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Are the toxic sediments deposited at Flix reservoir affecting the Ebro river biota? Purple heron eggs and nestlings as indicators

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Abstract

The Flix reservoir, in the low course of the Ebro River, contains thousands of tons of polluted sediments, accumulated from the activities of a chemical factory. An ongoing project is working toward removing these pollutants. Piscivore birds like the purple heron (Ardea purpurea) may be useful bioindicators, so eggs and nestling feathers were sampled during the 2006–2008 breeding seasons at three localities: a reference site situated upstream and two potentially affected by the toxic muds; one at the focal area and one at a distal area, the Ebro Delta. The samples were analyzed for isotopic signatures of 15N and 13C and concentrations of heavy metals and selenium. Baseline nitrogen signatures were higher in riverine sites than in the delta. Nitrogen together with carbon signatures adequately discriminated riverine and deltaic ecosystems. Mercury levels are highly influenced by the polluted sediments at Flix and pose potential risks for the birds, as they are among the highest ever recorded in heron species. Selenium and copper concentrations probably derive from other sources. Except for mercury, heavy metals and selenium levels were below toxic levels. Purple heron eggs and nestling feathers have demonstrated their usefulness as bioindicators for pollution in the river biota; feathers in particular show pollutant impacts on a strict local basis. A long series of study years is necessary in dynamic ecosystems such as this, so continued monitoring of the heron population at Flix is advisable to trace the effects of the toxic muds, particularly during their removal, because of the high levels of mercury detected.

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References

  • Abdennadher A, Ramirez F, Romdhane MS, Ruiz X, Jover L, Sanpera C (2011) Little egret (Egretta garzetta) as a bioindicator of trace element pollution in Tunisian aquatic ecosystems. Environ Monit Assess 1–4:677–684

    Article  Google Scholar 

  • Attia YA, Abdalah AA, Zeweil HS, Bovera F, El-Din AAT, Araft MA (2011) Effect of inorganic or organic copper additions on reproductive performance, lipid metabolism and morphology of organs of dual-purpose breeding hens. Arch Geflugelkd 3:169–178

    Google Scholar 

  • Baker SD, Sepulveda MS (2009) An evaluation of the effects of persistent environmental contaminants on the reproductive success of great blue herons (Ardea herodias) in Indiana. Ecotoxicology 3:271–280

    Article  Google Scholar 

  • Baos R, Jovani R, Pastor N, Tella J, Jimenez B, Gomez G (2006) Evaluation of genotoxic effects of heavy metals and arsenic in wild nestling white storks (Ciconia ciconia) and black kites (Milvus migrans) from southwestern Spain after a mining accident. Environ Toxicol Chem 10:2794–2803

    Article  Google Scholar 

  • Barata C, Fabregat MC, Cotin J, Huertas D, Sole M, Quiros L, Sanpera C, Jover L, Ruiz X, Grimalt JO, Piña B (2010) Blood biomarkers and contaminant levels in feathers and eggs to assess environmental hazards in heron nestlings from impacted sites in Ebro basin (NE Spain). Environ Pollut 3:704–710

    Article  Google Scholar 

  • Benejam L, Benito J, Garcia-Berthou E (2010) Decreases in condition and fecundity of freshwater fishes in a highly polluted reservoir. Water Air Soil Pollut 1–4:231–242

    Article  Google Scholar 

  • Benito V, Devesa V, Munoz O, Suner M, Montoro R, Baos R, Hiraldob F, Ferrer M, Fernandez M, Gonzalez MJ (1999) Trace elements in blood collected from birds feeding in the area around Donana National Park affected by the toxic spill from the Aznalcollar mine. Sci Total Environ 1–3:309–323

    Google Scholar 

  • Boncompagni E, Muhammad A, Jabeen R, Orvini E, Gandini C, Sanpera C, Ruix X, Fasola M (2003) Egrets as monitors of trace-metal contamination in wetlands of Pakistan. Arch Environ Contam Toxicol 3:399–406

    Google Scholar 

  • Bosch C, Olivares A, Faria M, Navas JM, del Olmo I, Grimalt JO, Pina B, Barata C (2009) Identification of water soluble and particle bound compounds causing sublethal toxic effects. A field study on sediments affected by a chlor-alkali industry. Aquat Toxicol 1:16–27

    Article  Google Scholar 

  • Burger J, Gochfeld M (1993) Heavy-metal and selenium levels in feathers of young egrets and herons from Hong-Kong and Szechuan, China. Arch Environ Contam Toxicol 3:322–327

    Article  Google Scholar 

  • Burger J, Gochfeld M (2000) Effects of lead on birds (Laridae): a review of laboratory and field studies. J Toxicol Environ Health 2:59–78

    Google Scholar 

  • Burger J, Gochfeld M (2009) Comparison of arsenic, cadmium, chromium, lead, manganese, mercury and selenium in feathers in bald eagle (Haliaeetus leucocephalus), and comparison with common eider (Somateria mollissima), glaucous-winged gull (Larus glaucescens), pigeon guillemot (Cepphus columba), and tufted puffin (Fratercula cirrhata) from the Aleutian Chain of Alaska. Environ Monit Assess 1–4:357–367

    Article  Google Scholar 

  • Burger J, Nisbet ICT, Gochfeld M (1992) Metal levels in regrown feathers—assessment of contamination on the wintering and breeding grounds in the same individuals. J Toxicol Environ Health 3:363–374

    Google Scholar 

  • Burger J, Gochfeld M, Jeitner C, Burke S, Volz CD, Snigaroff R, Snigaroff D, Shukla T, Shukla S (2009) Mercury and other metals in eggs and feathers of glaucous-winged gulls (Larus glaucescens) in the Aleutians. Environ Monit Assess 1–4:179–194

    Article  Google Scholar 

  • Cabana G, Rasmussen J (1994) Modeling food-chain structure and contaminant bioaccumulation using stable nitrogen isotopes. Nature 6503:255–257

    Article  Google Scholar 

  • Carrasco L, Diez S, Soto D, Catalan J, Bayona J (2008) Assessment of mercury and methylmercury pollution with zebra mussel (Dreissena polymorpha) in the Ebro River (NE Spain) impacted by industrial hazardous dumps. Sci Total Environ 1:178–184

    Google Scholar 

  • Carrasco L, Benejam L, Benito J, Bayona JM, Diez S (2011) Methylmercury levels and bioaccumulation in the aquatic food web of a highly mercury-contaminated reservoir. Environ Int 7:1213–1218

    Article  Google Scholar 

  • Champoux L, Rodrigue J, Trudeau S, Boily MH, Spear PA, Hontela A (2006) Contamination and biomarkers in the great blue heron, an indicator of the state of the St. Lawrence River. Ecotoxicology 1:83–96

    Article  Google Scholar 

  • Cherel Y, Le Corre M, Jaquemet S, Menard F, Richard P, Weimerskirch H (2008) Resource partitioning within a tropical seabird community: new information from stable isotopes. Mar Ecol Prog Ser 366:281–291

    Article  CAS  Google Scholar 

  • Connell D, Wong B, Lam P, Poon K, Lam M, Wu R (2002) Risk to breeding success of Ardeids by contaminants in Hong Kong: evidence from trace metals in feathers. Ecotoxicology 1:49–59

    Article  Google Scholar 

  • Connell D, Fung C, Minh T, Tanabe S, Lam P, Wong B (2003) Risk to breeding success of fish-eating Ardeids due to persistent organic contaminants in Hong Kong: evidence from organochlorine compounds in eggs. Water Res 2:459–467

    Article  Google Scholar 

  • Cotin J, García-Tarrasón M, Sanpera C, Jover L, Ruiz X (2011) Sea, freshwater or saltpans? Foraging ecology of terns to assess mercury inputs in a wetland landscape: the Ebro Delta. Estuar Coast Shelf Sci 1:188–194

    Article  Google Scholar 

  • De Luca-Abbott S, Wong B, Peakall D, Lam P, Young L, Lam M (2001) Review of effects of water pollution on the breeding success of waterbirds, with particular reference to Ardeids in Hong Kong. Ecotoxicology 6:327–349

    Article  Google Scholar 

  • DesGranges J, Rodrigue J, Champoux L (2009) Geographic distribution of selected contaminants in great blue herons from the St. Lawrence River system, Quebec (1989–1994). Can Wildl Serv Occas Paper 116:1–18

    Google Scholar 

  • Eisler R (1987) Mercury hazards to fish, wildlife, and invertebrates: a synoptic review. U.S. Fish and Wildlife Service Biological Report 85(1.10)

  • Faria M, Huertas D, Soto D, Grimalt J, Catalan J, Riva M (2010) Contaminant accumulation and multi-biomarker responses in field collected zebra mussels (Dreissena polymorpha) and crayfish (Procambarus clarkii), to evaluate toxicological effects of industrial hazardous dumps in the Ebro river (NE Spain). Chemosphere 3:232–240

    Article  Google Scholar 

  • Fasola M, Movalli PA, Gandini C (1998) Heavy metal, organochlorine pesticide, and PCB residues in eggs and feathers of herons breeding in northern Italy. Arch Environ Contam Toxicol 1:87–93

    Article  Google Scholar 

  • Fernandez M, Alonso C, Gonzalez M, Hernandez L (1999) Occurrence of organochlorine insecticides, PCBs and PCB congeners in waters and sediments of the Ebro River (Spain). Chemosphere 1:33–43

    Article  Google Scholar 

  • Focardi S, Fossi C, Lambertini M, Leonzio C, Massi A (1988) Long-term monitoring of pollutants in eggs of yellow-legged herring gull from Capraia Island (Tuscan Archipelago). Environ Monit Assess 1:43–50

    Article  Google Scholar 

  • Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1:497–509

    Google Scholar 

  • Forero MG, Hobson KA (2003) Using stable isotopes of nitrogen and carbon to study seabird ecology: applications in the Mediterranean seabird community. Scientia Marina 67:23–32

    Article  Google Scholar 

  • Forero MG, Gonzalez-Solis J, Hobson KA, Doncazar JA, Bertellotti M, Blanco G, Bortolotti GR (2005) Stable isotopes reveal trophic segregation by sex and age in the southern giant petrel in two different food webs. Mar Ecol Prog Ser 296:107–113

    Article  Google Scholar 

  • Frederick PC, Hylton B, Heath JA, Spalding MG (2004) A historical record of mercury contamination in southern Florida (USA) as inferred from avian feather tissue. Environ Toxicol Chem 6:1474–1478

    Article  Google Scholar 

  • Golden NH, Rattner BA, McGowan PC, Parsons KC, Ottinger MA (2003) Concentrations of metals in feathers and blood of nestling black-crowned night-herons (Nycticorax nycticorax) in Chesapeake and Delaware Bays. Bull Environ Contam Toxicol 2:385–393

    Article  Google Scholar 

  • Gomez G, Baos R, Gomara B, Jimenez B, Benito V, Montoro R (2004) Influence of a mine tailing accident near Donana National Park (Spain) on heavy metals and arsenic accumulation in 14 species of waterfowl (1998 to 2000). Arch Environ Contam Toxicol 4:521–529

    Article  Google Scholar 

  • Goutner V, Furness RW (1997) Mercury in feathers of little egret Egretta garzetta and night heron Nycticorax nycticorax chicks and in their prey in the Axios Delta, Greece. Arch Environ Contam Toxicol 2:211–216

    Article  Google Scholar 

  • Heinz GH, Hoffman DJ, Klimstra JD, Stebbins KR, Kondrad SL, Erwin CA (2009) Species differences in the sensitivity of avian embryos to methylmercury. Arch Environ Contam Toxicol 1:129–138

    Article  Google Scholar 

  • Henny CJ, Hill EF, Grove RA, Kaiser JL (2007) Mercury and drought along the lower Carson River, Nevada: I. Snowy egret and black-crowned night-heron annual exposure to mercury, 1997–2006. Arch Environ Contam Toxicol 2:269–280

    Article  Google Scholar 

  • Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 3:314–326

    Article  Google Scholar 

  • Hobson KA, Piatt JF, Pitocchelli J (1994) Using stable isotopes to determine seabird trophic relationships. J Anim Ecol 4:786–798

    Article  Google Scholar 

  • Hobson KA, Sirois J, Gloutney ML (2000) Tracing nutrient allocation to reproduction with stable isotopes: a preliminary investigation using colonial waterbirds of Great Slave Lake. Auk 3:760–774

    Article  Google Scholar 

  • Hughes K, Ewins P, Clark K (1997) A comparison of mercury levels in feathers and eggs of osprey (Pandion haliaetus) in the North American Great Lakes. Arch Environ Contam Toxicol 4:441–452

    Article  Google Scholar 

  • Janz D, DeForest D, Brooks M, Chapman P, Gilron G, Hoff D, Hopkins W, McIntyre D, Mebane C, Palace V, Skorupa J, Wayland M (2010) Selenium toxicity to aquatic organisms. In: Chapman PM, Adams WJ, Brooks ML, Delos CG, Luoma SN, Maher WA, Ohlendorf HM, Presser TS, Shaw DP (eds) Ecological assessment of selenium in the aquatic environment. SETAC, Pensacola, pp 141–231

    Chapter  Google Scholar 

  • Koiadinovic J, Menard F, Bustamante P, Cosscon RP, Le Corre M (2008) Trophic ecology of marine birds and pelagic fishes from Reunion Island as determined by stable isotope analysis. Mar Ecol Prog Ser 361:239–251

    Article  Google Scholar 

  • Llorente G, Farran A, Ruiz X, Albaiges J (1987) Accumulation and distribution of hydrocarbons, polychlorobyphenyls, and DDT in tissues of 3 species of Anatidae from the Ebro Delta (Spain). Arch Environ Contam Toxicol 5:563–572

    Article  Google Scholar 

  • Mañosa S, Mateo R, Guitart R (2001) A review of the effects of agricultural and industrial contamination on the Ebro delta biota and wildlife. Environ Monit Assess 2:187–205

    Article  Google Scholar 

  • Michener RH, Schell DM (1994) Stable isotope ratios as tracers in marine aquatic food webs. In: Lajtha K, Michener RH (eds) Stable isotopes in ecology and environmental science. Blackwell Scientific Publications, London, pp 138–157

    Google Scholar 

  • Moreno R, Jover L, Munilla I, Velando A, Sanpera C (2010) A three-isotope approach to disentangling the diet of a generalist consumer: the yellow-legged gull in northwest Spain. Mar Biol 3:545–553

    Article  Google Scholar 

  • Moreno R, Jover L, Diez C, Sanpera C (2011) Seabird feathers as monitors of the levels and persistence of heavy metal pollution after the Prestige oil spill. Environ Pollut 10:2454–2460

    Article  Google Scholar 

  • Navarro A, Quiros L, Casado M, Faria M, Carrasco L, Benejam L (2009) Physiological responses to mercury in feral carp populations inhabiting the low Ebro River (NE Spain), a historically contaminated site. Aquat Toxicol 2–3:150–157

    Article  Google Scholar 

  • Navarro A, Tauler R, Lacorte S, Barcelo D (2010) Occurrence and transport of pesticides and alkylphenols in water samples along the Ebro River Basin. J Hydrol 1–2:18–29

    Article  Google Scholar 

  • Nisbet ICT, Montoya JP, Burger J, Hatch JJ (2002) Use of stable isotopes to investigate individual differences in diets and mercury exposures among common terns Sterna hirundo in breeding and wintering grounds. Mar Ecol Prog Ser 242:267–274

    Article  CAS  Google Scholar 

  • Ohlendorf HM, Heinz GH (2011) Selenium in birds. In: Beyer WN, Meador JP (eds) Environmental contaminants in biota: interpreting tissue concentrations, 2nd edn. CRC Press/Taylor and Francis Group, Boca Raton, pp 669–701

    Chapter  Google Scholar 

  • Ohlendorf HM, Covington SM, Byron ER, Arenal CA (2011) Conducting site-specific assessments of selenium bioaccumulation in aquatic systems. Integr Environ Assess Manag 7(3):314–324

    Article  CAS  Google Scholar 

  • Padula V, Burger J, Newman S, Elbin S, Jeitner C (2010) Metals in feathers of black-crowned night-heron (Nycticorax nycticorax) chicks from the New York Harbor Estuary. Arch Environ Contam Toxicol 1:157–165

    Article  Google Scholar 

  • Pastor D, Sanpera C, Gonzalez-Solis J, Ruiz X, Albaiges J (2004) Factors affecting the organochlorine pollutant load in biota of a rice field ecosystem (Ebro Delta, NE Spain). Chemosphere 4:567–576

    Article  Google Scholar 

  • Quiros L, Ruiz X, Sanpera C, Jover L, Pina B (2008) Analysis of micronucleated erythrocytes in heron nestlings from reference and impacted sites in the Ebro basin (NE Spain). Environ Pollut 1:81–87

    Article  Google Scholar 

  • Ramirez F, Abdennadher A, Sanpera C, Jover L, Hobson KA, Wassenaar LI (2011) Tracing waterbird exposure to total mercury and selenium: a case study at the solar saltworks of Thyna (Sfax, Tunisia). Environ Sci Technol 12:5118–5124

    Article  Google Scholar 

  • Ramos L, Fernandez M, Gonzalez M, Hernandez L (1999) Heavy metal pollution in water, sediments, and earthworms from the Ebro River, Spain. Bull Environ Contam Toxicol 3:305–311

    Article  Google Scholar 

  • Ruiz X, Jover L, Pedrocchi V (1998) Audouin’s gull intraspecific variability in yolk and albumen egg contents: why is yolk size so constant? Biologia e Conservazione della Fauna 102:327–334

    Google Scholar 

  • Sakellarides T, Konstantinou I, Hela D, Lambropoulou D, Dimou A, Albanis T (2006) Accumulation profiles of persistent organochlorines in liver and fat tissues of various waterbird species from Greece. Chemosphere 8:1392–1409

    Article  Google Scholar 

  • Sanpera C, Ruiz X, Moreno R, Jover L, Waldron S (2007) Mercury and stable isotopes in feathers of Audouin’s gulls as indicators of feeding habits and migratory connectivity. Condor 2:268–275

    Article  Google Scholar 

  • Sanpera C, Valladares S, Moreno R, Ruiz X, Jover L (2008) Assessing the effects of the Prestige oil spill on the European shag (Phalacrocorax aristotelis): trace elements and stable isotopes. Sci Total Environ 1:242–249

    Google Scholar 

  • Sell JL (1977) Comparative effects of selenium on metabolism of methylmercury by chickens and quail—tissue distribution and transfer into eggs. Poult Sci 3:939–948

    Article  Google Scholar 

  • Suarez-Serrano A, Alcaraz C, Ibanez C, Trobajo R, Barata C (2010) Procambarus clarkii as a bioindicator of heavy metal pollution sources in the lower Ebro River and Delta. Ecotoxicol Environ Saf 3:280–286

    Article  Google Scholar 

  • Taggart M, Figuerola J, Green A, Mateo R, Deacon C, Osborn D (2006) After the Aznalcollar mine spill: arsenic, zinc, selenium, lead and copper levels in the livers and bones of five waterfowl species. Environ Res 3:349–361

    Article  Google Scholar 

  • Tavares PC, Kelly A, Lopes RJ, Pereira ME, Duarte AC, Furness RW (2007) The influence of dietary specialization and trophic status on mercury levels in two species using common coastal wetlands, Himantopus himantopus and Sterna albifrons. Ardeola 2:275–288

    Google Scholar 

  • Vericat D, Batalla RJ (2006) Sediment transport in a large impounded river: the lower Ebro, NE Iberian Peninsula. Geomorphology 1–2:72–92

    Article  Google Scholar 

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Acknowledgments

We dedicate this work to the memory of Xavier Ruiz, who passed away on 27th April 2008. The authors wish to acknowledge the kindly cooperation of the personnel at the Reserva Natural de Sebes (Flix), Parc Natural del Delta de l’Ebre and Estació Biològica de l’Aiguabarreig for the facilities during fieldwork. Thanks are given to Sergi Ferrer and the staff at the Serveis Científicotècnics (UB, Spain) for their help during the sample collection and laboratory analysis and to Gretchen Wagner for her suggestions and corrections of the English draft. Javier Cotín was supported by a BRD grant from the Universitat de Barcelona (Spain). This work was funded by the project ‘Metalls pesants i organoclorats en el curs inferior i delta del riu Ebre: La ornitofauna com a bioindicadora.’ (Ministry of the Environment, Spain, the Catalan Water Agency, Department of the Environment and Housing, Catalan Government) and by Spanish MEyC grant project CGL2008-05448-C02-01/02/BOS.

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  1. Department Biologia Animal, Facultat de Biologia, Univesitat de Barcelona, Diagonal 645, 08028, Barcelona, Spain

    Javier Cotín, Manuel García-Tarrasón & Carolina Sanpera

  2. Department Salut Pública, Facultat de Medicina, Universitat de Barcelona, Casanova 143, 08036, Barcelona, Spain

    Lluis Jover

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  1. Javier Cotín
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  2. Manuel García-Tarrasón
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  4. Carolina Sanpera
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Correspondence to Javier Cotín.

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Cotín, J., García-Tarrasón, M., Jover, L. et al. Are the toxic sediments deposited at Flix reservoir affecting the Ebro river biota? Purple heron eggs and nestlings as indicators. Ecotoxicology 21, 1391–1402 (2012). https://doi.org/10.1007/s10646-012-0893-4

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