Skip to main content
Log in

RETRACTED ARTICLE: Latitude affects degree of advancement in laying by birds in response to food supplementation: a meta-analysis

  • Concepts, Reviews and Syntheses
  • Published:
Oecologia Aims and scope Submit manuscript

This article was retracted on 01 May 2012

Abstract

Food supplementation experiments have provided considerable information about the importance of resource availability in timing reproduction. Supplemented birds usually advance breeding over non-supplemented controls. Initial observations suggested that degree of advancement in studies conducted at higher latitudes was less than in those at lower latitudes. We hypothesized that birds at high latitudes are less responsive to the “supplementary” cue of food. We tested this hypothesis using a literature-based meta-analysis of 36 papers which, because several papers presented separate data sets from different years, yielded 56 “studies.” We used step-wise regression to determine whether latitude, elevation, the duration of supplementation, and the migratory status of the species predicted the degree to which mean clutch initiation dates of food supplemented birds differed from non-supplemented controls (i.e., effect size = \(\overline {\text{X}} _{{{\text{cnt}}}} - \overline {\text{X}} _{{{\text{suppl}}}}\)). Consistent with our predictions, there was a significant inverse relationship between effect size and latitude: elevation, migratory status, and duration of treatment contributed little to the model. Because the response of animals’ reproductive systems to environmental information is mediated by the neuroendocrine system, we discuss two models: (1) the adaptive specialization hypothesis in which higher latitude species that experience a relatively short breeding season have evolved a reliance on photic cues while exhibiting reduced sensitivity to non-photic cues; and (2) the conditional plasticity hypothesis in which an individual might show a marked response to non-photic information if it lived at low latitudes, but be largely driven by photic cues, endogenous rhythms, or both to the relative exclusion of non-photic information if it lived at higher latitudes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Aparicio JM, Bonal R (2002) Effects of food supplementation and habitat selection on timing of lesser kestrel breeding. Ecology 83:873–877

    Article  Google Scholar 

  • Arcese P, Smith JNM (1988) Effects of population density and supplemental food on reproduction in song sparrows. J Anim Ecol 57:119–136

    Article  Google Scholar 

  • Amar A, Redpath SM (2002) Determining the cause of hen harrier decline on the islands: an experimental test of two hypotheses. Anim Conserv 5:21–28

    Article  Google Scholar 

  • 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 70:1904–1911

    Article  Google Scholar 

  • Arnold TW (1994) Effects of supplemental food on egg production in American coots. Auk 111:337–350

    Google Scholar 

  • Baker JR (1938) The evolution of breeding seasons. In: DeBeer GB (ed) Evolution: essays on aspects of evolutionary biology. Clarendon Press, Oxford, pp 161–177

    Google Scholar 

  • Ball GF (1993) The neural integration of environmental information by seasonally breeding birds. Am Zool 33:185–199

    Google Scholar 

  • 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. Shuppan, Tokyo, pp 325–342

    Google Scholar 

  • 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 37:179–189

    Article  PubMed  CAS  Google Scholar 

  • Both C, Bouwhuls S, Lessells CM, Visser ME (2006) Insufficient responses to climate change cause population declines in a long-distance migratory bird. Nature 44:81–83

    Article  Google Scholar 

  • Clamens A, Isenmann P (1989) Effect of supplemental food on the breeding of blue and great tits in Mediterranean habitats. Ornis Scand 20:36–42

    Article  Google Scholar 

  • Cockrem JF (1995) Timing of seasonal breeding in birds, with particular reference to New Zealand birds. Reprod Fertil Dev 7:1–19

    Article  PubMed  CAS  Google Scholar 

  • Davies NB, Lundberg A (1985) The influence of food on time budgets and timing of breeding of the dunnock Prunella modularis. Ibis 127:100–110

    Article  Google Scholar 

  • Dawson A (2002) Photoperiodic control of the annual cycle in birds and comparison with mammals. Ardea 90:355–367

    Google Scholar 

  • Dhindsa MS, Boag DA (1990) The effect of food supplementation on the reproductive success of black-billed magpies Pica pica. Ibis 132:595–602

    Article  Google Scholar 

  • Eldridge JL, Krapu GL (1988) The influence of diet quality on clutch size and laying pattern in mallards. Auk 105:102–110

    Google Scholar 

  • 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 51:429–450

    Article  Google Scholar 

  • Farner DS, Gwinner E (1980) Photoperiodicity, circannual and reproductive cycles. In: Epple A, Stetson MH (eds) Avian endocrinology. Academic Press, New York, pp 331–366

    Google Scholar 

  • Farner DS, Wilson AC (1957) A quantitative examination of testicular growth in the white-crowned sparrow. Biol Bull 113:254–267

    Article  Google Scholar 

  • Farner DS, Donham RS, Moore MC (1981) Induction of testicular development in house sparrows, Passer domesticus, and white-crowned sparrows, Zonotrichia leucophrys gambelii, with very long days and continuous light. Physiol Zool 54:372–378

    CAS  Google Scholar 

  • Follett BK, Nicholls TP (1984) Photorefractoriness in Japanese quail: possible involvement of the thyroid gland. J Exp Zool 232:573–580

    Article  PubMed  CAS  Google Scholar 

  • Gwinner E (1986) Circannual rhythms. Springer, Berlin

    Book  Google Scholar 

  • Hahn TP, MacDougall-Shackleton SA (2008) Adaptive specialization, conditional plasticity, and phylogenetic history in the reproductive cue response systems of birds. Philos Trans Roy Soc B 363:267–286

    Article  Google Scholar 

  • Hahn TP, Boswell T, Wingfield JC, Ball GF (1997) Temporal flexibility in avian reproduction: patterns and mechanisms. In: Nolan V Jr, Ketterson E (eds) Current ornithology, vol 14. Plenum, New York, pp 39–80

    Google Scholar 

  • 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, New Delhi, pp 167–180

    Google Scholar 

  • Hiom L, Bolton M, Monaghan P, Worrall D (1991) Experimental evidence for food limitation of egg production in gulls. Ornis Scand 22:94–97

    Article  Google Scholar 

  • Hochachka WM, Boag DA (1987) Food shortage for breeding black-billed magpies (Pica pica): an experiment using supplemental food. Can J Zool 65:1270–1274

    Article  Google Scholar 

  • Högstedt G (1981) Effect of additional food on reproductive success in the magpie (Pica pica). J Anim Ecol 50:219–229

    Article  Google Scholar 

  • Hörnfeldt B, Eklund U (1990) The effect on laying date and clutch-size in Tengmalm’s owl Aegolius funereus. Ibis 132:395–406

    Article  Google Scholar 

  • Inouye DW, Barr B, Armitage KB, Inouye BD (2000) Climate change is affecting altitudinal migrants and hibernating species. Proc Natl Acad Sci USA 97:1630–1633

    Article  PubMed  CAS  Google Scholar 

  • Jacobs JD, Wingfield JC (2000) Endocrine control of life-cycle stages: a constraint on response to the environment? Condor 102:35–51

    Article  Google Scholar 

  • 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 270:1467–1471

    Article  Google Scholar 

  • Källander H (1974) Advancement of laying of great tits by the provision of food. Ibis 116:365–367

    Article  Google Scholar 

  • Källander H, Karlsson J (1993) Supplemental food and laying date in the European starling. Condor 95:1031–1034

    Article  Google Scholar 

  • Kelly JF, Van Horne B (1997) Effects of food supplementation on the timing of nest initiation in belted kingfishers. Ecology 78:2504–2511

    Article  Google Scholar 

  • Knight RL (1988) Effects of supplemental food on the breeding biology of the black-billed magpie. Condor 90:956–958

    Article  Google Scholar 

  • Korpimäki E (1989) Breeding performance of Tengmalm’s owl Aegolius funereus: effects of supplementary feeding in a peak vole year. Ibis 131:51–56

    Article  Google Scholar 

  • Korpimäki E, Wiehn J (1998) Clutch size of kestrels: seasonal decline and experimental evidence for food limitation under fluctuating food conditions. Oikos 83:259–272

    Article  Google Scholar 

  • Lack D (1968) Ecological adaptations for breeding in birds. Chapman and Hall, London

  • Lambrechts MM, Perret P (2000) A long photoperiod overrides non-photoperiodic factors in blue tits’ timing of reproduction. Proc R Soc Lond B 267:585–588

    Article  CAS  Google Scholar 

  • Lofts B, Murton RK (1968) Photoperiodic and physiological adaptations regulating avian breeding cycles and their ecological significance. J Zool Lond 155:327–394

    Article  Google Scholar 

  • Marshall AJ (1959) Internal and environmental control of breeding. Ibis 101:456–478

    Article  Google Scholar 

  • Martinez-Padilla J (2006) Prelaying maternal condition modifies the association between egg mass and T cell-mediated immunity in kestrels. Behav Ecol Sociobiol 60:510–515

    Google Scholar 

  • McDougall-Shackleton SA, Pereyra ME, Hahn TP (2005) GnRH, photorefractoriness, and breeding schedules of cardueline finches. In: Dawson A, Sharp PJ (eds) Functional avian endocrinology. Narosa, New Deli, pp 97–110

    Google Scholar 

  • Meijer T, Daan S, Dijkstra C (1988) Female condition and reproduction: effects of food manipulation in free-living and captive kestrels. Ardea 76:141–154

    Google Scholar 

  • 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 68:37–44

    Article  PubMed  Google Scholar 

  • Nager RG, Rüegger, van Noordwijk AJ (1997) Nutrient or energy limitation on egg formation: a feeding experiment in great tits. J Anim Ecol 66:495–507

  • Nakamura M (1995) Effects of supplemental feeding and female age on timing of breeding in the alpine accentor Prunella collaris. Ibis 137:56–63

    Google Scholar 

  • Newton I, Marquiss M (1981) Effect of additional food on laying dates and clutch sizes of sparrowhawks. Ornis Scand 12:224–229

    Article  Google Scholar 

  • Nicholls TP, Goldsmith AR, Dawson A (1988) Photorefractoriness in birds and comparison with mammals. Physiol Rev 68:133–176

    PubMed  CAS  Google Scholar 

  • Nilsson J-Å (1994) Energetic bottle-necks during breeding and the reproductive cost of being too early. J Anim Ecol 63:200–208

    Article  Google Scholar 

  • Perrins C (1970) The timing of birds’ breeding seasons. Ibis 112:242–255

    Article  Google Scholar 

  • Preston KL, Rotenberry JT (2006) The role of food, nest predation, and climate in timing of wrentit reproductive activities. Condor 108:832–841

    Article  Google Scholar 

  • Poole A (1985) Courtship feeding and osprey reproduction. Auk 102:479–492

    Google Scholar 

  • Reynolds SJ, Schoech SJ, Bowman R (2003a) Nutritional quality of prebreeding diet influences breeding performance of the Florida scrub-jay. Oecologia 134:308–316

    PubMed  Google Scholar 

  • 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 Lond 261:217–226

    Article  Google Scholar 

  • 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 17:171–180

    Article  PubMed  Google Scholar 

  • Schoech SJ (1996) The effect of supplemental food on body condition and the timing of reproduction in a cooperative breeder, the Florida scrub-jay. Condor 98:234–244

    Article  Google Scholar 

  • Schoech SJ, Bowman R, Reynolds SJ (2004) Food supplementation and possible mechanisms underlying early breeding in the Florida Scrub-Jay (Aphelocoma coerulescens). Horm Behav 46:565–573

    Article  PubMed  CAS  Google Scholar 

  • Silverin B, Viebke PA (1994) Low temperature affects the photoperiodically induced LH and testicular cycles differently in closely related species of tits (Parus spp.). Horm Behav 28:199–206

    Article  PubMed  CAS  Google Scholar 

  • Smith JNM, Montgomerie RD, Taitt MJ, Yom-Tov Y (1980) A winter feeding experiment on an island song sparrow population. Oecologia 47:164–170

    Article  Google Scholar 

  • Soler M, Soler JJ (1996) Effects of experimental food provisioning on reproduction in the jackaw Corvus monedula, a semi-colonial species. Ibis 138:377–383

    Article  Google Scholar 

  • SPSS (2005) SPSS for Windows, version 14.0. SPSS, Chicago

    Google Scholar 

  • 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 265:1867–1870

    Article  Google Scholar 

  • 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 11:173–178

    Article  Google Scholar 

  • Wimberger PH (1988) Food supplementation effects on breeding time and harem size in the red-winged blackbird (Agelaius phoeniceus). Auk 105:799–802

    Google Scholar 

  • Wingfield JC (1980) Fine temporal adjustments of reproductive function. In: Epple A, Stetson MH (eds) Avian endocrinology. Academic Press, New York, pp 367–389

    Google Scholar 

  • 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 265–288

    Google Scholar 

  • Wingfield JC, Farner DS (1993) Endocrinology of reproduction in wild species. Avian Biol 9:163–327

    Google Scholar 

  • Wingfield JC, Kenagy GJ (1991) Natural regulation of reproductive cycles. In: Schreibman M, Jones RE (eds) Vertebrate endocrinology: fundamentals and biomedical implications. Academic Press, New York, pp 181–241

    Google Scholar 

  • Wingfield JC, Hahn TP, Levin RN, Honey P (1992) Environmental predictability and control of gonadal cycles in birds. J Exp Zool 261:214–231

    Article  Google Scholar 

  • 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 101:242–255

    Article  PubMed  CAS  Google Scholar 

  • 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 107:44–62

    Article  PubMed  CAS  Google Scholar 

  • 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 131:143–158

    Article  PubMed  CAS  Google Scholar 

  • Woolfenden GE, Fitzpatrick JW (1984) The Florida scrub jay: demography of a cooperative-breeding bird. Princeton University Press, New Jersey

    Google Scholar 

  • Wolfson A (1959) The role of light and darkness in the regulation of spring migration and reproductive cycles in birds. In: Withrow RB (ed) Photoperiodism. American Association for the Advancement of Science, publication no. 55. American Association for the Advancement of Science, Washington, pp 679–716

  • 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 43:479–498

    Article  Google Scholar 

Download references

Acknowledgements

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 (S. J. S., IBN-9722823, IBN-0049026, and IOB-0346328; T. P. H., IBN-0988470, IBN-0196093, and IBN-0310995). L. Robinson at UM assisted with our understanding of the statistics of meta-analysis. N. Davies, R. Nager, A. Scheuerlein, and J. Martinez-Padilla kindly provided data from their studies that allowed calculation of effect sizes. Thanks to E. Bridge who provided support in many ways and the Animal Behaviour Group of McMaster University who offered constructive input to the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephan J. Schoech.

Additional information

Communicated by Craig Osenberg.

This article has been retracted due to copyright violation.

The retraction note to this article can be found online at http://dx.doi.org/10.1007/s00442-012-2345-5.

Electronic supplementary material

Below is the link to the Electronic supplementary material.

MOESM1 (XLS 35 kb)

About this article

Cite this article

Schoech, S.J., Hahn, T.P. RETRACTED ARTICLE: Latitude affects degree of advancement in laying by birds in response to food supplementation: a meta-analysis. Oecologia 157, 369–376 (2008). https://doi.org/10.1007/s00442-008-1091-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-008-1091-1

Keywords

Navigation