Infertility in the Southern White Rhino: is diet the source of the problem?

As numerous species find themselves in peril due to human activity, the need to develop captive breeding strategies to save the most endangered among them has taken on an elevated sense of urgency. The Southern White Rhinoceros (Ceratotherium simum simum) has made a remarkable comeback in the wild but is still considered threatened due to habitat loss and poaching. Unfortunately, females born in captivity are subfertile, a phenomenon that is generating the risk of a significant population crash if the source of the problem cannot be identified. Numerous hypotheses including reproductive suppression by other females and continual close proximity to males have been purported and successively unsubstantiated. Could it come down to something as simple as diet? In this issue of Endocrinology, Tubbs et al. (26) provide evidence that it very well could. Their data suggest that the fertility of captive rhinos is being compromised, not by malnutrition but through endocrine disruption by phytoestrogens. Zoo animals receive zoo food. The goal of a zoo diet is to recapitulate the wild diet as closely as possible, but sometimes this is not economical or practical. Cheetahs, for example, are carnivores. In the wild they chase and capture prey to survive, and the biomechanical marvel, which is a body built for speeds achievable by no other land mammal, evinces the long history of evolutionary pressures constraining them to excel at this one pivotal task. They do not graze on the sea of grass that camouflages their whereabouts from the objects of their gustatory desires, nor could they perceive it as food, even when faced with starvation. Thus, it may seem odd that a zoo would elect to rear a captive population on soy-based cheetah chow, but from a fiscal and practical standpoint, it makes a certain amount of sense. Soy is a whole protein (meaning it contains all of the essential amino acids), making it a mainstay for most vegetarians. It is also lactose free, low in cholesterol, cheap, easy to obtain, and more acceptable to distribute to a hungry carnivore in front of a zoo full of visitors than, say, a baby gazelle. But cheetahs did not evolve to consume soy and the diversity of endocrine disrupting phytochemicals it contains. They become sick. In a case strikingly similar to that of the Southern White Rhinoceros, by the mid-1980s reproductive and liver disease threatened to derail the captive breeding program for the cheetah (1). The isoflavone phytoestrogens genistein and daidzein (Table 1) were to blame. Could a similar situation be affecting an herbivore like the Southern White Rhinoceros, a species that evolved to graze? Phytoestrogens are nonsteroidal, estrogen-like compounds produced by plants, most notably the legumes (2), and play an important role in plant defense (3) including the recruitment of nitrogen fixing bacteria (4) and conferring resistance to fungi (5). Thus, plants produce them when under stress including disease, drought, and extreme temperatures. There are several classes of phytoestrogens (Table 1), all of which structurally resemble mammalian estrogens, and many are capable of binding and activating nuclear estrogen receptors (EsR1 and EsR2) (6). The most well-known class, the isoflavones, are most abundant in soybeans and soy-based foods, whereas the coumestans are prevalent in alfalfa, clover, and other pasture legumes such as the ones rhinos and other herbivores might graze on. It is the coumestans that appear to be contributing to the reproductive impairments reported in captive born Southern White Rhinoceros.