Oviduct, Egg, and Egg Sac Structures in the Siberian Salamander, Salamandrella keyserlingii (Caudata, Hynobiidae): a Histological and Histochemical Study

Vadim Vadimovich Yartsev, Jean-Marie Exbrayat, Valintina Nikolaevna Kuranova


Unraveling morphological and chemical features of the eggs’ jelly layers and other clutch elements, formed by the oviduct of a female, is necessary for the understanding of reproductive adaptation in amphibians. Our study is the first microstructural and histochemical descriptions about the complexity of oviduct, ovisac, jelly layer of the ovum, and egg sac in hynobiid salamanders. We examined female Salamandrella keyserlingii in preovulatory (gravid) and ovulatory (spent) conditions using anatomical, histological, and histochemical methods. Each ovum was covered with two jelly layers. All ova from one oviduct fell into one egg sac. Inner space of the oviduct, in which ova were passed through, was filled with jelly-like substances designated as «intermediate fluids». We named the membrane-like outer layer of the egg sac as «theca». Jelly layers surrounding the ovum were formed by the oviducal tubular glands of the pars recta and pars convoluta of the oviduct, consisting of acidic and neutral glycoproteins. In the ovisac (i.e., homologous uterus), there were three glandular regions and one aglandular dilatable ovisac. Of the ovisac, glands A, B, and C secreted acidic and neutral glycoproteins for the intermediate fluids, neutral glycoproteins for the theca, and mucus-like materials with a neutral glycoprotein nature, respectively. We suggest that these mucus-like materials are essential to attaching the adhesive tips of the egg sacs to some substrates during oviposition.


amphibians; salamanders; anatomy; female reproductive system; clutch; egg jelly; reproduction

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Altig R. and McDiarmid R. W. (2007), «Morphological diversity and evolution of egg and clutch structure in amphibians», Herpetol. Monogr., No. 21, 1 – 32.

Bulakhova N. A. and Berman D. I. (2012), «Reproductive system of Schrenckii salamander (Salamandrella schrenckii, Amphibia, Caudata, Hynobiidae) in spring and autumn», Zool. Zh., 91(11), 1315 – 1329 [in Russian].

Exbrayat J. M. (2013a), «Classical methods of visualization», in: J. M. Exbrayat (ed.), Histochemical and Cytochemical Methods of Visualization, CRC Press Taylor and Francis Group, Boca Raton – London – New York, pp. 3 – 58.

Exbrayat J. M. (2013b), «Histochemical Methods», in: J. M. Exbrayat (ed.), Histochemical and Cytochemical Methods of Visualization, CRC Press Taylor and Francis Group, Boca Raton – London – New York, pp. 59 – 138.

Greven H. (2003), «Oviduct and Egg-Jelly», in: D. M. Sever (ed.), Reproductive Biology and Phylogeny of Urodeles, Science Publishers, pp. 151 – 182.

Hasumi M. (1996a), «Times required for ovulation, egg sac formation, and ventral gland secretion in the salamander Hynobius nigrescens», Herpetologica, 52(4), 605 – 611.

Hasumi M. (1996b), «Seasonal fluctuations of female reproductive organs in the salamander Hynobius nigrescens», Herpetologica, 52(4), 598 – 605.

Hasumi M. (2015), «Social interactions during the aquatic breeding phase of the family Hynobiidae (Amphibia: Caudata)», Acta Ethol., 18(3), 243 – 253.

Hasumi M., Hasegawa Y., and Iwasawa H. (1994), «Water absorption in the egg sac of the salamander Hynobius nigrescens», Jap. J. Herpetol., 15(3), 97 – 100.

Joly J. and Boisseau C. (1995), «L’oviduct», in: P. P. Grassé, M. Delsol (eds.), Traité de zoologie: anatomie, systématique, biologie. Tome XIV, Fasc. 1A, Masson, Paris, pp. 1231 – 1264.

Kusa M. and Ozu E. (1961), «Monosaccharide pattern of egg jellies in three species of Hynobius», Proc. Jap. Acad., 37(4), 223 – 226.

Makino S. (1934), «A cytological study on the maturation and fertilization of the egg of Hynobius retardatus (an Urodelan amphibian)», J. Fac. Sci. Hokkaido Imp. Univ. Ser. VI Zool., 3(3), 117 – 167.

Matsui M. and Matsui M. (1980), «Preliminary notes on a salamander of the Hynobius lichenatus complex found in Nagano Prefecture», Jap. J. Herpetol., 8(4), 103 – 111 [in Japanese].

Nishikawa K., Sato S., and Matsui M. (2008), «A note on the clutch size and shape of egg sacs of Hynobius boulengeri from the Sobo-Katamuki Mountains, Kyushu, Japan (Urodela: Hynobiidae)», Curr. Herpetol., 27(1), 29 – 34.

Park D. and Sung H.-C. (2006), «Male Hynobius leechii (Amphibia: Hynobiidae) discriminate female reproductive states based on chemical cues», Integr. Biosci., 10(3), 137 – 143.

Poyarkov N. A. (2010), Phylogenetic Relationships and Systematics of Asiatic Salamanders of the Family Hynobiidae (Amphibia: Caudata, Hynobiidae). Unpublished Ph.D. Dissertation, M. V. Lomonosov Moscow State University [in Russian].

Salthe S. N. (1963), «The egg capsules in the Amphibia», J. Morphol., 113(2), 161 – 171.

Sever D. M., Rania L. C., and Krenz J. D. (1996), «Reproduction of the salamander Siren intermedia Le Conte with especial reference to oviducal anatomy and mode of fertilization», J. Morphol., 227(3), 335 – 348.

Sytina L. A., Medvedeva I. M., and Godina L. B. (1987), Development of Siberian Salamander, Nauka, Moscow [in Russian].

Wake M. H. and Dickie R. (1998), «Oviduct structure and function and reproductive modes in amphibians», J. Exp. Zool., 282(4 – 5), 477 – 506.

Yamagiwa S. (1924), «Das Urogenitalsystem der Urodelen», J. Coll. Agricult. Hokkaido Imp. Univ., 15(2), 37 – 82.

Yartsev V. V., Exbrayat J. M., and Kuranova V. N. (2015), «Oogenesis in the Siberian salamander, Salamandrella keyserlingii (Amphibia: Caudata, Hynobiidae)», Vestn. Tomsk. Gos. Univ. Biol., No. 4, 127 – 144 [in Russian].

Yartsev V. V. and Kuranova V. N. (2015), «Seasonal dynamics of male and female reproductive systems in the Siberian salamander, Salamandrella keyserlingii (Caudata, Hynobiidae)», Asian Herpetol. Res., 6(3), 169 – 183.

DOI: https://doi.org/10.30906/1026-2296-2019-26-2-98-106


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