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Journal of Ornithology

, Volume 148, Supplement 2, pp 625–632 | Cite as

Food supplementation and timing of reproduction: does the responsiveness to supplementary information vary with latitude?

  • Stephan J. Schoech
  • Thomas P. Hahn
Original Article

Abstract

Food supplementation usually advances the timing of laying. Here, we report a meta-analysis of 35 food supplementation studies demonstrating that species at high latitudes are less responsive to food supplementation than those at lower latitudes. Because the length of the breeding season varies with latitude, species at high latitudes may rely mostly upon photic cues and be less responsive to other environmental information. Lower latitude species, where times suitable for breeding vary from year-to-year, are predicted to be more responsive to “supplementary” information to adjust reproduction to coincide with conditions that favor the successful rearing of young. Studies by Wingfield et al. (Gen Comp Endocrinol 101:242–255, 1996; Gen Comp Endocrinol 107:44–62, 1997; Gen Comp Endocrinol 131:143–158, 2003) suggest a physiological underpinning to this reduced responsiveness to supplementary information in high-latitude species. Given that temperature increases resulting from global climate change are most pronounced at high latitude, reduced plasticity to respond to these changes in individuals of high-latitude species could cause high-latitude breeders to be poorly synchronized with a resource base that emerges earlier than usual. If high-latitude breeders indeed lack sufficient individual-level plasticity to cope effectively with climate fluctuations, effective optimization of reproductive timing in a rapidly changing environment would require similarly rapid evolutionary change. It remains to be seen whether this will be possible.

Keywords

Adaptive specialization Conditional plasticity Environmental cues Food supplementation Timing of reproduction 

Notes

Acknowledgments

During the time when some of the ideas that led to this paper were being formulated and during the writing of the manuscript we have been supported in part by NSF grants (SJS: IBN-9722823, -0049026, and IOB-0346328; TPH: IBN-0988470, -0196093, and -0310995). N. Davies, R. Nager, A. Scheuerlein, and J. Martinez-Padilla kindly provided raw data from their studies.

References

  1. Arcese P, Smith JNM (1988) Effects of population density and supplemental food on reproduction in song sparrows. J Anim Ecol 57:119–136CrossRefGoogle Scholar
  2. Aparicio JM, Bonal R (2002) Effects of food supplementation and habitat selection on timing of lesser kestrel breeding. Ecology 83:873–877Google Scholar
  3. Arnold TW (1994) Effects of supplemental food on egg production in American coots. Auk 111:337–350Google Scholar
  4. Arnold TW (1992) Variation in laying date, clutch size, egg size, and egg composition on yellow-headed blackbirds (Xanthocephalus xanthocephalus): a supplemental feeding experiment. Can J Zool 70:1904–1911CrossRefGoogle Scholar
  5. Baker JR (1938) The evolution of breeding seasons. In: DeBeer GB (ed) Evolution: essays on aspects of evolutionary biology. Clarendon, Oxford, pp 161–177Google Scholar
  6. Ball GF (1993) The neural integration of environmental information by seasonally breeding birds. Am Zool 33:185–199Google Scholar
  7. Ball GF, Hahn TP (1997) GnRH neuronal systems in birds and their relation to the control of seasonal reproduction. In: Parhar IS, Sakuma Y (eds) GnRH neurons: gene to behavior. Brain Shuppan Publ, Tokyo, pp 325–342 Google Scholar
  8. Bentley GE, Wingfield JC, Morton ML, Ball GF (2000) Stimulatory effects on the reproductive axis in female songbirds by conspecific and heterospecific male song. Horm Behav 37:179–189PubMedCrossRefGoogle Scholar
  9. Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Insufficient responses to climate change cause population declines in a long-distance migratory bird. Nature 441:81–83PubMedCrossRefGoogle Scholar
  10. Clamens A, Isenmann P (1989) Effect of supplemental food on the breeding of blue and great tits in Mediterranean habitats. Ornis Scand 20:36–42CrossRefGoogle Scholar
  11. Cockrem JF (1995) Timing of seasonal breeding in birds, with particular reference to New Zealand birds. Reprod Fert Dev 7:1–19CrossRefGoogle Scholar
  12. Coppack T, Pulido F, Berthold P (2001) Photoperiodic response to early hatching in a migratory bird species. Oecologia 128:811–186CrossRefGoogle Scholar
  13. Davies NB, Lundberg A (1985) The influence of food on time budgets and timing of breeding of the dunnock Prunella modularis. Ibis 127:100–110CrossRefGoogle Scholar
  14. De Neve L, Soler JJ, Pérez-Contreras T, Vartin-Vivaldi M, Martinez JG (2004) Effects of a food supplementation experiment on reproductive investment and a post-mating sexually selected train in magpies Pica pica. J Avian Biol 35:246–251CrossRefGoogle Scholar
  15. Dhindsa MS, Boag DA (1990) The effect of food supplementation on the reproductive success of black-billed magpies Pica pica. Ibis 132:595–602CrossRefGoogle Scholar
  16. Eldridge JL, Krapu GL (1988) The influence of diet quality on clutch size and laying pattern in Mallards. Auk 105:102–110Google Scholar
  17. Ewald PW, Rohwer S (1982) Effects of supplemental feeding on timing of breeding, clutch size and polygyny in red-winged blackbirds Agelaius phoeniceus. J Anim Ecol 51:429–450CrossRefGoogle Scholar
  18. Hahn TP, MacDougall-Shackleton SA (2007) Adaptive specialization, conditional plasticity, and phylogenetic history in the reproductive cue response systems of birds. Philos Trans R Soc Lond B (in press)Google Scholar
  19. Hahn TP, Boswell T, Wingfield JC, Ball GF (1997) Temporal flexibility in avian reproduction: patterns and mechanisms. In: Nolan V Jr, Ketterson ED (eds) Current ornithology, vol 14. Plenum, New York, pp 39–80Google Scholar
  20. Hahn TP, Katti M, Pereyra ME, Ward G, MacDougall-Shackleton SA (2005) Effects of food availability on the reproductive system. In: Dawson A, Sharp PJ (eds) Functional avian endocrinology. Narosa Publishing House, New Delhi, pp 167–180Google Scholar
  21. Hiom L, Bolton M, Monaghan P, Worrall D (1991) Experimental evidence for food limitation of egg production in gulls. Ornis Scand 22:94–97CrossRefGoogle Scholar
  22. Hochachka WM, Boag DA (1987) Food shortage for breeding black-billed magpies (Pica pica): an experiment using supplemental food. Can J Zool 65:1270–1274CrossRefGoogle Scholar
  23. Högstedt G (1981) Effect of additional food on reproductive success in the magpie (Pica pica). J Anim Ecol 50:219–229CrossRefGoogle Scholar
  24. Hörnfeldt B, Eklund U (1990) The effect on laying date and clutch-size in Tengmalm’s owl Aegolius funereus. Ibis 132:395–406CrossRefGoogle Scholar
  25. Inouye DW, Barr B, Armitage KB, Inouye BD (2000) Climate change is affecting altitudinal migrants and hibernating species. Proc Natl Acad Sci USA 97:1630–633PubMedCrossRefGoogle Scholar
  26. Jenni L, Kéry M (2003) Timing of autumn bird migration under climate change: advances in long-distance migrants, delays in short-distance migrants. Proc R Soc Lond B 270:1467–1471CrossRefGoogle Scholar
  27. Källander H (1974) Advancement of laying of great tits by the provision of food. Ibis 116:365–367CrossRefGoogle Scholar
  28. Källander H, Karlsson J (1993) Supplemental food and laying date in the European starling. Condor 95:1031–1034CrossRefGoogle Scholar
  29. Kelly JF, Van Horne B (1997) Effects of food supplementation on the timing of nest initiation in belted kingfishers. Ecology 78:2504–2511CrossRefGoogle Scholar
  30. Knight RL (1988) Effects of supplemental food on the breeding biology of the black-billed magpie. Condor 90:956–958CrossRefGoogle Scholar
  31. Korpimäki E (1989) Breeding performance of Tengmalm’s owl Aegolius funereus: effects of supplementary feeding in a peak vole year. Ibis 131:51–56CrossRefGoogle Scholar
  32. Korpimäki E, Wiehn J (1998) Clutch size of kestrels: seasonal decline and experimental evidence for food limitation under fluctuating food conditions. Oikos 83:259–272CrossRefGoogle Scholar
  33. Lack D (1968) Ecological adaptations for breeding in birds. Chapman & Hall, LondonGoogle Scholar
  34. Martinez-Padilla J (2006) Prelaying maternal condition modifies the association between egg mass and T cell-mediated immunity in kestrels. Behav Ecol Sociobiol 60:510–515CrossRefGoogle Scholar
  35. Meijer T, Daan S, Dijkstra C (1988) Female condition and reproduction: effects of food manipulation in free-living and captive kestrels. Ardea 76:141–154Google Scholar
  36. Moore IT, Bentley GE, Wotus C, Wingfield JC (2006) Photoperiod-independent changes in immunoreactive brain gonadotropin-releasing hormone (GnRH) in a free-living, tropical bird. Brain Behav Evol 68:37–44PubMedCrossRefGoogle Scholar
  37. Nager RG, Rüegger van Noordwijk AJ (1997) Nutrient or energy limitation on egg formation: a feeding experiment in great tits. J Anim Ecol 66:495–507CrossRefGoogle Scholar
  38. Nakamura M (1995) Effects of supplemental feeding and female age on timing of breeding in the alpine accentor Prunella collaris. Ibis 137:56–63CrossRefGoogle Scholar
  39. Newton I, Marquiss M (1981) Effect of additional food on laying dates and clutch sizes of sparrowhawks. Ornis Scand 12:224–229CrossRefGoogle Scholar
  40. Nilsson J-Å (1994) Energetic bottle-necks during breeding and the reproductive cost of being too early. J Anim Ecol 63:200–208CrossRefGoogle Scholar
  41. Perrins C (1970) The timing of birds’ breeding seasons. Ibis 112:242–255CrossRefGoogle Scholar
  42. Poole A (1985) Courtship feeding and osprey reproduction. Auk 102:479–492Google Scholar
  43. Preston KL, Rotenberry JT (2006) The role of food, nest predation, and climate in timing of wren tit reproductive activities. Condor 108:832–841Google Scholar
  44. Reynolds SJ, Schoech SJ, Bowman R (2003a) Nutritional quality of prebreeding diet influences breeding performance of the Florida scrub-jay. Oecologia 134:308–316PubMedGoogle Scholar
  45. Reynolds SJ, Schoech SJ, Bowman R (2003b) Diet quality during prelaying and nestling periods influences growth and survival of Florida scrub-jay, Aphelocoma coerulescens, chicks. J Zool 261:217–226CrossRefGoogle Scholar
  46. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds A (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60PubMedCrossRefGoogle Scholar
  47. Scheuerlein A, Gwinner E (2002) Is food availability a circannual zeitgeber in tropical birds? A field experiment on stonechats in tropical Africa. J Biol Rhythms 17:171–180PubMedCrossRefGoogle Scholar
  48. Schoech SJ (1996) The effect of supplemental food on body condition and timing of reproduction in a cooperative breeder, the Florida scrub-jay. Condor 93:234–244Google Scholar
  49. Schoech SJ, Bowman R, Reynolds SJ (2004) Food supplementation and possible mechanisms underlying early breeding in the Florida Scrub-Jay (Aphelocoma coerulescens). Horm Behav 46:565–573PubMedCrossRefGoogle Scholar
  50. Silverin B (1994) Low temperature affects the photoperiodically induced LH and testicular cycles differently in closely related species of tits (Parus spp.). Horm Behav 28:199–206PubMedCrossRefGoogle Scholar
  51. Simmons RE (1993) Effects of supplementary food on density-reduced breeding in an African eagle: adaptive restraint or ecological constraint? Ibis 135:394–402CrossRefGoogle Scholar
  52. Simmons RE (1994) Supplemental food alters egg size hierarchies within harrier clutches. Oikos 71:341–348CrossRefGoogle Scholar
  53. Smith JNM, Montgomerie RD, Taitt MJ, Yom-Tov Y (1980) A winter feeding experiment on an island song sparrow population. Oecologia 47:164–170CrossRefGoogle Scholar
  54. Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. Freeman, New YorkGoogle Scholar
  55. Soler M, Soler JJ (1996) Effects of experimental food provisioning on reproduction in the jackaw Corvus monedula, a semi-colonial species. Ibis 138:377–383CrossRefGoogle Scholar
  56. SPSS (2005) SPSS for Windows, ver. 14.0. SPSS, ChicagoGoogle Scholar
  57. Thomas CD, Lennon JJ (1999) Birds extend their ranges northwards. Nature 399:213CrossRefGoogle Scholar
  58. Visser ME, van Nordwijk AJ, Tinbergen JM, Lessells CM (1998) Warmer springs lead to mis-timed reproduction in Great Tits (Parus major). Proc R Soc Lond B 265:1867–1870CrossRefGoogle Scholar
  59. von Brömssen A, Jansson C (1980) Effects of food addition to willow tit Parus montanus and crested tit P. cristatus at the time of breeding. Ornis Scand 11:173–178CrossRefGoogle Scholar
  60. Wimberger PH (1988) Food supplementation effects on breeding time and harem size in the red-winged blackbird (Agelaius phoeniceus). Auk 105:799–802Google Scholar
  61. Wingfield JC (1980) Fine temporal adjustments of reproductive function. In: Epple A, Stetson MH (eds) Avian endocrinology. Academic, New York, pp 367–389Google Scholar
  62. Wingfield JC (1983) Environmental and endocrine control of reproduction: an ecological approach. In: Mikami SI, Homma K, Wada M (eds) Avian endocrinology: environmental and ecological perspectives. Japan Scientific Society Press/Springer, Tokyo/Berlin, pp 265–288Google Scholar
  63. Wingfield JC, Farner DS (1993) Endocrinology of reproduction in wild species. Avian Biol 9:163–327Google Scholar
  64. Wingfield JC, Kenagy GJ (1991) Natural regulation of reproductive cycles. In: Schreibman M, Jones RE (eds) Vertebrate endocrinology: fundamentals and biomedical implications. Academic, New York, pp 181–241Google Scholar
  65. Wingfield JC, Hahn TP, Wada M, Astheimer LB, Schoech SJ (1996) Interrelationship of daylength and temperature in the control of gonadal development, body mass and fat depots in white-crowned sparrows, Zonotrichia leucophrys gambelii. Gen Comp Endocrinol 101:242–255PubMedCrossRefGoogle Scholar
  66. Wingfield JC, Hahn TP, Wada M, Schoech SJ (1997) Effects of day length and temperature on gonadal development, body mass and fat depots in white-crowned sparrows, Zonotrichia leucophrys pugetensis. Gen Comp Endocrinol 107:44–62PubMedCrossRefGoogle Scholar
  67. Wingfield JC, Hahn TP, Maney DL, Schoech SJ, Wada M, Morton ML (2003) Effects of temperature on photoperiodically-induced reproductive development, circulating plasma luteinizing hormone and thyroid hormones, body mass, fat deposition and molt in mountain white-crowned sparrows, Zonotrichia leucophrys oriantha. Gen Comp Endocrinol 131:143–158PubMedCrossRefGoogle Scholar
  68. Yom-Tov Y (1974) The effect of food and predation on breeding density and success, clutch size and laying date of the crow (Corvus corone L.). J Anim Ecol 43:479–498CrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2007

Authors and Affiliations

  1. 1.Department of BiologyUniversity of MemphisMemphisUSA
  2. 2.Section of Neurobiology, Physiology and BehaviorUniversity of California–DavisDavisUSA

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