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Assessment of Fish Embryo Survival and Growth by In Situ Incubation in Acidic Boreal Streams Undergoing Biomining Effluents

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Abstract

The applicability of an in situ incubation method in monitoring the effects of metal mining on early life stages of fish was evaluated by investigating the impacts of a biomining technology utilizing mine on the mortality, growth, and yolk consumption of brown trout (Salmo trutta) and whitefish (Coregonus lavaretus) embryos. Newly fertilized eggs were incubated from autumn 2014 to spring 2015 in six streams under the influence of the mine located in North-Eastern Finland and in six reference streams. Although the impacted streams clearly had elevated concentrations of several metals and sulfate, the embryonic mortality of the two species did not differ between the impacted and the reference streams. Instead, particle accumulation to some cylinders had a significant impact on the embryonic mortality of both species. In clean cylinders, mortality was higher in streams with lower minimum pH. However, low pH levels were evident in both the reference and the mine-impacted groups. The embryonic growth of neither species was impacted by the mining activities, and the growth and yolk consumption of the embryos was mainly regulated by water temperature. Surprisingly, whitefish embryos incubated in streams with lower minimum pH had larger body size. In general, the applied in situ method is applicable in boreal streams for environmental assessment and monitoring, although in our study, we did not observe a specific mining impact differing from the effects of other environmental factors related to catchment characteristics.

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References

  • Arola HE, Karjalainen J, Vehniäinen E-R, Väisänen A, Kukkonen JVK, Karjalainen AK (2017) Tolerance of whitefish (Coregonus lavaretus) early life stages to manganese sulfate is affected by the parents. Environ Toxicol Chem 36:1343–1353. https://doi.org/10.1002/etc.3667

    Article  CAS  Google Scholar 

  • Campbell PGC, Stokes PM (1985) Acidification and toxicity of metals to aquatic biota (a review). Can J Fish Aquat Sci 42:2034–2049. https://doi.org/10.1139/f85-251

    Article  CAS  Google Scholar 

  • Carrick TR (1979) The effect of acid water on the hatching of salmonid eggs. J Fish Biol 14:165–172. https://doi.org/10.1111/j.1095-8649.1979.tb03506.x

    Article  Google Scholar 

  • Directive 2008/105/EC European Union Directive 2008/105/EC of the European Parliament and of the Council on environmental quality standards in the field of water policy, amending and subsequently repealing Council Directives 82/176/EEC, 83/513/EEC, 84/156/EEC, 84/491/EEC, 86/280/EEC and amending Directive 2000/60/EC of the European Parliament and of the Council. Brussels, Belgium

  • Elphick JR, Davies M, Gilron G, Canaria EC, Lo B, Bailey HC (2011) An aquatic toxicological evaluation of sulfate: the case for considering hardness as a modifying factor in setting water quality guidelines. Environ Toxicol Chem 30:247–253. https://doi.org/10.1002/etc.363

    Article  CAS  Google Scholar 

  • Finnish Environment Institute. Catchment Areas and National Database of Regional Land Use Plans. Download Service LAPIO, Finnish Environment Institute. Data retrieved 11/2016

  • González-Doncel M, Larrea M, Sánchez-Fortún S, Hinton DE (2003) Influence of water hardening of the chorion on cadmium accumulation in medaka (Oryzias latipes) eggs. Chemosphere 52:75–83. https://doi.org/10.1016/S0045-6535(03)00227-3

    Article  CAS  Google Scholar 

  • Government Decree 1090/2016. Government Decree of amended Government Decree on substances dangerous and harmful to the aquatic environment. Government of Finland. 2016. Helsinki, Finland (in Finnish)

  • Government Decree 868/2010. Government Decree 868/2010. Government Decree on substances dangerous and harmful to the aquatic environment. Helsinki, Finland (in Finnish)

  • Gustavsson N, Loukola-Ruskeeniemi K, Tenhola M (2012) Evaluation of geochemical background levels around sulfide mines—a new statistical procedure with beanplots. Appl Geochem 27:240–249. https://doi.org/10.1016/j.apgeochem.2011.10.008

    Article  CAS  Google Scholar 

  • Haakana H, Huuskonen H (2012) The endangered whitefish (Coregonus lavaretus pallasi) population in the Koitajoki River, eastern Finland: the present state and threats. Adv Limnol 63:519–533. https://doi.org/10.1127/advlim/63/2012/519

    Article  Google Scholar 

  • Harris GS (1973) A simple egg box planting technique for estimating the survival of eggs deposited in stream gravel. J Fish Biol 5:85–88. https://doi.org/10.1111/j.1095-8649.1973.tb04432.x

    Article  Google Scholar 

  • Hogsden KL, Harding JS (2012) Consequences of acid mine drainage for the structure and function of benthic stream communities: a review. Freshw Sci 31(1):108–120. https://doi.org/10.1899/11-091.1

    Article  Google Scholar 

  • Hutchinson TH, Solbé J, Kloepper-Sams PJ (1998) Analysis of the ECETOX aquatic toxicity (EAT) database III—comparative toxicity of chemical substances to different life stages of aquatic organisms. Chemosphere 36:129–142. https://doi.org/10.1016/S0045-6535(97)10025-X

    Article  CAS  Google Scholar 

  • Jezierska B, Ługowska K, Witeska M (2009) The effects of heavy metals on embryonic development of fish (a review). Fish Physiol Biochem 35:625–640. https://doi.org/10.1007/s10695-008-9284-4

    Article  CAS  Google Scholar 

  • Kamler E (2002) Ontogeny of yolk-feeding fish: an ecological perspective. Rev Fish Biol Fish 12:79–103. https://doi.org/10.1023/A:1022603204337

    Article  Google Scholar 

  • Karjalainen J, Keskinen T, Pulkkanen M, Marjomäki TJ (2015) Climate change alters the egg development dynamics in cold-water adapted coregonids. Environ Biol Fish 98:979–991. https://doi.org/10.1007/s10641-014-0331-y

    Article  Google Scholar 

  • Kauppi S, Mannio J, Hellsten S, Nystén T, Jouttijärvi T, Huttunen M, Ekholm P, Tuominen S, Porvari P, Karjalainen A, Sara-Aho T, Saukkoriipi J, Maunula M (2013) Assessment of the potential impacts on water environment caused by the gypsum pond leakage at the Talvivaara mine. Reports of the Finnish Environment Institute 11/2013 (in Finnish, English abstract)

  • Keinänen M, Tigerstedt C, Kålax P, Vuorinen PJ (2003) Fertilization and embryonic development of whitefish (Coregonus lavaretus lavaretus) in acidic low-ionic-strength water with aluminum. Ecotox Environ Safe 55:314–329. https://doi.org/10.1016/S0147-6513(02)00128-8

    Article  CAS  Google Scholar 

  • Keinänen M, Tigerstedt C, Peuranen S, Vuorinen PJ (2004) The susceptibility of early developmental phases of an acid-tolerant and acid-sensitive fish species to acidity and aluminum. Ecotox Environ Safe 58:160–172. https://doi.org/10.1016/j.ecoenv.2004.03.005

    Article  CAS  Google Scholar 

  • Korsu K, Kiljunen M, Karjalainen J, Syrjänen J, Eloranta A (2003) Taimenen (Salmo trutta) ja harjuksen (Thymallus thymallus) mädin hautoutuminen Rautavaaran seudun happamissa joissa. Kala- ja riistahallinnon julkaisuja 64:52–78 (in Finnish)

    Google Scholar 

  • Laine A, Heikkinen K, Sutela T (2001) Incubation success of brown trout (Salmo trutta) eggs in boreal humic rivers affected by peatland drainage. Arch Hydrobiol 150:289–305

    Article  CAS  Google Scholar 

  • Loukola-Ruskeeniemi K, Uutela A, Tenhola M, Paukola T (1998) Environmental impact of metalliferous black shales at Talvivaara in Finland, with indication of lake acidification 9000 years ago. J Geochem Explor 64:395–407. https://doi.org/10.1016/S0375-6742(98)00047-8

    Article  CAS  Google Scholar 

  • Meinelt T, Playle RC, Pietrock M, Burnison BK, Wienke A, Steinberg CEW (2001) Interaction of cadmium toxicity in embryos and larvae of zebrafish (Danio rerio) with calcium and humic substances. Aquat Toxicol 54:205–215. https://doi.org/10.1016/S0166-445X(01)00145-X

    Article  CAS  Google Scholar 

  • National Land Survey of Finland. General and Topographic maps of Finland, File service of open data, National Land Survey of Finland. Data retrieved in 11/2016

  • Oraluoma M, Kivinen J, Sivonen K (2015) Mädinhaudontakoe Viitasaaren Kärnänkoskella & Kyrönpurolla 2014–2015. Kala- ja vesistötutkimus Vesi-Visio. A report (in Finnish)

  • Peterson RH (1984) Influence of varying pH and some inorganic cations on the perivitelline potential of eggs of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 41:1066–1069. https://doi.org/10.1139/f84-124

    Article  CAS  Google Scholar 

  • Peterson HG, Healey FP, Wagemann R (1984) Metal toxicity to algae: a highly pH dependent phenomenon. Can J Fish Aquat Sci 41:974–979. https://doi.org/10.1139/f84-111

    Article  CAS  Google Scholar 

  • Pyle GG, Swanson SM, Lehmkuhl DM (2002) The influence of water hardness, pH, and suspended solids on nickel toxicity to larval fathead minnows (Pimephales promelas). Water Air Soil Pollut 133:215–226. https://doi.org/10.1023/A:1012973728628

    Article  CAS  Google Scholar 

  • Rawlings DE, Silver S (1995) Mining with microbes (review). Nat Biotechnol 13:773–778. https://doi.org/10.1038/nbt0895-773

    Article  CAS  Google Scholar 

  • Rawlings DE, Dew D, du Plessis C (2003) Biomineralization of metal-containing ores and concentrates (review). Trends Biotechnol 21:38–44. https://doi.org/10.1016/S0167-7799(02)00004-5

    Article  CAS  Google Scholar 

  • Reader JP, Everall NC, Sayer MDJ, Morris R (1989) The effects of eight trace metals in acid soft water on survival, mineral uptake and skeletal calcium deposition in yolk-sac fry of brown trout, Salmo trutta L. J Fish Biol 35:187–198. https://doi.org/10.1111/j.1095-8649.1989.tb02968.x

    Article  CAS  Google Scholar 

  • Riekkola-Vanhanen M (2013) Talvivaara mining company—from a project to a mine. Miner Eng 48:2–9. https://doi.org/10.1016/j.mineng.2013.04.018

    Article  CAS  Google Scholar 

  • Salmelin J, Leppänen MT, Karjalainen AK, Vuori K-M, Gerhardt A, Hämäläinen H (2017) Assessing ecotoxicity of biomining effluents in stream ecosystems by in situ invertebrate bioassays: a case study in Talvivaara, Finland. Environ Toxicol Chem 36:147–155. https://doi.org/10.1002/etc.3511

    Article  CAS  Google Scholar 

  • Sayer MDJ, Reader JP, Morris R (1991) Embryonic and larval development of brown trout, Salmo trutta L.: exposure to aluminum, copper, lead or zinc in soft, acid water. J Fish Biol 38:431–455. https://doi.org/10.1111/j.1095-8649.1991.tb03132.x

    Article  CAS  Google Scholar 

  • Sivil M (2015) Kokonaisselvitys Kuortaneenjärven alapuolisen Lapuanjoen ekologisen tilan parantamismahdollisuuksista – hankeselvitysten tulokset ja suositukset vesienhoidolle. Etelä-Pohjanmaan elinkeino-, liikenne- ja ympäristökeskus. A report (in Finnish)

  • Sivonen O, Oraluoma M (2014) Mädinhaudontakoe Petäjäveden Pengerjoella ja Ohrajoella 2013–2014. Kala- ja vesistötutkimus Vesi-Visio. A report (in Finnish)

  • Sivonen K, Syrjänen J, Kivinen J, Sivonen O (2017) Taimenen mädin ja poikasten säilyvyys sekä kasvu haudontakokeessa Äänekosken Kapeenkosken ja Laukaan Kuusaankosken vesistöissä talvella 2016–2017. Kala- ja vesistötutkimus Vesi-Visio. a report (in Finnish)

  • Stasiūnaitė P (2005) Toxicity of copper to embryonic development of rainbow trout (Oncorhynchus mykiss). Acta Zool Litu 15(3):259–265. https://doi.org/10.1080/13921657.2005.10512620

    Article  Google Scholar 

  • Stubblefield WA, Brinkman SF, Davies PH, Garrison TD, Hockett JR, McIntyre MW (1997) Effects of water hardness on the toxicity of manganese to developing brown trout (Salmo trutta). Environ Toxicol Chem 16:2082–2089. https://doi.org/10.1002/etc.5620161014

    Article  CAS  Google Scholar 

  • Syrjänen J (2016) Taimenen mädin säilyvyys haudontakokeessa Jyväskylän Tourujoen vesistössä talvella 2015–2016. Konneveden kalatutkimus ry:n työraportteja 2(2016):1–14 (in Finnish)

    Google Scholar 

  • Syrjänen J, Valkeajärvi P (2010) Gillnet fishing drives lake-migrating brown trout to near extinction in the Lake Päijänne region, Finland. Fish Manag Ecol 17:199–208. https://doi.org/10.1111/j.1365-2400.2010.00738.x

    Article  Google Scholar 

  • Syrjänen J, Kiljunen M, Karjalainen J, Eloranta A, Muotka T (2008) Survival and growth of brown trout Salmo trutta L. embryos and the timing of hatching and emergence in two boreal lake outlet streams. J Fish Biol 72:985–1000. https://doi.org/10.1111/j.1095-8649.2007.01779.x

    Article  Google Scholar 

  • Syrjänen JT, Sivonen K, Sivonen O (2014) Redd counting in monitoring salmonids in Finnish inland waters. In: Carline RF, LoSapio C (eds) Wild Trout XI: looking back and moving forward. Wild trout symposium, West Yellowstone. Bozeman, Montana, pp 288–294

  • Syrjänen JT, Norrgård J, Sivonen K, Sivonen O (2018) Survival of brown trout eggs in the River Rottnan in winters 2015–2017 (manuscript)

  • Talvivaara (2015a) Talvivaara Mine Monitoring report 2014. Part V: Surface water monitoring. Ramboll Oy, Finland (in Finnish)

  • Talvivaara (2015b) Talvivaara Mine Monitoring report 2014. Part III: effluent discharge monitoring. Ramboll Oy, Finland (in Finnish)

  • Tenhola M, Tarvainen T (2008) Element concentrations in stream water and organic stream sediment in Finland in 1990, 1995, 2000, and 2006. Geological Survey of Finland, Report of Investigation 172 (in Finnish, English abstract)

  • Terrafame Oy (2016a) Terrafame Mine Monitoring report 2015. Part V: surface water monitoring. Ramboll Oy, Finland (in Finnish)

  • Terrafame Oy (2016b) Terrafame Mine Monitoring report 2015. Part I: summary. Ramboll Oy, Finland (in Finnish)

  • Terrafame Oy (2016c) Terrafame Mine Monitoring report 2015. Part III: effluent discharge monitoring. Ramboll Oy, Finland (in Finnish)

  • Terrafame Oy (2016d) Terrafame Mine Monitoring report 2015. Part VII: fisheries monitoring. Ramboll Oy, Finland (in Finnish)

  • US-EPA (2001) US-EPA METHOD 200.7, Revision 4.4, Cincinnati

  • Vuorinen PJ (1984) Rautaruukki OY:n Rautuvaaran kaivoksen jätevesien vaikutuksesta taimenen alkionkehitykseen ja poikasiin. Rep Finn Game Fish Res Inst 24:193–206 (in Finnish)

    Google Scholar 

  • Wang W (1987) Factors affecting metal toxicity to (and accumulation by) aquatic organisms—overview (a review). Environ Int 13:437–457. https://doi.org/10.1016/0160-4120(87)90006-7

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by Academy of Finland (Project No. 281800), the Finnish Doctoral Programme on Environmental Science and Technology (EnSTe), Emil Aaltonen Foundation and Olvi Foundation. The authors thank the local fishery associations, Metsähallitus and Talvivaara Sotkamo Mine, for the permits to conduct this research and the Natural Resources Institute Finland at Paltamo and Enonkoski for delivery of fertilized eggs of brown trout and whitefish. They thank N. Foore, O. Hewitt, O. Nousiainen and A. Eloranta for their contribution to the field work and the technicians and laboratory staff at the Department of Biological and Environmental Science for their contribution to the field work preparations and laboratory work. They also thank I. Rintala and A. Lensu for the map constructions.

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Correspondence to Hanna E. Arola.

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Arola, H.E., Karjalainen, A.K., Syrjänen, J.T. et al. Assessment of Fish Embryo Survival and Growth by In Situ Incubation in Acidic Boreal Streams Undergoing Biomining Effluents. Arch Environ Contam Toxicol 76, 51–65 (2019). https://doi.org/10.1007/s00244-018-0558-2

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