Sublethal Pb exposure produces season-dependent effects on immune response, oxidative balance and investment in carotenoid-based coloration in red-legged partridges

Environmental Science and Technology

Volumn 49, Issue 6, 2015, Pages 3839-3850

  Vallverdú Coll, Núria ^a   Ortiz Santaliestra, Manuel E ^a,b   Mougeot, François ^c   Vidal, Dolors ^d   Mateo, Rafael ^a  

^a INSTITUTO DE INVESTIGACIÓN EN RECURSOS CINEGÉTICOS IREC CSIC UCLM JCCM   (Spain)

^b University of Koblenz Landau   (Germany)

^c DEPARTAMENTO DE ECOLOGÍA FUNCIONAL Y EVOLUTIVA   (Spain)

^d Universidad de Castilla La Mancha   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ABRASIVES; ANTIBODIES; ANTIOXIDANTS; COLIFORM BACTERIA; ECONOMIC AND SOCIAL EFFECTS; ENZYMES; OXIDATIVE STRESS; PIGMENTS;

ALECTORIS RUFA; BACTERIAL ABUNDANCE; GUT BACTERIA; IMMUNE RESPONSE; IMMUNITY TESTING; OXIDATIVE STRESS BIOMARKERS; PB POISONING; PHAGOCYTIC ACTIVITY;

LEAD;

ALKALINE PHOSPHATASE; ANTIOXIDANT; LEAD; LYSOZYME; PHOSPHORUS; PHYTOHEMAGGLUTININ; PROTEIN; RETINOL; TRIACYLGLYCEROL; XANTHOPHYLL; BIOLOGICAL MARKER; CAROTENOID; PORPHOBILINOGEN SYNTHASE;

ABUNDANCE; AVIFAUNA; BACTERIUM; BIOMARKER; CAROTENOID; COLOR; GAMEBIRD; IMMUNE RESPONSE; LEAD; OXIDATION; POLLUTION EXPOSURE; REPRODUCTIVE COST; TRADE-OFF;

ADULT; ALKALINE PHOSPHATASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY BLOOD LEVEL; ANTIBODY RESPONSE; ARTICLE; AUTUMN; BACTERICIDAL ACTIVITY; BODY CONSTITUTION; CONTROLLED STUDY; ENZYME BLOOD LEVEL; FECAL COLIFORM; FEMALE; HEMAGGLUTINATION; IMMUNE RESPONSE; LEAD BLOOD LEVEL; LEAD POISONING; MALE; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PARTRIDGE; PHAGOCYTOSIS; PHOSPHATE BLOOD LEVEL; PROTEIN BLOOD LEVEL; PROTEIN INTERACTION; SEASONAL VARIATION; SEX DIFFERENCE; SPRING; TRIACYLGLYCEROL BLOOD LEVEL; VITAMIN BLOOD LEVEL; ANALYSIS; ANIMAL; ANTIBODY PRODUCTION; BLOOD; BREEDING; CELLULAR IMMUNITY; CHEMISTRY; ENVIRONMENTAL EXPOSURE; ERYTHROCYTE; FECES; GALLIFORMES; IMMUNITY; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; PARASITOLOGY; PIGMENTATION; SEASON; SHEEP;

ALECTORIS RUFA; BACTERIA (MICROORGANISMS); NEGIBACTERIA;

ANIMALS; ANTIBODY FORMATION; BIOMARKERS; BREEDING; CAROTENOIDS; ENVIRONMENTAL EXPOSURE; ERYTHROCYTES; FECES; FEMALE; GALLIFORMES; IMMUNITY; IMMUNITY, CELLULAR; LEAD; MALE; OXIDATION-REDUCTION; OXIDATIVE STRESS; PIGMENTATION; PORPHOBILINOGEN SYNTHASE; SEASONS; SHEEP;

EID: 84924973745     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es505148d     Document Type: Article

References (79)

1. Mateo, R.; Vallverdú-Coll, N.; López-Antia, A.; Taggart, M. A.; Martínez-Haro, M.; Guitart, R.; Ortiz-Santaliestra, M. E. Reducing Pb poisoning in birds and Pb exposure in game meat consumers: The dual benefit of effective Pb shot regulation Environ. Int. 2014, 63, 163-168
2. Espín, S.; Martínez-López, E.; Jiménez, P.; María-Mojica, P.; García-Fernández, A. J. Effects of heavy metals on biomarkers for oxidative stress in griffon vulture (Gyps fulvus) Environ. Res. 2014, 129, 59-68
3. Taggart, M. A.; Green, A. J.; Mateo, R.; Svanberg, F.; Hillström, L.; Meharg, A. A. Metal levels in the bones and livers of globally threatened marbled teal and white-headed duck from El Hondo, Spain Ecotoxicol. Environ. Saf. 2009, 72 (1) 1-9
4. Stroud, R.; Hunt, W. G. Gunshot wounds: A source of lead in the environment. In Ingestion of Lead From Spent Ammunition: Implications for Wildlife and Humans; Watson, R. T.; Fuller, M.; Pokras, M.; Hunt, W. G., Eds.; The Peregrine Fund: Boise, ID, 2009; pp 119-125.
5. Mateo, R.; Belliure, J.; Dolz, J. C.; Aguilar Serrano, J. M.; Guitart, R. High prevalences of lead poisoning in wintering waterfowl in Spain Arch. Environ. Contam. Toxicol. 1998, 35 (2) 342-347
6. Fairbrother, A.; Smits, J.; Grasman, K. Avian immunotoxicology J. Toxicol. Environ. Health, Part B 2004, 7 (2) 105-137
7. Dietert, R. R.; Piepenbrink, M. S. Lead and immune function Crit. Rev. Toxicol. 2006, 36 (4) 359-385
8. Knowles, S. O.; Donaldson, W. E. Lead disrupts eicosanoid metabolism, macrophage function, and disease resistance in birds Biol. Trace Elem. Res. 1997, 60 (1-2) 13-26
9. Rocke, T. E.; Samuel, D. Effects of lead shot ingestion on selected cells of the mallard immune system J. Wildl. Dis. 1991, 27 (1) 1-9
10. Vodela, J. K.; Renden, J. A.; Lenz, S. D.; McElhenney, W. H.; Kemppainen, B. W. Drinking water contaminants (arsenic, cadmium, lead, benzene, and trichloroethylene). Interaction of contaminants with nutritional status on general performance and immune function in broiler chickens Poult. Sci. 1997, 76 (11) 1474-1492
11. Lee, K. A. Linking immune defenses and life history at the levels of the individual and the species Integr. Comp. Biol. 2006, 46 (6) 1000-1015
12. Fair, J. M.; Myers, O. B. The ecological and physiological costs of lead shot and immunological challenge to developing western bluebirds Ecotoxicology 2002, 11 (3) 199-208
13. Lee, J. E.; Dietert, R. R. Developmental immunotoxicity of lead: Impact on thymic function Birth Defects Res., Part A 2003, 67 (10) 861-867
14. Hussain, I.; Piepenbrink, M. S.; Dietert, R. R. Impact of in ovo-administered lead and testosterone on developing female thymocytes J. Toxicol. Environ. Health, Part A 2005, 68 (15) 1309-1319
15. Trust, K. A.; Miller, M. W.; Ringelman, J. K.; Orme, I. M. Effects of ingested lead on antibody production in mallards (Anas platyrhynchos) J. Wildl. Dis. 1990, 26 (3) 316-322
16. Grasman, K. A.; Scanlon, P. F. Effects of acute lead ingestion and diet on antibody and T-cell-mediated immunity in Japanese quail Arch. Environ. Contam. Toxicol. 1995, 28 (2) 161-167
17. Gleichmann, E.; Kimber, I.; Purchase, I. F. H. Immunotoxicology: Suppressive and stimulatory effects of drugs and environmental chemicals on the immune system Arch. Toxicol. 1989, 63 (4) 257-273
18. Nain, S.; Smits, J. E. G. Subchronic lead exposure, immunotoxicology and increased disease resistance in Japanese quail (Corturnix coturnix japonica) Ecotoxicol. Environ. Saf. 2011, 74 (5) 787-792
19. Friend, M.; Trainer, D. O. Polychlorinated biphenyl: Interaction with duck hepatitis virus Science 1970, 170 (3964) 1314-1316
20. Karol, M. H. Target organs and systems: Methodologies to assess immune system function Environ. Health Perspect. 1998, 106 (suppl 2) 533-540
21. Dowling, D. K.; Simmons, L. W. Reactive oxygen species as universal constraints in life-history evolution Proc. Biol. Sci. 2009, 276 (1663) 1737-1745
22. Hoffman, D. J.; Heinz, G. H.; Sileo, L.; Audet, D. J.; Campbell, J. K.; Lecaptain, L. J. Developmental toxicity of lead-contaminated sediment to mallard ducklings Arch. Environ. Contam. Toxicol. 2000, 39 (2) 221-232
23. Mateo, R.; Hoffman, D. J. Differences in oxidative stress between young Canada geese and mallards exposed to lead-contaminated sediment J. Toxicol. Environ. Health, Part A 2001, 64 (7) 531-545
24. Mateo, R.; Beyer, W. N.; Spann, J. W.; Hoffman, D. J.; Ramis, A. Relationship between oxidative stress, pathology, and behavioral signs of lead poisoning in mallards J. Toxicol. Environ. Health, Part A 2003, 66 (14) 1371-1389
25. Martinez-Haro, M.; Green, A. J.; Mateo, R. Effects of lead exposure on oxidative stress biomarkers and plasma biochemistry in waterbirds in the field Environ. Res. 2011, 111 (4) 530-538
26. Pérez-Rodríguez, L. Carotenoid-based ornamentation as a dynamic but consistent individual trait Behav. Ecol. Sociobiol. 2008, 62 (6) 995-1005
27. Pérez-Rodríguez, L. Carotenoids in evolutionary ecology: Re-evaluating the antioxidant role BioEssays 2009, 31 (10) 1116-1126
28. Pérez-Rodríguez, L.; Martínez-Padilla, J.; Mougeot, F. Evidences from two galliform species, the red legged partridge (Alectoris rufa) and the red grouse (Lagopus lagopus scoticus). In Carotenoids: Food Sources, Production and Health Benefits; Yamaguchi, M., Ed.; Nova Science Publishers: New York, 2013; pp 2-23.
29. Goodwin, T. W. In The Biochemistry of the Carotenoids II. Animals; Chapman and Hall: London, 1984.
30. Peters, A.; Delhey, K.; Denk, A. G.; Kempenaers, B. Trade-offs between immune investment and sexual signaling in male mallards Am. Nat. 2004, 164 (1) 51-59
31. Alonso-Alvarez, C.; Pérez-Rodríguez, L.; Mateo, R.; Chastel, O.; Viñuela, J. The oxidation handicap hypothesis and the carotenoid allocation trade-off J. Evol. Biol. 2008, 21 (6) 1789-1797
32. Ferrandis, P.; Mateo, R.; López-Serrano, F. R.; Martínez-Haro, M.; Martínez-Duro, E. Lead-shot exposure in red-legged partridge (Alectoris rufa) on a driven shooting estate Environ. Sci. Technol. 2008, 42 (16) 6271-6277
33. Møller, A. P.; Erritzøe, J.; Saino, N. Seasonal changes in immune response and parasite impact on hosts Am. Nat. 2003, 161 (4) 657-671
34. Mateo, R.; Martínez-Vilalta, A.; Guitart, R. Lead shot pellets in the Ebro delta, Spain: Densities in sediments and prevalence of exposure in waterfowl Environ. Pollut. 1997, 96 (3) 335-341
35. Peig, J.; Green, A. J. New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method Oikos 2009, 118 (12) 1883-1891
36. Mateo, R.; Estrada, J.; Paquet, J. Y.; Riera, X.; Domínguez, L.; Guitart, R.; Martínez-Vilalta, A. Lead shot ingestion by marsh harriers Circus aeruginosus from the Ebro delta, Spain Environ. Pollut. 1999, 104, 435-440
37. Martínez-Haro, M.; Taggart, M. A.; Mateo, R. Pb-Al relationships in waterfowl feces discriminate between sources of Pb exposure Environ. Pollut. 2010, 158 (7) 2485-2489
38. Pain, D. J. Haematological parameters as predictors of blood lead and indicators of lead poisoning in the black duck (Anas rubripes) Environ. Pollut. 1989, 60 (1-2) 67-81
39. Papp, Z.; Smits, J. E. G. Validation and novel applications of the whole-blood chemiluminescence assay of innate immune function in wild vertebrates and domestic chickens J. Wildl. Dis. 2007, 43 (4) 623-634
40. Millet, S.; Bennett, J.; Lee, K. A.; Hau, M.; Klasing, K. C. Quantifying and comparing constitutive immunity across avian species Dev. Comp. Immunol. 2007, 31 (2) 188-201
41. Gill, J. Serum lysozyme level in the European bison, Bison bonasus (L.) Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol. 1995, 110 (1) 235-240
42. Matson, K. D.; Ricklefs, R. E.; Klasing, K. C. A hemolysis-hemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds Dev. Comp. Immunol. 2005, 29 (3) 275-286
43. Goto, N.; Kodama, H.; Kosuke, O.; Fujimoto, Y. Suppression of phytohemagglutinin skin response in thymectomized chickens Poult. Sci. 1978, 57 (1) 246-250
44. Jordan, J. S.; Bellrose, F. C. Lead poisoning in wild waterfowl Illinois Nat. Hist. Surv. Biol. Notes 1951, 26, 1-27
45. Blakley, B. R.; kouassi, E. Structural and functional complexity of the immune system and its relationship to immunotoxicology. In Investigative Immunotoxicology; Tryphonas, H.; Fournier, M.; Blakley, B. R.; Smits, J. E. G.; Brousseau, P., Eds.; Taylor and Francis, CRC Press LLC: London, 2005; pp 3-9.
46. Mougeot, F.; Redpath, S. M. Sexual ornamentation relates to immune function in male red grouse Lagopus lagopus scoticus J. Avian Biol. 2004, 35 (5) 425-433
47. Reglero, M. M.; Taggart, M. A.; Monsalve-González, L.; Mateo, R. Heavy metal exposure in large game from a lead mining area: Effects on oxidative stress and fatty acid composition in liver Environ. Pollut. 2009, 157 (4) 1388-1395
48. Romero-Haro, A. A.; Alonso-Alvarez, C. Covariation in oxidative stress markers in the blood of nestling and adult birds Physiol. Biochem. Zool. 2014, 87 (2) 353-362
49. Bradford, M. M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding Anal. Biochem. 1976, 72 (1-2) 248-254
50. Rodríguez-Estival, J.; Martínez-Haro, M.; Martín-Hernando, M. P.; Mateo, R. Sub-chronic effects of nitrate in drinking water on red-legged partridge (Alectoris rufa): Oxidative stress and T-cell mediated immune function Environ. Res. 2010, 110 (5) 469-475
51. Alonso-Alvarez, C.; Pérez-Rodríguez, L.; Ferrero, M. E.; García de-Blas, E.; Casas, F.; Mougeot, F. Adjustment of female reproductive investment according to male carotenoid-based ornamentation in a gallinaceous bird Behav. Ecol. Sociobiol. 2012, 66 (5) 731-742
52. Mougeot, F.; Pérez-Rodríguez, L.; Sumozas, N.; Terraube, J. Parasites, condition, immune responsiveness and carotenoid-based ornamentation in male red-legged partridge Alectoris rufa J. Avian Biol. 2009, 40 (1) 67-74
53. Pain, D. J.; Fisher, I. J.; Thomas, V. G. A global update of lead poisoning in terrestrial birds from ammunition sources. In Ingestion of Lead From Spent Ammunition: Implications for Wildlife and Humans; Watson, R. T.; Fuller, M.; Pokras, M.; Hunt, G., Eds.; The Peregrine Fund: Boise, ID, 2009; pp 99-118.
54. Irwin, J. C. The influence of diet on the pathogenesis of lead poisoning in waterfowl. Ph.D. Dissertation, University of Guelph, Guelph, ON, 1977.
55. Scheuhammer, A. M. Influence of reduced dietary calcium on the accumulation and effects of lead, cadmium, and aluminum in birds Environ. Pollut. 1996, 94 (3) 337-343
56. Tejedor, M. C.; Gonzalez, M. Comparison between lead levels in blood and bone tissue of rock doves (Columba livia) treated with lead acetate or exposed to environment of Alcalá de Henares Bull. Environ. Contam. Toxicol. 1992, 48 (6) 835-842
57. Minnema, D. J.; Michaelson, I. A.; Cooper, G. P. Calcium efflux and neurotransmitter release from rat hippocampal synaptosomes exposed to lead Toxicol. Appl. Pharmacol. 1988, 92 (3) 351-357
58. Kendall, R. J.; Anderson, T. A.; Baker, R. J.; Bens, C. M.; Carr, J. A.; Chiodo, L. A. G. P. I. C.; Dickerson, R. L.; Dixon, K. R.; Frame, L. T.; Hooper, M. J.; Ecotoxicology. In Casarett and Doulls Toxicology: The Basic Science of Poisons; Klaassen, C. D., Ed.; McGraw-Hill: New York, 2001; pp 1013-1045.
59. Apanius, V. Ontogeny of immune function. In Avian Growth and Development; Starck, J. M.; Ricklefs, R. E., Eds.; Oxford University Press: Oxford, U. K., 1998; pp 203-222.
60. Ochsenbein, A. F.; Fehr, T.; Lutz, C.; Suter, M.; Brombacher, F.; Hengartner, H.; Zinkernagel, R. M. Control of early viral and bacterial distribution and disease by natural antibodies Science 1999, 286 (5447) 2156-2159
61. Ochsenbein, A. F.; Zinkernagel, R. M. Natural antibodies and complement link innate and acquired immunity Immunol. Today 2000, 21 (12) 624-630
62. Teijón, C.; Olmo, R.; Blanco, M. D.; Romero, A.; Teijón, J. M. Effects of lead administration at low doses by different routes on rat spleens. Study of response of splenic lymphocytes and tissue lysozyme Toxicology 2003, 191 (2-3) 245-258
63. Gordon, S.; Todd, K.; Cohn, Z. A. In vitro synthesis and secretion of lysozyme by mononuclear phagocytes J. Exp. Med. 1974, 139 (5) 1228-1248
64. Kowolenko, M.; Tracy, L.; Mudzinski, S.; Lawrence, D. A. Effect of lead on macrophage function J. Leukocyte Biol. 1988, 43 (4) 357-364
65. Fair, J. M.; Ricklefs, R. E. Physiological, growth, and immune responses of Japanese quail chicks to the multiple stressors of immunological challenge and lead shot Arch. Environ. Contam. Toxicol. 2002, 42 (1) 77-87
66. Redig, P. T.; Lawler, E. M.; Schwartz, S.; Dunnette, J. L.; Stephenson, B.; Duke, G. E. Effects of chronic exposure to sublethal concentrations of lead acetate on heme synthesis and immune function in red-tailed hawks Arch. Environ. Contam. Toxicol. 1991, 21 (1) 72-77
67. Smits, J. E. G.; Baos, R. Evaluation of the antibody mediated immune response in nestling American kestrels (Falco sparverius) Dev. Comp. Immunol. 2005, 29 (2) 161-170
68. Peng, L.; Lifang, R.; Hongyu, X.; Xi, L.; Chaocan, Z. Study on the toxic effect of lead(II) ion on Escherichia coli Biol. Trace Elem. Res. 2007, 115 (2) 195-202
69. Callewaert, L.; Michiels, C. W. Lysozymes in the animal kingdom J. Biosci. 2010, 35 (1) 127-160
70. Rzucidlo, L. Immunologia Ogblna i Dowiadczalna; PWN: Warszawa, Poland, 1978.
71. Benkerroum, N. Antimicrobial activity of lysozyme with special relevance to milk African J. Biotechnol. 2008, 7 (25) 4856-4867
72. Pastoret, P. P.; Griebel, P.; Bazicn, H.; Govaerts, A. Avian immunology. In Handbook of Vertebrate Immunology; Academic Press, 1998; pp 73-136.
73. Breton, J.; Massart, S.; Vandamme, P.; De Brandt, E.; Pot, B.; Foligné, B. Ecotoxicology inside the gut: Impact of heavy metals on the mouse microbiome BMC Pharmacol. Toxicol. 2013, 14 (62) 2050-6511
74. Rodríguez-Estival, J.; Martinez-Haro, M.; Monsalve-González, L.; Mateo, R. Interactions between endogenous and dietary antioxidants against Pb-induced oxidative stress in wild ungulates from a Pb polluted mining area Sci. Total Environ. 2011, 409 (14) 2725-2733
75. Griffith, O. W. Biologic and pharmacologic regulation of mammalian glutathione synthesis Free Radical Biol. Med. 1999, 27 (9-10) 922-935
76. Velando, A.; Beamonte-Barrientos, R.; Torres, R. Enhanced male coloration after immune challenge increases reproductive potential J. Evol. Biol. 2014, 27 (8) 1-8
77. García-de Blas, E.; Mateo, R.; Guzmán Bernardo, F. J.; Rodríguez Martín-Doimeadios, R. C.; Alonso-Alvarez, C. Astaxanthin and papilioerythrinone in the skin of birds: A chromatic convergence of two metabolic routes with different precursors? Naturwissenschaften 2014, 101 (5) 407-416
78. Townsend, D. M.; Tew, K. D.; Tapiero, H. The importance of glutathione in human disease Biomed. Pharmacother. 2003, 57 (3-4) 145-155
79. Ward, N. E.; Pierce, D. S.; Chung, S. E.; Gravitt, K. R.; OBrian, C. A. Irreversible inactivation of protein kinase C by glutathione J. Biol. Chem. 1998, 273 (20) 12558-12566