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Prodiamesa olivacea Meigen and Prodiamesa bureshi Michailova (Diptera, Chironomidae, Prodiamesinae) as a candidate for assessing the genotoxicity of trace metals in fluvial sediments

  • Julia Ilkova
  • Paraskeva Michailova
  • Ewa Szarek-Gwiazda
  • Andrzej Kownacki
  • Dariusz Ciszewski
Article
  • 46 Downloads

Abstract

The genome response, realized by structure chromosome rearrangements in the polytene chromosomes of two sibling species Prodiamesa bureshi Michailova and Prodiamesa olivacea Mg., was studied. The larvae of the species were collected in May and September, 2016, from Biała Przemsza River, a metal-mine-affected site in southern Poland, where Zn, Cd, and Pb concentrations in the sediment exceeded many times the reference data and those from unpolluted sites. The water had high contents of different major ions and nutrients. A high spectrum of somatic chromosome aberrations was detected in the salivary gland chromosomes of both species, which defined a high somatic index (from 1.2 to 7), indicating the sensitivity of both genomes to anthropogenic stress. The cells with somatic rearrangements of both species were significantly higher (P. bureshi: G = 25.636, P < 0.001 May, G = 32.722, P < 0.001 September; P. olivacea: G = 47.863, P < 0.001 May, G = 38.742, P < 0.001 September) than the control. Both species from polluted and unpolluted sites showed a high frequency of ectopic conjugations, as between arms B, CD (centromere regions), and E (NOR). Some deformities of mentum and mandibles of P. bureshi (20%) and P. olivacea (35%) were detected. We postulate that the appearances of somatic chromosome aberrations are more sensitive indicators of genotoxicity in the studied species than changes in external morphology. The sensitivity of the P. olivacea and P. bureshi genomes shows that these species are good candidates for detecting the presence of genotoxic compounds in aquatic basins and evaluating their genotoxic effects.

Keywords

Prodiamesa species Metal-mine-contaminated river Polytene chromosomes Somatic aberrations Genome instability 

Notes

Funding information

Research was funded by the National Science Center, Poland, grant no. 2014/15/B/ST10/03862.

References

  1. Adamu, C. I., & Nganje, T. N. (2010). Heavy metal contamination of soil and surface water in the Arufu lead-zinc mining district, Middle Benue trough, Nigeria. Ghana Mining Journal, 12, 17–23.Google Scholar
  2. Arambourou, H., Beisel, J. N., Branchu, P., & Debat, V. (2014). Exposure to sediments from polluted rivers has limited phenotypic effects on larvae and adults of Chironomus riparius. Science of the Total Environment, 484, 92–101.CrossRefGoogle Scholar
  3. Banerjee, U. S., & Gupta, S. (2017). Metal contamination in cultivated vegetables and agricultural soils irrigated with untreated industrial wastewater. Environmental Pollution and Protection, 2(1), 15–22.Google Scholar
  4. Beneberu, G., & Mengistou, S. (2014). Head capsule deformities in Chironomus spp. (Diptera: Chironomidae) as indicator of environmental stress in Sebeta River, Ethiopia. African Journal of Ecology, 53, 268–277.CrossRefGoogle Scholar
  5. Bernabo, P., Gaglio, M., Bellamoli, F., Viero, G., & Lencioni, V. (2017). DNA damage and translational response during detoxification from copper exposure in a wild population of Chironomus riparius. Chemosphere, 173, 235–244.CrossRefGoogle Scholar
  6. Bhattacharyay, G., Sadhu, A., Mazumdar, A., Majumdar, U., Chaudhuri, P., & Ali, A. (2006). Assessment of impact of heavy metals on the communities and morphological deformities of Chironomidae larvae in the River Damodar (India, West Bengal). Supplementa ad Acta Hydrobiologica, 8, 21–32.Google Scholar
  7. Ciszewski, D. (1998). Channel processes as a factor controlling accumulation of heavy metals in river bottom sediments: consequences for pollution monitoring (Upper Silesia, Poland). Environmental Geology, 36, 45–54.CrossRefGoogle Scholar
  8. Ciszewski, D. (2001). Flood related changes in heavy metal concentrations within sediment of the Biała Przemsza River. Geomorphology, 40, 205–218.CrossRefGoogle Scholar
  9. Ciszewski, D., Aleksander-Kwaterczak, U., Pociecha, A., Szarek-Gwiazda, E., Waloszek, A., & Wilk-Woźniak, E. (2013). Small effects of a large sediments contamination with heavy metals on aquatic organisms in the vicinity of an abandoned lead and zinc mine. Environmental Monitoring and Assessment, 185, 9825–9842.CrossRefGoogle Scholar
  10. De Wolf, H., Blust, R., & Backeljau, T. (2004). The population genetic structure of Littorina littorea (Mollusca: Gastropoda) along a pollution gradient in the Scheldt estuary (The Netherlands) using RAPD analysis. Science of the Total Environmen, 325, 59–69.CrossRefGoogle Scholar
  11. Di Veroli, A., Santoro, F., Pallottini, M., Selvaggi, R., Scardazza, F., Cappelletti, D., & Goretti, E. (2014). Deformities of chironomid larvae and heavy metal pollution: from laboratory to field studies. Chemosphere, 112, 9–17.CrossRefGoogle Scholar
  12. Förstner, U., & Salomons, W. (1980). Trace metal analysis in polluted sediments. Environmental and Technology Letters, 1, 1–494.CrossRefGoogle Scholar
  13. Ilkova, J., Michailova, P., Szarek-Gwiazda, E., Kownacki, A., & Ciszewski, D. (2017). The response of Chironomidae (Diptera) genome to heavy metal pollution in two rivers of southern Poland. Acta Zoologica Bulgarica, Suppl. 8, 9–15.Google Scholar
  14. Janssens de Bisthoven, L., Huysmans, C., Vannevel, R., Goemans, G., & Ollevier, F. (1997). Field and experimental morphological response of Chironomus larvae (Diptera, Nematocera) to xylene and toluene. Netherlands Journal of Zoology, 47, 227–239.CrossRefGoogle Scholar
  15. Janssens de Bisthoven, L., Postma, J., Vermeulen, A., Goemans, G., & Ollevier, F. (2001). Morphological deformities in Chironomus riparius Meigen larvae after exposure to cadmium over several generations. Water, Air and Soil Pollution, 129, 167–179.CrossRefGoogle Scholar
  16. Jeyasingham, K., & Ling, N. (2000). Seasonal influence on head capsule deformities in Chironomus zealandicus (Hudson) (Diptera: Chironomidae). Hydrobiologia, 427, 75–82.CrossRefGoogle Scholar
  17. Kabata-Pendias, A., & Pendias, H. (1999). Trace metals biogeochemistry. Warszawa: PWN [in Polish].Google Scholar
  18. Krastanov, B. (2005). Chromosome polymorphism in Chironomus balatonicus Devai, Wulker, Scholl (Diptera, Chironomidae) from Bourgas lake. In: Proceedings of the Balkan scientific conference of Biology, Plovdiv (Bulgaria), 19–21 July 2005 (Eds. B. Gruev, M. Nikolova, A. Donev), 560–567.Google Scholar
  19. Kuhlmann, M. L., Hayashida, C. Y., & Araujo, R. P. (2000). Using Chironomus (Chironomidae: Diptera) mentum deformities in environmental assessment. Acta Limnologica Brasiliensia, 12, 55–61.Google Scholar
  20. Madden, C. P., Suter, P. J., Nicholson, B. C., & Austin, A. D. (1992). Deformities in chironomid larvae as indicators of pollution (pesticide) stress. Netherlands Journal of Aquatic Ecology, 26, 551–557.CrossRefGoogle Scholar
  21. Martinez, E. A., Moore, B. C., Schaumloffel, J., & Dasgupta, N. (2002). The potential association between menta deformities and trace elements in Chironomidae (Diptera) taken from a heavy metal contaminated river. Archives of Environmental Contamination and Toxicology, 42, 286–291.CrossRefGoogle Scholar
  22. Martínez-Paz, P., Morales, M., Martín, R., Martínez-Guitarte, J. L., & Morcillo, G. (2014). Characterization of the small heat shock protein Hsp27 gene in Chironomus riparius (Diptera) and its expression profile in response to temperature changes and xenobiotic exposures. Cell Stress & Chaperones, 19(4), 529–540.CrossRefGoogle Scholar
  23. Meregalli, G., Pluymers, L., & Ollevier, F. (2001). Induction of mouthpart deformities in Chironomus riparius larvae exposed to 4-n-nonylphenol. Environmental Pollution, 111, 241–246.CrossRefGoogle Scholar
  24. Michailova, P. (1977). Karyotaxonomische Charakteristik der Prodiamesa olivacea Meigen und Prodiamesa bureshi sp.n. (Diptera, Chironomidae). Zoologische Beiträge, 3, 384–404.Google Scholar
  25. Michailova, P. (1989). The polytene chromosomes and their significance for the systematics of family Chironomidae, Diptera. Acta Zoologica Fennica (Helsinki), 186(1), 1–107.Google Scholar
  26. Michailova, P., Ilkova, J., & White, K. (2003). Cytogenetic alterations in Prodiamesinae species (Diptera, Chironomidae) from different polluted regions. Folia Biologica (Krakow), 51, 70–79.Google Scholar
  27. Michailova, P., Sella, G., & Petrova, N. (2012a). Chironomids (Diptera) and their salivary gland chromosomes as indicators of trace metal genotoxicology. Italian Journal of Zoology, 79, 218–230.CrossRefGoogle Scholar
  28. Michailova, P., Warchałowska-Śliwa, E., Szarek-Gwiazda, E., & Kownacki, A. (2012b). Does biodiversity of macroinvertebrates and genome response of Chironomidae larvae (Diptera) reflect heavy metal pollution in a small pond? Environmental Monitoring and Assessment, 184, 1–14.CrossRefGoogle Scholar
  29. Michailova, P., Ilkova, J., Dean, A. P., & White, K. N. (2015). Cytogenetic index and functional genome alterations in Chironomus piger Strenzke (Diptera, Chironomidae) in the assessment of sediment pollution: a case study of Bulgarian and UK rivers. Ecotoxicology and Environmental Safety, 111, 220–227.CrossRefGoogle Scholar
  30. Michailova, P., Ilkova, J., & White, K. (2016). Implications of genome alterations in Chironomus bernensis Klotzli (Diptera) for assessment of trace metal pollution in two Bulgarian rivers. River Research and Applications, 32, 914–924.CrossRefGoogle Scholar
  31. Müller, G. (1981). Sedimente als Kriterien der Wassergüte: Die Schwermetallbelastung der Sedimente des Neckars und seiner Nebenflüsse. Umschau, 81(15), 455–459.Google Scholar
  32. Odume, O. N., Muller, W. J., Palmer, C. G., & Arimoro, F. O. (2012). Mentum deformities in Chironomidae communities as indicators of anthropogenic impacts in Swartkops River. Physics and Chemistry of the Earth, 50–52, 140–148.CrossRefGoogle Scholar
  33. Pasieczna, A., Dusza-Dobek, A., & Markowski, W. (2010). Influence of hard coal mining and metal smelting on quality of Biała Przemsza and Bobrek rivers water. Górnictwo i Geologia, 5(4), 181–190.Google Scholar
  34. Persaud, D., Jaagumagi, R., & Hayton, A. (1993). Guidelines for the protection and management of aquatic sediment quality in Ontario. Ontario Ministry of the Environment. Queen’s Printer of Ontario, 27.Google Scholar
  35. Regulation of the Ministry of Environment of 21 July 2016 (Dz.U. 2016. poz. 1187)Google Scholar
  36. Saether, O. (1979). Chironomids communities as water quality indicators. Holarctic Ecology, 2, 65–74.Google Scholar
  37. Sella, G., Bovero, S., Ginepro, M., Michailova, P., Petrova, N., Robotti, C., & Zelano, V. (2004). Inherited and somatic variability in Palearctic populations of Chironomus riparius Meigen 1804 (Diptera, Chironomidae). Genome (Canada), 47, 322–344.Google Scholar
  38. Servia, M. J., Cobo, F., & González, M. (1998). Deformities in larval Prodiamesa olivacea (Meigen, 1818) (Diptera, Chironomidae) and their use as bioindicators of toxic sediment stress. Hydrobiologia, 385, 153–162.CrossRefGoogle Scholar
  39. Servia, M. J., Cobo, F., & Gonzalez, M. A. (2000). Seasonal and interannual variations in the frequency and severity of deformities in larvae of Chironomus riparius (Meigen, 1804) and Prodiamesa olivacea (Meigen, 1818) (Diptera, Chironomidae) collected in a polluted site. Environmental Monitoring and Assessment, 64, 617–626.CrossRefGoogle Scholar
  40. Swansburg, E. O., Fairchild, W. L., Fryer, B. J., & Ciborowski, J. (2002). Mouthpart deformities and community composition of Chironomidae (Diptera) larvae downstream of metal mines in New Brunswick, Canada. Environmental Toxicology and Chemistry, 21(12), 2675–2684.CrossRefGoogle Scholar
  41. Sokal, R.R., & Rohlf, F.G. (1995). Biometry, 3rd ed. W.H. Freeman and Company. 887 p.Google Scholar
  42. Szarek-Gwiazda, E., Maurkiewicz-Boroń, G., Gwiazda, R., & Urban, J. (2018). Chemical variability of water and sediment over time and along a mountain river subjected to natural and human impact. Knowledge and Management of Aquatic Ecosystems, 419(5), 1–14.Google Scholar
  43. Szarek-Gwiazda, E., Michailova, P., Ilkova, J., Kownacki, A., Ciszewski, D., & Aleksander-Kwaterczak, U. (2013). Effect of long term contamination by heavy metals on community and genome alterations of Chironomidae (Diptera) in stream with mine water (Southern Poland). Oceanological and Hydrobiological Studies, 42(4), 460–469.CrossRefGoogle Scholar
  44. Szito, A., & Mуzes, K. (1995). The Oligochaeta and the Chironomid fauna as pollution indicators in the Cris/Koros river system. Acta biologica Debrecina. Supplementum oecologica Hungarica, 3, 329–338.Google Scholar
  45. Vinokurova, N. V., Kalinina, E. A., & Stol’, E. E. (2016). Karyotype and inversion polymorphism of natural populations of Glyptotendipes glaucus (Meigen), 1818 (Diptera, Chironomidae) from the small reservoirs of Kaliningrad. Ecological Genetics, 14(4), 41–51 (In Russian).CrossRefGoogle Scholar
  46. Zhimulev, I. (1996). Morphology and structure of polytene chromosomes. Advances in Genetics, 34, 1–489.Google Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Julia Ilkova
    • 1
  • Paraskeva Michailova
    • 1
  • Ewa Szarek-Gwiazda
    • 2
  • Andrzej Kownacki
    • 2
  • Dariusz Ciszewski
    • 3
  1. 1.Institute of Biodiversity and Ecosystem ResearchBulgarian Academy of SciencesSofiaBulgaria
  2. 2.Institute of Nature ConservationPolish Academy of SciencesKrakowPoland
  3. 3.AGH-University of Science and TechnologyKrakowPoland

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