Estrogenicity of captive southern white rhinoceros diets and their association with fertility

Tubbs, Christopher W.; Moley, Laura A.; Ivy, Jamie A.; Metrione, Lara C.; LaClaire, Sydney; Felton, Rachel G.; Durrant, Barbara S.; Milnes, Matthew R.

doi:10.1016/j.ygcen.2016.05.004

Cited by 30 publications

(37 citation statements)

References 24 publications

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“…However, wild SWR now face an uncertain future due to the recent dramatic increase in poaching (2). An additional challenge facing the species is the reproductive failure of the once robust ex situ assurance populations (3, 4). Together, poaching, long gestational length (∼16 months) and intercalving interval (∼2.5 years) (5), and captive infertility (3, 4) have rendered both wild and captive populations no longer self-sustaining.…”

Section: Introductionmentioning

confidence: 99%

“…An additional challenge facing the species is the reproductive failure of the once robust ex situ assurance populations (3, 4). Together, poaching, long gestational length (∼16 months) and intercalving interval (∼2.5 years) (5), and captive infertility (3, 4) have rendered both wild and captive populations no longer self-sustaining. Without any change in poaching rates, wild SWR populations will likely face the threat of extinction within the next 2 decades (6).…”

Section: Introductionmentioning

confidence: 99%

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Gut Microbiota and Phytoestrogen-Associated Infertility in Southern White Rhinoceros

Williams

Ybarra

Meredith

et al. 2019

mBio

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With recent poaching of southern white rhinoceros (SWR [Ceratotherium simum simum]) reaching record levels, the need for a robust assurance population is urgent. However, the global captive SWR population is not currently self-sustaining due to the reproductive failure of captive-born females. Dietary phytoestrogens have been proposed to play a role in this phenomenon, and recent work has demonstrated a negative relationship between diet estrogenicity and fertility of captive-born female SWR. To further examine this relationship, we compared gut microbial communities, fecal phytoestrogens, and fertility of SWR to those of another rhinoceros species—the greater one-horned rhinoceros (GOHR [Rhinoceros unicornis]), which consumes a similar diet but exhibits high levels of fertility in captivity. Using 16S rRNA amplicon sequencing and mass spectrometry, we identified a species-specific fecal microbiota and three dominant fecal phytoestrogen profiles. These profiles exhibited various levels of estrogenicity when tested in an in vitro estrogen receptor activation assay for both rhinoceros species, with profiles dominated by the microbial metabolite equol stimulating the highest levels of receptor activation. Finally, we found that SWR fertility varies significantly not only with respect to phytoestrogen profile, but also with respect to the abundance of several bacterial taxa and microbially derived phytoestrogen metabolites. Taken together, these data suggest that in addition to species differences in estrogen receptor sensitivity to phytoestrogens, reproductive outcomes may be driven by the gut microbiota’s transformation of dietary phytoestrogens in captive SWR females. IMPORTANCE Southern white rhinoceros (SWR) poaching has reached record levels, and captive infertility has rendered SWR assurance populations no longer self-sustaining. Previous work has identified dietary phytoestrogens as a likely cause of this problem. Here, we investigate the role of gut microbiota in this phenomenon by comparing two rhinoceros species to provide the first characterizations of gut microbiomes for any rhinoceros species. To our knowledge, our approach, combining parallel sequencing, mass spectrometry, and estrogen receptor activation assays, provides insight into the relationship between microbially mediated phytoestrogen metabolism and fertility that is novel for any vertebrate species. With this information, we plan to direct future work aimed at developing strategies to improve captive reproduction in the hope of alleviating their threat of extinction.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Gut Microbiota and Phytoestrogen-Associated Infertility in Southern White Rhinoceros

Williams

Ybarra

Meredith

et al. 2019

mBio

Self Cite

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“…In this study conception rates were higher during periods of supplemental feeding, therefore further research into nutritional influences of captive and wild diets on reproduction would be of great value. Previous studies pointed out that phytoestrogens might play a negative role in the reproductive success of captive white rhinoceros [ 17 , 18 , 42 , 43 ].…”

Section: Discussionmentioning

confidence: 99%

“…In fact, only 50% of all captive females reproduce successfully, and only 38% of the females born in captivity have produced offspring [ 5 , 16 ]. In these captive-born a diet-related loss of fertility has been reported as well [ 17 , 18 ]. Interestingly, male-biased sex ratios at birth have long been observed in the captive rhino populations [ 19 ].…”

Section: Introductionmentioning

confidence: 99%

Reproductive performance parameters in a large population of game-ranched white rhinoceroses (Ceratotherium simum simum)

Ververs

Langhout²,

Hostens

et al. 2017

PLoS ONE

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The population of free-roaming white rhinoceroses (Ceratotherium simum) is under serious threat. Captive breeding of this species is therefore becoming more important, but this is challenging and often not successful. Obtaining reproductive reference values is a crucial aspect of improving these breeding results. In this study performed between 2008 and 2016, reproductive performance was analysed in 1,354 animals kept in a 8000 hectares game-ranched environment. Descriptive statistics of this captive population showed an average annual herd growth (%) of 7 .0±0.1 (min -9 –max 15). Average calving rates were calculated as an annual calving rate of 20% and biennial calving rate of 37% adult females calving per year. Females had a median age of 83.2 months at first calving (IQR 72.9–110.7) and inter-calving intervals of 29.2 (IQR 24.6–34.8) months. Furthermore, translocations of animals did not interfere with reproductive success in terms of inter-calving periods or age at first calving. Multivariate models showed a clear seasonal calving pattern with a significant increase of the number of calvings during December–April when compared to April–December. Our results did not show any significant skewed progeny sex ratios. Weather observations showed no significant influence of rain or season on sex ratios of the calves.

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“…Feeding cattle and sheep on forage that is high in phytoestrogens induces female infertility [35]. Similarly, a recent study on the effects of diet on captive white rhinoceros discovered that lowering the phytoestrogen content of their feed significantly improved breeding success for this critically endangered species [36]. These few examples highlight the fundamental need to monitor reproductive fitness and health in both wild species and humans.…”

Section: Commonalities Between Wild Species and Human Fertility Issuesmentioning

confidence: 99%

The mutual benefits of research in wild animal species and human-assisted reproduction

Comizzoli

Paulson

McGinnis

2018

J Assist Reprod Genet

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Studying the reproductive biology of wild animal species produces knowledge beneficial to their management and conservation. However, wild species also share intriguing similarities in reproductive biology with humans, thereby offering alternative models for better understanding the etiology of infertility and developing innovative treatments. The purpose of this review is to raise awareness in different scientific communities about intriguing connections between wild animals and humans regarding infertility syndromes or improvement of fertility preservation. The objectives are to (1) highlight commonalities between wild species and human fertility, (2) demonstrate that research in wild species-assisted reproductive technologies can greatly enhance success in human reproductive medicine, and (3) recognize that human fertility preservation is highly inspiring and relevant to wild species conservation. In addition to having similar biological traits in some wild species and humans, the fact of sharing the same natural environment and the common needs for more options in fertility preservation are strong incentives to build more bridges that will eventually benefit both animal conservation and human reproductive medicine.

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Estrogenicity of captive southern white rhinoceros diets and their association with fertility

Cited by 30 publications

References 24 publications

Gut Microbiota and Phytoestrogen-Associated Infertility in Southern White Rhinoceros

Gut Microbiota and Phytoestrogen-Associated Infertility in Southern White Rhinoceros

Reproductive performance parameters in a large population of game-ranched white rhinoceroses (Ceratotherium simum simum)

The mutual benefits of research in wild animal species and human-assisted reproduction

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