Morphological and physiological traits of the mesonephros in a freshwater fish, grayling Thymallus thymallus

Keywords: microanatomy; ultrastructure; leukocytes; antioxidants; ethoxyresorufin-O-deethylase; kidney


The study presents new data on the structural and functional organization of the mesonephros of the grayling Thymallus thymallus (Linnaeus, 1758). Adult grayling were sampled in the middle course of the Unya River, a tributary of the Pechora River (Komi Republic, Russia). The mesonephros of the grayling, as of other freshwater fishes, is composed by nephrons, blood vessels and hematopoietic tissue forming the renal interstice. In the interstice, сells with a radial vesicle array and chloride cells were discovered; the latter were mostly localized near the renal tubules. The degree of the interstice development in the mesonephros of the grayling was determined. New data on the ultrastructure of leukocytes, cells with a radial vesicle array, chloride cells, and nephron segments were obtained. A lack of mesangial cells, a small number of podocytes, and a thin basement membrane were observed on the sections of a renal corpuscle, being characteristic features of the ultrathin organization of the mesonephros in freshwater members of Salmoniformes and Esociformes. In the grayling’s nephrons, no neck segment was found, which was reported earlier for several species, including mammals. On the sections of proximal tubules, the ciliated cells were rare, and large amounts of the tubular-vesicular network in the zone of endocytosis of the type II epithelial cells were observed. On the sections of distal tubules, short blade-shaped cytoplasmic processes, with large numbers of invaginations of cytoplasmic membrane, were found. On the basis of the distinctive ultrastructure features mentioned above, the inference that grayling show the cytological markers of adaptation to euryhalinity was made. Thus, the results contribute to the knowledge of mesonephros development in fishes during their life history. From the species protection standpoint, our study provides baseline data on a WBC differential in the mesonephros as well as superoxide dismutase, catalase, glutathione S-transferase, and ethoxyresorufin-O-deethylase activities, which can be used in further studies addressing the health status of grayling populations.


Anderson, B. G., & Loewen, R. D. (1975). Renal morphology of freshwater trout. American Journal of Anatomy, 143(1), 93–113.

Atli, G., & Canli, M. (2010). Response of antioxidant system of freshwater fish Oreochromis niloticus to acute and chronic metal (Cd, Cu, Cr, Zn, Fe) exposures. Ecotoxicology and Environmental Safety, 73(8), 1884–1889.

Balabanova, L. V. (2006). Kletki s radialno raspolozhennymi vezikulami u ryb raznyh vidov [Cells with radiating vesicles in different fish species]. Cyto logy, 48(8), 636–640 (in Russian).

Björnsson, B. T., & Bradley, T. M. (2007). Epilogue: Past successes, present misconceptions and future milestones in salmon smoltification research. Aquaculture, 273, 384–391.

Boeuf, G. (1993). Salmonid smolting: A pre-adaptation to the oceanic environ ment. In: Rankin, J. C., & Jensen, F. B. (eds.). Fish Ecophysiology. Chapman and Hall Fish and Fisheries Series. Vol 9. Springer, Dordrecht.

Flerova, E. A. (2017). Osobennosti struktury mezonefrosa obyknovennoy shuki Esox lucius L. [Features of mesonephros structures common pike Esox lucius]. Problems of Fisheries, 18(4), 487–498 (in Russian).

Flerova, E. A., & Balabanova, L. B. (2013). Ultrastructure of granulocytes of teleost fish (Salmoniformes, Cypriniformes, Perciformes). Journal of Evolu tionary Biochemistry and Physiology, 49(2), 223–233.

Freyhof, J. (2011). Thymallus thymallus. The IUCN Red list of threatened species, 2011, e.T21875A9333742.

Katoh, F., Cozzi, R. R. F., Marshall, W. S., & Goss, G. G. (2008). Distinct Na+/K+/2Cl– cotransporter localization in kidneys and gills of two euryhaline species, rainbow trout and killifish. Cell and Tissue Research, 334(2), 265–281.

Keyster, I. A. (2009). Morfologicheskiy sostav krovi ryapushki i eyo izmeneniya kak bioindikatsionnyie pokazateli usloviy obitaniya v Belom ozere (Volo godskaya oblast) [Morphological structure of blood of vendace and its changes as bioindicators of Beloe Lake (Vologda Region)]. Modern Pro blems of Science and Education, 3, 117–125 (in Russian).

Kocabatmaz, M., & Ekingen, G. (1987). Comparative studies on leucocytes of some freshwater fish species. Selçuk Üniversitesi Veteriner Fakültesi Dergisi, 3(1), 71–81.

Langdon, J. S. (1985). Smoltification physiology in the culture of salmonids. In: Muir, J. F., & Roberts, R. J. (Eds.). Recent Advances in Aquaculture. Springer, Boston. Pp. 79–118.

Lapirova, T. B., Flerova, E. A., Yurchenko, V. V., & Morozov, A. A. (2017). Pro tective systems of immune-competent organs in the fish of various ecological and systematic groups. Journal of Ichthyology, 57(3), 458–466.

Mizuno, S, Misaka, N., & Kasahara, N. (2001). Morphological changes in juxta glomerular cells of the kidney during smoltification in masu salmon Onco rhynchus masou. Fisheries Science, 67(3), 538–540.

Morozov, А. А., & Yurchenko, V. V. (2018). Seasonal changes in hepatic antioxi dant enzyme activities of the perch Perca fluviatilis in the Upper Volga basin, Russia. Ichthyological Research, 65(2), 265–269.

Nykänen, M., Huusko, A., & Mäki-Petäys, A. (2001). Seasonal changes in the habitat use and movements of adult European grayling in a large subarctic river. Journal of Fish Biology, 58(2), 506–519.

Ojeda, J. L., & Icardo, J. M. (1991). A scanning electron microscope study of the neck segment of the rabbit nephron. Anatomy and Embryology, 184(6), 605–610.

Ojeda, J. L., Icardo, J. M., Wong, W. P., & Ip, Y. K. (2006). Microanatomy and ultrastructure of the kidney of the African lungfish Protopterus dolloi. The Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology, 288A(6), 609–625.

Rondeau, E. B., Minkley, D. R., Leong, J. S., Messmer, A. M., Jantzen, J. R., von Schalburg, K. R., Lemon, C., Bird, N. H., & Koop, B. F. (2014). The genome and linkage map of the northern pike (Esox lucius): Conserved synteny revealed between the salmonid sister group and the Neoteleostei. PloS One, 9(7), e102089.

Sayeed, I., Parvez, S., Pandey, S., Bin-Hafeez, B., Haque, R., & Raisuddin, S. (2003). Oxidative stress biomarkers of exposure to deltamethrin in freshwater fish, Channa punctatus Bloch. Ecotoxicology and Environmental Safety, 56(2), 295–301.

Scott, A. (1985). Distribution, growth, and feeding of postemergent grayling Thy mallus thymallus in an English River. Transactions of the American Fisheries Society, 114(4), 525–531.

Sinha, A. K., AbdElgawad, H., Giblen, T., Zinta, G., De Rop, M., Asard, H., Blust, R., & De Boeck, G. (2014). Anti-oxidative defences are modulated different tially in three freshwater teleosts in response to ammonia-induced oxidative stress. PLoS One, 9(4), e95319.

Talbot, C., Stagg, R. M., & Eddy, F. B. (1992). Renal, respiratory and ionic regu lation in Atlantic salmon (Salmo salar L.) kelts following transfer from fresh water to seawater. Journal of Comparative Physiology B, 162(4), 358–364.

Timakova, T. K., Flerova, E. A., & Zabotkina, E. A. (2014). Metody svetovoy i elektronnoy mikroskopii v biologii i veterenarii [Methods of light and electronic microscopy for biology and veterinary science]. Yaroslavskaya GSHA, Yaroslavl (in Russian).

Yasuike, M., Jantzen, S., Cooper, G. A., Leder, E., Davidson, W. S., & Koop, B. F. (2010). Grayling (Thymallinae) phylogeny within salmonids: Complete mi tochondrial DNA sequences of Thymallus arcticus and Thymallus thymallus. Journal of Fish Biology, 76(2), 395–400.

Yurchenko, V. V., & Morozov, A. A. (2018). Intra-annual variability of hepatic ethoxyresorufin-O-deethylase activity in freshwater bream Abramis brama. Biological Rhythm Research, 2018, in press.

How to Cite
Flerova, E. A., Morozov, A. A., Bogdanova, A. A., Chupov, D. V., Ustiuzhinskii, G. M., & Yurchenko, V. V. (2019). Morphological and physiological traits of the mesonephros in a freshwater fish, grayling Thymallus thymallus . Regulatory Mechanisms in Biosystems, 10(1), 9-15.