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Heavy metal concentration in feathers of Little Egret (Egretta garzetta) nestlings in three coastal breeding colonies in Spain

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Abstract

The colonial ardeid Little Egret (Egretta garzetta), which is is protected under the European Birds Directive (2009/147/EC), can be a reliable bioindicator of aquatic environmental pollution. Concentrations of the heavy metals Cd, Cr, Cu, Hg, Ni, Pb and Zn in nestling feathers were assessed for three different breeding colonies of Little Egret on the Spanish coast during 2013 (5 individuals in Urdaibai, 10 in Santoña and 26 in Odiel). There were no significant differences in mean tissue residues of Cd, Ni, Pb and Zn between the colonies; however, mean concentration of Hg in Odiel nestlings was approximately three times lower than that of the other colonies, while Cr and Cu were significantly higher. In general, Little Egret nestlings from the three study sites had low levels of most of the measured metals, and thus the breeding populations did not appear to be at risk from heavy metal pollution. Baseline metal concentration in feathers derived from this study and calculated as the 90th percentile values were: 0.02 μg Cd g−1 dw, 0.42 μg Cr g−1 dw, 1.63 μg Hg g−1 dw, 0.40 μg Pb g−1 dw and 122 μg Zn g−1 dw. However, mean Cu residues attained relatively high levels (17.6–26.9 μg Cu g−1 dw) compared with data reported elsewhere, which raises concern and indicates a need for further research.

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References

  • Abdennadher A, Ramírez 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 175:677–684. doi:10.1007/s10661-010-1560-y

    Article  CAS  Google Scholar 

  • Adams WJ, Blust R, Borgmann U, Brixx KV, DeForest DK, Green AS, Meyer JS, McGeer JC, Paquin PR, Rainbow PS, Wood CM (2010) Utility of tissue residues for predicting effects of metals on aquatic organisms. Integr Environ Assess Manag 7(1):75–98

    Article  CAS  Google Scholar 

  • Ansara-Ross TM, Ross MJ, Wepener V (2013) The use of feathers in monitoring bioaccumulation of metals and metalloids in the South African endangered African grass-owl (Tyto capensis). Ecotoxicology 22:1072–1083. doi:10.1007/s10646-013-1095-4

    Article  CAS  Google Scholar 

  • Barata C, Fabregat MC, Cotín J, Huertas D, Solé M, Quirós LC, 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 158:704–710. doi:10.1016/j.envpol.2009.10.018

    Article  CAS  Google Scholar 

  • Beyer WN, Meador J (2011) Environmental contaminants in biota: interpreting tissue concentrations, 2nd edn. CRC Press, Boca Raton

    Google Scholar 

  • Boncompagni E, Muhammad A, Jabeen R, Orvini E, Gandini C, Sanpera C, Ruiz X, Fasola M (2003) Egrets as monitors of trace-metal contamination in Wetlands of Pakistan. Arch Environ Contam Toxicol 45:399–406. doi:10.1007/s00244-003-0198-y

    Article  CAS  Google Scholar 

  • Borghesi F (2009) Metal exposure assessment in Flamingo fledglings (Phoenicopterus roseus) from six colonies of the Mediterranean area by feather analysis. Dissertation, University of Bologna

  • Borghesi F, Andreotti A, Baccetti N, Bianchi N, Birke M, Migani F, Dinelli E (2011) Flamingo feathers to monitor metal contamination of coastal wetlands: methods and initial results concerning the presence of mercury at six Mediterranean sites. Chem Ecol 27(supp 2):137–151. doi:10.1080/02757540.2011.625942

    Article  Google Scholar 

  • Burger J (2013) Temporal trends (1989–2011) in levels of mercury and other heavy metals in feathers of fledgling great egrets nesting in Barnegat Bay, NJ. Environ Res 122:11–17. doi:10.1016/j.envres.2013.01.003

    Article  CAS  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 25:322–327. doi:10.1007/BF00210724

    Article  CAS  Google Scholar 

  • Burger J, Gochfeld M (1997a) Risk, mercury levels, and birds: relating adverse laboratory effects to field biomonitoring. Environ Res 75:160–172. doi:10.1006/enrs.1997.3778

    Article  CAS  Google Scholar 

  • Burger J, Gochfeld M (1997b) Heavy metal and selenium concentrations in feathers of Egrets from Bali and Sulawesi, Indonesia. Arch Environ Contam Toxicol 32:217–221. doi:10.1007/s002449900178

    Article  CAS  Google Scholar 

  • Burger J, Gochfeld M (2000) Metal levels in feathers of 12 species of seabirds from Midway Atoll in the northern Pacific Ocean. Sci Total Environ 257:37–52. doi:10.1016/S0048-9697(00)00496-4

    Article  CAS  Google Scholar 

  • Burger J, Gochfeld M (2009a) 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 152(1–4):357–367. doi:10.1007/s10661-008-0321-7

    Article  CAS  Google Scholar 

  • Burger J, Gochfeld M (2009b) Mercury and other metals in feathers of Common Eider (Somateria mollissima) and Tufted Puffin (Fratercula cirrhata) from the Aleutian Chain of Alaska. Arch Environ Contam Toxicol 56(3):596–606. doi:10.1007/s00244-008-9207-5

    Article  CAS  Google Scholar 

  • Burger J, Seyboldt S, Morganstein N, Clark K (1993) Heavy metals and selenium in feathers of three shorebird species from Delaware Bay. Environ Monit Assess 28:189–198. doi:10.1007/BF00547037

    Article  CAS  Google Scholar 

  • Chapman PM, Wang F (2000) Issues in Ecological Risk Assessment of inorganic metals and metalloids. Hum Ecol Risk Assess 6(6):1–24. doi:10.1080/10807030091124392

    Article  Google Scholar 

  • Clarke KR, Gorley R (2006) PRIMER v6: User manual/tutorial. PRIMER-E: Plymouth

  • Connell DW, Wong BS, Lam PK, Poon KF, Lam MH, Wu RS, Richardson BJ, Yen YF (2002) Risk to breeding success of ardeids by contaminants in Hong Kong: evidence from trace metals in feathers. Ecotoxicology 11(1):49–59. doi:10.1023/A:1013745113901

    Article  CAS  Google Scholar 

  • Cosson RP, Amiard J-CL, Amiard-Triquet C (1988) Trace elements in Little Egrets and Flamingos of Camargue, France. Ecotoxicol Environ Saf 15:107–116. doi:10.1016/0147-6513(88)90047-4

    Article  CAS  Google Scholar 

  • De Vega L, González-Sánchez F (2014) Censos de aves acuáticas en el Parque Natural de las Marismas de Santoña, Victoria y Joyel. Año 2014. SEO/BirdLife and Dirección General de Montes y Conservación de la Naturaleza del Gobierno de Cantabria

  • Dmowski K (1999) Birds as bioindicators of heavy metal pollution: review and examples concerning European species. Acta Ornithol 34:1–25. doi:10.3161/068.035.0209

    Google Scholar 

  • Eisler R (1986) Chromium hazards to fish, wildlife, and invertebrates: a synoptic review. US Fish and Wildlife Service. Biological Report 85 (1.6)

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

  • Eisler R (2000) Handbook of chemical risk assessment: health hazards to humans, plants, and animals, vol 1., MetalsLewis Publishers, Boca Raton

    Book  Google Scholar 

  • Eisler R (2010) Birds. In: Compendium of trace metals and marine biota. Vertebrates, vol 2. Elsevier, Amsterdam, pp 253–361

  • European Commission (2009) Directive 2009/147/EC of the European Parliament and of the Council on the conservation of wild birds. Official Journal of the European Union, L 0/7

  • Evers DC, Wiener JG, Basu N, Bodaly RA, Morrison HA, Williams KA (2011) Mercury in the Great Lakes region: bioaccumulation, spatiotemporal patterns, ecological risks, and policy. Ecotoxicology 20:1487–1499. doi:10.1007/s10646-011-0784-0

    Article  CAS  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 34:87–93. doi:10.1007/s002449900289

    Article  CAS  Google Scholar 

  • Fu J, Wang Q, Wang H, Yu H, Zhang X (2014) Monitoring of non-destructive sampling strategies to assess the exposure of avian species in Jiangsu Province, China to heavy metals. Environ Sci Pollut Res 21:2898–2906. doi:10.1007/s11356-013-2242-4

    Article  CAS  Google Scholar 

  • Galarza A, Arizaga A (2014) Population dynamics of a colony of Little Egrets (Egretta garzetta) at an estuary in Northern Spain. Ardeola 61(2):285–296. doi:10.13157/arla.61.2.2014.285

    Article  Google Scholar 

  • Garrido JR, Molina B, Del Moral JC (2012) Las garzas en España, población reproductora e invernante en 2010-2011 y método de censo. SEO/BirdLife, Madrid

    Google Scholar 

  • Goede AA, De Bruin M (1986) The use of bird feathers for indicating heavy metal pollution. Environ Monit Assess 7:249–256. doi:10.1007/BF00418017

    Article  CAS  Google Scholar 

  • Golden NH, Rattner BA, Cohen JB, Hoffman DJ, Russek-Cohen E, Ottinger MA (2003) Lead accumulation in feathers of nestling Black-Crowned Night Herons (Nycticorax nycticorax) experimentally treated in the field. Environ Toxicol Chem 22(7):1517–1524. doi:10.1002/etc.5620220713

    Article  CAS  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 32:211–216. doi:10.1007/s002449900177

    Article  CAS  Google Scholar 

  • Guillén MT, Delgado J, Albanese S, Nieto JM, Lima A, De Vivo B (2011) Environmental geochemical mapping of Huelva municipality soils (SW Spain) as a tool to determine background and baseline values. J Geochem Explor 109:59–69. doi:10.1016/j.gexplo.2011.03.003

    Article  CAS  Google Scholar 

  • Irabien MJ, Rada M, Gómez J, Soto J, Mañanes A, Viguri J (2008) An assessment of anthropogenic impact in a nature reserve: the Santoña Marshes (Northern Spain). J Iber Geol 34(2):235–242

    Google Scholar 

  • Jerez S, Motas MI, Palacios MJ, Valera F, Cuervo JJ, Barbosa A (2011) Concentration of trace elements in feathers of three Antarctic Penguins: geographical and interspecific differences. Environ Pollut 159:2412–2419. doi:10.1016/j.envpol.2011.06.036

    Article  CAS  Google Scholar 

  • Kim J, Oh JM (2014) Lead and cadmium contaminations in feathers of Heron and Egret chicks. Environ Monit Assess 186:2321–2327. doi:10.1007/s10661-013-3540-5

    Article  CAS  Google Scholar 

  • Lodenius M, Solonen T (2013) The use of feathers of birds of prey as indicators of metal pollution. Ecotoxicology 22:1319–1334. doi:10.1007/s10646-013-1128-z

    Article  CAS  Google Scholar 

  • Luque CJ, Castellanos EM, Castillo JM, González M, González Vilches MC, Figueroa ME (1997) Distribución de metales pesados en los sedimentos de las marismas del Odiel (Huelva, SO. España). Cuatern Geomorfol 12(3-4):77–85

    Google Scholar 

  • Monteiro LR, Granadeiro JP, Furness RW (1998) Relationship between mercury levels and diet in Azores seabirds. Mar Ecol Prog Ser 166:259–265

    Article  CAS  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 159:2454–2460. doi:10.1016/j.envpol.2011.06.033

    Article  CAS  Google Scholar 

  • Morillo J, Usero J, Rojas R (2008) Fractionation of metals and As in sediments from a biosphere reserve (Odiel salt marshes) affected by acidic mine drainage. Environ Monit Assess 139:329–337. doi:10.1007/s10661-007-9839-3

    Article  CAS  Google Scholar 

  • Newman MC (1995) Quantitative methods in aquatic ecotoxicology. CRC Press/Lewis Publishers, Florida

    Google Scholar 

  • Nieto JM, Sarmiento AM, Olías MR, Canovas CR, Riba I, Kalman JT, Delvalls A (2007) Acid mine drainage pollution in the Tinto and Odiel rivers (Iberian Pyrite Belt, SW Spain) and bioavailability of the transported metals to the Huelva estuary. Environ Int 33(4):445–455. doi:10.1016/j.envint.2006.11.010

    Article  Google Scholar 

  • Nota Y (2003) Effects of body size and sex on foraging territoriality of the Little Egret (Egretta garzetta) in Japan. Auk 120:781–798

    Article  Google Scholar 

  • Pietrelli L, Biondi M (2009) Notes on Little Egret breeding biology and on mercury content in egg shells and feathers. Rend Fis Acc Lincei 20:219–224. doi:10.1007/s12210-009-0050-z

    Article  Google Scholar 

  • Riba I, García-Luque E, Blasco J, DelValls TA (2003) Bioavailability of heavy metals bound to estuarine sediments as a function of pH and salinity values. Chem Speciat Bioavailab 15(4):101–114. doi:10.3184/095422903782775163

    Article  CAS  Google Scholar 

  • Riba I, DelValls TA, Forja JM, Gómez-Parra A (2004) The influence of pH and Salinity values in the toxicity of heavy metals in sediments to the estuarine clam “Ruditapes philippinarum”. Environ Toxicol Chem 23(5):1100–1107. doi:10.1897/023-601

    Article  CAS  Google Scholar 

  • Rogers K, Ralph TJ (1996) Floodplain wetland biota in the Murray-Darling Basin: water and habitat requirements. CSIRO Publishing, Collingwood

    Google Scholar 

  • Salazar RD, Riddiford NJ, Vicens P (2005) A comparative dietary study of Cattle Egrets (Bubulcus ibis) and Little Egrets (Egretta garzetta) in S’Albufera Natural Park, Mallorca. Boll Soc Hist Nat Balears 48:153–162

    Google Scholar 

  • Sanpera C, Moreno R, Ruiz X, Jover L (2007) Audouin’s Gull chicks as bioindicators of mercury pollution at different breeding locations in the western Mediterranean. Mar Pollut Bull 54(6):691–696. doi:10.1016/j.marpolbul.2007.01.016

    Article  CAS  Google Scholar 

  • Scheuhammer AM (1987) The chronic toxicity aluminium, cadmium, mercury and lead in birds: a review. Environ Pollut 46:263–295. doi:10.1016/0269-7491(87)90173-4

    Article  CAS  Google Scholar 

  • Shahbaz M, Hashmi MZ, Malik RN, Yasmin A (2013) Relationship between heavy metals concentrations in egret species, their environment and food chain differences from two headworks of Pakistan. Chemosphere 93:274–282. doi:10.1016/j.chemosphere.2013.04.078

    Article  CAS  Google Scholar 

  • Sunde ML (1972) Zn requirement for normal feathering of commercial leghorn-type pullets. Poult Sci 51:1316–1322. doi:10.3382/ps.0511316

    Article  CAS  Google Scholar 

  • Thompson DR, Hamer KC, Furness RW (1991) Mercury accumulation in Great Skuas Catharacta Skua of known age and sex, and its effects upon breeding and survival. J Appl Ecol 28:672–684. doi:10.2307/2404575

    Article  Google Scholar 

  • Tueros I, Borja A, Larreta J, Rodríguez JG, Valencia V, Millán E (2009) Integrating long-term water and sediment pollution data, in assessing chemical status within the European Water Framework Directive. Mar Pollut Bull 58:1389–1400. doi:10.1016/j.marpolbul.2009.04.014

    Article  CAS  Google Scholar 

  • Veses O, Mosteo R, Ormad MP, Ovelleiro JL (2013) Sediment quality assessment of two industrialized areas of Spain. Int J Environ Res 7(4):1039–1046

    CAS  Google Scholar 

  • Zamani-Ahmadmahmoodi R, Esmaili-Sari A, Savabieasfahani M, Bahramifar N (2010) Cattle Egret (Bubulcus ibis) and Little Egret (Egretta garzetta) as monitors of mercury contamination in Shadegan Wetlands of south-western Iran. Environ Monit Assess 166:371–377. doi:10.1007/s10661-009-1008-4

    Article  CAS  Google Scholar 

  • Zhang Y, Ruan L, Fasola M, Boncompagni E, Dong Y, Dai N, Gandini C, Orvini E, Ruiz X (2006) Little Egrets Egretta garzetta and trace-metal contamination in wetlands of China. Environ Monit Assess 118:355–368. doi:10.1007/s10661-006-1496-4

    Article  CAS  Google Scholar 

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Acknowledgments

This research has been supported by the project of the University of the Basque Country (EHU13/24) and by the Basque Government (IT-405-10). Sampling feathers in the Little Egret colonies was possible thanks to the active collaboration of Jose Manuel Sayago (Junta de Andalucía) and Ludo de Vega (SEO/Birdlife ornithologist). Thanks also to the County Council of Biscay and Paula Caviedes (Director of the Biosphere Reserve of Urdaibai), Lourdes González Azpiri (Director of the Natural Park of the Marshes of Santoña, Victoria and Joyel) and Enrique Martínez Montes (Director of the Odiel Biosphere Reserve) for providing support for sampling campaigns. To Beatriz Arce of SOSPROCAN Unit for analysing the samples. We are truly grateful to Leire Paz for her help in samples preparation. Finally, we gratefully acknowledge the anonymous reviewers who helped improving this manuscript with useful comments and suggestions.

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Correspondence to Maite Martinez-Madrid.

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Rubio, I., Martinez-Madrid, M., Méndez-Fernández, L. et al. Heavy metal concentration in feathers of Little Egret (Egretta garzetta) nestlings in three coastal breeding colonies in Spain. Ecotoxicology 25, 30–40 (2016). https://doi.org/10.1007/s10646-015-1563-0

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