Abstract
Although renal hypertrophy during the reproductive period has been reported previously in species of Cottus, the function of the kidney in reproduction remains unknown. In order to clarify the role of the kidney in reproduction, seasonal changes in gonad and kidney weight, serum androgen levels, kidney histology, and the protein content of urine, were examined in the small-egged Kajika, Cottus pollux SE sensu Yokoyama and Goto (2005). Compared to the non-reproductive period (August), renal hypertrophy of male fish during the reproductive period (December) was equivalent to a twofold increase in kidney-somatic index values. A marked increase in epithelial cell height in the proximal convoluted tubule (PT) was correlated with elevated serum 11-ketotestosterone levels, suggesting that total kidney weight increased from the non-reproductive to the reproductive period. Periodic acid-Schiff (PAS)-positive granules containing polysaccharides were observed in the cytoplasm of PT epithelia during the reproductive period. Urine retained in the urinary bladders of males exhibiting nesting behavior contained glycoproteins and low-molecular-weight substances containing polysaccharides during the reproductive period. We discussed the role of the kidney and kidney secretions in nesting male species of Cottus.
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References
Borg B (1994) Androgens in teleost fishes. Comp Biochem Physiol 109C:219–245
Borg B, Antonopoulou E, Andersson E, Carlberg T, Mayer I (1993) Effectiveness of several androgens in stimulation kidney hypertrophy, a secondary sexual character, in castrated male three-spined sticklebacks, Gasterosteus aculeatus. Can J Zool 71:2327–2329
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Bucher F, Hofer R (1993) Histological and enzyme histochemical changes in the kidney of male bullhead (Cottus gobio) during the spawning period. J Fish Biol 42:403–409
Fukui K, Fujii R, Tahara D, Hayakawa Y. Koya Y. (2007) Annual changes in gonadal histology and serum profiles of sex steroids in KAJIKA, Cottus sp. SE (small egg type), under rearing conditions. Jpn J Ichthyol 54:173–186
Goto A (1974) Hypertrophy of the kidney of the male freshwater sculpin, Cottus hangiongensis Mori in the spawning period. Bull Fac Fish Hokkaido Univ 25:211–214
Goto A (1982) Reproductive behavior of a river sculpin, Cottus nozawae. Jpn J Ichthyol 28:453–457
Goto A (1983) Spawning habits and reproductive isolating mechanism of two closely related river-sculpins, Cottus amblystomopsis and C. nozawae. Jpn J Ichthyol 30:168–175
Goto A (1988) Reproductive behavior and homing after downstream spawning migration in the river sculpin, Cottus hangiongensis. Jpn J Ichthyol 34:488–496
Goto A (1994) Land-locking and speciation in diadromous fishes, with special reference to polypatric speciation and sympatric speciation. In: Goto A, Tsukamoto K, Maekawa K (eds) Freshwater fishes migrating between rivers and sea: life-history and evolution. Tokai University Press, Tokyo, pp 222–241
Goto A, Hasegawa T, Yamazaki F (1979) Secretory granules in the renal tubules of male freshwater sculpin, Cottus hangiongensis, during the spawning period. Jpn J Ichtyol 26:302–307
Hentschel H (1982) Histochemical observations on glycoproteins in the urinary apparatus of the bullhead Cottus gobio L. and the bull rout Myoxocephalus scorpius (L.). Zeitschrift fur Mikroskopish-anatomische Forschung 96:171–179
Keller-Costa T, Hubbard PC, Paetz C, Nakamura Y, da Silva JP, Rato A, Barata EN, Schneider B, Canario VM (2014) Identity of a tilapia pheromone released by dominant males that primes females for reproduction. Current Biology 24:2130–2135
Kastel PL, Dmitrieva TM, Valeyev RB, Kozlov YP (1992) Sex pheromones of male yellowfin Baikal sculpin (Cottocomephorus grewingki): isolation and chemical studies. J Chem Ecol 18:2003–2010
Koya Y, Fujii R, Yambe H, Tahara D (2015) Nesting behavior is associated with increased urinary volume in the urinary bladder during the reproductive period in small-egged Kajika, Cottus pollux SE. Ichthyol Res doi 10.1007/s10228-015-0475-6
Kumagai M, Sugiyama H, Goto A (2013) Polymorphic spawning-nest in a local population of the fluvial sculpin, Cottus nozawae (Teleostei: Cottidae). Ichthyol Res 60:396–400
Natsumeda T (2005) Biotic and abiotic influences on nest-hatching outcome in the Japanese fluvial sculpin, Cottus pollux. Environ Biol Fish 74:349–356
Okada S (1936) Breeding habits of a river sculpin, Cottus pollux Günther. Zool Mag 48:923–928
Rasotto MB, Sadovy Y (1995) Peculiarities of the male urogenital apparatus of two grunt species (Teleostei, Haemulidae). J Fish Biol 46:936–948
Savage T (1963) Reproductive behavior of the mottled sculpin, Cottus bairdi Girard. Copeia 1963:317–325
Varsamos S, Nebel C, Charmantier G. (2005) Ontogeny of osmoregulation in postembryonic fish: A review. Comp Biochem Physiol A 141:401–429
Villeret M, Jolly S, Weist L, Vulliet E, Bado-Nilles A, Porcher J-M, Betoulle S, Minier C, Sanchez W (2013) A potential biomarker of androgen exposure in European bullhead (Cottus sp.) kidney. Fish Physiol Biochem 39:573–580
Yokoyama R, Goto A (2005) Evolutionary history of freshwater sculpins, genus Cottus (Teleostei; Cottidae) and related taxa, as inferred from mitochondrial DNA phylogeny. Mol Phyl Evol 36:645–668
Zacharius RM, Zell TE, Morrison JH, Woodlock JJ (1969) Glycoprotein staining following electrophoresis on acrylamide gels. Anal Biochem 30:148–152
Acknowledgments
We are grateful to Mr. Issei Kawashiro, and Mrs. Miya Itoh of Gifu University for laboratory assistance. This study was supported in part by a Grant-in-Aid from the Japan Society for the Promotion of Science KAKENHI (Grant Number 26450277).
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Koya, Y., Fujii, R., Yambe, H. et al. Hypertrophy and polysaccharide production in the kidney associated with sexual maturation of male small-egged Kajika, Cottus pollux SE. Ichthyol Res 63, 260–266 (2016). https://doi.org/10.1007/s10228-015-0496-1
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DOI: https://doi.org/10.1007/s10228-015-0496-1