Abstract
Vaccination has recently become a widely considered factor influencing the development of farmed fishes. In the present study, developmental stability of bone structures of vaccinated and nonvaccinated Atlantic salmon is investigated using two parameters, the frequency of deformities and fluctuating asymmetry (FA, nondirectional deviations from perfect bilateral symmetry). Vaccinated salmon show a higher frequency of bone deformities, suggesting a decrease in developmental stability caused by vaccination. On the contrary, the level of FA does not differ in vaccinated and nonvaccinated fishes. The results are discussed from the point of view of influence of mechanical load on the development of bone structures of the Atlantic salmon.
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Aunsmo, A., Guttvik, A., Midtlyng, P.J., et al., Association of spinal deformity and vaccine induced abdominal lesions in harvest-sized Atlantic salmon, Salmo salar L., J. Fish Dis., 2008, vol. 31, pp. 515–524.
Ballintijn, C.M. and Hughes, G.M., The muscular basis of the respiratory pumps in the trout, J. Exp. Biol., 1965, vol. 43, pp. 349–362.
Berg, A., Rødseth, O.M., Tångeras, A., and Hansen, T., Time of vaccination influences development of adhesions, growth and spinal deformities in Atlantic salmon Salmo salar, Des. Aquat. Org., 2006, vol. 69, nos. 2–3, pp. 239–248.
Berg, A., Rødseth, O.M., and Hansen, T., Fish size at vaccination influence the development of side-effects in Atlantic salmon (Salmo salar L.), Aquaculture, 2007, vol. 265, pp. 9–15.
Berg, A., Yurtseva, A., Hansen, T., et al., Vaccinated farmed Atlantic salmon are susceptible to spinal and skull deformities, J. Appl. Ichthyol., 2012, vol. 28, pp. 446–452.
Developmental Instability: Causes and Consequences, Polak, M., Ed., Oxford: Oxford Univ. Press. 2003.
Diogo, R., Hinits, Y., and Hughes, S.M., Development of mandibular, hyoid and hypobranchial muscles in the zebrafish: Homologies and evolution of these muscles within bony fishes and tetrapods, BMC Develop. Biol., 2008, vol. 8, no. 24, pp. 1–22.
Fjelldal, P.G., Grotmol, S., Kryvi, H., et al., Pinealectomy induces malformation of the spine and reduces the mechanical strength of the vertebrae in Atlantic salmon, Salmo salar, J. Pineal Res., 2004, vol. 36, pp. 132–139.
Fjelldal, P.G., Hansen, T.J., and Berg, A.E., A radiological study on the development of vertebral deformities in cultured Atlantic salmon (Salmo salar L.), Aquaculture, 2007, vol. 273, pp. 721–728.
Fjelldal, P.G., Lock, E.J., Grotmol, S., et al., Impact of smolt production strategy on vertebral growth and mineralisation during smoltification and the early seawater phase in Atlantic salmon (Salmo salar L.), Aquaculture, 2006, vol. 261, pp. 715–728.
Glowacki, J., Cox, K.A., O’Sullivan, J., et al., Osteoclasts can be induced in fish having an acellular bony skeleton, Proc. Nat. Acad. Sci. USA, 1986, vol. 83, pp. 4101–4107.
Graham, J.H., Freeman, D.C., and Emlen, J.M., Developmental stability: A sensitive indicator of populations under stress, in Environmental Toxicology and Risk Assessment, Landis, W.G., Hughes, J.S., and Lewis, M.A, Eds., Philadelphia: Am. Soc. Test. Mater., 1993, pp. 136–158.
Grini, A., Hansen, T., Berg, A., et al., The effect of water temperature on vertebral deformities and vaccine-induced abdominal lesions in Atlantic salmon (Salmo salar L.), J. Fish Dis., 2011, vol. 34, pp. 531–546.
Helland, S., Denstadli, V., Witten, P.E., et al., Hyper dense vertebrae and mineral content in Atlantic salmon (Salmo salar L.) fed diets with graded levels of phytic acid, Aquaculture, 2006, vol. 261, no. 2, pp. 603–614.
Helland, S., Refstie, S., Hjelde, K., and Baeverfjord, G., Morphological description of skeletal deformities in Atlantic salmon subject to restricted mineral supply, in Workshop on Bone Disorders in Intensive Aquaculture of Salmon and Cod, Bergen: NIFES, 2005, p..
Huysseune, A., Skeletal system, in The Laboratory Fish: Part 4. Microscopic Functional Anatomy, Ostrander, G.K., Eds., San Diego: Academic Press, 2000, pp. 307–317.
Kranenbarg, S., van Cleynenbreugel, T., Schipper, H., and van Leeuwen, J., Adaptive bone formation in acellular vertebrae of sea bass (Dicentrarchus labrax L.), J. Exp. Biol., 2005, vol. 208, pp. 3493–3502.
Kvellestad, A., Hoie, S., Thorud, K., et al., Platyspondyly and shortness of vertebral column in farmed Atlantic salmon Salmo salar in Norway—description and interpretation of pathological changes, Dis. Aquat. Org., 2000, vol. 39, pp. 97–108.
Lajus, D.L., Variation patterns of bilateral characters: Variation among characters and among populations in the White Sea herring (Clupea pallasi marisalbi), Biol. J. Linn. Soc., 2001, vol. 74, pp. 237–253.
Lajus, D., Knust, R., and Brix, O., Fluctuating asymmetry and other parameters of morphological variation of eelpout Zoarces viviparus (Zoarcidae, Teleostei) from different parts of its distributional range, Sarsia, 2003, vol. 88, pp. 247–260.
Lakin, G.F., Biometriya (Biometrics), Moscow: Vyssh. Shkola, 1990.
Larssen, R.B. and Djupvik, H.O., Early life risk indicators of skeletal deformities in salmon at slaughter, in Workshop on Bone Disorders in Intensive Aquaculture of Salmon and Cod, Bergen: NIFES, 2005, p. 36.
Lillehaug, A., Lunder, T., and Poppe, T.T., Field testing of adjuvanted furunculosis vaccines in Atlantic salmon, Salmo salar L., J. Fish Des., 1992, vol. 15, pp. 485–496.
Martens, L.G., Lock, E.J., Fjelldal, P.G., et al., Dietary fatty acids and inflammation in the vertebral column of Atlantic salmon, Salmo salar L., smolts: A possible link to spinal deformities, J. Fish Dis., 2010, vol. 33, pp. 957–972.
Midtlyng, P.J. and Lillehaug, A., Growth of Atlantic salmon Salmo salar after intraperitoneal administration of vaccines containing adjuvants, Dis. Aquat. Org., 1998, vol. 32, pp. 91–97.
Midtlyng, P.J., Reitan, L.J., and Speilberg, L., Experimental studies on the efficacy and side-effects of intraperitoneal vaccination of Atlantic salmon (Salmo salar L.) against furunculosis, Fish Shellfish Immunol., 1996, vol. 6, pp. 335–350.
Møller, A.P. and Swaddle, J.P., Asymmetry, Developmental Stability, and Evolution, Oxford: University Press, 1997.
Oppedal, F., Berg, A., Olsen, R.E., et al., Photoperiod in seawater influence seasonal growth and chemical composition in autumn sea-transferred Atlantic salmon (Salmo salar L.) given two vaccines, Aquaculture, 2006, vol. 254, pp. 396–410.
Palmer, A.R., Fluctuating asymmetry analyses: A primer, in Developmental Instability: Its Origins and Evolutionary Implications, Markow, T.A., Ed., 1994, pp. 335–364.
Palmer, A.R. and Strobeck, C., Fluctuating asymmetry: Measurement, analysis, patterns, Ann. Rev. Ecol. Syst., 1986, vol. 17, pp. 391–421.
Reist, J.D., An empirical evaluation of coefficients used in residual and allometric adjustment of size covariation, Can. J. Zool., 1986, vol. 64, pp. 1363–1368.
Sørum, U. and Damsgå, B., Effects of anaesthetization and vaccination on feed intake and growth in Atlantic salmon (Salmo salar L.), Aquaculture, 2004, vol. 232, pp. 333–341.
Tchernavin, V.V., On the mechanical working of the head of bony fishes, Proc. Zool. Soc., London, 1948, vol. 118,part 1, pp. 129–143.
Treasurer, J. and Cox, C., Intraperitoneal and dorsal median sinus vaccination effects on growth, immune response, and reproductive potential in farmed Atlantic salmon Salmo salar, Aquaculture, 2008, vol. 275, pp. 51–57.
Vågsholm, I. and Djupvik, O., Risk factors for spinal deformities in Atlantic salmon, Salmo salar L., J. Fish Dis., 1998, vol. 21, pp. 47–53.
Van Valen, L., A study of fluctuating asymmetry, Evolution, 1962, vol. 16, no. 2, pp. 125–142.
Waagbø, R., Kryvi, H., Breck, O., and Ønsrud, R., Final Report from Workshop on Bone Disorders in Intensive Aquaculture of Salmon and Cod, Bergen: NIFES, 2005, Report, no. 164773, pp. 1–41.
Waddington, C.H., The Strategy of the Genes: A Discussion of Some Aspects of Theoretical Biology, London, 1957.
Wargelius, A., Fjelldal, P.G., and Hansen, T., Heat shock during early somitogenesis induces caudal vertebral column defects in Atlantic salmon (Salmo salar), Dev. Genes Evol., 2005, vol. 215, pp. 350–357.
Westneat, M.W., Feeding mechanics of teleost fishes (Labridae; Perciformes): A test of four-bar linkage models, J. Morphol., 1990, vol. 205, pp. 269–295.
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.
Witten, P.E. and Hall, B.K., Seasonal changes in the lower jaw skeleton in male Atlantic salmon (Salmo salar L.): Remodeling and regression of the kype after spawning, J. Anat., 2003, vol. 203, pp. 435–450.
Witten, P.E., Obach, A., Huysseune, A., and Baeverfjord, G., Vertebrae fusion in Atlantic salmon (Salmo salar): Development, aggravation and pathways of containment, Aquaculture, 2006, vol. 258, nos. 1–4, pp. 164–172.
Witten, P.E. and Villwock, W., Growth requires bone resorption at particular skeletal elements in a teleost fish with acellular bone (Oreochromis niloticus, Teleostei: Cichlidae), J. Appl. Ichthyol., 1997, vol. 13, pp. 149–158.
Yurtseva, A., Lajus, D., Artamonova, V., and Makhrov, A., Effect of hatchery environment on cranial morphology and developmental stability of Atlantic salmon (Salmo salar L.) from north-west Russia, J. Appl. Ichthyol., 2010, vol. 26, no. 2, pp. 307–314.
Zakharov, V.M., Asimmetriya zhivotnykh (populyatsionno-fenogeneticheskii podkhod) (Asymmetry of Animals: Population Phenogenetic Approach), Moscow: Nauka, 1987.
Zakharov, V.M., Future prospects for population phenogenetics, Sov. Sci. Rev. F. Physiol. Gen. Biol., 1989, vol. 4, pp. 1–79.
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Yurtseva, A.O., Lajus, D.L., Berg, A. et al. Developmental stability in vaccinated Atlantic salmon (Salmo salar L.): Deformities and fluctuating asymmetry of bone structures. Paleontol. J. 48, 1266–1274 (2014). https://doi.org/10.1134/S0031030114120156
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DOI: https://doi.org/10.1134/S0031030114120156