The vertebral abnormalities in eelpout Zoarces viviparus (Linnaeus, 1758) (Pisces, Zoarcidae)

P.N. Yershov

Proceedings of the Zoological Institute RAS, 2008, 312(1/2): 74–82 · https://doi.org/10.31610/trudyzin/2008.312.1-2.74

Full text

Abstract

The different vertebral abnormalities in eelpout are described for the first time. Population differences in the malformation frequency for eelpout have been found. The high incidence of vertebral abnormalities have been recorded in eelpout from the Wadden Sea (North Sea) as compared to the samples from the Chupa Inlet (White Sea) and Gulf of Finland (Baltic Sea). The degree of malformations in fishes correlates with the levels of various water toxicants in the same areas.

Key words

Baltic Sea, eelpout, North Sea, vertebral abnormalities, Zoarces viviparus

Submitted May 20, 2008 · Accepted July 25, 2008 · Published December 10, 2008

References

Alderdice D.F., Wickett W.P. and Brett J.R. 1958. Some effects of temporary exposure of low dissolved oxygen levels on Pacific salmon eggs. Journal of the Fisheries Research Board of Canada, 15: 229–250. https://doi.org/10.1139/f58-013

Alderdice D.F. and Velsen F.P. 1971. Some effects of salinity and temperature on early development of Pacific herring (Clupea pallasi). Journal of the Fisheries Research Board of Canada, 28: 1545–1562. https://doi.org/10.1139/f71-234

Atuma S., Bergh A., Hansson L., Wicklund-Glynn A. and Johnsson H. 1998. Non-ortho PCB levels in various fish species from the east and west coast of Sweden. Chemosphere, 37: 2451–2457. https://doi.org/10.1016/S0045-6535(98)00301-4

Bengtsson B.-E. 1975. Vertebral damage in fish induced by pollutants. Pp. 23–30. In: J.H. Koeman and J.J.T.W.A. Strik (Eds.). Sublethal effects of toxic chemicals on aquatic animals. Elsevier Sci. Publ. Co., Amsterdam.

Bengtsson B.-E. 1979. Biological variables, especially skeletal deformities in fish, for monitoring marine pollution. Philosophical Transactions of the Royal Society of London, 286: 457–464. https://doi.org/10.1098/rstb.1979.0040

Bengtsson B.-E. 1980. Ryggradsskador hos fisk fran Bottenviken – en effekt av tungmetallspridning? Statens Naturvardsverk, Rapport, 93: 1–13.

Bengtsson A. and Bengtsson B.-E. 1983. A method to registrate spinal and vertebral anomalies in fourhorn sculpin, Myoxocephalus quadricornis L. (Pisces). Aquilo. Series Zoologica, 22: 61–64.

Boglione C., Costa C., Giganti M., Cecchetti M., Di Dato P., Scardi M. and Cataudella S. 2006. Biological monitoring of wild thicklip grey mullet (Chelon labrosus), golden grey mullet (Liza aurata), thinlip mullet (Liza ramada) and flathead mullet (Mugil cephalus) (Pisces: Mugilidae) from different Adriatic sites: meristic counts and skeletal anomalies. Ecological Indicators, 6: 712–732. https://doi.org/10.1016/j.ecolind.2005.08.032

Broeg K., Zander S., Diamant A., Körting W., Krüner G., Paperna I. and Westernhagen H. 1999. The use of fish metabolic, pathological and parasitological indices in pollution monitoring I. North Sea. Helgoland Marine Research, 53: 171–194. https://doi.org/10.1007/s101520050023

Cameron P. and Berg J. 1992. Morphological and chromosomal aberrations during embryonic development in dab Limanda limanda. Marine Ecology Progress Series, 91: 163–169. https://doi.org/10.3354/meps091163

Chapman P.M. 1992. Pollution status of North Sea sediments – an international integrative study. Marine Ecology Progress Series, 91: 313–322. https://doi.org/10.3354/meps091313

Christensen N.O. 1980. Diseases and anomalies in fish and invertebrates in Danish littoral regions which might be connected with pollution. Rapports et Proces-Verbaux des Reunions Conseil Permanent International pour l’exploration de la Mer, 179: 103–109.

Ciereszko W. 2002. Polychlorinated hydrocarbons in fishes, blue mussel (Mytilus edulis), and bottom sediments of the south-western Baltic Sea. Acta Ichthyologica et Piscatoria, 32: 127–135. https://doi.org/10.3750/AIP2002.32.2.03

Cofino W.P., Smedes F., de Jong S.A., Abarnou A., Boon J.P., Oostingh I.M., Davies I.M., Klungsoyr J., Wilhelmsen S., Law R.J., Whinnett J.A., Schmidt D. and Wilson S. 1992. The chemistry programme. Marine Ecology Progress Series, 91: 47–56. https://doi.org/10.3354/meps091047

Cook M.A., Guthrie K.M., Rust M.B. and Plesha P.D. 2005. Effects of salinity and temperature during incubation on hatching and development of lingcod Ophiodon elongatus Girard, embryos. Aquaculture Research, 36: 1298–1303. https://doi.org/10.1111/j.1365-2109.2005.01346.x

Couch J.A., Winstead J.T. and Goodman L.R. 1977. Kepone-induced scoliosis and its histological consequences in fish. Science, 197: 585–587. https://doi.org/10.1126/science.69318

Dahlberg M.D. 1970. Frequencies of abnormalities in Georgia estuarine fishes. Transactions of the American Fisheries Society, 99: 95–97. https://doi.org/10.1577/1548-8659(1970)99<95:FOAIGE>2.0.CO;2

Dawson C.E. 1971. A bibliography of anomalies of fishes. Supplement 2. Gulf Research Reports, 3: 215–239. https://doi.org/10.18785/grr.0302.05

Dethlefsen V. 1980. Observations on fish diseases in the German Bight and their possible relation to pollution. Rapports et Proces-Verbaux des Reunions Conseil Permanent International pour l’exploration de la Mer, 179: 110–117.

Dethlefsen V., Westernhagen H. and Cameron P. 1996. Malformations in North Sea pelagic fish embryos during the period 1984–1995. ICES Journal of Marine Science, 53: 1024–1035. https://doi.org/10.1006/jmsc.1996.0128

Eggens M., Galdani F., Klungsoyr J. and Evert J. 1992. Hepatic EROD activity in dab Limanda limanda in the German Bight using an improved plate-reader method. Marine Ecology Progress Series, 91: 71–75. https://doi.org/10.3354/meps091071

Falandysz J. and Lorenc-Biala H. 1984. Trace metals in fish from Southern Baltic. Meeresforschung, Reports on Marine Research, 30: 111–119.

Falandysz J., Strandberg L., Strandberg B. and Rappe Christoffer. 1998. Polychlorinated naphthalenes in three-spined stickleback Gasterosteus aculeatus from the gulf of Gdansk. Chemosphere, 37: 2473–2487. https://doi.org/10.1016/S0045-6535(97)10241-7

Ford E. and Bull H.O. 1926–27. Abnormal vertebrae in herring. Journal Marine Biological Association of the United Kingdom, 14: 509–517. https://doi.org/10.1017/S0025315400007979

Galdani F., Bocquene G. and Cadiou Y. 1992. Evidence of variation in cholinesterase activity in fish along a pollution gradient in the North Sea. Marine Ecology Progress Series, 91: 77–82. https://doi.org/10.3354/meps091077

Garside E.T. 1959. Some effects of oxygen in relation to temperature on the development of Lake Trout embryos. Canadian Journal of Zoology, 37: 689–698. https://doi.org/10.1139/z59-069

Gercken J., Forlin L. and Andersson J. 2006. Developmental disorders in larvae of eelpout (Zoarces viviparus) from German and Swedish Baltic coastal waters. Marine Pollution Bulletin, 53: 497–507. https://doi.org/10.1016/j.marpolbul.2005.11.009

Gill C.D. and Fisk D.M. 1966. Vertebral abnormalities in sockeye, pink, and chum salmon. Transactions of the American Fisheries Society, 95: 177–182. https://doi.org/10.1577/1548-8659(1966)95[177:VAISPA]2.0.CO;2

Hansson S., Bengtsson B.-E. and Bengtsson A. 1984. Stomach content in Baltic fourhorn sculpin (Myoxocephalus quadricornis L.) with normal and deformed spinal vertebrae. Marine Pollution Bulletin, 15: 375–377. https://doi.org/10.1016/0025-326X(84)90171-1

Herut B., Kress N., Shefer E. and Hornung H. 1999. Trace element levels in mollusks from clean and polluted coastal marine sites in the Mediterranean, Red and North Seas. Helgoland Marine Research, 53: 154–162. https://doi.org/10.1007/s101520050021

Holm J., Palace V., Siwik P., Sterling G., Evans R., Baron C., Werner J. and Wautier K. 2005. Developmental effects of bioaccumulated selenium in eggs and larvae of two salmonid species. Environmental Toxicology and Chemistry, 24: 2373–2381. https://doi.org/10.1897/04-402R1.1

Hubbs C. 1959. High incidence of vertebral deformities in two natural populations of fishes inhabiting warm springs. Ecology, 40: 154–155.

ICES. 1977. Studies of the pollution of the Baltic Sea. ICES Cooperative Research Report, 63.

Jagadeesan G. 2005. Studies on skeletal deformation in the fingerlings stages of freshwater fish, Labeo rohita, induced by mercury. Journal of Experimental Zoology, 8: 429–433.

Kamp van de G. 1977. Vertebral deformities in herring around the British Isles and their usefulness for a pollution monitoring programme. ICES CM 1977 Documents, E, 5: 1–9.

Kandler R. 1932. Unsicherheiten bei der Bestimmung der Wirbelzahl infolge Verwachsungserscheinungen. Journal du Conseil pour l‘exploration de la Mer, Copenhagen, 7: 373–385. https://doi.org/10.1093/icesjms/7.3.373

Kasherwani D., Verma R.S., Shukla S. and Sharma U.D. 2007. Cadmium induced skeletal deformities in freshwater catfish, Heteropneustes fossilis (Bloch). Environment and Ecology, 25: 348–351.

Kent M.L., Watral V.G., Whipps C.M., Cunningham M.E., Criscione C.D., Heidel J.R., Curtis L.R., Spitsbergen J. and Markle D.F. 2004. A digenean metacercaria (Apophallus sp.) and a myxozoan (Myxobolus sp.) associated with vertebral deformities in cyprinid fishes from the Willamette River, Oregon. Journal of Aquatic Animal Health, 16: 116–129. https://doi.org/10.1577/H04-004.1

Kersten M., Dicke M., Kriews M., Naumann K., Schmidt D., Schulz M., Schwikowski M. and Steiger M. 1988. Distribution and fate of heavy metals in the North Sea. Pp. 300–347. In: W. Salomons et al. (Eds.). Pollution of the North Sea. Springer-Verlag, Berlin. https://doi.org/10.1007/978-3-642-73709-1_19

Kress N., Herut B., Shefer E. and Hornung H. 1999. Trace element levels in fish from clean and polluted coastal marine sites in the Mediterranean Sea, Red Sea and North Sea. Helgoland Marine Research, 53: 163–170. https://doi.org/10.1007/s101520050022

Lall S.P. and Lewis-McCrea Leah M. 2007. Role of nutrients in skeletal metabolism and pathology in fish – an overview. Aquaculture, 267: 3–19. https://doi.org/10.1016/j.aquaculture.2007.02.053

Larsen B. and Pheiffer M.P. 1986. Heavy metal budgets for selected Danish sea areas. Rapports et Proces-Verbaux des Reunions Conseil Permanent International pour l’exploration de la Mer, 186: 244–250.

Lohse J. 1990. Chlorierte organische Verbindungen in Wasser und Sediment. Pp. 75–85. In: J. Lozan et al. (Eds.). Warnsignale aus der Nordsee. Verlag Paul Parey, Berlin-Hamburg.

Louiz I., Menif D., Ben Attia M. and Ben Hassine O.K. 2007. Incidence of skeletal deformities in three species of Gobiidae from Bizerta lagoon (Tunisia). Cybium, 31: 199–206.

Malabarba L.R., Pereira E.H.L., da Silva J.F.P., Bruschi W. and Flores-Lopez F. 2004. Water quality evaluation using frequencies of abnormalities in fishes: a case study in the lago Guaiba, Rio Grande do Sul, Brasil [Brazil]. Comunicacoes do Museu de Ciencias e Tecnologia da PUCRS, Serie Zoologia, 17: 97–128.

Mathieson S., George S.G. and McLusky D.S. 1996. Temporal variation of total mercury concentrations and burdens in the liver of eelpout Zoarces viviparus from the Forth Estuary, Scotland: Implications for mercury biomonitoring. Marine Ecology Progress Series, 138: 41–49. https://doi.org/10.3354/meps138041

Meeuwig M.H., Bayer J.M. and Seelye J.G. 2005. Effects of temperature on survival and development of early life stage Pacific and western brook lampreys. Transactions of the American Fisheries Society, 34: 19–27. https://doi.org/10.1577/FT03-206.1

Mehrle P.M. and Mayer J.F.L. 1977. Bone development and growth of fish as affected by toxaphene. Pp. 301–314. In: I.H. Suffet (Ed.). Fate of pollutants in air and water environments. Part 2. Wiley Interscience Publishers, New York.

Moore M.N. 1992. Molecular cell pathology of pollutant-induced liver injury in flatfish: use of fluorescent probes. Marine Ecology Progress Series, 91: 127–133. https://doi.org/10.3354/meps091127

Muscatello J.R., Bennett P.M., Himbeault K.T., Belknap A.M. and Janz D.M. 2006. Larval deformities associated with selenium accumulation in northern pike (Esox lucius) exposed to metal mining effluent. Environmental Science and Technology, 40: 6506–6512. https://doi.org/10.1021/es060661h

Murcia S., Kerans B.L., MacConnell E. and Koel T.M. 2006. Myxobolus cerebralis infection patterns in Yellowstone cutthroat trout after natural exposure. Diseases of Aquatic Organisms, 71: 191–199. https://doi.org/10.3354/dao071191

Murphy C.E., Hoover J.J., George S.G., Lewis B.R. and Killgore K.J. 2007. Types and occurrence of morphological anomalies in Scaphirhynchus spp. of the Middle and Lower River. Journal of Applied Ichthyology, 23: 354–358. https://doi.org/10.1111/j.1439-0426.2007.00882.x

Napierska D. and Podolska M. 2005. Biomarkers of contaminant exposure: results of a field study with flounder (Platichthys flesus) from the southern Baltic Sea. Marine Pollution Bulletin, 50: 758–767. https://doi.org/10.1016/j.marpolbul.2005.02.007

Olszewska A., Kowalewska M. and Korzeniewski K. 1994. Trace metals in the body of Pomatoschistus minutus (Pisces) from the Southern Baltic. Polish Archives of Hydrobiology, 41: 109–121.

Orska J. 1957. The influence of temperature on the development of the skeleton in teleosts. Zoologica Poloniae, 7: 271–325.

Orska J. 1962. Anomalies in the vertebral columns of the pike (Esox lucius L.). Acta Zoologica Cracoviensia, 5: 327–345.

Pavlov D.A. and Moksness E. 1997. Development of the axial skeleton in wolffish, Anarhichas lupus (Pisces, Anarhichadidae), at different temperatures. Environmental Biology of Fishes, 49: 401–416. https://doi.org/10.1023/A:1007352802352

Protasowicki M. 1991. Heavy metals in Southern Baltic fish: present situation and future trends. Acta Ichthyologica et Piscatoria, 21: 291–299. https://doi.org/10.3750/AIP1991.21.S.31

Protasowicki M. 1992. Preliminary studies on selected elements in organs of dab Limanda limanda and their relation to fish disease state. Marine Ecology Progress Series, 91: 57–60. https://doi.org/10.3354/meps091057

Rosenthal H. and Alderdice D.F. 1976. Sublethal effects of environmental stressors, natural and pollutional, on marine fish eggs and larvae. Journal of the Fisheries Research Board of Canada, 33: 2047–2065.

Schmidt D. 1980. Comparison of trace heavy-metal levels from monitoring in the German Bight and the southwestern Baltic Sea. Helgolander Meeresuntersuchungen, 33: 576–586. https://doi.org/10.1007/BF02414781

Schmidt V., Zander S., Körting W., Broeg K., Westernhagen H., Dizer H., Hansen P.D., Skouras A and Steinhagen D. 2003. Parasites of flounder (Platichthys flesus L.) from the German Bight, North Sea, and their potential use in biological effects monitoring. C. Pollution effects on the parasite community and a comparison to biomarker responses. Helgoland Marine Research, 57: 262–271. https://doi.org/10.1007/s10152-003-0159-x

Schmolke S.R., Broeg K., Zander S., Bissinger V., Hansen P.D., Kress N., Herut B., Jantzen E., Kruner G., Sturm A., Korting W. and Westernhagen H. 1999. Multivariate statistical approach to the temporal and spatial patterns of selected bioindicators observed in the North Sea during the years 1995–1997. Helgoland Marine Research, 53: 257–266. https://doi.org/10.1007/s101520050029

Seymour A. 1959. Effects of temperature upon the formation of vertebrae and fin rays in young chinook salmon. Transactions of the American Fisheries Society, 88: 58–69. https://doi.org/10.1577/1548-8659(1959)88[58:EOTUTF]2.0.CO;2

Sfakianakis D.G., Koumoundouros G., Divanach P. and Kentouri M. 2004. Osteological development of the vertebral column and of the fins in Pagellus erythrinus (L.). Temperature effect on the developmental plasticity and morpho-anatomical abnormalities. Aquaculture, 232: 407–424. https://doi.org/10.1016/j.aquaculture.2003.08.014

Sindermann C.J. 1979. Pollution-associated diseases and abnormalities in fish and shellfish: a review. Fishery Bulletin, U.S. Department of Commerce, 76: 717–749.

Sindermann C.J. 1984. Fish and environmental impacts. Archiv für Fischereiwissenschaft, 35: 125–160.

Skouras A., Broeg K., Dizer H., Westernhagen H., Hansen P.-D. and Steinhagen D. 2003. The use of innate immune responses as biomarkers in a programme of integrated biological effects monitoring on flounder (Platichthys flesus) from the southern North Sea. Helgoland Marine Research, 53: 190–198. https://doi.org/10.1007/s10152-003-0141-7

Stockard C.R. 1921. Developmental rate and structural expression: an experimental study of twins, “double monsters” and single deformities, and the interaction among embryonic organs during their origin and development. American Journal of Anatomy, 28: 115–277. https://doi.org/10.1002/aja.1000280202

Strand J., Andersen L., Dahllof I. and Korsgaard B. 2004. Impaired larval development in broods of eelpout (Zoarces viviparus) in Danish coastal waters. Fish Physiology and Biochemistry, 30: 37–46. https://doi.org/10.1007/s10695-004-6003-7

Turner J.L. and Farley T.C. 1971. Effects of temperature, salinity and dissolved oxygen on the survival of striped bass eggs and larvae. California Fish and Game, 57: 268–273.

Valentine D.W. and Bridges K.W. 1969. High incidence of deformities in the serranid fish, Paralabrax nebulifer, from southern California. Copeia, 3: 637–638. https://doi.org/10.2307/1441956

Valentine D.W. 1975. Skeletal anomalies in marine teleosts. Pp. 695–718. In: W.E. Ribelin and G.Megaki (Eds.). The Pathology of Fishes. Wisconsin Press, Madison.

Villeneuve D.L., Curtis L.R., Jenkins J.J., Warner K.E., Tilton F., Kent M.L., Watral V.G., Cunningham M.E., Markle D.F., Sethajintanin D., Krissanakriangkrai O., Johnson E.R., Grove R. and Anderson K.A. 2005. Environmental stresses and skeletal deformities in fish from the Willamette River, Oregon. Environmental Science and Technology, 39: 3495–3506. https://doi.org/10.1021/es048570c

Vuorinen P.J., Haahti H., Leivuori M. and Miettinen V. 1998. Comparisons and temporal trends of organochlorines and heavy metals in fish from the Gulf of Bothnia. Marine Pollution Bulletin, 36: 236–240. https://doi.org/10.1016/S0025-326X(97)00016-7

Westernhagen H. 1970. Erbrutung der Eier von Dorsch (Gadus morhua), Flunder (Pleuronectes flesus) und Scholle (Pleuronectes platessa) unter kombinierten Temperatur- und Salzgehaltsbedingungen. Helgolander Meeresuntersuchungen, 21: 21–102. https://doi.org/10.1007/BF01630518

Westernhagen H., Rosenthal H. and Sperling K.-R. 1974. Combined effects of cadmium and salinity on development and survival of herring eggs. Helgolander Meeresuntersuchungen, 26: 416–433. https://doi.org/10.1007/BF01627625

Whitehead P.J.P., Bauchot M.-L., Hureau J.C., Nielsen J. and Tortonese E. (Eds.). 1986. Fishes of the North-Eastern Atlantic and the Mediterranean. The Chaucer Press, Bungay, 1473 p. https://doi.org/10.2307/1444931

Wunder W. 1971. Missbildungen beim Kabeljau (Gadus morhua) verursacht durch Wirbelsaulenverkurzung. Helgolander Meeresuntersuchungen, 22: 201–212. https://doi.org/10.1007/BF01609461

Yokoyama H., Freeman M.A., Itoh N. and Fukuda Y. 2005. Spinal curvature of cultured Japanese mackerel Scomber japonicus associated with a brain myxosporean, Myxobolus acanthogobii. Diseases of Aquatic Organisms, 66: 1–7. https://doi.org/10.3354/dao066001

Yamauchi M., Kim E.-Y., Iwata H., Shima Y. and Tanabe S. 2006. Toxic effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in developing red seabream (Pagrus major) embryo: An association of morphological deformities with AHR1, AHR2 and CYP1A expressions. Aquatic Toxicology, 80: 166–179. https://doi.org/10.1016/j.aquatox.2006.08.006