Viviparous stingrays avoid contamination of the embryonic environment through faecal accumulation mechanisms

Taketeru Tomita,Kiyomi Murakumo,Masaru Nakamura,Yasuhisa Kobayashi,Atsushi Yoshinaka

doi:10.1038/s41598-020-64271-2

Taketeru Tomita, Kiyomi Murakumo + Show 3 more

Open Access

https://doi.org/10.1038/s41598-020-64271-2

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Abstract

In viviparous (live-bearing) animals, embryos face an embryo-specific defecation issue: faecal elimination in utero can cause fatal contamination of the embryonic environment. Our data from the viviparous red stingray (Hemitrygon akajei) reveals how viviparous elasmobranchs circumvent this issue. The exit of the embryonic intestine is maintained closed until close to birth, which allows the accumulation of faeces in the embryonic body. Faecal accumulation abilities are increased by (1) the large intestine size (represents about 400–600% of an adult intestine, proportionally), and (2) the modification in the intestinal inner wall structure, specialized to increase water uptake from the faecal matter. According to the literature, faecal accumulation may occur in embryos of the lamniform white shark as well. The reproductive biology of myliobatiform stingrays and lamniform sharks is characterized by the onset of oral feeding before birth (i.e. drinking of uterine milk and eating of sibling eggs, respectively), which is expected to result in the production of large amounts of faeces during gestation. The strong ability of faecal accumulation in these lineages is therefore likely an adaptation to their unique embryonic nutrition mechanism.

Highlights

In viviparous animals, embryos face an embryo-specific defecation issue: faecal elimination in utero can cause fatal contamination of the embryonic environment
The embryo of viviparous animals faces an embryo-specific defecation issue: the passage of faeces in utero fatally contaminates the uterine environment[7]. This issue should be critical in lipid histotrophy as (1) active digestion should produce a large amount of undigested materials and (2) the functional stomach and intestine frequently renew epithelial cells, both increasing the rate of faecal production during gestation
This phenomenon is supported by three lines of evidence: (1) the rectal canal is kept closed at the junction between the intestine and rectum until close to birth, which prevents the passage of faeces through the rectum; (2) the embryonic intestine is largely filled with faecal matters; and (3) the newborn juveniles of some myliobatiform stingrays, Himantura uarnak and Urogymnus asperrimus, were observed to eliminate faeces before the first food intake after birth (K.M., unpublished data based on five observations at Okinawa Churaumi Aquarium between 2016–2019)

Summary

Introduction

In viviparous (live-bearing) animals, embryos face an embryo-specific defecation issue: faecal elimination in utero can cause fatal contamination of the embryonic environment. The embryo of viviparous animals faces an embryo-specific defecation issue: the passage of faeces in utero fatally contaminates the uterine environment[7] This issue should be critical in lipid histotrophy as (1) active digestion should produce a large amount of undigested materials and (2) the functional stomach and intestine frequently renew epithelial cells, both increasing the rate of faecal production during gestation. The present study reports for the first time faecal accumulation abilities in embryos of red stingray Hemitrygon akajei (Myliobatiformes, Dasiatidae), which is likely the mechanism allowing maintenance of a clean uterine environment This species is commonly distributed around the main island of Japan, and its reproductive features were well described by ref. The aim of the present study was double: first, describe the ability of faecal accumulation in red stingray embryos, and explore the morphological features that allow this ability

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