Immune function in a free-living bird varies over the annual cycle, but seasonal patterns differ between years
详细信息 查看全文
- 作者：Arne Hegemann (1) a.hegemann@rug.nl
Kevin D. Matson (1)
Christiaan Both (1)
B. Irene Tieleman (1) - 关键词：Ecoimmunology – ; Immunity – ; Life cycle – ; Seasonality – ; Trade ; off
- 刊名：Oecologia
- 出版年：2012
- 出版时间：November 2012
- 年：2012
- 卷：170
- 期：3
- 页码：605-618
- 全文大小：568.4 KB
- 参考文献：1. Ardia DA (2005) Tree swallows trade off immune function and reproductive effort differently across their range. Ecology 86:2040–2046
2. Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Faivre B, Sorci G (2003) Assessing the cost of mounting an immune response. Am Nat 161:367–379
3. Boughton RK, Joop G, Armitage SAO (2011) Outdoor immunology: methodological considerations for ecologists. Funct Ecol 25:81–100. doi:
4. Buehler DM, Piersma T (2008) Travelling on a budget: predictions and ecological evidence for bottlenecks in the annual cycle of long-distance migrants. Philos Trans R Soc Lond B 363:247–266. doi:
5. Buehler DM, Bhola N, Barjaktarov D, Goymann W, Schwabl I, Tieleman BI, Piersma T (2008a) Constitutive immune function responds more slowly to handling stress than corticosterone in a shorebird. Physiol Biochem Zool 81:673–681. doi:
6. Buehler DM, Piersma T, Matson K, Tieleman BI (2008b) Seasonal redistribution of immune function in a migrant shorebird: annual-cycle effects override adjustments to thermal regime. Am Nat 172:783–796. doi:
7. Buehler DM, Versteegh MA, Matson KD, Tieleman I (2011) One problem, many solutions: simple statistical approaches help unravel the complexity of the immune system in an ecological context. PLoS ONE 6:e18592. doi:
8. Campbell TW (1995) Avian hematology and cytology, 2nd edn. Iowa State University Press, Ames
9. Cosgrove CL, Wood MJ, Day KP, Sheldon BC (2008) Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. J Anim Ecol 77:540–548. doi:
10. Davis AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22:760–772. doi:
11. Demas GE, Zysling DA, Beechler BR, Muehlenbein MP, French SS (2011) Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts. J Anim Ecol 80:710–730. doi:
12. Donald PF, Buckingham DL, Moorcroft D, Muirhead LB, Evans AD, Kirby WB (2001) Habitat use and diet of skylarks Alauda arvensis wintering on lowland farmland in southern Britain. J Appl Ecol 38:536–547
13. Donald PF (2004) The skylark. Poyser, London
14. Dowell SF (2001) Seasonal variation in host susceptibility and cycles of certain infectious diseases. Emerg Infect Dis 7:369–374
15. Feldman BF, Zinkl JG, Jain NC (2000) Schalm’s veterinary hematology, 5th edn. Lippincott Williams & Wilkins, Philadelphia, London
16. Glutz von Blotzheim UN, Bauer K (1985) Handbuch der V枚gel Mitteleuropas. vol 10 (CD-ROM version 2001). AULA, Wiesbaden
17. Green R (1978) Factors affecting diet of farmland skylarks, Alauda arvensis. J Anim Ecol 47:913–928
18. Hasselquist D (2007) Comparative immunoecology in birds: hypotheses and tests. J Ornithol 148:S571–S582. doi:
19. Hegemann A, van der Jeugd HP, de Graaf M, Oostebrink LL, Tieleman BI (2010) Are Dutch skylarks partial migrants? Ring recovery data and radio-telemetry suggest local coexistence of contrasting migration strategies. Ardea 98:135–143
20. Hegemann A, Matson KD, Versteegh MA, Tieleman BI (2012a) Wild skylarks seasonally modulate energy budgets but maintain energetically costly inflammatory immune responses throughout the annual cycle. PLoS ONE 7(5):e36358. doi:10.1371/journal.pone.0036358
21. Hegemann A, Voesten R, van Eerde K, van der Velde M, Tieleman BI (2012b) The use of tongue spots for aging and wing length for sexing Skylarks Alauda arvensis—A critical evaluation. Ring Migrat 27 (in press)
22. Horrocks NPC, Matson KD, Tieleman BI (2011) Pathogen pressure puts immune defense into perspective. Integr Comp Biol. doi:
23. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometr J 50:346–363
24. Ilmonen P, Taarna T, Hasselquist D (2000) Experimentally activated immune defence in female pied flycatchers results in reduced breeding success. Proc R Soc Lond B 267:665–670
25. Janeway CA, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197–216. doi:
26. Janeway CA, Travers P, Walport M, Shlomchik MJ (2005) Immunobiology: the immune system in health and disease, 6th edn. Garland, New York
27. Klasing KC (2004) The costs of immunity. Acta Zool Sinica 50:961–969
28. Kurtz J (2004) Memory in the innate and adaptive immune systems. Microb Infect 6:1410–1417. doi:
29. Latimer KS, Bienzle D (2000). Determination and interpretation of the avian leukogram. In: BF Feldman, JG Zinkl, NC Jain and OW Schalm (eds) Lippincott Williams & Wilkins, Philadelphia p 417–432
30. Lee KA, Martin LB, Hasselquist D, Ricklefs RE, Wikelski M (2006) Contrasting adaptive immune defenses and blood parasite prevalence in closely related Passer sparrows. Oecologia 150:383–392
31. Lee KA (2006) Linking immune defenses and life history at the levels of the individual and the species. Integr Comp Biol 46:1000–1015. doi:
32. Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98. doi:
33. LWVT/SOVON (2002). Vogeltrek over nederland 1976–1993. Schuyt, Haarlem
34. Martin LB, Weil ZM, Nelson RJ (2008) Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philos Trans R Soc Lond B 363:321–339. doi:
35. Martin LB, Hasselquist D, Wikelski M (2006) Investment in immune defense is linked to pace of life in house sparrows. Oecologia 147:565–575
36. Martin LB (2005) Trade-offs between molt and immune activity in two populations of house sparrows (Passer domesticus). Can J Zool 83:780–787. doi:
37. Matson KD, Horrocks NPC, Versteegh MA, Tieleman BI (2012) Baseline haptoglobin concentrations are repeatable and predictive of certain aspects of a subsequent experimentally-induced inflammatory response. Comp Biochem Phys A (in press)
38. Matson KD, Ricklefs RE, Klasing KC (2005) A hemolysis-hemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Dev Comp Immunol 29:275–286
39. Matson K, Cohen A, Klasing K, Ricklefs R, Scheuerlein A (2006) No simple answers for ecological immunology: relationships among immune indices at the individual level break down at the species level in waterfowl. Proc R Soc Lond B 273:815–822
40. Mendes L, Piersma T, Hasselquist D, Matson KD, Ricklefs RE (2006) Variation in the innate and acquired arms of the immune system among five shorebird species. J Exp Biol 209:284–291. doi:
41. M酶ller AP, Erritz酶e J, Saino N (2003) Seasonal changes in immune response and parasite impact on hosts. Am Nat 161:657–671
42. Moreno-Rueda G (2010) Experimental test of a trade-off between moult and immune response in house sparrows Passer domesticus. J Evol Biol 23:2229–2237. doi:
43. Nelson RJ, Demas GE, Klien SL, Kriegsfeld LJ (2002) Seasonal patterns of stress, immune function and disease. Cambridge University Press, Cambridge
44. Nelson RJ, Demas GE (1996) Seasonal changes in immune function. Q Rev Biol 71:511–548
45. Norris K, Evans MR (2000) Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 11:19–26. doi:
46. Ochsenbein AF, Zinkernagel RM (2000) Natural antibodies and complement link innate and acquired immunity. Immunol Today 21:624–630
47. Owen JC, Moore FR (2008) Swainson’s thrushes in migratory disposition exhibit reduced immune function. J Ethol 26:383–388. doi:
48. Owen JC, Moore FR (2006) Seasonal differences in immunological condition of three species of thrushes. Condor 108:389–398
49. Owen-Ashley NT, Wingfield JC (2007) Acute phase responses in passerine birds: characterization and seasonal variation. J Ornithol 148:583–591
50. Owen-Ashley NT, Turner M, Hahn TP, Wingfield JC (2006) Hormonal, behavioral, and thermoregulatory responses to bacterial lipopolysaccharide in captive and free-living white-crowned sparrows (Zonotrichia leucophrys gambelii). Horm Behav 49:15–29. doi:
51. Owen-Ashley NT, Wingfield JC (2006) Seasonal modulation of sickness behavior in free-living northwestern song sparrows (Melospiza melodia morphna). J Exp Biol 209:3062–3070. doi:
52. Palacios MG, Cunnick JE, Winkler DW, Vleck CM (2012) Interrelations among immune defense indexes reflect major components of the immune system in a free-living vertebrate. Physiol Biochem Zool 85:1–10
53. Pap PL, Vagasi CI, Tokolyi J, Czirjak GA, Barta Z (2010a) Variation in haematological indices and immune function during the annual cycle in the Great Tit Parus major. Ardea 98:105–112
54. Pap PL, Czirjak GA, Vagasi CI, Barta Z, Hasselquist D (2010b) Sexual dimorphism in immune function changes during the annual cycle in house sparrows. Naturwissenschaften 97:891–901. doi:
55. Parejo D, Silva N (2009) Immunity and fitness in a wild population of Eurasian kestrels Falco tinnunculus. Naturwissenschaften 96:1193–1202. doi:
56. Pedersen AB, Babayan SA (2011) Wild immunology. Mol Ecol 20:872–880. doi:
57. Piersma T (1997) Do global patterns of habitat use and migration strategics co-evolve with relative investments in immunocompetence due to spatial variation in parasite pressure? Oikos 80:623–631
58. R Development Core Team (2009). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org
59. Raberg L, Stjernman M, Hasselquist D (2003) Immune responsiveness in adult blue tits: heritability and effects of nutritional status during ontogeny. Oecologia 136:360–364. doi:
60. Roitt IM, Brostoff J, Male DK (1998) Immunology, 5th edn. Mosby, London
61. Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc Lond B 270:357–366
62. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321
63. Svensson E, Raberg L, Koch C, Hasselquist D (1998) Energetic stress, immunosuppression and the costs of an antibody response. Funct Ecol 12:912–919
64. Thomas JS (2000) Overview of plasma proteins. In: Feldman BF, Zinkl JG, Jain NC and OW Schalm (eds) Lippincott Williams & Wilkins, Philadelphia, p 891–1344
65. Tieleman BI, Dijkstra TH, Klasing KC, Visser GH, Williams JB (2008) Effects of experimentally increased costs of activity during reproduction on parental investment and self-maintenance in tropical house wrens. Behav Ecol 19:949–959. doi:
66. Van de Crommenacker J, Horrocks NPC, Versteegh MA, Tieleman BI, Komdeur J, Matson KD (2010) Effects of immune supplementation and immune challenge on oxidative status and physiology in a model bird: implications for ecologists. J Exp Biol 213:3527–3535
67. van de Pol M, Wright J (2009) A simple method for distinguishing within—versus between—subject effects using mixed models. Anim Behav 77:753–758. doi: - 作者单位：1. Animal Ecology Group, Centre for Ecological and Evolutionary Studies, University of Groningen, P.O. Box 11103, 9700 CC Groningen, The Netherlands
- ISSN：1432-1939
文摘
A central hypothesis of eco-immunology proposes trade-offs between immune defences and competing physiological and behavioural processes, leading to immunological variation within and among annual-cycle stages, as has been revealed for some species. However, few studies have simultaneously investigated patterns of multiple immune indices over the entire annual cycle in free-living birds, and none has investigated the consistency of seasonal patterns across multiple years. We quantified lysis, agglutination, haptoglobin, leukocyte profiles, and body mass in free-living skylarks (Alauda arvensis) through two complete annual cycles and within and between four breeding seasons. The skylarks’ annual cycle is characterised by annually repeated changes in energy and time budgets, social structure and diet. If trade-offs relating to these cyclic changes shape evolution, predictable intra-annual immune patterns may result. Alternatively, intra-annual immune patterns may vary among years if fluctuating environmental changes affect the cost–benefit balances of immune function. We found significant variation in immune indices and body mass across the annual cycle, and these patterns differed between years. Immune parameters differed between four breeding seasons, and in all years, lysis and agglutination increased as the season progressed independent of average levels. Population-level patterns (intra-annual, inter-annual, within breeding season) were consistent with within-individual patterns based on repeated measurements. We found little evidence for sex differences, and only haptoglobin was correlated (negatively) with body mass. We conclude that immune modulation is not simply a pre-programmed phenomenon that reflects predictable ecological changes. Instead, fluctuating environmental conditions that vary among years likely contribute to the immunological variation that we observed.