Effect of heavy metals on phytobenthos assemblages in mine pit lakes of Bosnia and Herzegovina

Ermin Mašić, Sabina Žero, Senka Barudanović, Mustafa Memić

Abstract


Mine pit lakes are a specific type of water accumulation, formed after exploitation process, by water filling the remaining crater or damming a watercourse with overburden material. Due to nature of their formation, these lakes may contain various heavy metals that might have an adverse effect on diversity of phytobenthos. The objective of this paper is the analysis of the phytobenthos assemblages in the mine pit lakes and assessment of the effects of certain heavy metals on diversity of this group of organisms. Special emphasis of this work is to determine the presence of tolerant species of algae on heavy metal pollution in mine pit lakes and their application in biomonitoring. The field research was performed during autumn season in 2014, at six mine pit lakes in the territory of B&H. The following heavy metals were analysed Al, Cr, Zn, Ni and Fe. The results were discussed in terms of confirmation or rejection of the hypothesis on the adverse effect of heavy metals on diversity of algae.

 


Keywords


heavy metals, mine pit lakes, algae, diversity, restoration.

Full Text:

PDF

References


Anderson M. J, Gorley R. N, Clarke K. R 2008: PERMANOVA + for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth. 214 p.

__________________________________________________

Barudanović, S., Mašić, E. 2014: State of the mine-pit lakes in the wider area of Zenica-Doboj region. 24th International Scientific-Expert Conference of Agriculture and Food Industry. Zbornik radova / Proceedings. 25-28.2013. Sarajevo, Bosna i Hercegovina. Izmir, Turska. 550-555.

__________________________________________________

Bey, M-Y., Ector, L. 2013a: Atlas des diatomées des course dʹeau de la région Rhône-Alpes. Tome 1: Centrique:Monoraphidées. Avec la collaboration de Rémy Chavaux et Patrick Béranger. DREAL Rhône-Alpes. 181 p.

__________________________________________________

Bey, M-Y., Ector, L. 2013b: Atlas des diatomées des course dʹeau de la région Rhône-Alpes. Tome 2: Araphidées, Brachyraphidées. Avec la collaboration de Rémy Chavaux et Patrick Béranger. DREAL Rhône-Alpes. 330 p.

__________________________________________________

Bey, M-Y., Ector, L. 2013c: Atlas des diatomées des course dʹeau de la région Rhône-Alpes. Tome 3: Naviculacées, Naviculoidées (a). Avec la collaboration de Rémy Chavaux et Patrick Béranger. DREAL Rhône-Alpes. 530 p.

__________________________________________________

Bey, M-Y., Ector, L. 2013d: Atlas des diatomées des course dʹeau de la région Rhône-Alpes. Tome 4: Naviculacées, Naviculoidées (b). Avec la collaboration de Rémy Chavaux et Patrick Béranger. DREAL Rhône-Alpes. 750 p.

__________________________________________________

Bey, M-Y., Ector, L. 2013e: Atlas des diatomées des course dʹeau de la région Rhône-Alpes. Tome 5: Naviculacées, Cymbelloidées, Gomphonématoidées. Avec la collaboration de Rémy Chavaux et Patrick Béranger. DREAL Rhône-Alpes. 972 p.

__________________________________________________

Bey, M-Y., Ector, L. 2013f: Atlas des diatomées des course dʹeau de la région Rhône-Alpes. Tome 5: Bacillariacées, Rhopalodiacées, Surirellacées. Avec la collaboration de Rémy Chavaux et Patrick Béranger. DREAL Rhône-Alpes. 1182 p.

__________________________________________________

Branković, S., Glišić, R., Pavlović-Muratspahić, D., Topuzović, M., Đekić, V. 2013: The bioconcentration of some metals in species Potentilla visianii Pančić. Biologica Nyssana, 4 (1/2): 57-64.

__________________________________________________

Bucko, K., Wojtal, Z. A., Magyari, E. K. 2013: Lectotypification, emeneded description and distribution of Planothidium distinctum (Achnanthaceae, Bacillariophyceae). Phytotaxa, 117 (1): 1-10.

__________________________________________________

Cantonati, M., Angeli, N., Virtanen, L., Wojtal, Z. A., Gabrieli, J., Falasco, E., Lavoie, I., Morin, S., Marchetti, A., Fortin, C., Smirnova, S. 2014: Achnanthidium minutissimum (Bacillariophyta) valve deformities as indicators of metal enrichment in diverse widely-distributed freshwater habitats. Science of The Total Environment. 475: 201-215.

__________________________________________________

Cantonati, M., Kelly, G. M., Lange-Bertalot, H. 2017: Freshwater Benthic Diatoms of Central Europe: Over 800 Common Species Used in Ecological Assesment. English edition with updated taxonomy and added species. Koeltz Botanical Book. 942 p.

__________________________________________________

Cantonati, M., Lange-Bertalot, H., Angeli, N. 2010: Neidomorpha gen. nov. (Bacillariophyta): A new freshwater diatom genus separated from Neidium Pfitzer. Botanical Studies, 51: 195-202.

__________________________________________________

Cattaneo, A., Couillard, Y., Wunsam, S., Fortin, C. 2011: Littoral diatoms as indicators of recent water and sediment contamination by metals in lakes. Journal of Environmental Monitoring, 13 (3): 572-582.

__________________________________________________

Cattaneo, A., Couillard, Y., Wunsan, S. 2008: Sedimentary diatoms along a temporal and spatial gradient of metal contamination. Journal of Paleolimnology, 40: 115-127.

__________________________________________________

Cattaneo, A., Asioli, A., Comoli, P., & Manca, M. 1998: Organisms' response in a chronically polluted lake supports hypothesized link between stress and size. Limnology and Oceanography, 43(8), 1938-1943

__________________________________________________

Carlise, D. M. 2000: Bioenergetic food webs as a means of linking toxicological effects across scales of ecological organisation. Journal of Aquatic Ecosystem Stress Recovery, 7: 155-165.

__________________________________________________

Chen, X., Li. C., McGowan, S., Yang, X. 2014: Diatom response to heavy metal pollution and nutrient enrichment in an urban lake: evidence from paleolimnology. Annales de Limnologie - International Journal of Limnology, 50: 121–130.

__________________________________________________

Ciszewski, D., Aleksander-Kwaterczak, U., Pociecha, A., Szarek-Gwaizda, E., Waloszek, A., Wilk-Wozniak, E., 2013: Small effects of a large sediment contamination with heavy metals on aquatic organisms in the vicinity of an abandoned lead and zinc mine. Environmental Monitoring and Assessment, 185 (12): 9825-9842.

__________________________________________________

Ciba, W. A. C., Passerini, M. D., Tundusi, J. G. 2011: Metal contaminant in benthic macroinvertebrates in sub-basin in the southeast of Brazil. Brazilan Journal of Biology., 2011, 71(2): 391-399.

__________________________________________________

Clements, W. H. 1999: Metal tolerance and predator-prey interactions in benthic macroinvertebrate stream communities. Ecological Application, 9: 1073-1084.

__________________________________________________

Clements, W. H. 1994: Benthic invertebrate community response to heavy metals in the Upper River Basin, Colorado. Journal of the North American Benthological Society, 13: 30-44.

__________________________________________________

Cvijan, M., Blaženčić, J. 1996: Cyanophyta. Naučna knjiga, Beograd. 290 p.

__________________________________________________

Dixit, S. S., Smol, J. P., Kingston, J. C., Charles, D. F. 1991: Diatoms: powerful indicators of environmental change. Environmental Science and Technology, 26: 21-33.

__________________________________________________

Falasco, E., Bona, F., Ginepro, M., Hlubikova, D., Hoffman, L., Ector, L. 2009: Morphological abnormalities of diatom silica wals in relation to heavy metal contamination and artificial growth conditions. Water SA, 35 (5): 595-606.

__________________________________________________

Guiry, M. D., Guiry, G. M. 2016: AlgaeBase. World-wide electronic publication, National University of Ireland, Glaway. http://algaebase.org; Access: 21.01.2018.

__________________________________________________

Hammer, Ø. 2017: PAST PAleontological STatistics Version 3.18. Reference manual. 259 p.

__________________________________________________

Hernandez, A. J., Pastor, J. 2008: Realtionship between plant biodiversity and heavy metal bioavailability in grasslands overlying an abondoned mine. Environemental Geochemistry and Health,30 (2): 127-133.

__________________________________________________

Hirst, H, Jüttner, I, Ormerod, S. J. 2002: Comparing the responses of diatoms and macroinvertebrates to metals in upland streams of Wales and Cornwall. Freshwater Biology 47: 1752–65.

__________________________________________________

Hofman, G., Lange-Bertalot, H., Werum, M. 2013: Diatomen im Süsswasser-Benthos von Mitteleuropa. Koeltz Scientific Book. 908 p.

__________________________________________________

Hustedt, F. 1930: Bacillariophyta (Diatomae). In: Die Üsserwasser-flora Mitteleuropas, Heft 10. Jena. 466 p.

__________________________________________________

John, D. M., Whitton, B. A., Brook, A. J. 2003: The freshwater Algae Flora of the British Isle. An Identification Guide to Freshwater and Terrestrial Algae. The Natural History Museum and the British Phycology Society, 2002, Cambridge. 714 p.

__________________________________________________

John, J. 2015: A Beginnerʹs guide to diatoms. Revised second edition. Koeltz Scientific Books. 174 p.

__________________________________________________

Kalinowska, R., Trzcińska, M., Pawlik-Skowrońska, B. 2008: Soil algae in post-mining areas contaminated with heavy metals. Wiadomości Botaniczne, 52 (3/4): 63-79.

__________________________________________________

Kamberović, J., Barudanović, S., Mašić, E., Dedić, A. 2014: Marshland vegetation of the order Phragmitetalia on shores of mine pit lakes in north-eastern Bosnia and Herzegovina. Biologica Nyssana, 5 (1): 1-10.

__________________________________________________

Kamberović, J., Barudanović, S. 2012: Algae and macrophytes of mine pit lakes in the wider area of Tuzla, Bosna and Herzegovina. Natura Croatica, 21 (1): 101-118.

__________________________________________________

Kovacik J, Klejdus B, Hedbavny J, Backor M. 2010: Effect of copper and salicylic acid on phenolic metabolites and free amino acids in Scenedesmus quadricauda (Chlorophyceae). Plant Science, 178 (3): 307–311.

__________________________________________________

Krammer, K. 1997a: Die cymbelloiden Diatomen. Eine Monographie der weltweit bekannten Arten. Teil 1. Allgemeines und Encyonema Part. Bibliotheca Diatomologica, 36. 382 p.

__________________________________________________

Krammer, K. 1997b: Die cymbelloiden Diatomen. Eine Monographie der weltweit bekannten Arten. Teil 2. Encyonema part., Encyonopsis und Cymbellopsis. Bibliotheca Diatomologica 37. 469 p.

__________________________________________________

Krammer, K. 2000: The genus Pinnularia. Diatoms of Europe. Diatoms of the European Inland Waters and Comparable Habitats. Edited by Horst Lange-Bertalot. Volume 1. A.R.G. Ganter Verlag K. G. 294 p.

__________________________________________________

Krammer, K. 2001: Cymbella. Diatoms of Europe. Diatoms of the European Inland Waters and Comparable Habitats. Edited by Horst Lange-Bertalot. Volume 3. A.R.G. Ganter Verlag K. G. 584 p.

__________________________________________________

Krammer, K. 2003: Cymbopleura, Delicata, Navicymbulla, Gomphocymbellopsis, Afrocymbella. Diatoms of Europe. Diatoms of the European Inland Waters and Comparable Habitats. Edited by Horst Lange-Bertalot. Volume 4. A.R.G. Ganter Verlag K. G. 530 p.

__________________________________________________

Krammer, K., Lange-Bertalot, H. 1986: Süsswasserflora von Mitteleuropa. Bacillariophyceae, 1. Teil: Naviculaceae. VEB Gustav Ficher Verlag, Jena. 876 p.

__________________________________________________

Krammer, K., Lange-Bertalot, H. 1988: Süsswasserflora von Mitteleuropa. Bacillariophyceae, 2. Teil: Bacillariophyceae, Epithemiaceae, Surirellaceae. VEB Gustav Ficher Verlag, Jena. 596 p.

__________________________________________________

Krammer, K., Lange-Bertalot, H. 1991: Süsswasserflora von Mitteleuropa. Bacillariophyceae, 3. Teil: Centrales, Fragilariaceae, Eunotiaceae. VEB Gustav Ficher Verlag, Jena. 576 p.

__________________________________________________

Krammer, K., Lange-Bertalot, H. 1991: Süsswasserflora von Mitteleuropa. Bacillariophyceae, 4. Teil: Achnanthaceae, Kritische Erganzungen zu Navicula (Lineolatae), und Gomphonema Gasamliteraturerzeichnis, Teil 1-4. VEB Gustav Ficher Verlag, Jena. 248 p.

__________________________________________________

Lange-Bartalot, H. 2001: Navicula sensu stricto. 10 Genera Separated from Navicula sensu lato Frustulia. Diatoms of the European Inland Waters and Comparable Habitats. Edited by Horst Lange-Bertalot. Volume 4. A.R.G. Ganter Verlag K. G. 526 p.

__________________________________________________

Lange-Bertalot, H. 1993: 85 Neue Taxa und über 100 weitere neu definierte Taxa ergänzend zur Süsswasserflora von Mitteleuropa Vol. 2/1-4. Bibliotheca Diatomologica, 27. 455 p.

__________________________________________________

Lange-Bertalot, H., Metzeltin, D. 1996: Oligotrophie-Indicatoren. 800 Taxa repräsentative fur drei diverse See-Typen. Iconographia Diatomologica, 2. 390 p.

__________________________________________________

Lange-Bertalot, H., Wojtal, A. Z. 2014: Diversity in species complexes of Placoneis clementis (Grunow) Cox and Paraplaconeis placentula (Ehrenberg) Kulikovskiy, Lange-Bertalot & Metzeltin. Nova Hedwigia. Beiheft 143: 403-420.

__________________________________________________

Lavoie, I., Lavoie, M., Fortin, C. 2012: A mine of information: benthic algal communities as

biomonitors of metal pollution leaching from abandoned tailings. Science of the Total Environment, 425: 231–241.

__________________________________________________

Levkov, Z., Williams, D. M. 2012: Checklist of diatoms (Bacillariophyta) from Lake Ohrid and Lake Prespa (Macedonia), and their watersheds. Phytotaxa, 45: 1-76.

__________________________________________________

Levkov, Z., Ector, L. 2010: A comparative study of Reimeria species (Bacillariophyceae). Nova Hedwigia, 90 (3/4): 469-489.

__________________________________________________

Levkov, Z., Mihalić, K. C., Ector, L. 2010: A taxonomical study of Rhoicosphenia Grunow (Bacillariophyceae) with a key for identification of selected taxa. Fottea, 10 (2): 145-200.

__________________________________________________

Levkov, Z., Krstić, S. 2002: Use of algae for monitoring of heavy metals in the River Vardar, Macedonia. Mediterranean Marine Science, 3 (1): 99-112.

__________________________________________________

Lukin, A., Dauvalter, V., Kashulin, N., Yakovlev, V., Sharov, A., Vandysh, O. 2003: Assessment of copper–nickel industry impact on subarctic lake ecosystem. The Science of the Total Environment, 306: 73–83.

__________________________________________________

Macfarlane, G. R., Burchett, M. D. 2001: Photosynthetic pigments and peroxidase activity as indicators of heavy metal stress in the grey mangrove, Avicennia marina (Forsk.) Vierh. Marine Pollution Bulletin, 42: 233–40.

__________________________________________________

Marques, M. J., Martinez-Conde, E., Rovira, J. V., Ordonez, S. 2001: Heavy metals pollution of aquatic ecosystems in the vicinity of a recently closed underground lead–zinc mine (Basque Country, Spain). Environmental of Geology, 40: 1125–1137.

__________________________________________________

Medley, C. N, Clements, W. H. 1998: Responses of diatom communities to heavy metals in streams: the influence of longitudinal variation. Ecological Application, 8: 631–644.

__________________________________________________

Mighanetara, K., Braungardt, C. B., Rieuwerts, J. S., Azizi, F. 2009: Contaminant fluxes from point and diffuse sources from abandoned mines in the river Tamar catchment, UK. Journal of Geochemicla Exploration, 100: 116–124.

__________________________________________________

Morin, S, Cordonier, A, Lavoie, I, Arini, A, Blanco, S, Thuy Duong T. 2012: Consistency in diatom response to metal-contaminated environments. In: Guasch H, et al, editors. Emerging and Priority Pollutants in Rivers, 19. The Handbook of Environmental Chemistry, 117–146.

__________________________________________________

Pandey, L. K., Kumar, D., Yadav, A., Rai, J., Gaur, J. P. 2014: Morphological abnormalities in periphitic diatoms as a tool for biomonitoring of heavy metal pollution in a river. Ecological Indictaors, 36: 272-279.

__________________________________________________

Pavlov, A., Jovanovska, E., Wetzel, C. E., Ector, L., Levkov, Z. 2016: Freshwater Mastogloia (Bacillariophyceae) taxa from Macedonia, with a description of the epizoic M. sterijovskii sp. nov. Diatom Research. 31 (2): 85-112.

__________________________________________________

Pavlov, A., Levkov, Z. 2013. Diversity and distribution of taxa in the genus Eunotia Ehrenberg (Bacillariophyta) in Macedonia. Phytotaxa, 86 (1): 1-117.

__________________________________________________

Pavlov, A., Levkov, Z., Williams, D. M., Edlund, M. B. 2013: Observations on Hippodonta (Bacillariophyceae) in selected ancient lakes. Phytotaxa, 90 (1): 1-53.

__________________________________________________

Pinto E., Sigaud-Kutner T. C. S., Leitao M.A.S., Okamoto O. K., Morse D., Colepicolo P. 2003: Heavy metalinduced oxidative stress in algae. Journal of Phycology, 39: 1008–1018.

__________________________________________________

Płachno, B. J., Wołowski, K., Augustynowicz, J., Łukaszek, M. 2015: Diversity of algae in a thallium and other heavy metals-polluted environment. Annales de Limnologie - International Journal of Limnology, 51: 139–146.

__________________________________________________

Reichardt, E. 1999: Zur Revision der Gattung Gomphonema. Die Arten um G. affine/G. insigne, G. angustatum/micropus, G. acuminatum sowie gomphonemoide Diatomeen aus dem Oberoligozän in Böhmen. Iconographia Diatomologica, 8: 1-203.

__________________________________________________

Schmidt, R., Kamenik, C., Lange-Bertalot, H., Klee, R. 2004: Fragilaria and Staurosira (Bacillariophyceae) from sediment surface of 40 lakes in the Austrian Alps in relation to environment variables, and their potential for paleoclimatology. Journal of. Limnology, 63 (2): 171-189.

__________________________________________________

Shanmugam V, Lo J. C, Wu C. L, Wang S.L, Lai C. C, Connolly E. L. 2011: Differential expression and regulation of iron-regulated metal transporters in Arabidopsis halleri and Arabidopsis thaliana - the role in zinc tolerance. New Phytologist, 190 (1):125–137.

__________________________________________________

Shannon, C.E., Weaver, W. 1949: The mathematical theory of communication. In Kent et Cocker, 1992: Vegetation description and analysis. A Practical Approach, CRC Press, Boca Roton.

__________________________________________________

Suchanek, T. H., Eagles-Smith, C. A., Harner, E. J. 2008: Is Clear Lake methylmercury distribution decoupled from bulk mercury loading? Ecology Application, 18, 107–127.

__________________________________________________

Taylor, J. C., Harding, W.R., Archibald, C. G. M. 2007: A Methods Manual for the Collection, Preparation and Analysis of Diatom Samples Version 1.0. 1-49.

__________________________________________________

Volland, S., Bayer, E., Baumgartner, V., Andossch, A., Lütz, C., Sima, E., Lütz-Meindl, U. 2014: Rescue of heavy metal effects on the cell physiology of the algal model system Micrasterias by divalent ions. Journal of Plant Physiology, 171 : 154-163.

__________________________________________________

Walne P. L., Kivic P.A., 1990: 15. Phylum Euglenida. In: Margulis L., Corliss J.O., Melkonian M. and Chapmann D.J. (eds.), Handbook of Protoctista, Jones and Bartlett, Boston, 270–287.

__________________________________________________

Witkowski, A., Lange-Bertalot, H., Kociolek J. P., Ruppel, M., Wawrzyniak-Wydrowska, B., Bak, M., Brezezinska, A. 2004: Four new species of Nitzschia sect. Tryblionella (Bacillariophyceae) resmbling N.parvula. Phycologia, 43 (5): 579-595.

__________________________________________________

Water quality -- Sampling -- Part 4: Guidance on sampling from lakes, natural and man made (ISO 5667-4:1987).

__________________________________________________

Wojtal, A. Z., Ector, L., Van de Vijver, B., Morales, E. A., Blanco, S., Piatek, J., Smieja, A. 2011: The Achnanthidium minutissimum complex (Bacillariophyceae) in southern Poland. Algological Studies, 136/137: 211-238.

__________________________________________________

Wojtal, A. Z. 2009: The diatoms of Kobylanka Stream near Krakow (Wyzyna Krakowsko-Czestochowska upland, S Poland). Polish Botanical Journal, 54 (2): 129-330.

__________________________________________________

Wojtal, A. Z., Kwandras, J. 2006: Diatoms of the Wyzyna Krakowsko-Czestochowska upland (S Poland) - Coscinodiscophyceae (Thalassiosirophycideae). Polish Botanica. Journal, 51 (2): 177-207.

__________________________________________________

Wojtal, A. 2003: Diatoms of the genus Gomphonema Ehr. (Bacillariophyceae) from karstic stream in the Krakowsko-Czestochowska upland. Acta Societatis Botanicorum poloniae, 72 (3): 213-220.

__________________________________________________

Wołowski , C., Saber, A. A., Cantonati, M. 2017: Euglenoids from the El-Farfara Oasis (Western Desert, Egypt). Polish Botanical Journal, 62 (2): 241–251.

__________________________________________________

Wołowski, K., Uzarowicz, Ł., Łukaszek, M., PawlikSkowron´ska, B., 2013: Diversity of algal communities in acid mine drainages of different physico-chemical properties. Nova Hedwigia, 97: 117–137.

__________________________________________________

Wołowski, K., Turnau, K., Henriques, F. S., 2008: The algal flora of an extremely acidic, metal-rich drainage pond of Sao Domingos pyrite mine (Portugal). Cryptogamie Algologie., 29: 313–324.

__________________________________________________

Younger, P. L. 1997: Longevity of mine water pollution: A basis for decision-making. The Science of the Total Environment, 194/195: 457–466.

__________________________________________________


Refbacks