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PCB Levels and Accumulation Patterns in Waterbird Eggs and in Their Prey at Lake Kerkini, a North-Eastern Mediterranean Wetland of International Importance

  • V. Antoniadou
  • I. K. Konstantinou
  • V. GoutnerEmail author
  • T. M. Sakellarides
  • T. A. Albanis
  • E. Bintoudi
Article

Abstract

Seven “target” PCB levels were determined and compared in waterbird eggs, in their prey, and in water at Lake Kerkini, northern Greece, to investigate PCB bioaccumulation patterns and to define the best bioindicator of target PCBs for this area. PCBs were analysed from eggs of Phalacrocorax carbo, Podiceps cristatus, Ardea cinerea, Egretta garzetta, and Nycticorax nycticorax and from prey types Alburnus alburnus, Rutilus rutilus, Lepomis gibbosus. Carassius auratus, and Rana sp. PCBs analysed were detected in all bird eggs, prey, and water but contamination patterns differed among these sample types. The lipid-corrected geometric means of the congeners analysed were significantly different among most bird species and among some prey species. PCB congeners 118, 138, 153, and 180 accounted for around 80% of the total PCB contamination in bird egg samples. Percent congener concentrations of high-chlorinated PCBs tended to increase from water through prey to most bird egg samples whereas the low chlorinated PCBs (28 and 52) decreased. Bioaccumulation factors (BAFs) also exhibited an increasing trend for higher chlorinated PCBs from prey types to bird eggs. The greatest BAFs of six of the congeners were shared between Phalacrocorax carbo and Ardea cinerea. Among prey, the BAFs of four PCBs were highest in Lepomis gibbosus. Biomagnification factors varied between 1.01 and 39.57. In contrast to low chlorinated PCBs, high chlorinated congeners biomagnified considerably through fish prey. The highest biomagnification took place in Phalacrocorax carbo. No relationship was found between the lipid content of samples and BAFs of PCBs probably due to biotransformation differences of the congeners in the biota sampled.

Due to the greatest PCB concentrations especially of the higher chlorinated PCBs in the eggs of Phalacrocorax carbo and its considerable bioaccumulation tendencies, it is proposed as the best PCB biomonitor of target PCBs at Lake Kerkini. Lepomis gibbosus had the highest concentrations of most congeners and exhibited the greatest bioaccumulative properties among prey and can be used as an alternative biomonitor.

Keywords

PCBs Biomagnification Bioaccumulation Factor Waterbird Species Grey Heron 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We are grateful to the Kerkini Information Center for hospitality and especially to Dr. T. Nazirides and Mr. P. Hatziyiannidis for aid in sample collection. Special thanks to K. Frigis for aid in the field and laboratory. Prof. A. Sinis and Dr. D. Bobori provided us with water sampling equipment. Thanks to the Ministry of Agricultural Development and Foods for the license for collecting the biological material analysed.

References

  1. Albaigés J (2005) Persistent organic pollutants in the Mediterranean Sea. In: The Mediterranean Sea. The handbook of environmental chemistry, Vol 5, part K, Springer, Heidelberg, Germany, pp 899–149Google Scholar
  2. Albanis TA, Hela DG, Sakellarides TM, Konstantinou IK (1998) Monitoring of pesticides residues and their metabolites in surface and underground waters from Imathia (N. Greece) by means of solid phase extraction disks and gas chromatography. J Chromatogr A 823:59–71CrossRefGoogle Scholar
  3. Albanis T, Goutner V, Konstantinou I, Frigis K (2003) Organochlorine contaminants in eggs of the yellow-legged gull (Larus cachinnans michaellis) in the northeastern Mediterranean: is this gull a suitable biomonitor for the region? Environ Pollut 126:245–255CrossRefGoogle Scholar
  4. Bachour G, Failing K, Georgii S, Elmadfa I, Brumi H (1998) Species and organ dependence of PCB contamination in fish, foxes, roe deed and humans. Arch Environ Contam Toxicol 35:666–673CrossRefGoogle Scholar
  5. Barren MG, Galbraith H, Beltman D (1995) Comparative reproductive and developmental toxicology of PCBs in birds. Comp Biochem Physiol 112C:1–14Google Scholar
  6. Bentzen E, Lean DRS, Taylor WD, Mackay D (1996) Role of food web structure on lipid and bioaccumulation on organic contaminants by lake trout (Salvelinus namaycush). Can J Fish Aquat Sci 53:2397–2407CrossRefGoogle Scholar
  7. Berglund O, Larsson P, Ewald G, Okla L (2000) Bioaccumulation and differential partitioning of polychlorinated biphenyls in freshwater planktonic food webs. Can J Fish Aquat Sci 57:1160–l168CrossRefGoogle Scholar
  8. Birtsas PK (2002) Ecology and conservation of the black-crowned night heron (Nycticorax nycticorax (L., 1758)) at the Kerkini reservoir, Macedonia, Greece. Doctoral Dissertation, Department of Forestry and Natural Environment, Aristotle University of Thessaloniki, p 151Google Scholar
  9. Blanchard M, Teil MJ, Carru AM, Chesterikoff A, Chevreuil M (1997) Organochlorine distribution and mono-orthosubstituted PCB pattern in the roach (Rutilus rutilus) from the river Seine. Wat Res 31:1455–1461CrossRefGoogle Scholar
  10. Bordajandi LR, Gómez G, Fernández MA, Abad E, Rivera J, González MJ (2003) Study on PCBs PCDD/Fs, organochlorine pesticides, heavy metals and arsenic content in freshwater fish species from the river Turia (Spain). Chemosphere 53:163–171CrossRefGoogle Scholar
  11. Borga K, Gabrielsen GW, Skaare JU (2001) Biomagnification of organochlorines along a Barents Sea food chain. Environ Poll 113:187–198CrossRefGoogle Scholar
  12. Borga K, Fisk AT, Hargrave B, Hoekstra PF, Swackhamer D, Muir DC (2005) Bioaccumulation factors of PCBs revisited. Environ Sci Teclinol 39:4523–4532CrossRefGoogle Scholar
  13. Boumphrey RS, Harrad SJ, Jones KC, Osborn D (1993) Polychlorinated biphenyl congener patterns in tissues from a selection of British birds. Arch Environ Contam Toxicol 25:346–352CrossRefGoogle Scholar
  14. Braune BM, Norstrom RJ (1989) Dynamics of organochlorine compounds in Herring Gulls: III. Tissue distribution and bioaccumulation in Lake Ontario gulls. Environ Toxicol Chem 8:957–968Google Scholar
  15. Burreau S, Zebuhr Y, Broman D, Ishaq R (2004) Biomagnification of polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) studied in pike (Esox lucius), perch (Perca fluviatilis) and roach (Rutilus rutilus) from the Baltic Sea. Chemosphere 55:1043–1052CrossRefGoogle Scholar
  16. Colombo JC, Bilos C, Lenicov MR, Colautti D, Landoni P, Brochu C (2000) Detritivorous fish contamination in the Rio de la Plata estuary: a critical accumulation pathway in the cycle of anthropogenic compounds. Can J Fish AquatSci 57:1139–1150CrossRefGoogle Scholar
  17. Connell DW, Fung CN, Minh TB, Tanabe S, Lam PKS, Wong BSF, Lam MHW, Wong LC, Richardson BJ (2003) Risk to breeding success of fish-eating ardeids due to persistent organic contaminants in Hong Kong: evidence from organochlorine compounds in eggs. Wat Res 37:459–467CrossRefGoogle Scholar
  18. Crimmins BS, Doelling Brown P, Kelso DP, Foster GD (2002) Bioaccumulation of PCBs in aquatic biota from a tidal freshwater marsh ecosystem. Arch Environ Contam Toxicol 42:396–404CrossRefGoogle Scholar
  19. Crivelli AJ, Marsili L, Focardi S, Renzoni A (1999) Organochlorine compounds in pelicans (Pelecanus crispus and Pelecanus onocrotalus) nesting at Lake Mikri Prespa, northwestern Greece. Bull Environ Contam Toxicol 62:383–389CrossRefGoogle Scholar
  20. Custer TW, Custer CM, Hines RK, Gutreuter S, Stromborg KL, Alien PD, Melancon MJ (1999) Organochlorine contaminants and reproductive success of double-crested cormorants from Green Bay, Wisconsin, USA. Environ Toxicol Chem 18:1209–1217CrossRefGoogle Scholar
  21. Dannenberger D, Andersson R, Rappe C (1997) Levels and patterns of polychlorinated dibenzo-p-dioxins, dibenzofurans and biphenyls in surface sediments from the Oder River estuarine system. Mar Pollut Bull 34:1016–1024CrossRefGoogle Scholar
  22. De Cruz I, Mougin C, Grolleau G (1997) Chlorinated hydrocarbons in eggs of grey heron (Ardea cinerea L.) in France. (Lac De Grandieu). Chemosphere 35: 1003–1009CrossRefGoogle Scholar
  23. De Luca-Abbott SB, Wong BSF, Peakall DB, Lam PKS, Young L, Lam MHW, Richardson BJ (2001) Review of effects of water pollution on the breeding success of waterbirds, with particular reference to ardeids in Hong Kong. Ecotoxicology 10:327–349CrossRefGoogle Scholar
  24. Dietrich S, Büthe A, Denker E, Hötker H (1997) Organochlorines in eggs and food organisms of avocets (Recurvirostra avosetta). Bull Environ Contam Toxicol 58:219–226CrossRefGoogle Scholar
  25. Dirksen S, Boudewijn T, Slager LK, Mes RG, Van Schaick MJM, De Voogt P (1995) Reduce breeding success of cormorants (Phalacrocorax carbo sinensis) in relation to persistent organochlorine pollution of aquatic habitats in the Netherlands. Environ Pollut 88:119–l32CrossRefGoogle Scholar
  26. Erickson MD (2001) Introduction: PCB properties, uses, occurrence and regulatory history. In: Robertson LW, Hansen LG (eds) PCBs: Recent advances in environmental toxicology and health effects. The University Press of Kentucky, U.S.A., pp xi–xxxGoogle Scholar
  27. 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 34:87–93CrossRefGoogle Scholar
  28. Fisk AT, Norstrom RJ, Cymbalisty CD, Muir DCG (1998) Dietary accumulation and depuration of hydrophobic organochlorines: Bioaccumulation parameters and their relationship with the octanol/water partition coefficient. Environ Toxicol Chem 17:951–961CrossRefGoogle Scholar
  29. Fitzner RE, Blus LJ, Henny CJ, Carlile DW (1988) Organochlorine residues in great blue herons from the northwest United States. Colon Watb 11:203–300Google Scholar
  30. Fossi MC, Massi A, Lari L, Marsili L, Focardi S, Leonzio C, Renzoni A (1995) Interspecies differences in mixed function oxidase activity in birds: Relationship between feeding habits, detoxication activities and organochlorine accumulation. Environ Pollut 90:15–24CrossRefGoogle Scholar
  31. Guruge KS, Tanabe S (1997) Congener specific accumulation and toxic assessment of polychlorinated biphenyls in common cormorants, Phalacrocorax carbo, from Lake Biwa, Japan. Environ Pollut 96:425–433CrossRefGoogle Scholar
  32. Guruge KS, Tanabe S, Fukuda M (2000) Toxic assessment of PCBs by the 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalent in common cormorant (Phalacrocorax carbo) from Japan. Arch Environ Contam Toxicol 38:509–521CrossRefGoogle Scholar
  33. Hebert CE, Nostrom RJ, Zhu J, Macdonald CR (1999) Historical changes in PCB patterns in Lake Ontario and Green Bay, Lake Michigan, 1971 to 1982, from herring gull egg monitoring data. J Gt Lakes Res 25:220–233CrossRefGoogle Scholar
  34. Henny CJ, Kaiser JL, Grove RA, Raymond Bentlet V, Elliott JE (2003) Biomagnification factors (fish to osprey eggs from Willamette river, Oregon, USA) for PCDDs, PCDFs, PCBs and OC pesticides. Environ Monit Assess 84:275–315CrossRefGoogle Scholar
  35. Hoffman DJ, Rattner BA, Bunck CM, Crynitsky A, Ohlendorf HM, Lowe RW (1986) Association between PCBs and lower embryonic weight in black-crowned night herons in San Francisco Bay. J Toxicol Environ Health 19:383–391CrossRefGoogle Scholar
  36. Hong CS, Xiao J, Bush B, Shaw SD (1998) Environmental occurrence and potential toxicity of planar, mono- and di-ortho polychlorinated biphenyls in the biota. Chemosphere 36: 1637–1651CrossRefGoogle Scholar
  37. Hoshi H, Minamoto N, Iwata H, Shiraki K, Tatsukawa R, Tanabe S, Fujita S, Hirai K, Kinjo T (1998) Organochlorine pesticides and polychlorinated biphenyl congeners in wild terrestrial mammals and birds from Chubu region, Japan: interspecies comparison of the residue levels and compositions. Chemosphere 36:3211–3221CrossRefGoogle Scholar
  38. Hothem RL, Roster PL, King KA, Keldsen TJ, Marois KG, Wainwright SE (1995) Spatial and temporal trends of contaminants in eggs of wading birds from San Francisco Bay, California. Environ Toxicol Chem 14:1319–1331Google Scholar
  39. Jenssen BM, Nilssen VH, Murvoll KM, Skaare JU (2001) PCBs, TEQs and plasma retinol in grey heron (Ardea cinerea) hatchlings from two rookeries in Norway. Chemosphere 44:483–489CrossRefGoogle Scholar
  40. Kamarianos A, Karamanlis X, Galoupi E (2002) Pollution of coastal areas of N. Creece by organochlorine pesticides and polychlorinated biphenyls (PCBs). In: Proceedings of the 1st Environmental Conference of Macedonia, 1–4 March, Thessaloniki, Greece, pp 116–121Google Scholar
  41. Katsoyiannis A (2006) Occurence of polychlorinated biphenyls (PCBs) in the Soulou stream in the power generation area of Eordea, nortwastern Greece. Chemosphere 65:1551–1561CrossRefGoogle Scholar
  42. Kelly BC, Gobas FAPC, McLachan MS (2004) Intestinal absorption and biomagnification of organic contaminants in fish, wildlife and humans. Environ Toxicol Chem 23:2324–2336CrossRefGoogle Scholar
  43. Kidd KA, Schindler DW, Hesslein RH, Muir DCG (1998) Effects of trophic position and lipid on organochlorine concentrations in fishes from subarctic lakes in Yukon Territory. Can J Fish Aquat Sci 55:869–881CrossRefGoogle Scholar
  44. Konstantinou IK, Goutner V, Albanis TA (2000) The incidence of polychlorinated biphenyl and organochlorine pesticide residues in the eggs of the cormorant (Phalacrocorax carbo sinensis): an evaluation of the situation in four Greek wetlands of international importance. Sci Total Environ 257:61–79CrossRefGoogle Scholar
  45. LeBlanc GA (1995) Trophic-level diffrences in the bioconcentration of chemicals: implications in assessing environmental biomagnification. Environ Sci Technol 29: 154–160CrossRefGoogle Scholar
  46. Liordos V (2004) Biology and ecology of great cormorant ((Phalacrocorax carbo L., 1758) populations breeding and wintering in Greek wetlands. Doctoral Dissertation, Department of Biology, Aristotle University of Thessaloniki, p 307Google Scholar
  47. Looser R, Ballschmiter K (1998) Biomagnification of polychlorinated biphenyls (PCBs) in freshwater fish. Fres J Anal Chem 360:816–819CrossRefGoogle Scholar
  48. Mackay D, Shiu WY, Ma KC (2000) Handbook of physical-chemical properties and environmental fate. CRCnetBase, Chapman & Hall, CRC Press, Boca Raton, FLGoogle Scholar
  49. Metcalfe TL, Metcalfe CD (1997) The trophodynamics of PCBs, including mono- and non-ortho congeners, in the food web of north-central Lake Ontario. Sci Total Environ 201:245–272CrossRefGoogle Scholar
  50. Meylan WM, Howard PH, Boethling RS, Aronson D, Printup H, Gouchie S (1999) Improved method for estimating bioconcentration/bioaccumulation factor from octanol/water partition coefficient. Environ Toxicol Chem 18:664–672CrossRefGoogle Scholar
  51. Muñoz Cifuentes J, Becker PH, Sommer U, Pacheco P, Schlatter R (2003) Seabird eggs as bioindicators of chemical contamination in Chile. Environ Pollut 126:123–137CrossRefGoogle Scholar
  52. Nazirides T (2004) Comparative biological-ecological study of the cormorant (Phalacrocorax carbo (Linnaeus, 1758)) and pygmy cormorant (Phalacrocorax pygmeus (Pallas, 1773)) at Lake Kerkini. Doctoral Dissertation, Department of Forestry and Natural Environment, Aristotle University of Thessaloniki, p 118Google Scholar
  53. Oliver BG, Niimi AJ (1988) Trophodynamic analysis of polychlorinated biphenyl congeners and other chlorinated hydrocarbons in the Lake Ontario ecosystem. Environ Sci Technol 22:388–397CrossRefGoogle Scholar
  54. Pastor D, Sanpera C, Gonzáles-Solís J, Ruiz X, Albaigés J (2004) Factors affecting the organochlorine pollutant load in biota of a rice field ecosystem (Ebro Delta, NE Spain). Chemosphere 55:567–576CrossRefGoogle Scholar
  55. Ryckman DP, Weseloh DV, Hamp P, Fox GA, Collins B, Ewins PJ, Norstrom RJ (1998) Spatial and temporal trends in organochlorine contamination and bill deformities in double-crested cormorants (Phalacrocorax auritus) from the Canadian Great Lakes. Environ Monitor Assess 53:169–195CrossRefGoogle Scholar
  56. Scharenberg W (1991) Cormorants (Phalacrocorax carbo sinensis) as bioindicators for chlorinated biphenyls. Arch Environ Contain Toxicol 21:536–540CrossRefGoogle Scholar
  57. Scharenberg W, Gramann P, Pfeiffer WH (1994) Bioaccumulation of heavy metals and organochlorines in a lake ecosystem with special reference to bream (Abramis brama). Sci Total Environ 155:187–197CrossRefGoogle Scholar
  58. Scharenberg W, Ebeling E (1998) Organochlorine pesticides in eggs of two waterbird species (Fulica atra, Podiceps cristatus) from the same habitat: reference site Lake Belau, Germany. Chemosphere 36:263–270CrossRefGoogle Scholar
  59. Serrano R, Simal-Julian A, Pitarch E, Hernandez F, Varo I, Navarro JC (2003) Biomagnification study on organochlorine compounds in marine aquaculture: The sea bass (Dicentrachus labrax) as a model. Environ Sci Technol 37:3375–3381CrossRefGoogle Scholar
  60. Singh AK, Spassova D, White T (1998) Quantitative analysis of polychlorinated biphenyls, organochlorine insecticides, polycyclic aromatic hydrocarbons, polychlorinated hydrocarbons and polynitrohydrocarbons in spiked samples of soil, water and plasma by selected-ion monitoring gas chromatography-mass spectrometry. J Chromatogr B 706:231–244CrossRefGoogle Scholar
  61. Swackhamer DL, Hites RA (1988) Occurrence and bioaccumulation of organochlorine compounds in fishes from Siskiwit Lake, Isle Royale, Lake Superior. Environ Sci Technol 22:543–548CrossRefGoogle Scholar
  62. Swindlehurst RJ, Johnston PA, Tröndle S, Stringer RL, Stephenson AD, Stone IM (1995) Regulation of toxic chemicals in the Mediterranean: the need for an adequate strategy. Sci Total Environ 171:243–264CrossRefGoogle Scholar
  63. Tanabe S, Kannan N, Subramanian A, Watanabe S, Tatsukawa R (1987) Highly toxic coplanar PCBs: occurrence, source, persistency and toxic implications to wildlife and humans. Environ Pollut 47:147–163CrossRefGoogle Scholar
  64. Tsachalidis EP (1989) Biology and behavioral ecology of little egret (Egretta garzetta) in the artificial Lake Kerkini, Serres. Doctoral dissertation, Department of Forestry and Natural Environment, Aristotle University of Thessaloniki, p 146Google Scholar
  65. Wainwright SE, Mora MA, Sericano JL, Thomas P (2001) Chlorinated hydrocarbons and biomarkers of exposure in wading birds and fish of the lower Rio Grande Valley, Texas. Arch Environ Contam Toxicol 40:101–111CrossRefGoogle Scholar
  66. Weseloh DV, Hamr P, Bishop CA, Norstrom RJ (1995) Organochlorine contaminant levels in waterbird species from Hamilton Harbour, Lake Ontario: an IJC area of concern. J Gt Lakes Res 21:12l–l37CrossRefGoogle Scholar
  67. Yamashita N, Tanabe S, Ludwig JP, Kurita H, Ludwig ME, Tatsukawa R (1993) Embryonic abnormalities and organochlorine contamination in double-crested cormorants (Phalacrocorax auritus) and Caspian terns (Hydroprogne caspia) from the upper Great Lakes in 1988. Environ Pollut 79:163–173CrossRefGoogle Scholar
  68. Zimmermann G, Dietrich DR, Schmid P, Schlatter C (1997) Congener-specific bioaccumulation of PCBs in different water bird species. Chemosphere 34:1379–1388CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • V. Antoniadou
    • 1
  • I. K. Konstantinou
    • 2
  • V. Goutner
    • 1
    Email author
  • T. M. Sakellarides
    • 3
  • T. A. Albanis
    • 3
  • E. Bintoudi
    • 1
  1. 1.Department of ZoologyAristotelian University of ThessalonikiThessalonikiGreece
  2. 2.Department of Environmental and Natural Resources ManagementUniversity of IoanninaAgrinioGreece
  3. 3.Department of ChemistryUniversity of IoanninaIoanninaGreece

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