Abstract
We identified and quantified organochlorine (OC) pesticide residues in the plasma of 28 osprey (Pandion haliaetus) nestlings from a dense population in Laguna San Ignacio, a pristine area of Baja California Sur, Mexico, during the 2001 breeding season. Sixteen OC pesticides were identified and quantified. α-, β-, δ- and γ-hexachlorocyclohexane, heptaclor, heptachlor epoxide, endosulfan I and II, endosulfan-sulfate, p,p′-DDE, p,p′-DDD, aldrin, dieldrin, endrin, endrin aldehyde, and endrin ketone were the OCs found in the plasma of nestlings, ranging from 0.002 to 6.856 pg/μl (parts per billion). No differences were found in the concentration of pesticides between genders (P > 0.05). In our work, the concentrations detected in the plasma were lower than those reported to be a threat for the species and that affect the survival and reproduction of birds. The presence of OC pesticides in the remote Laguna San Ignacio osprey population is an indication of the ubiquitous nature of these contaminants. OCs are apparently able to travel long distances from their source to the study area. A significant relationship between hemoglobin and mean corpuscular hemoglobin concentrations and OC concentrations were found suggesting that a potential effect on the health of chicks may exist in this osprey population caused by the OC, e.g. anemia. The total proteins were positively correlated with α-BHC, endosulfan I, and p,p′-DDD. It has been suggested that OC also affects competitive interactions and population status over the long term in vertebrate species, and our results could be used as reference information for comparison with other more exposed osprey populations.
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References
Ames PL, Mersereau GS (1964) Some factors in the decline of the osprey in Connecticut. Auk 81:173–185
Becker PH (2003) Biomonitoring with birds. In: Markert BA, Breuare AM, Zechmeister HG (eds) Bioindicators & Biomonitors. Elsevier Science, Amsterdam, The Netherlands, pp 677–735
Bidleman TE, Leone AD (2004) Soil-air exchange of organochlorine pesticides in the Southern United States. Environ Pollut 128:49–57
Blus LJ (1996) DDT, DDD, and DDE in Birds. In: Beyer WN, Heinz GH, Redmon-Norwood AW (eds) Environmental contaminants in wildlife—interpreting tissue concentrations. Lewis Publishers, Boca Raton, FL, pp 49–71
Blus LJ (2003) Organochlorine pesticides. In: Hoffman DJ, Rattner BA, Burton GA, Cairns J (eds) Handbook of Ecotoxicology, 2nd edn. Lewis Publishers, Boca Raton, FL, pp 313–339
Bowerman WW, Best DA, Grubb TG, Sikarskie JG, Giesy JP (2000a) Assessment of environmental endocrine disruptors in bald eagles of the Great Lakes. Chemosphere 4:1569–1574
Bowerman WW, Stickle JE, Sikarskie JG, Giesy JP (2000b) Hematology and serum chemistries of nestling bald eagles (Haliaeetus leucocephalus) in the lower peninsula of MI, USA. Chemosphere 41:1575–1579
Bowerman WW, Roe AS, Gilbertson MJ, Best DA, Sikarskie JG, Mitchell RS, Summer CL (2002) Using bald eagles to indicate the health of the Great Lake’s environment. Lakes Reserv Res Manag 7:183–187
Casado E, Balbontin J, Ferrer M (2002) Plasma chemistry in Booted Eagle (Hieraaetus pennatus) during breeding season. Comp Biochem Physiol Part A 131:233–241
Chu I, Villeneuve DC, Yagminas A, LeCavalier P, Poon R, Feeley M, Kennedy SW, Seegal RF, Häkansson H, Ahlborg UG, Valli VE (1994) Subchronic toxicity of 3,3′,4,4′,5-pentachlorobiphenyl in the rat. I. Clinical, biochemical, hematological, and histopathological changes. Fundam Appl Toxicol 22:457–468
Comisión Intersecretarial para el Control del Proceso y Uso de Plaguicidas, Fertilizantes y Sustancias Tóxicas CICOPLAFEST (2004) (Secretaría de Salud, Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación, Secretaría de Medio Ambiente y Recursos Naturales, Secretaría de Economía Catálogo Oficial de Plaguicidas, México
Dahlgren RB, Linder RL (1970) Eggshell thickness in pheasants given dieldrin. J Wildl Manage 34:226–228
Danemann G (1994) Biología reproductiva del águila pescadora (Pandion haliaetus) en Isla Ballena, Laguna San Ignacio, Baja California Sur, México, Master Dissertation Centro Interdisciplinario de Ciencias Marinas (CICIMAR)
Dirksen S, Boudewijn TJ, Slager LK, Mes RG, van Schaick JM, de Voogt P (1995) Reduced breeding success of cormorants (Phalacrocorax carbo sinensis) in relation to persistent organochlorine pollution of aquatic habitats in the Netherlands. Environ Pollut 88:119–132
Doblado P, Tella JL, Cevallos O, Donazar JA (1998) Effect of age and captivity on plasma chemistry values of the Egyptian Vulture. Condor 100:719–725
Elliott JE, Machmer MM, Wilson LK, Henny CJ (2000) Contaminants in ospreys from the Pacific Northwest: II. Organochlorine pesticides, polychlorinated biphenyls, and mercury, 1991–1997. Arch Environ Contam Toxicol 38:93–106
Elliott JE, Morrissey CA, Henny CJ, Inzunza ER, Shaw P (2007) Satellite telemetry and prey sampling reveal contaminant sources to Pacific Northwest Ospreys. Ecol Appl 17:1223–1233
Fleming WJ, MClane MAR, Cromatie E (1982) Endrin decreases screech owl productivity. J Wildl Manage 46:462–468
Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121
Fyfe RW, Campbell J, Hayson B, Hodson K (1969) Regional population declines and organochlorine insecticides in Canadian Prairie falcons. Can Field Nat 83:189–200
Gee G, Carpenter J, Hensler G (1981) Species differences in hematological values of captive cranes, geese, raptors and quail. J Wildl Manage 45:463–483
Grove R, Henny C, Kaiser J (2009) Osprey: World sentinel species for assessing and monitoring environmental contamination in rivers, lakes, reservoirs and estuaries. J Toxicol Environ Health, Part B 12:25–44
Henny CJ, Anderson DW (2004) Status of nesting ospreys in coastal Baja California, Sonora, and Sinaloa, Mexico, 1977 and 1992–1993. Bull South Calif Acad Sci 103:95–114
Henny CJ, Ogden JC (1970) Estimated status of osprey populations in the United States. J Wildl Manage 34:214–217
Henny C, Blus LJ, Hoffman DJ, Grove RA, Hatfield JS (1991) Lead accumulation and osprey production near a mining site on the coeur d’Alene River. Idaho Arch Environ Contam Toxicol 21:415–424
Henny CJ, Kaiser JK, Grove RA, Bentley VR, Elliott EJ (2002) Biomagnification factors (fish to osprey eggs from Willamette River, Oregon, U.S.A.) for PCDDS, PCDFS, PCBS and OC pesticides. Environ Monit Assess 84:275–315
Henny CJ, Grove RA, Kaiser JL, Bentley VR (2004) An evaluation of osprey eggs to determine spatial residue patterns and effects of contaminants along the Lower Columbia River, U.S.A. In: Chancellor RD, Meyburg BU (eds) Raptors worldwide. World Working Group on Birds of Prey and Owls and MME/Bird Life Hungary, Budapest, Hungary, pp 369–388
Henny CH, Kaiser JL, Grove RA (2009) PCDDs, PCDFs, PCBs, OC pesticides and mercury in fish and osprey eggs from Willamette River, Oregon (1993, 2001 and 2006) with calculated biomagnification factors. Ecotoxicology 18:151–173
Hickey J, Anderson D (1968) Chlorinated hydrocarbons and eggshell changes in raptorial and fish-eating birds. Science 162:271–273
Jiménez B, Rodríguez-Estrella R, Merino R, Gómez G, Rivera-Rodríguez L, González MJ, Abad E, Rivera J (2005) Results and evaluation of the first study of organochlorine contaminants (PCDDs, PCDFs, PCBs and DDTs), heavy metals and metalloids in birds from Baja California, México. Environ Pollut 133:139–146
Johnson B, Henny C, Kaiser J, Davis J, Schulz E (2009) Assessment of contaminant exposure and effects on ospreys nesting along the Lower Duwamish River, Washington, 2006–07. U.S Geological Survey Open-File Report 2009-1255, pp. 88
Keithmaleesatti S, Varanusupakul P, Siriwong W, Thirakhupt K, Robson M, Kitana N (2009) Contamination of organochlorine pesticides in nest soil, egg, and blood of the snail-eating turtle (Malayemys macrocephala) from the Chao Phraya River Basin, Thailand. Proc World Acad Sci Eng Technol 40:459–464
Keller JM, Kucklick JR, Harms CA, McClellan-Green PD (2004a) Organochlorine contaminants in sea turtles: correlations between whole blood and fat. Environ Toxicol Chem 23:726–738
Keller JM, Kucklick JR, Stamper MA, Harms CA, McClellan-Green PD (2004b) Associations between organochlorine contaminant concentrations and clinical health parameters in loggerhead sea turtles from North Carolina, USA. Environ Health Perspect 112:1074–1079
Kenntner N, Krone O, Oehme G, Heidecke D, Tataruch F (2003) Organochlorine contaminants in body tissue of free ranging white-tailed eagles from northern regions of Germany. Environ Toxicol Chem 22:1457–1464
Lehner PN, Egbert A (1969) Dieldrin and eggshell thickness in ducks. Nature 224:1218–1219
Lemus JA, Blanco G, Rodríguez-Estrella R (2006) High infestation by blood parasites (Haematozoa) in nestlings of colonial ospreys (Pandion haliaetus) from Baja California, México. In: Rodríguez-Estrella R. (ed) Current raptor studies in Mexico. Centro de Investigaciones Biológicas del Noroeste and CONABIO. México. pp 163–180
Martin P, de Solla SR, Ewins P (2002) Chlorintated hydrocarbon contamination in osprey egg and nestlings from the Canadian Great Lakes Basin, 1991–1995. Ecotoxicology 12:209–224
Maura L (1987) Hematology and blood chemistry. In: Giron Pendleton BA, Millsap BA, Cline KW, Bird DM (eds) Raptor Management Techniques Manual. Natl Wildl Fed, Washington, DC, pp 269–275
Mealey B, Parks GM, Pages CM, Millsap BA, Bass OL, Bossart GD (2004) Serum chemistry values for nestling bald eagles (Haliaeetus Leucocephalus) in Florida Bay, Everglades National Park. J Raptor Res 38:96–100
Mendenhall M, Klaas EE, Mclane MAR (1983) Breeding success of barn owls (Tyto alba) fed low levels of DDE and dieldrin. Arch Environ Contam Toxicol 12:235–240
Nebeker AV, Griffis WL, Stutzman TW, Schuytema GS, Carey LA, Scherer SM (1992) Effects of aqueous and dietary exposure of dieldrin on survival, growth and bioconcentration in mallard ducklings. Environ Toxicol Chem 11:687–699
Newton I, Wyllie I, Aasher (1991) Mortality causes in British barn owls Tyto alba, with a discussion of aldrin-dieldrin poisoning. Ibis 133:164–169
Peakall DB, Lincer JL (1996) Do PCBs cause eggshell thinning? Environ Pollut 91:127–129
Plan Estatal de Desarrollo 2005–2011. Gobierno del Estado de Baja California Sur http://www.lib.utexas.edu/benson/lagovdocs/mexico/bajacaliforniasur/ped.html. Accessed 28 March 2010
Polo F, Celdrán J, Peinado V, Viscor G, Palomeque J (1992) Hematological values for four species of birds of prey. Condor 94:1007–1013
Postupalsky S (1969) The status of the osprey in Michigan in 1965. In: Hickey JJ (ed) Peregrine Falcon Populations. University of Wisconsin Press, Madison, WI, USA, pp 338–340
Reese JG (1972) Osprey nesting success along the Choptank River, Maryland. Chesapeake Sci 13:233–235
Rivera-Rodríguez L (2003) Determinación de la condición física de pollos de águila pescadora (Pandion haliaetus carolinensis), en la población reproductora de la Laguna de San Ignacio, Baja California Sur, relacionada al sexo y a la presencia de ectoparásitos, Master Dissertation, Centro de Investigaciones Biológicas del Noroeste, S.C., La Paz, B.C.S. México
Rivera-Rodríguez LB, Rodríguez Estrella R, Ellington J, Evans J (2007) Quantification of low levels of organochlorine pesticides using small volumes (≤100 μl) of plasma of wild birds through gas chromatography negative chemical ionization mass spectrometry. Environ Pollut 148:654–662
Rodríguez-Estrella R, Donázar JA, Hiraldo F (1998) Raptors as indicators of environmental change in the scrub habitat of Baja California Sur, Mexico. Conserv Biol 12:921–925
Rodríguez-Estrella R, Rivera-Rodríguez L B, Morales E (2006) Breeding biology and success of the osprey (Pandion haliaetus) in Laguna San Ignacio, Baja California Sur, México in 1998, 2000, and 2001. In: Rodríguez-Estrella R. (ed) Current raptor studies in Mexico. Centro de Investigaciones Biológicas del Noroeste and CONABIO. México. pp 149–162
Shen L, Wania F, Lei YD, Teixeira C, Muir DC, Bidleman TF (2004) Atmospheric distribution and long-range transport behavior of organochlorine pesticides in North America. Environ Sci Technol 39:409–420
Spitzer PR (1980) Dynamics of a discrete coastal breeding population of ospreys (Pandion haliaetus) in the northeastern United States during a period of decline and recovery, 1969–1978. Ph.D. dissertation, Cornell Univ., Ithaca, NY
Toschik P, Rattner BA, McGrowan PC, Christman MC, Carter DB, Hale RC, Matson CW, Ottinger MA (2005) Effects on contaminant exposure on reproductive success of ospreys (Pandion haliaetus) nestling in Delaware River and Bay, U.S.A. Environ Toxicol Chem 24:617–628
Wiemeyer SN, Lamont TG, Locke LN (1980) Residues of environmental pollutants and necropsy data for eastern United States osprey, 1964–1973. Estuaries 3:155–167
Acknowledgments
Field assistance was provided by A. Cota, M. Lobato, B. Granados, I. Guerrero and V. Anguiano. EPA Athens, Georgia provided the equipment and materials for the chromatographic analyses. J.M. Godoy determined the gender of nestling ospreys at the Laboratory of Molecular Ecology, Estación Biológica de Doñana, Spain. Ch. Henny and one anonymous reviewer provided useful comments that improved an early version of the manuscript. This study was partially supported by Consejo Nacional de Ciencia y Tecnología grant SEMARNAT-CONACYT C01-0318, Agencia Española de Cooperación Internacional AECI (155/03/05) and CIBNOR funds to RRE. LBRR received a doctoral scholarship from CONACyT (61099). RRE also received a sabbatical grant in the EBD, Spain during the writing of this ms. Thanks to Dr. Ellis Glazier for editing this English-language text.
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Rivera-Rodríguez, L.B., Rodríguez-Estrella, R. Incidence of organochlorine pesticides and the health condition of nestling ospreys (Pandion haliaetus) at Laguna San Ignacio, a pristine area of Baja California Sur, Mexico. Ecotoxicology 20, 29–38 (2011). https://doi.org/10.1007/s10646-010-0553-5
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DOI: https://doi.org/10.1007/s10646-010-0553-5