Cost of reproduction in a long-lived bird: Incubation effort reduces immune function and future reproduction

Proceedings of the Royal Society B: Biological Sciences

Volumn 272, Issue 1567, 2005, Pages 1039-1046

  Hanssen, Sveinn Are ^a,b,c   Hasselquist, Dennis ^b   Folstad, Ivar ^a   Erikstad, Kjell Einar ^a,c  

^a UNIVERSITY OF TROMSØ   (Norway)

^b LUND UNIVERSITY   (Sweden)

^c NORWEGIAN INSTITUTE FOR NATURE RESEARCH   (Norway)

Author keywords

Immune function; Incubation cost; Life history; Precocial; Seabird; Trade off

Indexed keywords

FECUNDITY; IMMUNOCOMPETENCE; INCUBATION; LIFE HISTORY THEORY; REPRODUCTIVE COST; TRADE-OFF;

ANIMAL EXPERIMENT; ANTIBODY TITER; ARTICLE; BIRD; BREEDING; COST; DIPHTHERIA; ENZYME LINKED IMMUNOSORBENT ASSAY; HEMAGGLUTINATION TEST; IMMUNE SYSTEM; INCUBATION TIME; LIFE HISTORY; NONHUMAN; PRIORITY JOURNAL; REPRODUCTION; TETANUS;

AVES; SOMATERIA MOLLISSIMA;

EID: 21744444108     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2005.3057     Document Type: Article

References (85)

1. Baillie, C. D. & Milne, H. 1982 The influence of female age on breeding in the common eider Somateria mollissima. Bird Study 29, 55-66.
2. Biebach, H. 1981 Energetic costs of incubation on different clutch sizes in starlings (Sturnus vulgaris). Ardea 69, 141-142.
3. Biebach, H. 1984 Effect of clutch size and time of day on the energy expenditure of incubating starlings (Sturnus vulgaris). Physiol. Zool. 57, 26-31.
4. Bruun, M. 2002 On starlings and farming: population decline, foraging strategies, cost of reproduction and breeding success. Doctoral dissertation, Department of Ecology, Animal Ecology, Lund University, Sweden.
5. Bustnes, J. O. & Erikstad, K. E. 1991 Parental care in the common eider (Somateria mollissima): factors affecting abandonment and adoption of young. Can. J. Zool. 69, 1538-1545.
6. Charlesworth, B. 1980 Evolution in age-structured populations. Cambridge: Cambridge University Press.
7. Charnow, E. L. & Krebs, J. R. 1974 On clutch size and fitness. Ibis 116, 217-219.
8. Cichon, M. 2000 Costs of incubation and immunocompetence in the collared flycatcher. Oecologia 125, 453-457.
9. Glutton-Brock, T. H. 1984 Reproductive effort and terminal investment in iteroparous animals. Am. Nat. 123, 212-229.
10. Coleman, R. M. & Gross, M. R. 1991 Parental investment theory: the role of past investment. Trends Ecol. Evol. 6, 404-406.
11. Coleman, R. M. & Whittall, D. 1988 Clutch size and the cost of incubation in the Bengalese finch (Lonchura striata var. domestica). Behav. Ecol. Sociobiol. 23, 367-372.
12. Deerenberg, C., Apanius, V., Daan, S. & Bos, N. 1997 Reproductive effort decreases antibody responsiveness. Proc. R. Soc. B 264, 1021-1029.
13. Dein, J. 1986 Hematology. In Clinical avian medicine (ed. G. J. Harrison & W. R. Harrison), pp. 178-191. London: Saunders.
14. Dijkstra, C., Bult, A., Bijlsma, S., Daan, S., Meijer, T. & Zijlstra, M. 1990 Brood size manipulation in the kestrel (Falco tinnunculus): effects on offspring and parent survival. J. Anim. Ecol. 59, 269-285.
15. Dufva, R. & Allander, K. 1995 Intraspecific variation in plumage colouration reflects immune response in great tits (Parus major). Funct. Ecol. 9, 786-789.
16. Eadie, J. McA. & Lyon, B. E. 1998 Cooperation, conflict, and creching behaviour in goldeneye ducks. Am. Nat. 151, 397-408.
17. Engstrand, S. M. & Bryant, D. M. 2002 A trade-off between clutch size and incubation efficiency in the barn swallow Hirundo rustica. Funct. Ecol. 16, 782-791.
18. Erikstad, K. E. & Tveraa, T. 1995 Does the cost of incubation set limits to clutch size in common eiders Somateria mollissima? Oecologia 103, 270-274.
19. Erikstad, K. E., Fauchald, P., Tveraa, T. & Steen, H. 1998 On the cost of reproduction in long-lived birds: the influence of environmental variability. Ecology 79, 1781-1788.
20. Fitzgerald, L. 1988 Exercise and the immune system. Immunol. Today 9, 337-339.
21. Folstad, I. & Karter, A. J. 1992 Parasites, bright males and the immunocompetence handicap. Am. Nat. 139, 603-622.
22. Golet, G. H., Irons, D. B. & Estes, J. A. 1998 Survival costs of chick rearing in black-legged kittiwakes. J. Anim. Ecol. 59, 269-285.
23. 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.
24. Gustafsson, L., Nordling, D., Andersson, M. S., Sheldon, B. C. & Quarnstrøm, A. 1994 Infectious disease, reproductive effort and the cost of reproduction in birds. Phil. Trans. R. Soc. B 346, 323-331.
25. Haftorn, S. & Reinertsen, R. E. 1985 The effect of temperature and clutch size on the energetic cost of incubation in a free-living blue tit Parus caeruleus. Auk 102, 470-478.
26. Hanssen, S. A., Erikstad, K. E., Johnsen, V. & Bustnes, J. O. 2003a Differential investment and costs during avian incubation determined by individual quality: an experimental study of the common eider Somateria mollissima. Proc. R. Soc. B 270, 531-537.
27. Hanssen, S. A., Folstad, I. & Erikstad, K. E. 2003 Reduced immunocompetence and cost of reproduction in common eiders. Oecologia 136, 457-464.
28. Hanssen, S. A., Folstad, L, Erikstad, K. E. & Oksanen, A. 2003c Costs of parasites in common eiders: effects of antiparasite treatment. Oikos 100, 105-111.
29. Hanssen, S. A., Hasselquist, D., Folstad, I. & Erikstad, K. E. 2004 Costs of immunity: immune responsiveness reduces survival in a vertebrate. Proc. R. Soc. B 271, 925-930.
30. Hasselquist, D., Marsh, J. A., Sherman, P. W. & Wingfield, J. C. 1999 Is avian humoral immunocompetence suppressed by testosterone? Behav. Ecol. Sociobiol. 45, 167-175.
31. Hasselquist, D., Wasson, M. F. & Winkler, D. W. 2001 Humoral immunocompetence predicts date of egg-laying and reflects female quality in tree swallows. Behav. Ecol. 12, 93-97.
32. Hay, L. & Hudson, F. C. 1989 Practical immunology. Oxford: Blackwell.
33. Heaney, V. & Monaghan, P. 1995 A within-clutch trade-off between egg production and rearing in birds. Proc. R. Soc. B 261, 361-365.
34. Heaney, V. & Monaghan, P. 1996 Optimal allocation of effort between reproductive phases: the trade-off between incubation costs and subsequent brood rearing capacity. Proc. R. Soc. B 263, 1719-1724.
35. Horak, P. 2003 When to pay the cost of reproduction? A brood size manipulation experiment in great tits (Parus major). Behav. Ecol. Sociobiol. 54, 105-112.
36. Ilmonen, P., Taarna, T. & Hasselquist, D. 2002 Are incubation costs in female pied flycatchers expressed in humoral immune responsiveness or breeding success? Oecologia 130, 199-204.
37. Ilmonen, P., Hasselquist, D., Langefors, Å. & Wiehn, J. 2003 Stress, immunocompetence and leucocyte profiles of pied flycatchers in relation to brood size manipulation. Oecologia 136, 148-154.
38. Jacobsen, K. O., Erikstad, K. E. & Ssether, B. E. 1995 An experimental study of the costs of reproduction in the kittiwake (Rissa tridactyla). Ecology 76, 1636-1642.
39. Jones, G. 1987 Time and energy constraints during incubation in free-living swallows (Hirundo rustica): an experimental study using precision electronic balance. J. Anim. Ecol. 56, 229-245.
40. Kehoe, F. P. 1989 The adaptive significance of crèching behaviour in the white-winged scoter (Melanitta fusca deglandi). Can. J. Zool. 67, 406-411.
41. Larsen, V. A., Lislevand, T. & Byrkjedal, I. 2003 Is clutch size limited by incubation ability in northern lapwings? J. Anim. Ecol. 72, 784-792.
42. Lazarus, J. & Inglis, I. R. 1978 The breeding behaviour of the pink-footed goose: parental care and vigilant behaviour during the fledging period. Behaviour 65, 62-88.
43. Lazarus, J. & Inglis, I. R. 1986 Shared and unshared parental investment, parent-offspring conflict and brood size. Anim. Behav. 34, 1791-1804.
44. Lehmann, T. 1993 Ectoparasites: direct impact on host fitness. Parasitol. Today 9, 8-13.
45. Lessells, C. M. 1991 The evolution of life histories. In Behavioural ecology. An evolutionary approach (ed. J. R. Krebs & N. B. Davies), pp. 32-68. Oxford: Blackwell.
46. Lessells, C. M. & Boag, P. T. 1987 Unrepeatable repeat-abilities: a common mistake. Auk 104, 116-121.
47. Linden, M. & Møller, A. P. 1989 Cost of reproduction covariation of life history traits in birds. Trends Ecol. Evol. 4, 367-371.
48. Lochmiller, R. L. & Deerenberg, C. 2000 Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87-98.
49. Maxwell, M. H. 1993 Avian blood leucocyte responses to stress. Worlds Poult. Sci. J. 49, 34-43.
50. Minchella, D. J. & Loverde, PT. 1981 A cost of increased early reproductive effort in the snail Biomphalaria glabrata. Am. Nat. 118,876-881.
51. Møller, A. P 1997 Parasitism and the evolution of host life history. In Host-parasite evolution (ed. D. H. Clayton & J. Moore), pp. 105-127. Oxford: Oxford University Press.
52. Monaghan, P & Nager, R. 1997 Why don't birds lay more eggs? Trends Ecol. Evol. 12, 270-274.
53. Moreno, J. & Carlson, A. 1989 Clutch size and the costs of incubation in the pied flycatcher Ficedula hypoleuca. Ornis Scand. 20, 123-128.
54. Moreno, J. & Sanz, J. J. 1994 The relationship between energy expenditure during incubation and clutch size in the pied flycatcher Ficedula hypoleuca. J. Avian Biol. 25, 125-130.
55. Moreno, J., Gustafsson, L., Carlson, A. & Pärt, T. 1991 The cost of incubation in relation to clutch-size in the collared flycatcher Ficedula albicollis. Ibis 133, 186-193.
56. Moreno, J., Sanz, J. J. & Arriero, E. 1999 Reproductive effort and T-lymphocyte cell-mediated immunocompetence in female pied flycatchers Ficedula hypoleuca. Proc. R. Soc. B 266, 1105-1109.
57. Munro, J. & Bédard, J. 1977 Crèche formation in the common eider. Auk 94, 759-771.
58. Nordling, D., Andersson, M., Zohari, S. & Gustafsson, L. 1998 Reproductive effort reduces specific immune response and parasite resistance. Proc. R. Soc. B 265, 1291-1298.
59. Parker, H. & Holm, H. 1990 Patterns of nutrient and energy expenditures in female common eider nesting in the high Arctic. Auk 107, 660-668.
60. Pugesek, B. H. & Diem, K. L. 1990 The relationship between reproduction and survival in known-age California gulls. Ecology 71, 811-817.
61. Raberg, L. & Stjernman, M. 2003 Natural selection on immune responsiveness in blue tits Parus caerukus. Evolution 57, 1670-1678.
62. Råberg, L., Grahn, M., Hasselquist, D. & Svensson, E. 1998 On the adaptive significance of stress-induced immunosuppression. Proc. R. Soc. B 265, 1637-1641.
63. Råberg, L., Nilsson, J. Å. . . , Ilmonen, P., Stjernman, M. & Hasselquist, D. 2000 The cost of an immune response: vaccination reduces parental effort. Ecol. Lett. 3, 382-386.
64. Reid, W. V. 1987 The cost of reproduction in the glaucous-winged gull. Oecologia 74, 458-467.
65. Reid, J. M., Monaghan, P. & Ruxton, G. D. 2000a Resource allocation between reproductive phases: the importance of thermal conditions in determining the cost of incubation. Proc. R. Soc. B 267, 37-41.
66. Reid, J. M., Monaghan, P. & Ruxton, G. D. 2000b The consequences of clutch size for incubation conditions and hatching success in starlings. Funct. Ecol. 14, 560-565.
67. Roff, D. A. 1992 The evolution of life histories. New York: Chapman & Hall.
68. Saino, N., Incagli, M., Martinelli, R. & Møller, A. P. 2002 Immune response of male barn swallows in relation to parental effort, corticosterone plasma levels, and sexual ornamentation. Behav. Ecol. 13, 169-174.
69. SAS Institute Inc. 1999 SAS OnlineDoc®, version 8. Cary, NC: SAS Institute Inc.
70. Sheldon, B. C. & Verhulst, S. 1996 Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11, 317-321.
71. Siegel, H. S. 1985 Immunological responses as indicators of stress. World's Poult. Sci. 41, 36-44.
72. Siikamäki, P. 1995 Are large clutches costly to incubate-the case of the pied flycatcher? J. Avian Biol. 26, 76-80.
73. Skarstein, F. & Folstad, I. 1996 Sexual dichromatism and the immunocompetence handicap: an observational approach using Arctic charr. Oikos 76, 359-367.
74. Smith, H. G. 1989 Larger clutches take longer to incubate. Ornis Scand. 20, 156-158.
75. Stearns, S. C. 1992 The evolution of life histories. Oxford: Oxford University Press.
76. Székely, T., Karsai, I. & Williams, T. D. 1994 Determination of clutch-size in the Kentish plover Charadrius alexandrinus. Ibis 136, 341-348.
77. Tamer, P. & Bryant, D. M. 1993 Interspecific variation in daily energy expenditure during avian incubation. J. Zool. 231, 215-232.
78. Thomson, D. L., Monaghan, P. & Furness R. W. 1998 The demands of incubation and avian clutch size. Biol. Rev. 73, 293-304.
79. Trivers, R. L. 1972 Parental investment and sexual selection. In Sexual selection and the descent of man (ed. B. Campbell), pp. 1871-1971. London: Heinemann.
80. Visser, M. E. & Lessells, C. M. 2001 The costs of egg production and incubation in great tits (Parus major). Proc. R. Soc. B 268, 1271-1277.
81. Watson, M. D., Robertson, G. J. & Cooke, F. 1993 Egg laying time and laying interval in the common eider. Condor 95, 869-878.
82. Westneat, D. F., Hasselquist, D. & Wingfield, J. C. 2003 Humoral immune response of free-living red-winged blackbirds (Age-laius phoeniceus): no association with plumage, testosterone, or reproductive success. Behav. Ecol. Sociobiol. 53, 315-323.
83. Williams, G. C. 1966 Natural selection, the cost of reproduction, and a refinement of Lack's principle. Am. Nat. 100, 687-690.
84. Wooller, R. D., Bradley, J. S. & Croxall, J. P. 1992 Long-term population studies of seabirds. Trends Ecol. Evol. 100, 111-114.
85. Yoccoz, N. G., Erikstad, K. E., Bustnes, J. O., Hanssen, S. A. & Tveraa, T. 2002 Costs of reproduction in common eiders (Somateria mollissima): an assessment of relationships between reproductive effort and future survival and reproduction based on observational and experimental studies. J. Appl. Stat. 29, 57-64.