Abstract
The adaptations which allowed the Siberian salamander (Salamandrella keyserlingii Dybowski, 1870) to form its exceptionally large, polyzonal range (forest-steppe, forests, and southern tundras of Siberia and part of European Russia) remain insufficiently studied. We checked the hypothesis that S. keyserlingii was able to colonize the northern territories, characterized by a short and cold summer and therefore unsuitable for other amphibians, due to multiyear maturation of its spermatozoa and eggs which was described in the southern part of Western Siberia. For this purpose, the male reproductive cycle of S. keyserlingii was studied during the entire 4-month active season in the Sea of Okhotsk coastal tundras. The complete development of gametes there took only 3 months: proliferation of spermatogonia started already in the spawning pond soon after spermiation in May and ended by the time the males left the water; spermatocytes were formed at the end of June, and spermatozoa, by the second half of August. Spermatogenesis occurred synchronously in all the maturing lobules along the entire length of the testis. Mature spermatozoa were stored in the testes until spring when external fertilization took place in the pond. Morphological and histological changes in the testes and vasa deferentia, the mode of fertilization, and annual reproduction of S. keyserlingii were similar to those of other studied species of the family. Our data disprove the previous conclusion about multiyear spermatogenesis of S. keyserlingii, which, therefore, cannot be considered among the possible adaptations which facilitated colonization of the northern territories by this species.
Similar content being viewed by others
References
Basarukin AM, Borkin LJ (1984) Distribution, ecology and morphological variability of the Siberian salamander, Hynobius keyserlingii, of Sakhalin Island. In: Borkin LJ (ed) Ecology and faunistics of amphibians and reptiles of the USSR and adjacent countries. USSR Academy of Sciences, Leningrad, pp 12–54 (In Russian with English summary)
Berman DI (1992) On places and conditions of hibernation of the Siberian salamander (Hynobius keyserlingii) in the mountain-forest Subarctic zone in North-East Asia. Zool Zh 71(7):75–95 (In Russian with English summary)
Berman DI, Boyko EA, Mikhailova EI (1983) Reproductive behavior of the Siberian salamander. In: Prikladnaya Etologiya 3. Nauka, Moscow, pp 167–171 (In Russian)
Berman DI, Leirikh AN, Mikhailova EI (1984) Winter hibernation of the Siberian salamander Hynobius keyserlingii. Zh Evolutsionnoi Biokhimii i Fiziologii 20(3):323–327 (In Russian with English summary)
Berman DI, Derenko MV, Malyarchuk BA, Grzybowski T, Kryukov AP, Miscicka-Sliwka D (2005) Intraspecific genetic differentiation of the Siberian newt (Salamandrella keyserlingii, Amphibia, Caudata) and the cryptic species S. schrenckii from Southeastern Russia. Entomol Rev 85(2):S228–S241
Bulakhova NA, Berman DI (2012) Reproductive system of Schrenck salamander (Salamandrella schrenckii, Amphibia, Caudata, Hynobiidae) in spring and autumn. Zool Zh 91(11):1315–1329 (In Russian with English summary)
Grigoriev OV (1973) Reproductive period and ecological peculiarities of distribution and development of the spawn of Siberian salamander in the forested steppe of Western Siberia. In: Darevskiy IS (ed) Voprosy herpetologii. Nauka, Leningrad, pp 66–68 (In Russian)
Grigoriev OV (1977) On the process of spawning in Siberian salamander. In: Darevskiy IS (ed) Voprosy herpetologii. Nauka, Leningrad, pp 72–73 (In Russian)
Hasumi M (1994) Reproductive behavior of the salamander Hynobius nigrescens: monopoly of egg sacs during scramble competition. J Herpetol 28:264–267
Hasumi M, Iwasawa H, Nagahama Y (1990) Seasonal dynamics of reproductive organs in male salamanders of the species Hynobius nigrescens. Copeia 1990:367–377
Iwasawa H, Kashiwakura K, Sato T (1992) Seasonal changes in the testes and Wolffian ducts in the salamander Hynobius retardatus. Jpn J Herpetol 14(3):116–123
Kashchenko NF (1896) Siberian tetradigitate newt. Uchenye trudy Tomskogo Universiteta 10:1–13 (In Russian)
Korotkov YM (1977) A contribution to the ecology of Onychodactylus fischeri and Hynobius keyserlingii in the Primorsky district. Zool Zh 56(8):1258–1260 (In Russian with English summary)
Kukal O, Kevan PG (1987) The influence of parasitism on life history of a high arctic insect, Gynaephora groenlandica (Wocke) (Lepidoptera: Lymantriidae). Can J Zool 65:156–163
Kuramoto M (1995) Scanning electron microscopic studies on the spermatozoa of some Japanese salamanders (Hynobiidae, Cryptobranchidae, Salamandridae). Jpn J Herpetol 16(2):49–58
Kuranova VN (1998) Fauna and ecology of amphibians and reptiles of the South-East of Western Siberia. Dissertation, Tomsk State University, Tomsk, Russia (In Russian)
Kuranova VN, Saveliev SV (2006) Reproductive cycles of the Siberian newt Salamandrella keyserlingii Dybowsky, 1870. In: Vences M, Kohler J, Ziegler T, Bohme W (eds) Herpetologia Bonnensis II. Proc 13th Congress Soc Eur Herpetol. Alexander Koenig Mus, Bonn, pp 73–76
Kuzmin SL (2012) Amphibians of the former USSR. KMK, Moscow (In Russian)
Lepeshkin VD (1916a) Spermatozoa of Isodactylium Schrenkii Str. Russ Zool Zh 1(1–2):8–16 (In Russian with English summary)
Lepeshkin VD (1916b) Note on the structure of testes of Isodactylium (Str.). Russ Zool Zh 1(9–10):257–261 (In Russian with English summary)
Lofts B (1987) Testicular function. In: Norris DO, Jones RE (eds) Hormones and reproduction in fishes, amphibians, and reptiles. Plenum Press, New York, pp 283–325
Long-term data (1990) Climate of the USSR: an Applied Reference Book. Series 3. Gidrometeoizdat, Leningrad (in Russian)
Makino S (1931) The residual spermatogonia in the adult salamander, Hynobius lichenatus Boul. and their behavior during the seasonal cycle of the germ cells (6 Text-figures and 2 plates). J Fac Sci Hokkaido Imp Univ VI 1(2):41–54
Malyarchuk M, Berman D, Perkova M, Grzybowski T, Leirikh A, Bulakhova N (2010) Phylogeography and molecular adaptation of Siberian salamander Salamandrella keyserlingii based on mitochondrial DNA variation. Mol Phylogenet Evol 56:562–571
Morewood WD, Ring RA (1998) Revision of the life history of the high Arctic moth Gynaephora groenlandica (Wocke) (Lepidoptera: Lymantriidae). Can J Zool 76:1371–1381
Olzhabekova KB (1994) The development of the gonads. In: Vorobyeva EI (ed) The Siberian newt (Salamandrella keyserlingii Dybowski, 1870): zoogeography, systematics and morphology. Nauka, Moskow, pp 273–276 (In Russian)
Park D (2005) The first observation of breeding of the Long-tailed clawed salamander, Onychodactylus fischeri, in the field. Curr Herpetol 24(1):7–12
Park D, Park SR (2000) Multiple insemination and reproductive biology of Hynobius leechii. J Herpetol 34:594–598
Savelev SV, Kuranova VN, Besova NV (1991) Über die innere Befruchtung bei Salamandrella keyserlingii Dybowski, 1870. Veröff Naturhist Mus Schleusingen 6:12–15
Saveliev SV, Kuranova VN, Besova NV (1993) Reproduction of Siberian salamander. Salamandrella keyserlingii. Zool Zh 72(8):59–69 (In Russian with English summary)
Sytina LA, Medvedeva IM, Godina LB (1994) Sexual dimorphism and reproductive system state in the reproductive period. In: Vorobyeva EI (ed) The Siberian newt (Salamandrella keyserlingii Dybowski, 1870): zoogeography, systematics and morphology. Nauka, Moskow, pp 268–273 (In Russian)
Vorobyeva EI (ed) (1994) The Siberian newt (Salamandrella keyserlingii Dybowski, 1870): zoogeography, systematics and morphology. Nauka, Moscow (in Russian)
Vorobyeva EI (ed) (1995) The Siberian newt (Salamandrella keyserlingii Dybowski, 1870): ecology, behaviour and conservation. Nauka, Moscow (in Russian)
Acknowledgments
The authors express their gratitude to E.N. Meshcheryakova, A.A. Poploukhin, G.V. Kuzminykh, and A.P. Belger (Laboratory of Biocenology, Institute of Biological Problems of the North, Magadan) for their help in organizing the field research, as well as to D.M. Sever, M. Hasumi and an anonymous reviewer for their help in improving the manuscript. Special thanks to O. Manylov and R. Knight (University of Edinburgh) for editing the text. The work was financially supported by the Russian Foundation for Basic Research (Grants 10-04-00425-a, 13-04-00156-a).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Bulakhova, N.A., Berman, D.I. Male reproductive cycle of the Siberian salamander Salamandrella keyserlingii (Caudata: Hynobiidae) in coastal tundra of the Sea of Okhotsk. Polar Biol 37, 123–133 (2014). https://doi.org/10.1007/s00300-013-1418-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-013-1418-1