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Features of the Changes in External Morphology and Axial Skeleton in Juvenile Salmonid Fishes (Salmonidae) Associated with Smoltification

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Abstract—

Changes in external morphological characters and relative lengths of vertebral centra from different regions of the vertebral column are analyzed during smoltification in wild juveniles of five salmonid fish species: Atlantic salmon Salmo salar, brown trout S. trutta, mikizha Parasalmo mykiss, coho salmon Oncorhynchus kisutch, and northern Dolly Varden Salvelinus malma. The changes in the body proportions and external morphology are similar in different salmonid species, but the patterns of differentiation of the vertebral column’s postanal part are different. In Atlantic salmon, all vertebral centra of the postanal part are subject to elongation; in mikizha and brown trout, a small number of the centra are elongated only in the anterior region of the postanal part; in coho salmon, the centra are elongated in the posterior region of the postanal part; in Dolly Varden, the centra are elongated in the middle region of the postanal part. Thus, despite observed universal changes in external morphology associated with smoltification in the family Salmonidae, the development of future marine migrants' phenotypes is species-specific due to different growth of various groups of vertebral centra in the vertebral column’s postanal part. The possible reasons for the species diversity in the growth of various groups of vertebral centra are discussed.

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REFERENCES

  1. Agathon, A., Thisse, C., and Thisse, B., The molecular nature of the zebrafish tail organizer, Nature, 2003, vol. 424, pp. 448–452.

    Article  CAS  PubMed  Google Scholar 

  2. Ahn, D. and Gibson, G., Axial variation in the threespine stickleback: relationship to Hox gene expression, Dev. Gen. Evol., 1999, vol. 209, pp. 473–481.

    Article  CAS  Google Scholar 

  3. Armstrong, R.H., Migration of anadromous Dolly Varden (Salvelinus malma) in Southeastern Alaska, J. Fish. Res. Board Can., 1974, vol. 31, no. 4, pp. 436–444.

    Google Scholar 

  4. Arratia, G. and Schultze, H.-P., Reevaluation of the caudal skeleton of certain actinopterygian fishes: III. Salmonidae. Homologization of caudal skeletal structures, J. Morphol., 1992, vol. 214, pp. 187?249.

    Article  PubMed  Google Scholar 

  5. Atlanticheskii losos’ (Atlantic Salmon), Kazakov, R.V., Ed., St. Petersburg: Nauka, 1998.

    Google Scholar 

  6. Barannikova, I.A., Bayunova, N.N., Krasnodembskaya, K.D., et al., Functional principles of smoltification and its role in the life cycle of salmons, in Ekologiya i sistematika lososevykh ryb (Ecology and Systematics of Salmon Fishes), Leningrad: Nauka, 1976, pp. 9–15.

    Google Scholar 

  7. Barrington, E.J.W., Metamorphic processes in fish and lampreys, Am. Zool., 1961, vol. 1, pp. 97–106.

    Article  Google Scholar 

  8. Beeman, J.W., Rondorf, D.W., Tilson, M.E., and Venditti, D.A., A nonlethal measure of smolt status of juvenile steelhead based on body morphology, Trans. Am. Fish. Soc., 1995, vol. 124, pp. 764–769.

    Article  Google Scholar 

  9. Björnsson, B.T., Young, G., Lin, R.J., et al., Smoltification and seawater adaptation in coho salmon (Oncorhynchus kisutch): plasma calcium regulation, osmoregulation, and calcitonin, Gen. Comp. Endocrinol., 1989, vol. 74, pp. 346–354.

    Article  PubMed  Google Scholar 

  10. Björnsson, B.T., Einarsdottir, I.E., and Power, D., Is salmon smoltification an example of vertebrate metamorphosis? Lessons learnt from work on flatfish larval development, Aquaculture, 2012, vols. 362–363, pp. 264–272.

    Article  CAS  Google Scholar 

  11. Chernitskii, A.G., Migration and transfer to the sea water of young salmons of the genus Salmo with natural and artificial reproduction, Extended Abstract of Doctoral (Biol.) Dissertation, Moscow: VNIRO, 1993.

  12. Chernitskii, A.G., Smoltification of Atlantic and brown salmons, Usp. Sovrem. Biol., 1994, vol. 114, no. 5, pp. 620–632.

    Google Scholar 

  13. Clarke, W.C. and Nagahama, Y., Effect of premature transfer to sea water on growth and morphology of the pituitary, thyroid, pancreas, and interrenal in juvenile coho salmon (Oncorhynchus kisutch), Can. J. Zool., 1977, vol. 55, pp. 1620–1630.

    Article  Google Scholar 

  14. Damsgard, B., Smolting characters in anadromous and resident Arctic char, Salvelinus alpinus (L.), J. Fish Biol., 1991, vol. 39, pp. 765–774.

    Article  Google Scholar 

  15. DeCicco, A., Long-distance movements of anadromous Dolly Varden between Alaska and the U.S.S.R., Arctic, 1992, vol. 45, no. 2, pp. 120–123.

    Article  Google Scholar 

  16. Dickhoff, W.W., Brown, C.L., Sullivan, C.V., and Bern, H.A., Fish and amphibian models for developmental endocrinology, J. Exp. Zool. Suppl., 1990, vol. 4, pp. 90–97.

    Article  Google Scholar 

  17. Ershov, P.N., Biology of the brown trout from the Pila and Shogui rivers (Kola Peninsula), in Issledovaniya populyatsionnoi biologii i ekologii lososevykh ryb vodoemov Severa (Studies in Population Biology and Ecology of Salmon Fishes in the Northern Reservoirs), Leningrad: Zool. Inst., Akad. Nauk SSSR, 1985, pp. 94–119.

    Google Scholar 

  18. Farmer, G.J., Ritter, J.A., and Ashfield, D., Seawater adaptation and parr-smolt transformation of juvenile Atlantic salmon, Salmo salar, J. Fish. Res. Board Can., 1978, vol. 35, pp. 93–100.

    Article  Google Scholar 

  19. Fessler, J.L., Some morphological and biochemical changes in steelhead trout during the parr-smolt transformation, PhD Thesis, Corvallis, OR: Oregon State Univ., 1969.

  20. Fjelldal, P.G., Nordgarden, U., Berg, A., et al., Vertebrae of the trunk and tail display different growth rates in response to photoperiod in Atlantic salmon, Salmo salar L., post-smolts, Aquaculture, 2005, vol. 250, pp. 516–524.

    Article  Google Scholar 

  21. Fjelldal, P.G., Lock, E.-J., Grotmol, S., et al., Impact of smolt production strategy on vertebral growth and mineralization during smoltification and the early seawater phase in Atlantic salmon (Salmo salar L.), Aquaculture, 2006, vol. 261, pp. 715–728.

    Article  Google Scholar 

  22. Fjelldal, P.G., Nordgarden, U., and Hansen, T., The mineral content affects vertebral morphology in underyearling smolt of Atlantic salmon (Salmo salar L.), Aquaculture, 2007, vol. 270, pp. 231–239.

    Article  CAS  Google Scholar 

  23. Folmar, L.C. and Dickhoff, W.W., The parr-smolt transformation (smoltification) and seawater adaptation in salmonids—a review of selected literature, Aquaculture, 1980, vol. 21, pp. 1–37.

    Article  CAS  Google Scholar 

  24. Helland, S., Refstie, S., Espmark, Å., et al., Mineral balance and bone formation in fast-growing Atlantic salmon parr (Salmo salar) in response to dissolved metabolic carbon dioxide and restricted dietary phosphorus supply, Aquaculture, 2005, vol. 250, pp. 364–376.

    Article  CAS  Google Scholar 

  25. Hoar, W.S., Smolt transformation: evolution, behavior, and physiology, J. Fish. Res. Board Can., 1976, vol. 33, pp. 1234–1252.

    Article  Google Scholar 

  26. Hoar, W.S., The physiology of the smolting salmonids, in Fish Physiology, Hoar, W.S. and Randall, D.J., Eds., New York: Academic, 1988, vol. 11B, pp. 275–343.

  27. Lundqvist, H. and Eriksson, L.-O., Annual rhythms of swimming behavior and seawater adaptation in young Baltic salmon, Salmo salar, associated with smolting, Environ. Biol. Fish., 1985, vol. 14, no. 4, pp. 259–267.

    Article  Google Scholar 

  28. Kacem, A., Meunier, F.J., and Bagliniere, J.L., A quantitative study of morphological and histological changes in the skeleton of Salmo salar during its anadromous migration, J. Fish Biol., 1998, vol. 53, pp. 1096–1109.

    Google Scholar 

  29. Kazakov, R.V., Biologicheskie osnovy razvedeniya atlanticheskogo lososya (Biological Principles of Farming of Atlantic Salmon), Moscow: Legkaya Pishchevaya Prom-st’, 1982.

    Google Scholar 

  30. Kazakov, R.V., Comparative morphological characteristics of smolts of Atlantic and brown salmon smolts from the Pyalitsa River (White Sea), Tr. Gos. Nauchno-Issled. Inst. Ozern. Rechn. Rybn. Khoz., 1987, no. 263, pp. 68–125.

  31. Kazakov, R.V., Atlantic salmon in freshwater reservoirs of Europe: terms and taxonomic status, Tr. Gos. Nauchno-Issled. Inst. Ozern. Rechn. Rybn. Khoz., 1992, no. 304, pp. 125–145.

  32. Kirillova, E.A., Biology of juveniles of the first-year brown trout Oncorhynchus kisutch in the Utkholok and Kalkaveem rivers (Northwestern Kamchatka), in Chteniya pamyati V.Ya. Levanidova (Vladimir Ya. Levanidov’s Biennial Memorial Meetings), Vladivostok: Dal’nauka, 2008, no. 4, pp. 292–301.

  33. Kuzishchin, K.V., Specific formation of intraspecific variety of the brown trout Salmo trutta L. from the White Sea, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Moscow: Moscow State Univ., 1997.

  34. Kuzishchin, K.V. and Novikov, G.G., Morphoecological differentiation of juveniles of the Atlantic Salmo salar and brown Salmo trutta salmons in slow flows (Northern Karelia), Vopr. Ikhtiol., 1994, vol. 34, no. 4, pp. 479–485.

    Google Scholar 

  35. Kuzishchin, K.V., Pustovit O.P., Pavlov D.S., and Savvaitova K.A., Morphobiological traits of downstream-migrating juveniles of Parasalmo mykiss from some rivers of Western Kamchatka in relation to smoltification, J. Ichthyol., 2002, vol. 42, no. 9, pp. 720–732.

    Google Scholar 

  36. Lakin, G.F., Biometriya (Biometry), Moscow: Vysshaya Shkola, 1990.

    Google Scholar 

  37. Mahnken, C.V.W., The size of coho salmon and time of entry into sea water, Part 1. Effects on growth and condition index, 24th Annual Northwest Fish Culture Conf., Wemme, 1973, p. 30.

  38. Martynov, V.G., Semga ural’skikh pritokov Pechory. Ekologiya, morfologiya, vosproizvodstvo (Atlantic Salmon from Ural Tributaries of the Pechora River: Ecology, Morphology, and Reproduction), Leningrad: Nauka, 1983.

    Google Scholar 

  39. Morin-Kensicki, E.M., Melancon, E., and Eisen, J.S., Segmental relationship between somites and vertebral column in zebrafish, Development, 2002, vol. 129, pp. 3851–3860.

    CAS  PubMed  Google Scholar 

  40. Morita, K., Morita, S.H., Fukuwaka, M., and Nagasava, T. Offshore Dolly Varden charr (Salvelinus malma) in the North Pacific, Environ. Biol. Fish., 2009, vol. 86, pp. 451–456.

    Article  Google Scholar 

  41. Nordvik, K., Kryvi, H., Totland, G.K., and Grotmol, S., The salmon vertebral body develops through mineralization of two preformed tissues that are encompassed by two layers of bone, J. Anat., 2005, vol. 206, pp. 103–114.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Paris, M. and Laudet, V., The history of a developmental stage: metamorphosis in chordates, Genesis, 2008, vol. 46, pp. 657–672.

    Article  CAS  PubMed  Google Scholar 

  43. Pavlov, D.A., Lososevye (biologiya razvitiya i vosproizvodstvo) (Salmon Fishes: Ontogenic Biology and Reproduction), Moscow: Mosk. Gos. Univ., 1989.

    Google Scholar 

  44. Pavlov, D.S., Savvaitova, K.A., Kuzishchin, K.V., et al., Tikhookeanskie blagorodnye lososi i foreli Azii (Pacific Noble Salmons and Trouts in Asia), Moscow: Nauchnyi Mir, 2001.

    Google Scholar 

  45. Pavlov, D.S., Savvaitova, K.A., Kuzishchin, K.V., et al., Sostoyanie i monitoring bioraznoobraziya lososevykh ryb i sredy ikh obitaniya na Kamchatke (na primere territorii zakaznika “Reka Kol’”) (The Status and Monitoring of Biological Diversity of Salmon Fishes and Their Habitat Conditions in Kamchatka by Example of Reka Kol’ Nature Nursery), Moscow: KMK, 2009.

    Google Scholar 

  46. Pavlov, D.S., Kirillova, E.A., and Kirillov, P.A., Downstream migration of salmon juveniles in the Utkholok River and its tributaries (Northwestern Kamchatka). 2. Downstream migration of juveniles of the second and next years, Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 2011, vol. 164, pp. 27–73.

    Google Scholar 

  47. Pavlov, D.S., Kirillov, P.I., Kirillova, E.A., et al., Sostoyanie bioraznoobraziya lososevykh ryb i ryboobraznykh i sredy ikh obitaniya v basseine reki Utkholok (Biological Diversity and Habitat of Salmon Fishes and Fish-Like Species in the Utkholok River Basin), Moscow: KMK, 2016.

    Google Scholar 

  48. Pichugin, M.Yu., Initiation and development of skeleton elements in early ontogenesis of chars of Salvelinus alpinus–S. malma complex, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Moscow: Moscow State Univ., 2002.

  49. Pichugin, M.Yu., Morphological characteristic of the rainbow trout (Parasalmo mykiss) larvae during first resettlement (Utkholok River), Materialy X Mezhdunarodnoi nauchnoi konferentsii “Sokhranenie bioraznoobraziya Kamchatki i prilegayushchikh morei” (Proc. X Int. Sci. Conf. “Conservation of Biological Diversity of Kamchatka and Adjacent Seas”), Petropavlovsk-Kamchatski: Kamchatpress, 2009, pp. 113–115.

  50. Pichugin, M.Yu., Peculiarities of growth and skeletal system development of prelarvae, larvae, and fingerlings of Dolly Varden Trout Salvelinus malma malma inhabiting the rivers of Western Kamchatka in regard to the temperature regime of the spawning grounds, J. Ichthyol., 2015, vol. 55, no. 4, pp. 549–566.

    Article  Google Scholar 

  51. Prince, V.E., Joly, L., Ekker, M., et al., Zebrafish Hox genes: genomic organization and modified collinear expression patterns in the trunk, Development, 1998, vol. 125, pp. 207–420.

    Google Scholar 

  52. Reddin, D.G., Atlantic salmon (Salmo salar L.) on and east of the Grand Bank of Newfoundland, J. Northw. Atl. Fish. Sci., 1985, vol. 6, no. 2, pp. 157–164.

    Article  Google Scholar 

  53. Reddin, D.G., Contribution of North American salmon (Salmo salar L.) to the Faroese fishery, Nat. Can. (Quebec), 1987, vol. 114, no. 2, pp. 187–193.

    Google Scholar 

  54. Reddin, D.G. and Friedland, K.D., Marine environmental factors influencing the movement and survival of Atlantic salmon, in Salmon in the Sea and New Enhancement Strategies, Mills, D., Ed., London: Wiley, 1993, pp. 79–103.

    Google Scholar 

  55. Reddin, D.G. and Short, P.B., Postsmolt Atlantic salmon (Salmo salar) in the Labrador Sea, Can. J. Fish. Aquat. Sci., 1991, vol. 48, no. 1, pp. 2–6.

    Article  Google Scholar 

  56. Seear, P.J., Carmichael, S.N., Talbot, R., et al., Differential gene expression during smoltification of Atlantic salmon (Salmo salar L.): a first large-scale microarray study, Mar. Biotechnol., 2010, vol. 12, pp. 126–140.

    Article  CAS  Google Scholar 

  57. Soivio, A., Virtanen, E., Backstrom, M., et al., Lohi-istukkaiden Kunnon javaellusvalminden seuranta, Suomen Kalatalous, 1988, no. 53, pp. 134–152.

  58. Suslova, G.N., Observation of the brown trout from several rivers of the White Sea basin, Izv. Gos. Nauchno-Issled. Inst. Ozern. Rechn. Rybn. Khoz., 1969, vol. 65, pp. 135–140.

    Google Scholar 

  59. Taylor, E.B. and McPhail, J.D., Variation in bode morphology among British Columbia populations of coho salmon, Oncorhynchus kisutch, Can. J. Fish. Aquat. Sci., 1985a, vol. 42, pp. 2020–2028.

    Article  Google Scholar 

  60. Taylor, E.B. and McPhail, J.D., Variation in burst and prolonged swimming performance among British Columbia populations of coho salmon, Oncorhynchus kisutch, Can. J. Fish. Aquat. Sci., 1985b, vol. 42, pp. 2029–2033.

    Article  Google Scholar 

  61. Thorpe, J.E., Reproductive strategies in Atlantic salmon, Salmo salar L., J. Aquacult. Fish. Manage., 1994, vol. 25, pp. 77–87.

    Google Scholar 

  62. Vernidub, M.F., External view of chum salmon and its changes during growth, Izv. Polar. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 1977, no. 32, pp. 119–131.

  63. Virtanen, E., Soivio, A., Westman, K., and Forsman, L., Lohen luonnonpoikasten fysiologinen tila ja vaellusvalmius simojoella, Suomen Kalatalous, 1988, no. 53, pp. 111–133.

  64. Winans, G.A. and Nishioka, R.S., A multivariate description of change in body shape of coho salmon (Oncorhynchus kisutch) during smoltification, Aquaculture, 1987, vol. 66, pp. 235–245.

    Article  Google Scholar 

  65. Witten, P.E., Gil-Martens, L., Hall, B.K., et al., Compressed vertebrae in Atlantic salmon Salmo salar: evidence for metaplastic chondrogenesis as a skeletogenic response late in ontogeny, Dis. Aquat. Org., 2005, vol. 64, pp. 237–246.

    Article  Google Scholar 

  66. Zorbidi, Zh.Kh., Kizhuch aziatskikh stad (Coho Salmon from Asian Herds), Petropavlovsk-Kamchatski: Kamchat. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 2010.

    Google Scholar 

  67. Zubchenko, A.V., Vorob’eva, N.K., Gorshkova, G.L., et al., Influence of egg incubation temperature on embryonic, larval development, and growth of early juveniles of Atlantic salmon, in Rannii ontogenez ob”ektov marikul’tury (Early Ontogenesis of Mariculture Objects), Moscow: VNIRO, 1989, pp. 71–81.

    Google Scholar 

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ACKNOWLEDGMENTS

We are grateful the Wild Salmon Center (WSC), Portland, Oregon, United States, for support of the field data collection in the rivers of Kamchatka.

Funding

This study was supported by the Russian Science Foundation, project no. 14-50-00029 (Moscow State University Data Depository) within the “Noev kovcheg” (Noah’s Ark) Project of Moscow State University.

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Authors and Affiliations

  1. Moscow State University, 119899, Moscow, Russia

    K. V. Kuzishchin, M. A. Gruzdeva, M. Yu. Pichugin & D. S. Pavlov

  2. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 117071, Moscow, Russia

    K. V. Kuzishchin & D. S. Pavlov

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  1. K. V. Kuzishchin
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  2. M. A. Gruzdeva
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Kuzishchin, K.V., Gruzdeva, M.A., Pichugin, M.Y. et al. Features of the Changes in External Morphology and Axial Skeleton in Juvenile Salmonid Fishes (Salmonidae) Associated with Smoltification. J. Ichthyol. 59, 664–679 (2019). https://doi.org/10.1134/S0032945219050084

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