Advertisement

Biology Bulletin

, Volume 45, Issue 4, pp 400–408 | Cite as

Contents of Trace Elements as Indicators of Ecological Divergence between Sympatric Spined Loaches (Teleostei, Cobitidae) from the Upper Dnieper

  • A. S. Golubtsov
  • L. A. Pelgunova
  • D. A. Medvedev
  • E. A. Saltykova
  • T. B. Demidova
Ecology
  • 3 Downloads

Abstract

The contents of eight trace elements (Ti, Mn, Ni, Cu, Zn, Sr, Ba, and Pb) in muscles of syntopic sexual and clonal spined loaches (the golden loach Sabanejewia baltica, diploid males and females of Cobitis taenia, and congeneric triploid clonal females) from the upper Dnieper River and in the syntopic spined loaches (males and females of C. melanoleuca and males of C. taenia) from the upper Volga River basin were determined using the X-ray fluorescence spectroscopy technique. The contents of Cu in the clonal triploid Cobitis females and diploid C. taenia females from the Dnieper are different. The intersexual differences in the contents of Pb and Zn between C. taenia males and females, as well as the interspecific differences in the content of Ti between the spined loaches from the Dnieper and Volga basins were revealed. The concentrations of Cu and Pb correlated with the individual fish size. The potential for the use of the revealed differences in the trace element contents as an indicator of the divergence of ecological niches in the syntopic spined loaches is discussed.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aktan, N. and Tekin–Özan, S., Levels of some heavy metals in water and tissues of chub mackerel (Scomber japonicus) compared with physico–chemical parameters, seasons and size of the fish, J. Anim. Plant Sci., 2012, vol. 22, pp. 605–613.Google Scholar
  2. Alabaster, D. and Lloid, R., Kriterii kachestva vody dlya presnovodnykh ryb (Water Quality Criteria for Freshwater Fish), Moscow: Leg. Pishch. Prom–st’, 1984.Google Scholar
  3. Avise, J.C., Clonality: the Genetics, Ecology, and Evolution of Sexual Abstinence in Vertebrates, Oxford: Oxford Univ. Press, 2008.Google Scholar
  4. Berg, L.S., Ryby presnykh vod SSSR i sopredel’nykh stran, Ch. 2 (Fishes of the USSR and Adjacent Countries. Part 2), 4th ed., Moscow: Izd. AN SSSR, 1949, pp. 469–925.Google Scholar
  5. Blank, N., Hudson, A.G., Vonlanthen, P., Seehausen, O., Hammerschmidt, C.R., and Senn, D.B., Speciation leads to divergent methylmercury accumulation in sympatric whitefish, Aquat. Sci., 2013, vol. 75, pp. 261–273.CrossRefGoogle Scholar
  6. Bobyrev, A., Burmensky, V., Vasil’ev, V., Kriksunov, E., and Lebedeva, E., Coexistence of triploid and diploid forms of spined loach, Cobitis taenia: a model–based approach, Folia Biol. (Krakow), 2003, vol. 51, suppl., pp. 55–60.Google Scholar
  7. Bogutskaya, N.G. and Naseka, A.M., Katalog beschelyustnykh i ryb presnykh i solonovatykh vod Rossii s nomenklaturnymi i taksonomicheskimi kommentariyami (Catalogue of Agnatha and Fishes of Fresh and Brackish Waters of Russia with Nomenclatural and Taxonomic Comments), Moscow: Tovar. Nauch. Izd. KMK, 2004.Google Scholar
  8. Borkin, L.Ya. and Darevskii, I.S., Reticular (hybridogenic) speciation in vertebrates, Zh. Obshch. Biol., 1980, vol. 41, pp. 381–398.Google Scholar
  9. Boroń, A., Use of erythrocyte measurements to detect natural triploids of spined loach Cobitis taenia (L.), Cytobios, 1994, vol. 78, pp. 197–202.Google Scholar
  10. Burger, J., Gaines, K.F., Shane Boring, C.S., Stephens, W.L., Snodgrass, J., Dixon, C., McMahon, M., Shukla, S., Shukla, T., and Gochfeld, M., Metal levels in fish from the Savannah River: potential hazards to fish and other receptors, Environ. Res., 2002, vol. 89A, pp. 85–97.Google Scholar
  11. Canpolat, O., The determination of some heavy metals and minerals in the tissues and organs of the Capoeta umbla fish species in relation to body size, sex, and age, Ekoloji, 2013, vol. 22, no. 87, pp. 64–72.CrossRefGoogle Scholar
  12. Chernoff, B. and Dooley, J.K., Heavy metals in relation to the biology of the mummichog, Fundulus heteroclitus, J. Fish. Biol., 1979, vol. 14, pp. 309–328.CrossRefGoogle Scholar
  13. Costa, S.C. and Hartz, S.M., Evaluation of trace metals (cadmium, chromium, copper and zinc) in tissues of a commercially important fish (Leporinus obtusidens) from Guaíba Lake, Southern Brazil, Braz. Arch. Biol. Technol., 2009, vol. 52, pp. 241–250.CrossRefGoogle Scholar
  14. Cowx, I.G., Concentrations of heavy metals in the tissues of trout Salmo trutta and char Salvelinus alpinus from two lakes in Northern Wales, Environ. Poll. Ser. A, 1982, vol. 29, pp. 101–110.CrossRefGoogle Scholar
  15. Desta, Z., Borgstrom, R., Rosseland, B.O., and Gebre–Mariam, Z., Major difference in mercury concentrations of the African big barb, Barbus intermedius (R.) due to shifts in trophic position, Ecol. Freshwater Fish, 2006, vol. 15, pp. 532–543.Google Scholar
  16. Doyon, J.F., Schetagne, R., and Verdon, R., Different mercury bioaccumulation rates between sympatric populations of dwarf and normal lake whitefish (Coregonus clupeaformis) in the La Grande complex watershed, James Bay, Quebec, Biogeochemistry, 1998, vol. 40, pp. 203–216.Google Scholar
  17. Evolution and Ecology of Unisexual Vertebrates, Dowley, R.M. and Bogart, J.B., Eds., Albany, New York: New York State Museum, 1989.Google Scholar
  18. Farkas, A., Salánki, J., and Specziár, A., Age–and size–specific patterns of heavy metal in the organs of freshwater fish Abramis brama L. populating a low–contaminated site, Water Res., 2003, vol. 37, pp. 959–964.CrossRefPubMedGoogle Scholar
  19. Fatima, M., Usmani, N., Hossain, M.M., Siddiqui, M.F., Zafeer, M.F., Firdaus, F., and Ahmad, S., Assessment of genotoxic induction and deterioration of fish quality in commercial species due to heavy–metal exposure in an urban reservoir, Arch. Environ. Contam. Toxicol., 2014, vol. 67, pp. 203–213.CrossRefPubMedGoogle Scholar
  20. Gause, G.F., The Struggle for Existence, Baltimore: Williams and Wilkins, 1934.CrossRefGoogle Scholar
  21. Golovanova, I.L., Effects of heavy metals on the physiological and biochemical status of fishes and aquatic invertebrates, Inland Water Biol., 2008, vol. 1, no. 1, pp. 93–101.CrossRefGoogle Scholar
  22. Gray, M.M. and Weeks, S.C., Niche breadth in clonal and sexual fish (Poeciliopsis): a test of the frozen niche variation model, Can. J. Fish. Aquat. Sci., 2001, vol. 58, pp. 1313–1318.CrossRefGoogle Scholar
  23. Gremyachikh, V.A., Grebenyuk, L.P., Komov, V.T., and Stepanova, I.K., Accumulation of mercury and its teratogenic effects on larvae of Chironumus riparius Meigen (Diptera: Chironomidae) (Diptera: Chironomidae), Biol. Vnutr. Vod, 2006, no. 1, pp. 99–107.Google Scholar
  24. Handbook of European Freshwater Fishes, Kottelat, M. and Freyhof, J., Eds., Published by Kottelat, M., Cornol, Switzerland/Freyhof, J., Berlin, 2007.Google Scholar
  25. Janko, K., Kotusz, J., De Gelas, K., Šlechtová, V., Opoldusová, Z., Drozd, P., Choleva, L., Popiołek, M., and Baláž, M., Dynamic formation of asexual diploid and polyploid lineages: multilocus analysis of Cobitis reveals the mechanisms maintaining the diversity of clones, PLoS One, 2012, vol. 7, no. 9. e45384. doi 10.1371/journal.pone.0045384CrossRefPubMedPubMedCentralGoogle Scholar
  26. Juchno, D., Boroń, A., and Gołaszewski, J., Comparative morphology and histology of the ovaries of the spined loach Cobitis taenia L. and natural allopolyploids of Cobitis (Cobitidae), J. Fish. Biol., 2007, vol. 70, pp. 1392–1411.CrossRefGoogle Scholar
  27. Juchno, D. and Boroń, A., Fecundity of the spined loach, Cobitis taenia (Pisces, Cobitidae) and natural allopolyploids of Cobitis from a diploid–polyploid population, Folia Zool., 2010, vol. 59, pp. 35–43.Google Scholar
  28. Juchno, D., Boroń, A., Kujawa, R., Szlachciak, J., Szacherski, S., Spóz, A., and Grabowski, A., Comparison of egg and offspring size of karyologically identified spined loach, Cobitis taenia L., and hybrid triploid Cobitis females (Pisces, Cobitidae), Arch. Pol. Fish., 2013, vol. 14, pp. 293–299.Google Scholar
  29. Kasimoglu, C., The effect of fish size, age and condition factor on the contents of seven essential elements in Anguilla anguilla from Tersakan Stream, Mugla (Turkey), J. Pollut. Eff. Cont., 2014, vol. 2, p. 123. doi 10.4172/2375–4397.1000123Google Scholar
  30. Kenney, L.A., Eagles–Smith, C.A., Ackerman, J.T., and von Hippel, F.A., Temporal variation in fish mercury concentrations within lakes from the Western Aleutian Archipelago, Alaska, PLoS One, 2014, vol. 9, no. 7. e102244. doi 10.1371/journal.pone.0102244CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kotusz, J., Popiołek, M., Drozd, P., De Gelas, K., Šlechtová, V., and Janko, K., Role of parasite load and differential habitat preferences in maintaining the coexistence of sexual and asexual competitors in fish of the Cobitis taenia hybrid complex, Biol. J. Linn. Soc., 2014, vol. 113, pp. 220–235.Google Scholar
  32. Lamatsch, D.K. and Stöck, M., Sperm–dependent parthenogenesis and hybridogenesis in teleost fishes, in Lost Sex. The Evolutionary Biology of Parthenogenesis, Schon, I., Martens, K., and Dijk, P., Eds., Heidelberg: Springer, 2009, pp. 399–432.Google Scholar
  33. Lebedeva, E.B., Structure and distribution of clonally bisexual complexes of fishes of the genus Cobitis (Cobitidae), Extended Abstract of Cand. Sci. (Biol.) Dissertation, Moscow: IPEE RAN, 2007.Google Scholar
  34. Leberg, P. and Vrijenhoek, R.C., Variation among desert topminnows in their susceptibility to attack by exotic parasites, Conserv. Biol., 1994, vol. 8, pp. 419–424.CrossRefGoogle Scholar
  35. Lively, C.M., Craddock, C., and Vrijenhoek, R.C., The red queen hypothesis supported by parasitism in sexual and clonal fish, Nature, 1990, vol. 344, pp. 864–866.CrossRefGoogle Scholar
  36. Łuczyńska, J. and Tońska, E., The effect of size on the content of zinc, iron, copper and manganese in the muscles of perch (Perca fluviatilis L.) and pike (Esox lucius L.), Arch. Pol. Fish., 2006, vol. 14, pp. 5–13.Google Scholar
  37. Maciak, S., Janko, K., Kotusz, J., Choleva, L., Boroń, A., Juchno, D., Kujawa, R., Kozlowski, J., and Konarzewski, M., Standard metabolic rate (SMR) is inversely related to erythrocyte and genome size in allopolyploid fish of the Cobitis taenia hybrid complex, Funct. Ecol., 2011, vol. 25, pp. 1072–1078.CrossRefGoogle Scholar
  38. Madenjian, C.P., Blanchfield, P.J., Hrenchuk, L.E., and Van Walleghem, J.L.A., Mercury elimination rates for adult northern pike Esox lucius: evidence for a sex effect, Bull. Environ. Contam. Toxicol., 2014, vol. 93, pp. 144–148.CrossRefPubMedGoogle Scholar
  39. Marszał, L., Grzybkowska, M., Przybylski, M., and Valladolid, M., Feeding activity of spined loach Cobitis sp. in Lake Lucień, Poland, Folia Biol. (Krakow), 2003, vol. 51, suppl., pp. 159–165.Google Scholar
  40. Mee, J.A. and Rowe, L., A comparison of parasite loads on asexual and sexual Phoxinus (Pisces: Cyprinidae), Can. J. Zool., 2006, vol. 84, pp. 808–816.CrossRefGoogle Scholar
  41. Mee, J.A., Brauner, C.J., and Taylor, E.B., Repeat swimming performance and its implications for inferring the relative fitness of asexual hybrid dace (Pisces: Phoxinus) and their sexually reproducing parental species, Physiol. Biochem. Zool., 2011, vol. 84, pp. 306–315.CrossRefPubMedGoogle Scholar
  42. Mičetić, V., Bučar, M., Ivković, M., Piria, M., Krulik, I., Mihoci, I., Delić, A., and Kučinić, M., Feeding ecology of Sabanejewia balcanica and Cobitis elongata in Croatia, Folia Zool., 2008, vol. 57, pp. 181–190.Google Scholar
  43. Moor, J. and Ramamutri, S., Tyazhelye metally v prirodnykh vodakh: kontrol’ i otsenka vliyaniya (Heavy Metals in Natural Waters: Monitoring and Impact Assessment), Moscow: Mir, 1987.Google Scholar
  44. Nicoletto, F. and Hendricks, S.C., Sexual differences in accumulation of mercury in four species of centrarchid fishes, Can. J. Zool., 1988, vol. 66, pp. 944–949.CrossRefGoogle Scholar
  45. Pavlov, D.A., Vasil’eva, E.D., and Vasil’ev, V.P., Embryonic and larval development of spined loaches of the genus Cobitis (Cobitidae, Cypriniformes): diploid bisexual species C. melanoleuca, triploid clonal form, and hybrid C. melanoleuca × C. taenia, J. Ichthyol., 2004, vol. 44, no. 4, pp. 284–299.Google Scholar
  46. Perdices, A., Doadrio, I., Economidis, P., Bohlen, J., and Bnrescu, P., Pleistocene effects on the European freshwater fish fauna: double origin of the cobitid genus Sabanejewia in the Danube basin (Osteichthyes: Cobitidae), Mol. Phylogenet. Evol., 2003, vol. 26, pp. 289–299.CrossRefPubMedGoogle Scholar
  47. Podgurskaya, O.V., Kavun, V.Ya., and Lukyanova, O.N., Heavy metal accumulation and distribution in organs of the mussel Crenomytilus grayanus from upwelling areas of the Sea of Okhotsk and the Sea of Japan, Russ. J. Mar. Biol., 2004, vol. 30, no. 3, pp. 188–195.CrossRefGoogle Scholar
  48. Pokorny, P., Dobicki, W., Tarbaj, K., Kowalska–Góralska, M., Polechoński, R., and Senze, M., Age–dependent heavy metal content in muscle tissue of brown bullhead (Ictalurus nebulosus, Le Suerur, 1819), Pol. J. Environ. Stud., 2015, vol. 24, pp. 2139–2146.CrossRefGoogle Scholar
  49. Rajkowska, M. and Protasowicki, M., Distribution of metals (Fe, Mn, Zn, Cu) in fish tissues in two lakes of different trophy in Northwestern Poland, Environ. Monit. Ass., 2013, vol. 185, pp. 3493–3502.Google Scholar
  50. Ritterbusch, D. and Bohlen, J., On the ecology of spined loach in Lake Müggelsee, Folia Zool., 2000, vol. 49, suppl. 1, pp. 187–192.Google Scholar
  51. Saltykova, E.A., Pel’gunova, L.A., Sokolova, E.L., Skomorokhov, M.O., Demidova, T.B., and Golubtsov, A.S., Changes in the contents of strontium, barium, and lead in scales of bream Abramis brama from the Mozhaisk Reservoir over a quarter century, Dokl. Biol. Sci., 2016, vol. 467, pp. 68–71.CrossRefPubMedGoogle Scholar
  52. Sanchez–Carmona, R., Encina, L., Rodriguez–Ruiz, A., and Rodriguez–Sanchez, V., Age, growth and diet of the Iberian loach, Cobitis paludica in two different environments, Folia Zool., 2008, vol. 57, pp. 420–434.Google Scholar
  53. Schenck, R.A. and Vrijenhoek, R.C., Coexistence among sexual and asexual Poeciliopsis: foraging behavior and microhabitat selection, in Evolution and Ecology of Unisexual Vertebrates, Dowley, R.M. and Bogart, J.B., Eds., Albany, New York: New York State Museum, 1989, pp. 39–48.Google Scholar
  54. Schlosser, I.J., Doeringsfeld, M.R., Elder, J.F., and Arzayus, L.F., Niche relationships of clonal and sexual fish in a heterogeneous landscape, Ecology, 1998, vol. 79, pp. 953–968.CrossRefGoogle Scholar
  55. Slavik, O., Mattas, D., Jiřinec, R., Bartoš, L., and Rebec, J., Substratum selection by different sizes of spined loach Cobitis sp., Folia Zool., 2000, vol. 49, suppl. 1, pp. 167–172.Google Scholar
  56. Szarek–Gwiazda, E. and Amirowicz, A., Bioaccumulation of trace elements in roach, silver bream, rudd, and perch living in an inundated opencast sulphur mine, Aquat. Ecol., 2006, vol. 40, pp. 221–236.CrossRefGoogle Scholar
  57. Tchounwou, P.B., Yedjou, C.G., Patlolla, A.K., and Sutton, D.J., Heavy metals toxicity and the environment, EXS, 2012, vol. 101, pp. 133–164.PubMedPubMedCentralGoogle Scholar
  58. Tobler, M. and Schlupp, I., Parasites in sexual and asexual molly species of the genus Poecilia (Poeciliidae Teleostei): a case for the red queen?, Biol. Lett., 2005, vol. 1, pp. 166–168.CrossRefPubMedPubMedCentralGoogle Scholar
  59. Vasil’ev, V.P., Chromosomal polymorphism in Spicara smaris (Pisces, Centracanthidae), Zool. Zh., 1978, vol. 57, pp. 1276–1278.Google Scholar
  60. Vasil’ev, V.P. and Vasil’eva, E.D., New diploid–polyploid complex in fishes, Dokl. Ross. Akad. Nauk, 1982, vol. 226, pp. 250–252.Google Scholar
  61. Vasil’ev, V.P., Diploid–triploid complex of spined loaches in the genus Cobitis (Pisces, Cobitidae), Dokl. Ross. Akad. Nauk, 1990, vol. 312, pp. 249–252.Google Scholar
  62. Vasil’ev, V.P., Lebedeva, E.B., and Vasil’eva, E.D., Evolutionary ecology of clonal–bisexual complexes in spined loaches from genus Cobitis (Pisces, Cobitidae), J. Ichthyol., 2011, vol. 51, pp. 932–940.CrossRefGoogle Scholar
  63. Vasil’eva, E.D., Populyarnyi atlas–opredelitel’. Ryby (Popular Atlas–Identification Guide: Fishes), Moscow: Drofa, 2004.Google Scholar
  64. Vrijenhoek, R.C. and Pfeiler, E., Differential survival of sexual and asexual Poeciliopsis during environmental stress, Evolution, 1997, vol. 51, pp. 1593–1600.CrossRefPubMedGoogle Scholar
  65. Weeks, S.C., Gaggiotti, O.E., Schenck, R.A., Spindler, K.P., and Vrijenhoek, R.C., Feeding behavior in sexual and clonal strains of Poeciliopsis, Behav. Ecol. Sociobiol., 1992, vol. 30, pp. 1–6.CrossRefGoogle Scholar
  66. Witkowski, A., Morphological characteristics of Sabanejewia aurata (de Filippi, 1865) from the Odra River basin, with description of a new subspecies (Teleostei: Cypriniformes: Cobitidae), Zool. Abhandl. Staatl. Mus. Tierkunde. Dresden, 1994, vol. 48, no. 3, pp. 23–51.Google Scholar
  67. Yi, Y.–J. and Zhang, S.–H., Heavy metal (Cd, Cr, Cu, Hg, Pb, Zn) concentrations in seven fish species in relation to fish size and location along the Yangtze River, Environ. Sci. Pollut. Res. Int., 2012, vol. 19, pp. 3989–3996.PubMedGoogle Scholar
  68. Zhang, Z., He, L., Li, J., and Wu, Z.–B., Analysis of heavy metals of muscle and intestine tissue in fish—in Banan section of Chongqing from Three Gorges Reservoir, China, Polish. J. Environ. Stud., 2007, vol. 16, pp. 949–958.Google Scholar

Copyright information

© Pleiades Publishing, Inc. 2018

Authors and Affiliations

  • A. S. Golubtsov
    • 1
    • 2
  • L. A. Pelgunova
    • 1
  • D. A. Medvedev
    • 1
  • E. A. Saltykova
    • 1
  • T. B. Demidova
    • 1
  1. 1.Severtsov Institute of Ecology and EvolutionRussian Academy of Sciences (IPEE RAS)MoscowRussia
  2. 2.Papanin Institute for Biology of Inland WatersRussian Academy of Sciences (IBIW RAS)BorokRussia

Personalised recommendations