Interspecific variation in avian blood parasites and haematology associated with urbanization in a desert habitat

Journal of Avian Biology

Volumn 39, Issue 3, 2008, Pages 300-310

  Bobby Fokidis, H ^a   Greiner, Ellis C ^b   Deviche, Pierre ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b University of Florida College of Veterinary Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABUNDANCE; DESERT; HEMATOLOGY; HEMOPARASITE; HOST-PARASITE INTERACTION; INTERSPECIFIC VARIATION; PARASITE INFESTATION; PARASITISM; PASSERINE; RESOURCE AVAILABILITY; URBANIZATION;

AVES; MIMUS POLYGLOTTOS; PASSERI; PIPILO ABERTI; PIPILO FUSCUS; TOXOSTOMA CURVIROSTRE;

EID: 44649148531     PISSN: 09088857     EISSN: 1600048X     Source Type: Journal    
DOI: 10.1111/j.0908-8857.2008.04248.x     Document Type: Article

References (97)

1. Adriano, E. A. Cordeiro, N. S. 2001. Prevalence and intensity of Haemoproteus columbae in three species of wild doves from Brazil Mem. Inst. Oswaldo Cruz 96 : 175 178.
2. Atkinson, C. T. Van Riper, III, C. 1991. Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoan, and Haemoproteus Loye, J. E. Zuk, M. Bird-parasite interactions: ecology, evolution and behaviour. Oxford Univ. Press, Oxford 19 48.
3. Baker, P. J., Bentley, A. J., Ansell, R. J. Harris, S. 2005. Impact of predation by domestic cats Felis catus in an urban area Mammal Rev. 35 : 302 312.
4. Barnard, C. J., Behnke, J. M., Gage, A. R., Brown, H. Smithurst, P. R. 1998. The role of parasite-induced immunodepression, rank, and social environment in the modulation of behavior and hormone concentration in male laboratory mice (Mus musculus) Proc. R. Soc. B 265 : 693 701.
5. Bennett, G. F. 1970. Simple techniques for making avian blood smears Can. J. Zool. 48 : 585 586.
6. Bennett, G. F., Earle, R. A., Du Toit, H. Huchzermeyer, F. W. 1992. A host-parasite catalogue of the haematoza of the sub-saharan birds Onderstepoort J. Vet. Res. 59 : 1 7.
7. Bennett, G.F., Parsons, D.S., Siikamäki, P., Huhta, E., Allander, K. Hillström, L. 1995. A comparison of the blood parasites of 3 Fenno-Scandian populations of the pied flycatcher Ficedula hypoleuca J. Avian Biol. 26 : 33 38.
8. Bentz, S., Rigaud, T., Barroca, M., Martin-Laurent, F., Bru, D., Moreau, J. Faivre, B. 2006. Sensitive measure of prevalence and parasitaemia of haemosporidia from European blackbird (Turdus merula) populations: value of PCR-RFLP and quantitative PCR Parasitology 133 : 685 692.
9. Blair, R. B. 1996. Land use and avian species diversity along an urban gradient Ecol. Appl. 6 : 506 519.
10. Blanton, F. S. Wirth, W. W. 1979. The sand flies (Culicoides) of Florida (Diptera: Ceratopogonidae) Florida Dept. Agri. and Consumer Serv. Gainesville 204 pp.
11. Bonier, F., Martin, P. R., Sheldon, K. S., Jensen, J. P., Foltz, S. L. Wingfield, J. C. 2007. Sex-specific consequences of life in the city Behav. Ecol. 18 : 121 129.
12. Burhans, D. E. Thompson, F. R. 2006. Songbird abundance and parasitism differ between urban and rural shrublands Ecol. Appl. 16 : 394 405.
13. Bush, A. O., Lafferty, K. D., Lotz, J. M. Shostak, A. W. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited J. Parasitol. 83 : 575 583.
14. Campbell, T. W. 1995. Avian hematology and cytology. Iowa State University Press, Ames 108.
15. Chace, J. F., Walsh, J. J., Cruz, A., Prather, J. Swanson, H. E. 2003. Spatial and temporal activity patterns of the brood parasitic brown-headed cowbird and an urban/wildland interface Landsc. Urban Plan. 64 : 179 190.
16. Clergeau, P., Savard, J. P. L., Mennechez, G. Falardeau, G. 1998. Bird abundance and diversity along an urban-rural gradient: a comparative study between two cities on different continents Condor 100 : 413 425.
17. Cox, F. E. G. 1989. Parasites and sexual selection Nature 341 : 289.
18. Demas, G. E., Chefer, V., Talan, M. I. Nelson, R. J. 1997. Metabolic costs of mounting an antigen-stimulated immune response in adult and aged C57BL/6J mice Am. J. Physiol., Reg. Integ. Comp. Physiol. 273 : 1631 1637.
19. Derrickson, K. C. Breitwisch, R. 1992. Northern mockingbird Poole, A., Stettenheim, P. Gill, F. The birds of North America, no. 7. The academy of natural sciences. The AOU, Washington, DC.
20. Deviche, P. Parris, J. 2006. Testosterone treatment to free-ranging male dark-eyed juncos, Junco hyemalis, exacerbates hemoparasitic infection Auk 123 : 548 562.
21. Deviche, P. Small, T. 2005. Environmental control of reproduction in Sonoran desert Aimophila sparrows Dawson, A. Sharp, P. J. Funct. Avian Endocr. Narosa Publishing House, New Delhi 153 166.
22. Deviche, P., Greiner, E. C. Manteca, X. 2001. Interspecific variability of prevalence in blood parasites of adult passerine birds during the breeding season in Alaska J. Wild. Dis. 37 : 28 35.
23. Drake, J. M. 2003. The paradox of the parasites: implications for biological invasion Proc. R. Soc. B 270 Suppl. 2 : 133 135.
24. Drake, J. M. 2003. The paradox of the parasites: implications for biological invasion. Proc. R. Soc. B' 270 133 135.
25. Eens, M., Pinxten, R., Verheyen, R. F., Blust, R. Bervoets, L. 1999. Great and blue tits as indicators of heavy metal contamination in terrestrial ecosystems Ecotox. Environ. Saf. 44 : 81 85.
26. Eeva, T., Hasselquist, D., Langefors, A., Tummeleht, L., Nikinmaa, M. Ilmonen, P. 2005. Pollution related effects on immune function and stress in a free-living population of pied flycatcher Ficedula hypoleuca J. Avian Biol. 36 : 405 412.
27. Emlen, J. T. 1974. Urban bird community in Tucson, Arizona-derivation, structure, regulation Condor 76 : 184 197.
28. Fallon, S. M., Ricklefs, R. E., Swanson, B. L. Bermingham, E. 2003. Detecting avian malaria: an improved polymerase chain reaction diagnostic J. Parasitol. 89 : 1044 1047.
29. Fernández-Juricic, E., Jimenez, M. D. Lucas, E. 2001. Bird tolerance to human disturbance in urban parks of Madrid (Spain), management implications Marzluff, J. M., Bowman, R. Donnelly, R. Avian ecology and conservation in an urbanizing world. Kluwer Academic Publishers, Boston 259 273.
30. French, S. S, Matt, K. S. Moore, M. C. 2006. The effects of stress on wound healing in male tree lizards (Urosaurus ornatus) Gen. Comp. Endocrinol. 145 : 128 132.
31. Fudge, A. M. 1989. Avian hematology: identification and interpretation 284 292 Proc. Ass. Avian Vet. Ann. Meet.
32. Gavett, A. P. Wakeley, J. S. 1986. Blood constituents and their relation to diet in urban and rural house sparrows Condor 88 : 279 284.
33. Gering, E. Atkinson, C. T. 2004. A rapid method for counting nucleated erythrocytes on stained blood smears by digital image analysis J. Parasitol. 90 : 879 881.
34. Gering, J. C. Blair, R. B. 1999. Predation on artificial bird nests along an urban gradient: predatory risk or relaxation in urban environments? Ecography 22 : 532 541.
35. Godfrey, R. D. Jr., Fedynich, A. M. Pence, D. B. 1987. Quantification of hematozoa in blood smears J. Wild. Dis. 23 : 558 565.
36. Green, A. J. 2001. Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82 : 1473 1483.
37. Green, D. M. Baker, M. G. 2003. Urbanization impacts on habitat and bird communities in a Sonoran desert ecosystem Landsc. Urban Plan. 63 : 225 239.
38. Gross, W. B. Siegel, P. B. 1986. Effects of initial and second periods of fasting on heterophil/lymphocyte ratios and body weight Avian Dis. 30 : 345 346.
39. Hamilton, W. D. Zuk, M. 1982. Heritable true fitness and bright birds: a role for parasites Science 218 : 384 387.
40. Harmon, B. G. 1998. Avian heterophils in inflammation and disease resistance Poultry Sci. 77 : 972 977.
41. Heltzel, J. M. Earnst, S. L. 2006. Factors influencing nest success of songbirds in aspen and willow riparian areas in the Great Basin Condor 108 : 842 855.
42. Jarvi, S. I., Atkinson, C. T. Fleischer, R. C. 2001. Immunogenetics and resistance to avian malaria in Hawaiian honeycreepers (Drepanidinae) Stud. Avian Biol. 22 : 254 263.
43. Johnson, R. R. Haight., L. T. 1996. Canyon towhee (Pipilo fuscus) Poole, A., Stettenheim, P. Gill, F. The birds of North America, no. 264. The academy of natural sciences. the AOU, Washington, DC.
44. Klasing, K. C. Leshchinsky, T. V. 1999. Functions, costs, and benefits of the immune system during development and growth Adams, N. J. Slotow, R. H. Proc. 22nd Int. Ornithol. Congr. BirdLife South Africa, Durban 2817 2835.
45. Lambrechts, M. M., Caro, S., Charmantier, A., Gross, N., Galan, M. J., Perret, P., Cartan-Son, M., Dias, P. C., Blondel, J. Thomas, D. W. 2004. Habitat quality as a predictor of spatial variation in blue tit reproductive performance: a multi-plot analysis in a heterogeneous landscape Oecologia 141 : 555 561.
46. Latimer, K. S. Bienzle, D. 2000. Determination and interpretation of avian leukogram Feldman, B. F., Zinkl, J. G. Jain, N. C. Schalm's veterinary hematology, 5th ed. Lippincott, Williams and Wilkins, New York 432 471.
47. Lauenroth, W. Sala, O. 1992. Long-term forage production of North American shortgrass steppe Ecol. Appl. 2 : 397 403.
48. Lee, K. A., Martin, II, L. B., Hasselquist, D., Ricklefs, R. E. Wikelski, M. 2006. Contrasting adaptive immune defenses and blood parasite prevalence in closely related Passer sparrows Oecologia 150 : 383 392.
49. Little, R. M. Earle, R. A. 1995. Sandgrouse (Pterocleidae) and sociable weavers Philetarius socius lack avian haematozoa in semi-arid regions of South Africa J. Arid Environ. 30 : 367 370.
50. Liu, H. Stiling, P. 2006. Testing the enemy release hypothesis: a review and meta-analysis Biol. Inv. 8 : 1535 1545.
51. Lochmiller, R. L. Deerenberg, C. 2000. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88 : 87 98.
52. Longcore, T. Rich, C. 2004. Ecological light pollution Front. Ecol. Environ. 2 : 191 198.
53. Lowther, P. E. Cink, C. L. 1992. House sparrow. (Passer domesticus) Poole, A., Stettenheim, P. Gill, F. The birds of North America, no. 12. The Academy of Natural Sciences. The American Ornithologists' Union, Washington, DC.
54. Luniak, M., Mulsow, R. Walasz, K. 1990. Urbanization of the European blackbird - expansion and adaptations of urban population Luniak, M. Urban ecological studies in central and eastern Europe; international symposium. Polish acad. sci, Warsaw 187 198.
55. Marquardt, W. C., Demaree, R. S. Grieve, R. B. 2000. Parasitology and vector biology, 2nd edition. Academic Press, San Diego 702.
56. Martin, L. B., Pless, M., Svoboda, J. Wikelski, M. 2004. Immune activity in temperate and tropical house sparrows: a common-garden experiment Ecology 85 : 2323 2331.
57. McKinney, M. L. 2002. Urbanization, biodiversity, and conservation Bioscience 52 : 883 890.
58. Merino, S., Moreno, J., Sanz, J. J. Arriero, E. 2000. Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus) Proc. R. Soc. B 267 : 2507 2510.
59. Norris, K. Evans, M. R. 2000. Ecological immunology: life history trade-offs and immune defense in birds Behav. Ecol. 11 : 19 26.
60. Oppliger, A., Clobert, J., Lecomte, J., Lorenzon, P., Boudjemadi, K. John-Alder, H. B. 1998. Environmental stress increases the prevalence and intensity of blood parasite infection in the common lizard (Lacerta vivipara) Ecol. Lett. 1 : 129 138.
61. Palacios, M. G. Martin, T. E. 2006. Incubation period and immune function: a comparative field study among coexisting birds Oecologia 146 : 505 512.
62. Partecke, J., Schwabl, I. Gwinner, E. 2006. Stress and the city: Urbanization and its effects on the stress physiology in European blackbirds Ecology 87 : 1945 1952.
63. Partecke, J., Van't Hof, T. Gwinner, E. 2004. Differences in the timing of reproduction between urban and forest European blackbirds (Turdus merula): result of phenotypic flexibility or genetic differences? Proc. R. Soc. B 271 : 1995 2001.
64. Partecke, J., Van't Hof, T. Gwinner, E. 2005. Underlying physiological control of reproduction in urban and forest-dwelling European blackbirds Turdus merula J. Avian Biol. 36 : 295 305.
65. Pulliam, H. R. 1988. Sources, sinks, and population regulation Am. Nat. 132 : 652 661.
66. Pyle, P. 1997. Identification guide to North American birds. Part 1, Columbidae to Ploceidae. Slate Creek Press, Bolinas.
67. Ruiz, G., Rosenmann, M., Novoa, F. F. Sabat, P. 2002. Hematological parameters and stress index in rufous-collared sparrows dwelling in urban environments Condor 104 : 162 166.
68. Salvante, K. G. 2006. Techniques for studying integrated immune function in birds Auk 123 : 575 586.
69. Sapolsky, R. M. 2000. Stress hormones: good and bad Neurobiol. Dis. 7 : 540 542.
70. Schoech, S. J. Bowman, R. 2001. Variation in the timing of breeding between suburban and wildland Florida scrub-jays: do physiologic measures reflect different environments? Marzluff, J. M., Bowman, R. Donnelly, R. Avian ecology and conservation in an urbanizing world. Kluwer Acad. Publ, Boston 259 273.
71. Schoech, S. J., Bowman, R. Reynolds, S. J. 2004. Food supplementation and the mechanisms underlying early breeding in the Florida scrub-jay: a role for corticosterone? Horm. Behav. 46 : 565 573.
72. Sheldon, B. C. Verhulst, S. 1996. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology Trends Ecol. Evol. 11 : 317 321.
73. Shochat, E, Lerman, S. B., Katti, M. Lewis, D. B. 2004. Linking optimal foraging behavior to bird community structure in an urban-desert landscape: field experiments with artificial food patches Am. Nat. 164 : 232 243.
74. Shurulinkov, P. Chakarov, N. 2006. Prevalence of blood parasites in different local populations of reed warbler (Acrocephalus scirpaceus) and great reed warbler (Acrocephalus arundinaceus) Parasitol. Res. 99 : 588 592.
75. Siegel, S. 1956. Nonparametric statistics for the behavioral sciences. McGraw-Hill Book Company, New York 312.
76. Slabbekoorn, H. Peet, M. 2003. Birds sing at a higher pitch in urban noise Nature 424 : 424.
77. Small, T. W., Sharp, P. J. Deviche, P. 2007. Environmental regulation of the reproductive system in a flexibly breeding Sonoran Desert bird, the rufous-winged sparrow, Aimophila carpalis Horm. Behav. 51 : 483 495.
78. Stevenson, R. D. Woods, W. A, Jr. 2006. Condition indices for conservation: new uses for evolving tools Integr. Comp. Biol. 46 : 1169 1190.
79. Tella, J. L., Blanco, G., Forero, M. G., Gajón, A., Donázar, J. A. Hiraldo, F. 1999. Habitat, world geographic range, and embryonic development of hosts explain the prevalence of avian hematozoa at small spatial and phylogenetic scales Proc. Natl. Acad. Sci. USA. 96 : 1785 1789.
80. Tripathi, A. Bhati., D. P. S. 1997. The effect of nutritional state on the differential leukocyte count of the Indian little brown dove Geobios. 24 : 66 67.
81. Tweit, R. C. 1996. Curve-billed thrasher (Toxostoma curvirostre) Poole, A., Stettenheim, P. Gill, F. The birds of North America, no. 235. The academy of natural sciences. The AOU, Washington, DC.
82. Tweit, R. C. Finch., D. M. 1994. Abert's towhee (Pipilo aberti) Poole, A., Stettenheim, P. Gill, F. The birds of North America, no. 111. The academy of natural sciences. The AOU, Washington, DC.
83. Valera, F., Carrillo, C. M., Barbosa, A. Moreno, E. 2003. Low prevalence of haematozoa in trumpeter finches Bucanetes githagineus from southeastern Spain: additional support for a restricted distribution of blood parasites in arid lands J. Arid Enviro. 55 : 209 213.
84. Valera, F., Hoi, H. Kristin, A. 2006. Parasite pressure and its effects on blood parameters in a stable and dense population of the endangered lesser grey shrike Biodiv. Conserv. 15 : 2187 2195.
85. Valkiunas, G., Iezhova, T. A., Bolshakov, C. V. Kosarev, V. 2006. Blood parasites of the house sparrow Passer domesticus from northwestern Russia, with remarks on trends of global geographical distribution in this bird J. Nat. Hist. 40 : 1709 1718.
86. Vleck, C. M. 1993. Hormones, reproduction, and behavior in birds of the Sonoran Desert Sharp, P. J. Avian endocrinology. J. Endocrinol, Bristol 73 86.
87. Vleck, C. M. 2000. Comparison of corticosterone and heterophil to lymphocyte ratios as indicators of stress in free-living birds Dawson, A. Perspectives in avian endocrinology. Narosa Publ, India.
88. Vleck, C. M., Vertalino, N., Vleck, D. Bucher, T. L. 2000. Stress, corticosterone and heterophil to lymphocyte ratios in free-living Adélie penguins Condor 102 : 392 400.
89. Walberg, J. 2001. White blood cell counting techniques in birds Semin. Avian Exotic Pet. Med. 10 : 72 76.
90. Weatherhead, P. J. Bennett, G. F. 1991. Ecology of red-winged blackbird parasitism by haematozoa Can. J. Zool. 69 : 2352 2359.
91. Webb, W., Szarek, S., Lauenroth, W., Kinerson, R. Smith, M. 1978. Primary productivity and water use in native forest, grassland, and desert ecosystem Ecology 59 : 1239 1247.
92. White, J. G., Antos, M. J., Fitzsimons, J. A. Palmer, G. C. 2005. Non-uniform bird assemblages in urban environments: the influence of streetscape vegetation Landsc. Urban Plan. 71 : 123 135.
93. Wiehn, J. Korpimäki, E. 1998. Resource levels, reproduction and resistance to haematozoan infections Proc. R. Soc. B 265 : 1197 1201.
94. Wirth, W. W. Hubert, A. A. 1960. Cerotopogonidae (Diptera) reared from cacti, with a review of the Copiosus group of Culicoides Ann. Ento. Soc. Am. 10 : 639 658.
95. Woods, M., McDonald, R. A. Harris, S. 2003. Predation of wildlife by domestic cats Felis catus in Great Britain Mammal Rev. 33 : 174 188.
96. Yorinks, N. Atkinson, C. T. 2000. Effects of malaria on activity budgets of experimentally infected juvenile Apapane (Himatione sanguinea) Auk 117 : 731 738.
97. Zaykin, D. V., Zhivotovsky, L. A., Westfall, P. H. Weir, B. S. 2002. Truncated product method for combining P-values Genet. Epidemiol. 22 : 170 185.