A novel mode of embryonic nutrition in the tiger shark,<i>Galeocerdo cuvier</i>

Castro, José Ignacio Fernández del; Sato, Keiichi; Bodine, A.B.

doi:10.1080/17451000.2015.1099677

Cited by 34 publications

(25 citation statements)

References 11 publications

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“…In aplacentary viviparous elasmobranchs, it has been assumed that the endometrium is not specialized to secrete nutrients to the embryo, participating only in the breathing process and osmoregulation (Hamlett et al 1999). However, various evidences have indicated that some lecitotrophic species, such as Centrophorus granulosus (Cotton et al 2015), M. antarcticus (Storrie et al 2009) and Galeocerdo cuvier (Castro et al 2016) do present some level of matrotrophy.…”

Section: Discussionmentioning

confidence: 99%

Morphological description of ovary and uterus of the nurse shark (Ginglymostoma cirratum) caught off at the Fortaleza coast, Northeast Brazil

et al. 2019

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The nurse shark, Ginglymostoma cirratum (Bonnaterre, 1778) is one of the most studied species of elasmobranchs. However, the knowledge of their reproductive biology is still relatively rare, particularly in the western South Atlantic. This study aimed to describe the morphology of the uterus and the ovary of G. cirratum, based on specimens caught off at the Fortaleza/CE coast, northeast Brazil. Samples were collected from September 2012 to June 2013, from regular landings of artisanal fishing, which commercialize this species freely. A total of ten females were collected. The methodologies followed for analyzing the ovaries and uterus of those females included both macroscopic and histological analysis. G. cirratum has internal type ovary morphology, with invaginations of connective tissue, which defines compartments and separate oocyte groups in ovigerous lots. The epithelium lining the ovary changes from simple columnar ciliated in the area without ovigerous lots, which turns into a simple cubic epithelium in the coating portion of the epigonal organ where ovarian tissue is absent. The uterine mucosa has secretory cells denoted by Alcian Blue staining, indicating the production of mucopolysaccharides, even in immature individuals. This lecithotrophic shark has a uterine vascularized mucosa that is one characteristic of viviparous elasmobranch species.

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Section: Discussionmentioning

confidence: 99%

Morphological description of ovary and uterus of the nurse shark (Ginglymostoma cirratum) caught off at the Fortaleza coast, Northeast Brazil

et al. 2019

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“…A viviparous reptile possesses a placentalike structure similar to those found in eutherians (8). In some viviparous chondrichthyans and teleosts, a nutrient-rich liquid is supplied to the embryo in the ovary during gestation (9,10). Diverse mechanisms of mother-to-embryo nutrient supply occur among viviparous vertebrates.…”

Section: Introductionmentioning

confidence: 98%

Mother-to-embryo vitellogenin transport in a viviparous teleostXenotoca eiseni

Iida

Arai

Someya

et al. 2019

Preprint

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Vitellogenin (Vtg), a yolk nutrient protein that is synthesized in the livers of female animals, and subsequently carried into the ovary, contributes to vitellogenesis in oviparous animals. Thus, Vtg levels are elevated during oogenesis. In contrast, Vtg have been genetically lost in viviparous mammals, thus the yolk protein is not involved in their oogenesis and embryonic development. In this study, we identified Vtg protein in the livers of females during the gestation of the viviparous teleost, Xenotoca eiseni.Although vitellogenesis is arrested during gestation, biochemical assays revealed that Vtg protein was present in ovarian tissues and lumen fluid. The Vtg protein was also detected in the trophotaenia of the intraovarian embryo. Immunoelectron microscopy revealed that Vtg protein is absorbed into intracellular vesicles in the epithelial cells of the trophotaenia. Furthermore, extraneous Vtg protein injected into the abdominal cavity of a pregnant female was subsequently detected in the trophotaenia of the intraovarian embryo. Our data suggest that the yolk protein is one of the matrotrophic factors supplied from the mother to the intraovarian embryo during gestation in X. eiseni. To our knowledge, this is the first report of the experimental verification of mother-to-embryo substance transport in a viviparous teleost.Breeding and experiments were performed in the laboratory of Dr. Atsuko Sehara-Fujisawa. We thank Yoshiko Aihara for helpful discussion. Ryo Kurokawa helped with the sample collection. This work was supported by crowdfunding via The Academist, Inc. The crowdfunding investors for this project were

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“…Recent studies suggest many lecithotrophic sharks have secretory tissues associated with their uterine walls, implying that maternal nourishment likely occurs in these species ( Hamlett et al, 2005 ; Cotton et al, 2015 ). These forms are classified as ‘mucoid histotrophy’ ( Conrath and Musick, 2012 ) when mucus-secreting cells are evident in the uterus; ‘embryotrophy’ ( Castro et al, 2016 ) when there is lipid-free but energy-rich uterine fluid evident, or ‘lipid histotrophy’ when trophonemata produce copious amounts of yellowish, milky secretions (currently known only in batoids). No histological or histochemical examination has ever been conducted on a white shark uterus throughout its gestation period because the white shark is listed as ‘Vulnerable’ on the IUCN Red List ( , 2016), therefore, there have been very few opportunities to observe pregnant females or to study the histology of the uterus.…”

Section: Introductionmentioning

confidence: 99%

How great white sharks nourish their embryos to a large size: evidence of lipid histotrophy in lamnoid shark reproduction

et al. 2016

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The great white shark (Carcharodon carcharias) exhibits viviparous and oophagous reproduction. A 4950 mm total length (TL) gravid female accidentally caught by fishermen in the Okinawa Prefecture, Southern Japan carried six embryos (543-624 mm TL, three in each uterus). Both uteri contained copious amounts of yellowish viscous uterine fluid (over 79.2 litres in the left uterus), nutrient eggs and broken egg cases. The embryos had yolk stomachs that had ruptured, the mean volume of which was approximately 197.9 ml. Embryos had about 20 rows of potentially functional teeth in the upper and lower jaws. Periodic acid Schiff (PAS)-positive substances were observed on the surface and in the cytoplasm of the epithelial cells, and large, secretory, OsO4-oxidized lipid droplets of various sizes were distributed on the surface of the villous string epithelium on the uterine wall. Histological examination of the uterine wall showed it to consist of villi, similar to the trophonemata of Dasyatidae rays, suggesting that the large amount of fluid found in the uterus of the white shark was likely required for embryo nutrition. We conclude that: (1) the lipid-rich fluid is secreted from the uterine epithelium only in early gestation before the onset of oophagy, (2) the embryos probably use the abundant uterine fluid and encased nutrient eggs for nutrition at this stage of their development, and (3) the uterine fluid is the major source of embryonic nutrition before oophagy onset. This is the first record of the lipid histotrophy of reproduction among all shark species.

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A novel mode of embryonic nutrition in the tiger shark,Galeocerdo cuvier

Cited by 34 publications

References 11 publications

Morphological description of ovary and uterus of the nurse shark (Ginglymostoma cirratum) caught off at the Fortaleza coast, Northeast Brazil

Morphological description of ovary and uterus of the nurse shark (Ginglymostoma cirratum) caught off at the Fortaleza coast, Northeast Brazil

Mother-to-embryo vitellogenin transport in a viviparous teleostXenotoca eiseni

How great white sharks nourish their embryos to a large size: evidence of lipid histotrophy in lamnoid shark reproduction

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