Environmental and genetic variation in body condition and blood profile of great tit Parus major nestlings

Journal of Avian Biology

Volumn 40, Issue 2, 2009, Pages 157-165

  Cláudia Norte, Ana ^a   Sheldon, Ben C ^b   Sousa, José P ^a   Ramos, Jaime A ^a  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; BIOINDICATOR; BLOOD; BODY CONDITION; ECOSYSTEM HEALTH; ENVIRONMENTAL CUE; ENZYME ACTIVITY; FOOD AVAILABILITY; GENETIC VARIATION; GENOTYPE; MORPHOLOGY; PASSERINE; PROTEIN;

AVES; PARUS MAJOR;

EID: 63049107341     PISSN: 09088857     EISSN: 1600048X     Source Type: Journal    
DOI: 10.1111/j.1600-048X.2008.04461.x     Document Type: Article

References (84)

1. Ames, B., Shigenaga, M. Hagen, T. 1993. Oxidants, antioxidants, and the degenerative diseases of aging Proc. Natl. A. Sci. USA 90 : 7915 7922.
2. Ardia, D. R. 2005. Cross-fostering reveals an effect of spleen size and nest temperatures on immune responses in nestling European starlings Oecologia 145 : 327 334.
3. Bańbura, J., Bańbura, M., Kaliński, A., Skwarska, J., Slomczyński, R., Wawrzyniak, J. Zieliński, P. 2007. Habitat and year-to-year variation in haemoglobin concentration in nestling blue tits Cyanistes caeruleus Comp. Biochem. Physiol. 148 : 572 577.
4. Bell, D. J. 1971. Plasma enzymes Bell, D. J. Freeman, B. M. Physiology and biochemistry of the domestic fowl. Acad. Press, New York 963 970.
5. Blakey, J. K. 1994. Genetic evidence for extra-pair fertilizations in a monogamous passerine, the great tit Parus major Ibis 136 : 457 462.
6. Boag, P. T. 1983. The heritability of external morphology in Darwin's ground finches (Geospiza) on Isla Daphne Major, Galapagos Evolution 37 : 877 894.
7. Bortolotti, G. R., Tella, J. L., Forero, M. G., Dawson, R. D. Negro, J. J. 2000. Genetics, local environment and health as factors influencing plasma carotenoids in wild American kestrels (Falco sparverius) Proc. R. Soc. B 267 : 1433 1438.
8. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 : 248 254.
9. Brinkhof, M. W. G., Heeb, P., Kölliker, M. Richner, H. 1999. Immunocompetence of nestling great tits in relation to rearing environment and parentage Proc. R. Soc. B 266 : 2315 2322.
10. Brown, M. E. 1996. Assessing body condition in birds Curr. Ornithol. 13 : 67 135.
11. Campbell, T. W. 1995. Avian hematology and cytology. Iowa State University Press, Ames.
12. Campo, J. L. Davila, S. G. 2002. Estimation of heritability for Heterophil: Lymphocyte ratio in chickens by restricted maximum likelihood. Effects of age, sex and crossing Poult. Sci. 81 : 1448 1453.
13. Christe, P., Møller, A. P., Saino, N. de Lope, F. 2000. Genetic and environmental components of phenotypic variation in immune response and body size of a colonial bird, Delichon urbica (the house martin) Heredity 85 : 75 83.
14. Çokuǧraş, N. 2003. Butyrylcholinesterase: Structure and Physiological Importance Turk. J. Biochem. 28 : 54 61.
15. Cornish, H. H. 1971. Problems posed by observations of serum enzyme changes in toxicology Crit. Rev. Toxicol. 1 : 1 32.
16. Costantini, D., Casagrande, S., De Filippis, S., Brambilla, G., Fanfani, A., Tagliavini, J. Dell'Omo, G. 2006. Correlates of oxidative stress in wild kestrel nestlings (Falco tinnunculus) J. Comp. Physiol. B 176 : 329 337.
17. Costantini, D. Dell'Omo, G. 2006. Environmental and genetic components of oxidative stress in wild kestrel nestlings (Falco tinnunculus) J. Comp. Physiol. B 176 : 575 579.
18. da Silva, I. B. M. dos Santos, H. M. 1991. Análise quantitativa da glutatião-redutase e da glutatião-peroxidase em plasma e eritrócitos humanos Rev. Port. Farm. 41 : 9 14.
19. Dawson, R. D. Bortolotti, G. R. 1997. Variation in hematocrit and total plasma proteins of nestling American kestrels (Falco sparverius) in the wild Comp. Biochem. Physiol. 117 : 383 390.
20. Dell'Omo, G., Shore, R. F. Fishwick, S. K. 1996. The relationships between brain, serum, and whole blood ChE activity in the wood mouse (Apodemus sylvaticus) and the common shrew (Sorex araneus) after acute sublethal exposure to dimethoate Biomarkers 1 : 202 207.
21. Dhondt, A. A. 1982. Heritability of blue tit tarsus length from normal and cross-fostered broods Evolution 36 : 418 419.
22. Dubiec, A. Cichoñ, M. 2001. Seasonal decline in health status of great tit (Parus major) nestlings Can. J. Zool. 79 : 1829 1833.
23. Dufva, R Allander, K. 1996. Variable effects of the hen flea Ceratophyllus gallinae on the breeding success of the Great Tit Parus major in relation to weather conditions Ibis 138 : 772 777.
24. Edwards, J. A. Brimijoin, S. 1982. Divergent regulation of acetylcholinesterase and butyrylcholinesterase in tissues of the rat J. Neurochem. 38 : 1393 1403.
25. Ellman, G. L., Courtney, K. D., Andres Jr., V. Featherstone, R. M. 1961. A new rapid colorimetric determination of acetylcholinesterase activity Biochem. Pharmacol. 7 : 88 95.
26. Falconer, D. S. Mackay, C. 1996. Introduction to quantitative genetics. Longman, Essex.
27. Garant, D., Kruuk, L. E. B., McCleery, R. H. Sheldon, B. C. 2004. Evolution in a changing environment: a case study with great tit fledging mass Am. Nat. 164 : E115 E129.
28. Garnett, M. C. 1981. Body size, its heritability and influence on juvenile survival among great tits, Parus major Ibis 123 : 31 41.
29. Gebhardt-Henrich, S. G. van Noordwijk, A. J. 1991. Nestling growth in the great tit I. Heritability estimates under different environmental conditions J. Evol. Biol. 4 : 341.
30. Gebhardt-Henrich, S. G. van Noordwijk, A. J. 1994. The genetical ecology of nestling growth in the great tit. Environmental influences on the expression of genetic variances during growth Funct. Ecol. 8 : 469 476.
31. Greig-Smith, P. W., Walker, C. H. Thompson, H. M. 1992. Ecotoxicological consequences of interactions between avian esterases and organophosphorus compounds Ballantyne, B. Mars, T. C. Clinical and experimental toxicology of organophosphates and carbamates. Butterworth-Heinemann, Oxford 295 303.
32. Gross, W. B. Siegel, H. S. 1983. Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chickens Avian Dis. 27 : 972 979.
33. Halliwell, B. Gutteridge, J. M. C. 1990. The antioxidants of human extracellular fluids Arch. Biochem. Biophys. 280 : 1 8.
34. Hart, A. D. M. 1993. Relationships between behavior and the inhibition of acetylcholinesterase in birds exposed to organophosphorus pesticides Environ. Toxicol. Chem. 12 : 321 336.
35. Henderson, Z. 1986. Is there a link between choline acetyltransferase- containing neurons and butyrylcholinesterase in rat cerebral cortex? Trends Neurosci 9 : 20.
36. Hõrak, P. 1994. Effect of nestling history on adult size and reproduction in the great tit Ornis Fenn. 71 : 47 54.
37. Hõrak, P., Tegelmann, L., Ots, I. Møller, A. P. 1999. Immune function and survival of great tit nestlings in relation to growth conditions Oecologia 121 : 316 322.
38. Ilmonen, P., Hasselquist, D., Langefors, A. Wiehn, J. 2003. Stress, immunocompetence and leukocyte profiles of pied flycatchers in relation to brood size manipulation Oecologia 136 : 148 154.
39. Johnston, R. D. 1993. Effects of diet quality on the nestling growth of a wild insectivorous passerine, the house martin Delichon urbica Funct. Ecol. 7 : 255 266.
40. Kappus, H. 1987. Oxidative stress in chemical toxicity Arch. Toxicol. 60 : 144 149.
41. Kilpimaa, J., Van de Casteele, T., Jokinen, I., Mappes, J. Alatalo, R. V. 2005. Genetic and environmental variation in antibody and T-cell mediated responses in the great tit Evolution 59 : 2483 2489.
42. Kinghorn, B. 1983. Genetic variation in food conversion efficiency and growth in rainbow trout Aquaculture 32 : 141 155.
43. Kostelecka-Myrcha, A., Jaroszewicz, M. Cholostiakow-Gromek, J. 1993. Relationship between the values of red blood indices and the body mass of birds Acta Ornithol. 28 : 47 53.
44. Kruuk, L. E. B., Merilä, J. Sheldon, B. C. 2001. Phenotypic selection on heritable size traits revisited Am. Nat. 158 : 557 571.
45. Kubena, L. F., Maty, J. D., Reece, F. N. Deaton, J. W. 1972. Hematocrit and hemoglobin of broilers as influenced by environmental temperature and dietary iron level Poult. Sci. 51 : 759 763.
46. Kutty, K. M. 1980. Review: Biological function of cholinesterase Clin. Biochem. 13 : 239 243.
47. Lewandowski, A. H., Campbell, T. W. Harrison, G. J. 1986. Clinical chemistries Harrison, G. J. Harrison, L. R. E. Clinical avian medicine and surgery. Saunders, Philadelphia 192 200.
48. Maxwell, M. H. 1993. Avian blood leukocyte responses to stress World's Poult. Sci. J. 49 : 34 43.
49. Merilä, J. 1996. Genetic variation in offspring condition: an experiment Funct. Ecol. 10 : 465 474.
50. Merilä, J. 1997. Expression of genetic variation in body size of the collared flycatcher under different environmental conditions Evolution 51 : 526 536.
51. Merilä, J., Kruuk, L. E. B. Sheldon, B. C. 2001. Natural selection on the genetical component of variance in body condition in a wild bird population J. Evol. Biol. 14 : 918 929.
52. Merilä, J., Przybylo, R. Sheldon, B. C. 1999. Genetic variation and natural selection on blue tit body condition in different environments Gen. Res. 73 : 165 176.
53. Merilä, J. Sheldon, B. C. 2001. Avian quantitative genetics Curr. Ornithol. 16 : 179 255.
54. Møller, A. P., Biard, C., Blount, J. D., Houston, D. C., Ninni, P., Saino, N. Surai, P. F. 2000. Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability Avian Poult. Biol. Rev. 11 : 137 159.
55. Norris, K. Evans, M. R. 2000. Ecological immunology: life history trade-offs and immune defence in birds Behav. Ecol. 11 : 19 26.
56. Norte, A. C. 2007. Physiological parameters and fitness in great tit Parus major populations as bioindicators of pulp mill pollution PhD thesis, Univ. of Coimbra, Portugal.
57. Norte, A. C., Sheldon, B., Sousa, J. P. Ramos, J. A. 2008. Repeatability of blood parameters and methodological sources of variation in wild great tits Parus major Acta Ornithol. 43 : 65 75.
58. Paglia, D. E. Valentine, W. N. 1967. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase J. Lab. Clin. Med. 70 : 158 169.
59. Parkinson, A. 1996. Biotransformation of xenobiotics Klaassen, C. D. Casarett and Doull's toxicology: the basic science of poisons. McGraw-Hill, pp, New York 113 186.
60. Peakall, D. B. Fournier, M. 1992. Animal biomarkers as pollution indicators. Chapman & Hall, London.
61. Perrins, C. M. 1965. Population fluctuations and clutch size in the great tit, Parus major J. Anim. Ecol. 34 : 601 647.
62. Perrins, C. 1979. British tits. Collins, London.
63. Perrins, C. M. 1991. Tits and their caterpillar food supply Ibis 133 : 49 54.
64. Potti, J. Merino, S. 1994. Heritability estimates and maternal effects on tarsus length in pied flycatchers, Ficedula hypoleuca Oecologia 100 : 331 338.
65. Potti, J., Moreno, J., Merino, S., Frías, O. Rodríguez, R. 1999. Environmental and genetic variation in the haematocrit of fledgling pied flycatchers Ficedula hypoleuca Oecologia 120 : 1 8.
66. Saino, N., Cuervo, J. J., Krivacek, M., Lope, F. Møller, A. P. 1997. Experimental manipulation of tail ornament size affects the hematocrit of male barn swallows (Hirundo rustica) Oecologia 110 : 186 190.
67. Satoh, T., Taylor, P., Bosron, W. F., Sanghani, S. P., Hosokawa, M. Du, B. N. L. 2002. Current progress on esterases: from molecular structure to function Drug Metab. Dispos. 30 : 488 493.
68. Sheldon, B. C. 1999. Revealing quantitative genetic relationships in sexual selection using molecular markers Adams, N. S. Slotow, R. Proc. 22 Int. Ornithol. Congr., Durban. University of Natal. Bird life, South Africa, Johannesburg 1099 1114.
69. Sies, H. 1993. Strategies in antioxidant defense Eur. J. Biochem. 215 : 213 219.
70. Simon, A., Thomas, D. W., Bourgault, P., Blondel, J., Perret, P. Lambrechts, M. M. 2005. Between-population differences in nestling size and hematocrit level in blue tits (Parus caeruleus): a cross-fostering test for genetic and environmental effects Can. J. Zool. 83 : 694 701.
71. Slomczyński, R., Kaliński, A., Wawrzyniak, J., Bańbura, M., Skwarska, J., Zieliński, P. Bańbura, J. 2006. Effects of experimental reduction in nest micro-parasite and macro-parasite loads on nestling hemoglobin level in blue tits Parus caeruleus Acta Oecol. 30 : 223 227.
72. Smith, F. M., West, N. H. Jones, D. R. 2000. The cardiovascular system Whittow, G. C. Sturkie's avian physiology. Academic Press, London 141 223.
73. Soler, J. J., Moreno, J. Potti, J. 2003. Environmental, genetic and maternal components of immunocompetence of nestling pied flycatchers from a cross- fostering study Evol. Ecol. Res. 5 : 259 272.
74. Swanson, D. L. 1990. Seasonal variation of vascular oxygen transport in the dark-eyed junco Condor 92 : 62 66.
75. Tella, J. L., Bortolotti, G. R., Forero, M. G. Dawson, R. D. 2000. Environmental and genetic variation in T-cell-mediated immune response of fledgling American kestrels Oecologia 123 : 453 459.
76. Thessing, A. Ekman, J. 1994. Selection on the genetical and environmental components of tarsal growth in juvenile willow tits (Parus montanus) J. Evol. Biol. 7 : 713.
77. Thompson, H. M. 1991. Serum "B" esterases as indicators of exposure to pesticides Mineau, P. Cholinesterase-inhibiting insecticides - their impact on wildlife and the environment. Elsevier, Amsterdam 109 125.
78. van Kampen, E. J. Zijlstra, W. G. 1961. Standardization of hemoglobinometry II. The hemiglobincyanide method Clin. Chim. Acta 6 : 538 544.
79. van Lith, H. A., Zutphen, L. F. Beynen, A. C. 1991. Butyrylcholinesterase activity in plasma of rats and rabbits fed high-fat diets Comp. Biochem. Phys. A 98 : 339 342.
80. van Noordwijk, A. J., van Balen, J. H. Scharloo, W. 1988. Heritability of body size in a natural population of the great tit (Parus major) and its relation to age and environmental conditions during growth Genet. Res. 51 : 149 162.
81. Verboven, N. Mateman, A. C. 1997. Low frequency of extra-pair fertilizations in the great tit Parus major revealed by DNA fingerprinting J. Avian Biol. 28 : 231 239.
82. Walker, C. H. Thompson, H. M. 1991. Phylogenetic distribution of cholinesterases and related esterases Mineau, P. Cholinesterase-inhibiting insecticides - their impact on wildlife and the environment. Elsevier, Amsterdam 1 17.
83. Westlake, G. E., Martin, A. D., Stanley, P. I. Walker, C. H. 1983. Control enzyme levels in the plasma, brain and liver from wild birds and mammals in Britain Comp. Biochem. Phys. C 76 : 15 24.
84. Williams, T. D. 1994. Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness Biol. Rev. 68 : 35 59.