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

Abstract

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.

The methanol-soluble fraction of Millettia macrophylla (Fabaceae) stem bark endowed with estrogenic properties has adverse effects on the male reproductive system of Wistar rats

“…The absence of ejaculation observed in animals treated with different doses of the MeOH extract of M. macrophylla strengthens the hypothesis that the copulation parameters have been impaired in these animals. These observations are in line with those of Wasserman et al who demonstrated sexual behavioral changes of male primates fed with the estrogenic young leaves of M. dura [32].…”

“…Despite such benefit in women, there is growing concern about the long-term consequences of exposure to these chemicals due to their capacity to disturb the hormonal systems in both women and men, which can lead to adverse health effects [29][30][31]. For instance, Wasserman et al [32] reported that the consumption of estrogenic Millettia dura young leaves by male red colobus (Procolobus rufomitratus) resulted in an increase of estradiol levels, which modified the social behavior (aggression, mating, and grooming) of this primate [32].…”

Baseline review and ecosystem services assessment of the Tana River Basin, Kenya

“…At issue here is that while planting various Eucalyptus spp. should in theory provide a source of fast-growing fuelwood and help preserve indigenous tree species, its popularity and demand has led to widespread expansion and undermined Colobus habitat and social behavior (Wasserman et al 2012). …”

Endocrine disruption of gene expression and microRNA profiles in hippocampus and hypothalamus of California mice: Association of gene expression changes with behavioural outcomes

“…Perinatal exposure of male mice to GEN led to significant changes in anxiety and aggressive behaviours 83 . In red colobus monkeys ( Procolobus rufomitratus ), consumption of plants containing phyto‐oestrogens was strongly associated with increased aggression and copulation rates but a reduced time spent grooming 84 . Soy infant formula consumption in humans correlates with reduced female‐typical play behaviour in girls and an increased risk of autistic behaviours 11,12 …”