cycling soon after the infanticide. Because the infanticidal male did not attempt to mate with the victim's mother, his actions were not consistent with the predictions of the sexual-selection hypothesis. We speculate that infanticide associated with intergroup aggression may help secure access to high-quality resources for the infanticidal male's group.