Abstract
The development of capelin Mallotus villosus from insemination to total resorption of the yolk is investigated at 5 and 8°C by the assessment of development of each individual (3850 eggs obtained from 77 spawning pairs). In total, ten malformation types are defined in early development. The frequency of their occurrence and embryonic mortality rate during incubation is described. The total malformation number and mortality rate are significantly higher at 8°С than at 5°С. A distinct relationship between early development quality and age or body size of the females is not revealed. In the majority of trials, the progenies of large females are characterized by better quality, but these data are not always significant. The qualitative composition and malformation rate of capelin differ from those observed in Atlantic cod Gadus morhua using the same methods of investigation. In addition, the malformation and mortality rates during early development are substantially lower in capelin than in Atlantic cod.
Similar content being viewed by others
REFERENCES
Armstrong, P.B., Mechanism of hatching in Fundulus heteroclitus,Biol. Bull., 1936, vol. 71, no. 2, p. 407.
Avery, T.S. and Brown, A.J., Investigating the relationship among abnormal patterns of cell cleavage, egg mortality and early larval condition in Limanda ferruginea,J. Fish Biol., 2005, vol. 67, pp. 890–896. https://doi.org/10.1111/j.0022-1112.2005.00783.x
Avery, T.S., Killen, S.S., and Hollinger, T.R., The relationship of embryonic development, mortality, hatching success, and larval quality to normal or abnormal early embryonic cleavage in Atlantic cod, Gadus morhua,Aquaculture, 2009, vol. 289, pp. 265–273. https://doi.org/10.1016/j.aquaculture.2008.12.011
Ballard, W.W., Morphogenetic movements in Salmo gairdneri Richandson, J. Exp. Zool., 1973a, vol. 184, no. 1, pp. 27–48.
Ballard, W.W., A new fate map for Salmo gairdneri,J. Exp. Zool., 1973b, vol. 184, no. 1, pp. 49–73.
Ballard, W.W., Morphogenetic movements and fate maps of vertebrates, Am. Zool., 1981, vol. 18, pp. 119–135.
Berkeley, S.A., Chapman, C., and Sogard, S.M., Maternal age as a determinant of larval growth and survival in marine fish, Ecology, 2004, vol. 85, pp. 1258–1264. https://doi.org/10.1890/03-0706
Blaxter, J.H., The effect of temperature on larval fishes, Neth. J. Zool., 1992, vol. 42, nos. 2–3, pp. 336–357. https://doi.org/10.1163/156854291X00379
Bromage, N.R. and Cumaranatunga, R., Egg production in the rainbow trout, in Recent Advances in Aquaculture, Muir, J.F. and Roberts, R., Eds., London: Croom Helm, 1988, pp. 65–138. https://doi.org/10.1007/978-94-011-9743-4_2
Brooks, S., Tyler, C.R., and Sumpter, J.P., Egg quality in fish: what makes a good egg? Rev. Fish Biol. Fish., 1997, vol. 7, pp. 387–416. https://doi.org/10.1023/A:1018400130692
Cameron, P. and Berg, J., Morphological and chromosomal aberrations during embryonic development in dab Limanda limanda,Mar. Ecol.: Progr. Ser., 1992, vol. 91, pp. 163–169.
Chambers, R.C. and Leggett, W.C., Maternal influences on variation in egg sizes in temperate marine fishes, Am. Zool., 1996, vol. 36, pp. 180–196. https://doi.org/10.1093/icb/36.2.180
Chambers, R.C., Leggett, W.C., and Brown, J.A., Egg size, female effects, and the correlations between early life history traits of capelin, Mallotus villosus: an appraisal at the individual level, Fish. Bull. U.S., 1989, vol. 87, pp. 515–523.
Christiansen, J.S., Præbel, K., Siikavuopio, S., and Carscadden, J.E., Facultative semelparity in capelin Mallotus villosus (Osmeridae)—an experimental test of a life history phenomenon in a sub-arctic fish, J. Exp. Mar. Biol. Ecol., 2008, vol. 360, pp. 47–55. https://doi.org/10.1016/j.jembe.2008.04.003
Collett, R., Meddelelser om Norges fiske i aarene 1884–1901, Mallotus villosus (Müller) 1776, Fork. Vitensk Sehk. Krist., 1903, no. 9, pp. 147–162.
Davenport, J. and Stene, A., Freezing resistance, temperature and salinity tolerance in eggs, larvae and adults of capelin, Mallotus villosus, from Balsfjord, J. Mar. Biol. Assoc. U.K., 1986, vol. 66, no. 1, pp. 145–157. https://doi.org/10.1017/S0025315400039710
Davenport, J., Vahl, O., and Lonning, S., Cold resistance in the eggs of the capelin Mallotus villosus,J. Mar. Biol. Assoc. U.K., 1979, vol. 59, pp. 443–453. https://doi.org/10.1017/S0025315400042764
Davoren, G.K., Divergent use of spawning habitat by male capelin (Mallotus villosus) in a warm and cold year, Behav. Ecol., 2013, vol. 24, no. 1, pp. 152–161. .https://doi.org/10.1093/beheco/ars147
Dodson, J.J., Carscadden, J.E., Bernatchez, L., and Colombani, F., Relationship between spawning mode and phylogeographic structure in mitochondrial DNA of North Atlantic capelin Mallotus villosus,Mar. Ecol.: Prog. Ser., 1991, vol. 76, pp. 103–113.
Donelson, J.M., McCormick, M.I., and Munday, P.L., Parental condition affects early life-history of a coral reef fish, J. Exp. Mar. Biol. Ecol., 2008, vol. 360, pp. 109–116. https://doi.org/10.1016/j.jembe.2008.04.007
Edsall, T.A., The effect of temperature on the rate of development and survival of alewife eggs and larvae, Trans. Am. Fish. Soc., 1970, vol. 99, no. 2, pp. 376–380. .https://doi.org/10.1577/1548-8659
Eriksen, E., Johansen, O.G., Tjelmeland, S., et al., Methodology for Assessment of the Capelin Spawning Migration in the Barents Sea, Spring 2009, Bergen: Inst. Mar. Res., 2009.
Frank, K.T. and Leggett, W.C., Prediction of egg development and mortality rates in capelin (Mallotus villosus) from meteorological, hydrographic, and biological factors, Can. J. Fish. Aquat. Sci., 1981, vol. 38, no. 11, pp. 1327–1338. https://doi.org/10.1139/f81-179
Friðgeirsson, E., Observations on spawning behavior and embryonic development of the Icelandic capelin, Rit. Fiskideildar., 1976, vol. 5, no. 4, pp. 1–35.
Gjøsæter, H., The population biology and exploitation of capelin (Mallotus villosus) in the Barents Sea, Sarsia, 1998, vol. 83, pp. 453–496. https://doi.org/10.1080/00364827.1998.10420445
Gjøsæter, H. and Gjøsæter, J., Observations on the embryonic development of capelin (Mallotus villosus Müller) from the Barents Sea, Fiskeridir. Skr. Ser. Havunders., 1986, vol. 18, pp. 59–68.
Guma’a, S.A., The effects of temperature on the development and mortality of eggs of perch, Perca fluviatilis,Freshwater Biol., 1978, vol. 8, pp. 221–227. https://doi.org/10.1111/j.1365-2427.1978.tb01443.x
Gunnes, K., Survival and development of Atlantic salmon eggs and fry at three different temperatures, Aquaculture, 1979, vol. 16, pp. 211–219. https://doi.org/10.1016/0044-8486(79)90109-1
Hamor, T. and Garside, E.T., Developmental rates of embryos of Atlantic salmon, Salmo salar L., in response to various levels of temperature, dissolved oxygen, and water exchange, Can. J. Zool., 1976, vol. 54, pp. 1912–1917. https://doi.org/10.1139/z76-221
Hansen, T.K. and Falk-Petersen, I.B., The influence of rearing temperature on early development and growth of spotted wolfish Anarhichas minor (Olafsen), Aquat. Res., 2001, vol. 32, pp. 369–378. https://doi.org/10.1046/j.1365-2109.2001.00567.x
Hop, H. and Gjøsæter, H., Polar cod (Boreogadus saida) and capelin (Mallotus villosus) as key species in marine food webs of the Arctic and the Barents Sea, Mar. Biol. Res., 2013, vol. 9, pp. 878–894. https://doi.org/10.1080/17451000.2013.775458
Kafiani, K.A. and Timofeeva, M.Ya., Nuclear RNA synthesis in early embryonic development, Dokl. Akad. Nauk SSSR, 1964, vol. 154, pp. 721–724.
Kamler, E., Early life history of fish, an energetics approach, in Fish and Fisheries, London: Chapman and Hall, 1992, vol. 4.
Kamler, E., Ontogeny of yolk-feeding fish: an ecological perspective, Rev. Fish Biol. Fish., 2002, vol. 12, no. 1, pp. 79–103. https://doi.org/10.1023/A:1022603204337
Kamler, E., Parent-egg-progeny relationships in teleost fishes: an energetics perspective, Rev. Fish Biol. Fish., 2005, vol. 15, pp. 399–421. https://doi.org/10.1007/s11160-006-0002-y
Kane, D.A. and Kimmel, C.B., The zebrafish midblastula transition, Development, 1993, vol. 119, pp. 447–456.
Kinne, O. and Kinne, E.M., Rates of development in embryos of a cyprinodont fish exposed to different temperature-salinity-oxygen combinations, Can. J. Zool., 1962, vol. 40, pp. 231–253. https://doi.org/10.1139/z62-025
Kjesbu, O.S., Klungsoyr, J., Kryvi, H., et al., Fecundity, atresia, and egg size of captive Atlantic cod (Gadus morhua) in relation to proximate body composition, Can. J. Fish Aquat. Sci., 1991, vol. 48, pp. 2333–2343. https://doi.org/10.1139/f91-274
Kjesbu, O.S., Solemdal, P., Bratland, P., and Fonn, M., Variation in annual egg production in individual captive Atlantic cod (Gadus morhua), Can. J. Fish Aquat. Sci., 1996, vol. 53, pp. 610–620. https://doi.org/10.1139/f95-215
Kjǿrsvik, E., Egg quality in wild and broodstock cod Gadus morhua L., World Aquacult. Soc., 1994, vol. 25, no. 1, pp. 22–29. https://doi.org/10.1111/j.1749-7345.1994.tb00800.x
Kjǿrsvik, E., Stene, A., and Lønning, S., Morphological, physiological and genetical studies of egg quality in cod (Gadus morhua L.), in The Propagation of Cod, Gadus morhua L. Flødevigen Rapportser, Dahl, E., et al., Eds., Skien: Oluf Rassmussen, 1984, no. 1, pp. 67–86.
Knutsen, G.M. and Tilseth, S., Growth, development, and feeding success of Atlantic cod larvae Gadus morhua related to egg size, Trans. Am. Fish. Soc., 1985, vol. 114, pp. 507–511. https://doi.org/10.1577/1548-8659
Laine, P. and Rajasilta, M., The hatching success of Baltic herring eggs and its relation to female condition, J. Exp. Mar. Biol. Ecol., 1999, vol. 237, pp. 61–73. https://doi.org/10.1016/S0022-0981(98)00213-5
Lakin, G.V., Biometriya (Biometry), Moscow: Vysshaya Shkola, 1990.
Lavigne, D.M., Ecological interactions between marine mammals, commercial fisheries and their prey: unraveling the tangled web, in High-Latitude Seabirds, Vol. 91, Part 4: Trophic Relationships and Energetics of Endotherms in Cold Ocean Systems, Montevecchi, W.A., Ed., Ottawa: Can. Wildl. Serv. Occas., 1996, pp. 59–71.
Longwell, A.C. and Hughes, J.B., Cytologic, cytogenetic and developmental state of Atlantic mackerel eggs from the sea surface of New York Bight, and prospects for biological effects monitoring with ichthyoplankton, Rapp. P.-V. Reun.-Cons. Int. Explor. Mer, 1980, vol. 179, pp. 275–291.
Luczynski, M., Strzezek, J., and Brzuzan, P., Secretion of hatching enzyme and its proteolytic activity in Coregoninae (Coregonus albula L. and C. lavaretus L.) embryos, Fish Physiol. Biochem., 1987, vol. 4, pp. 57–62. https://doi.org/10.1007/BF02044314
Makhotin, V., Solemdal, P., Korsbrekke, K., and Salthaug, A., Types and frequency of malformations and mortality in eggs of Arcto-Norwegian cod: a field study, ICES CM 2001/N:12, Copenhagen: Int. Counc. Explor. Sea, 2001.
Marteinsdottir, G. and Begg, G.A., Essential relationships incorporating the influence of age, size and condition on variables required for estimation of reproductive potential in Atlantic cod Gadus morhua,Mar. Ecol.: Progr. Ser., 2002, vol. 235, pp. 235–256.
Marteinsdottir, G. and Steinarsson, A., Maternal influence on the size and viability of Iceland cod (Gadus morhua) eggs and larvae, J. Fish Biol., 1998, vol. 52, pp. 1241–1258. https://doi.org/10.1111/j.1095-8649.1998.tb00969.x
Nakashima, B.S. and Wheeler, J.P., Capelin (Mallotus villosus) spawning behavior in Newfoundland waters—the interaction between beach and demersal spawning, ICES J. Mar. Sci., 2002, vol. 59, pp. 909–916. https://doi.org/10.1006/jmsc.2002.1261
Nelson, J.S., Grande, T.C., and Wilson, M.V.H., Fishes of the World, Hoboken: Wiley, 2016.
Neyfakh, A.A., X-ray inactivation of nuclei as a method for studying their function in the early development of fishes, J. Embryol. Exp. Morphol., 1959, vol. 7, pp. 173–192.
Nikol’skii, G.V., The reasons of population fluctuation in fishes, Vopr. Ikhtiol., 1962, vol. 1, no. 4 (21), pp. 659–665.
Okamura, A., Yamada, Y., Horie, N., et al., Effects of water temperature on early development of Japanese eel Anguilla japonica,Fish. Sci., 2007, vol. 73, pp. 1241–1248. https://doi.org/10.1111/j.1444-2906.2007.01461.x
Oppenheim, R.W., Cell death during development of the nervous system, Ann. Rev. Neurosci., 1991, vol. 14, pp. 453–501.
Penton, P.M. and Davoren, G.K., A common garden experiment on capelin (Mallotus villosus) early life history stages to examine use of beach and deepwater spawning habitats, J. Exp. Mar. Biol. Ecol., 2013, vol. 439, pp. 54–60. https://doi.org/10.1016/j.jembe.2012.10.009
Penton, P., Davoren, G., Montevecchi, W., and Andrews, D., Beach and demersal spawning in capelin (Mallotus villosus) on the northeast Newfoundland coast: egg developmental rates and mortality, Can. J. Zool., 2012, vol. 90, no. 2, pp. 248–256. https://doi.org/10.1139/z11-132
Penton, P.M., McFarlane, C.T., Spice, E.K., et al., Lack of genetic divergence in capelin (Mallotus villosus—Osmeridae) spawning at beach versus subtidal habitats in coastal embayments of Newfoundland, Can. J. Zool., 2014, vol. 92, pp. 377–382. https://doi.org/10.1139/cjz-2013-0261
Pepin, P., Effect of temperature and size on development, mortality and survival rates of the pelagic early life history stages of marine fish, Can. J. Fish. Aquat. Sci., 1991, vol. 48, pp. 503–518. https://doi.org/10.1139/f91-065
Pozdnyakov, Yu.F., Spawning of the capelin in aquarium, Izv. Karel. Kol’sk. Fil.,Akad. Nauk SSSR, 1959, vol. 3, pp. 145–147.
Pozdnyakov, Yu.F., Development of the capelin in the Barents Sea, Tr. Murmansk.Morsk. Biol. Inst., 1960, vol. 2, no. 6, pp. 211–225.
Pozdnyakov, Yu.F., Distribution of the capelin larvae in the southern and southeastern part of the Barents Sea, Tr. Murmansk.Morsk. Biol. Inst., 1962, vol. 8, no. 4, pp. 134–145.
Præbel, K., Christiansen, J.S., and Fevolden, S.E., Temperature and salinity conditions in a sub-Arctic intertidal spawning habitat for capelin, Mar. Biol. Res., 2009, vol. 5, pp. 511–514. https://doi.org/10.1080/17451000902729670
Rass, T.S., Spawning of the capelin Mallotus villosus in the Barents Sea, Tr. Gos. Okeanogr. Inst., 1933, vol. 4, no. 1, pp. 3–35.
Sætre, R. and Gjøsæter, J., Ecological investigations on the spawning grounds of the Barents Sea capelin, Fiskeridir. Skr.,Ser. Havunders., 1975, vol. 16, pp. 203–227.
Scott, B.E., Marteinsdottir, G., Begg, G.A., et al., Effects of population size/age structure, condition and temporal dynamics of spawning on reproductive output in Atlantic cod (Gadus morhua), Ecol. Model., 2006, vol. 191, pp. 383–415. https://doi.org/10.1016/j.ecolmodel.2005.05.015
Solemdal, P., Kjesbu, O.S., and Fonn, M., Egg mortality in recruit- and repeat-spawning cod—an experimental study, ICES CM 1995/G:35, Copenhagen: Int. Counc. Explor. Sea, 1995.
Solemdal, P., Makhotin, V., and Fonn, M., Long-term studies on spawning in Arcto-Norwegian cod—mortality pattern of eggs and early larvae, ICES CM 1998/DD:8, Copenhagen: Int. Counc. Explor. Sea, 1998.
Stene, A., Light microscopical studies of chromosomes in embryos of cod, Gadus morhua L., J. Fish. Biol., 1987, vol. 31, pp. 445–450. https://doi.org/10.1111/j.1095-8649.1987.tb05250.x
Trippel, E.A., Egg size and viability and seasonal offspring production of young Atlantic cod, Trans. Am. Fish. Soc., 1998, vol. 127, pp. 339–359. https://doi.org/10.1577/1548-8659(1998)127<0339:ESAVAS>2.0.CO;2
Trippel, E.A., Kjesbu, O.S., and Solemdal, P., Effects of adult age and size structure on reproductive output in marine fishes, in Early Life History and Recruitment in Fish Populations, Chambers, R.C. and Trippel, E.A., Eds., New York: Springer-Verlag, 1997, pp. 31–62. https://doi.org/10.1007/978-94-009-1439-1
Vladimirov, V.I., Influence of growth rate of fish producers on survival and offspring population, Vopr. Ikhtiol., 1973, vol. 13, no. 6, pp. 963–976.
Vladimirov, V.I., Variability of fish sizes on early stages and survival rate, in Raznokachestvennost’ rannego ontogeneza u ryb (Different Early Ontogenesis in Fishes), Kiev: Naukova Dumka, 1974, pp. 227–254.
Vladimirov, V.I., Critical periods of development of fishes, Vopr. Ikhtiol., 1975, vol. 15, no. 6, pp. 955–975.
Wallin, L. and Nissling, A., Cell morphology as an indicator of viability of cod eggs, Gadus morhua—results from an experimental study, Fish. Res., 1988, vol. 38, no. 3, pp. 247–255. https://doi.org/10.1016/S0165-7836(98)00157-X
Yamagami, K., Mechanisms of hatching in fish: secretion of hatching enzyme and enzymatic choriolysis, Am. Zool., 1981, vol. 21, pp. 459–471. https://doi.org/10.1093/icb/21.2.459
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest. The authors declare that they have no conflict of interest.
Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Additional information
Translated by D. Pavlov
Rights and permissions
About this article
Cite this article
Shadrin, A.M., Makhotin, V.V. & Eriksen, E. Incubation Temperature Effect on Qualitative and Quantitative Composition of Abnormalities and Mortality Rate in Embryogenesis of the Barents Sea Capelin Mallotus villosus (Osmeridae). J. Ichthyol. 60, 79–89 (2020). https://doi.org/10.1134/S0032945220010142
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0032945220010142