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Oecologia

, Volume 166, Issue 1, pp 79–90 | Cite as

Coping with uncertainty: breeding adjustments to an unpredictable environment in an opportunistic raptor

  • Fabrizio SergioEmail author
  • J. Blas
  • L. López
  • A. Tanferna
  • R. Díaz-Delgado
  • J. A. Donázar
  • F. Hiraldo
Population ecology - Original Paper

Abstract

No environment is truly constant in time. As a result, animals have evolved multiple adjustments to cope with such fluctuations. However, the allocation of effort to costly activities that imply long-term commitments, such as breeding, may be extremely challenging when future resources change constantly and unpredictably, a context that has received little investigation. To fill this gap, we studied the breeding response by a wetland-dependent raptor, the black kite Milvus migrans, to within and between-years fluctuations in resource availability (inundation levels). The breeding performance of the population was decomposed into reproductive components expressed in a sequence of successive tasks along the breeding cycle (e.g. timing of laying, clutch size, hatching success, brood reduction). Variation in each component was related to resource levels observed at different key dates of the season in order to test whether and when population-level reproduction was adjusted to available resources. Along a 22-year time-series, inundation levels fluctuated unpredictably within and among years, and mostly affected the later components of kites’ reproduction, such as hatching success and the incidence of brood reduction, which were the main determinants of the population yearly breeding output. Results were consistent with multiple adjustments to cope with uncertainty. As the season progressed and resources became easier to assess, a bet-hedging waiting strategy based on a conservatively small, invariant and asynchronous clutch gave way to real-time resource-tracking mechanisms mediated by progressive adjustments to current prey availability, so that population-level breeding rates were determined and tuned to resources rather late in the season. Such adjustments were the likely outcome of the interaction between parental tactics and environmental constraints. Behavioural flexibility, such as dietary opportunism, probably promoted further resistance to resource oscillations. Given that all ecosystems show some degree of unpredictability, resource-tracking adjustments, such as the ones depicted here, are likely to be commonplace in most communities.

Keywords

Brood reduction Environmental uncertainty Hydrology Inundation-rates Resource fluctuations Water-levels 

Notes

Acknowledgments

We thank F.G. Vilches, R. Baos, S. Cabezas, M.G. Forero, G. García, L. García, J. Giralt, M. Guerrero and A. Sánchez for help in the field. We thank H. Pietiäinen, J. Valkama and an anonymous reviewer for comments on a previous draft of the manuscript. Data on rabbits road-transects were kindly provided by the “Equipo de Seguimiento de Procesos Naturales” of the Estación Biológica de Doñana. Part of this study was funded by the research projects CGL2008-01781 of the Ministerio de Ciencia e Innovación, JA-58 of the Consejería de Medio Ambiente de la Junta de Andalucía and by the Excellence Project RNM 1790 and RNM 03822 of the Junta de Andalucía to F.S.

Supplementary material

442_2010_1795_MOESM1_ESM.pdf (57 kb)
Supplementary material 1 (PDF 57 kb)
442_2010_1795_MOESM2_ESM.pdf (284 kb)
Supplementary material 2 (PDF 284 kb)

References

  1. Béchet A, Johnson AR (2008) Anthropogenic and environmental determinants of Greater Flamingo Phoeniricus roseus breeding numbers and productivity in the Camargue (Rhone delta, southern France). Ibis 150:69–79CrossRefGoogle Scholar
  2. Béchet A, Germain C, Sandoz A, Hirons GJM, Green RE, Walmsley JG, Johnson AR (2009) Assessment of the impacts of hydrological fluctuations and salt pans abandonment on Greater flamingoes in the Camargue, South of France. Biodivers Conserv 18:1575–1588CrossRefGoogle Scholar
  3. Beissinger SR (1986) Demography, environmental uncertainty, and the evolution of mate desertion in the snail kite. Ecology 67:1445–1459CrossRefGoogle Scholar
  4. Beissinger SR (1995) Modelling extinction in periodic environments: Everglades water levels and snail kite population viability. Ecol Appl 5:618–631CrossRefGoogle Scholar
  5. Beja P, Santos CD, Santana J, Pereira, MJ, Marques JT, Queiroz HL, Palmeirim JM (2010) Seasonal patterns of spatial variation in understory bird assemblages across a mosaic of flooded and unflooded Amazonian forests. Biodivers Conserv 19:129–152Google Scholar
  6. Bennets RE, Kitchens WM, Dreitz VJ (2002) Influence of an extreme high water event on survival, reproduction, and distribution of snail kites in Florida, USA. Wetlands 22:366–373CrossRefGoogle Scholar
  7. Blas J, Sergio F, Hiraldo F (2009) Age-related improvement in reproductive performance in a long-lived raptor: a cross-sectional and longitudinal study. Ecography 32:647–657CrossRefGoogle Scholar
  8. Bren LJ (1992) Tree invasion of an intermittent wetland in relation to changes in the flooding frequency of the River Murray, Australia. Aust J Ecol 17:395–408CrossRefGoogle Scholar
  9. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information–theoretic approach. Springer, New YorkGoogle Scholar
  10. Bustamante J, Pacios F, Díaz-Delgado R, Aragonés D (2009) Predictive models of turbidity and water depth in the Doñana marshes using Landsat TM and ETM+ images. J Environ Manage 90:2219–2225PubMedCrossRefGoogle Scholar
  11. Clutton-Brock TH (ed) (1988) Reproductive success. University of Chicago Press, ChicagoGoogle Scholar
  12. Crawley MJ (1993) GLIM for ecologists. Blackwell, OxfordGoogle Scholar
  13. Crawley MJ (2007) The R book. Wiley, ChichesterCrossRefGoogle Scholar
  14. Díaz-Delgado R, Bustamante J, Aragonés D, Pacios F (2006) Determining water body characteristics of Doñana shallow marshes through remote sensing. In: Proceedings of the 2006 IEEE International Geoscience and Remote Sensing Symposium and 27th Canadian Symposium Remote Sensing (IGARSS2006). Geoscience and Remote Sensing Society, Denver, pp 3662–3664Google Scholar
  15. Fargallo JA, Martínez-Padilla J, Viñuela J, Blanco J, Torre I, Vergara P, De Neve L (2009) Kestrel-prey dynamic in a Mediterranean region: the effect of generalist predation and climatic factors. PLoS ONE 4:e4311. doi: 10.1371/journal.pone.0004311 PubMedCrossRefGoogle Scholar
  16. García F, Marín C (2006) Doñana: water and biosphere. Spanish Ministry of the Environment, MadridGoogle Scholar
  17. Goodman D (1979) Regulating reproductive effort in a changing environment. Am Nat 113:735–748CrossRefGoogle Scholar
  18. Grant PR (1999) Ecology and evolution of Darwin’s finches. Princeton University press, PrincetonGoogle Scholar
  19. Harris MB, Tomas W, Mourão G, Da Silva CJ, Guimarães E, Sonoda F, Fachim E (2005) Safeguarding the Pantanal wetlands: threats and conservation initiatives. Conserv Biol 19:714–720CrossRefGoogle Scholar
  20. Hiraldo F, Veiga JP, Mañez M (1990) Growth of nestling black kites Milvus migrans: effects of hatching order, weather and season. J Zool 222:197–214CrossRefGoogle Scholar
  21. Høberg P, Lindholm M, Ramberg L, Hessen DO (2002) Aquatic food web dynamics on a floodplain in the Okavango delta, Botswana. Hydrobiologia 470:23–30CrossRefGoogle Scholar
  22. Kingsford RT, Jenkins KM, Porter JL (2004) Imposed hydrological stability on lakes in arid Australia and effects on waterbirds. Ecology 85:2478–2492CrossRefGoogle Scholar
  23. Korpimäki E, Hakkarainen H (1991) Fluctuating food supply affects the clutch size of Tengmalm’s owl independent of laying date. Oecologia 85:543–552CrossRefGoogle Scholar
  24. Martin J, Kitchens WM, Cattau CE, Oli MK (2008) Relative importance of natural disturbances and habitat degradation on snail kite population dynamics. Endanger Species Res 6:25–39CrossRefGoogle Scholar
  25. Newton I (1979) Population ecology of raptors. T & AD Poyser, BerkhamstedGoogle Scholar
  26. Newton I (1998) Population limitation in birds. Academic Press, LondonGoogle Scholar
  27. Nilsson C, Berggren K (2000) Alterations of riparian ecosystems caused by river regulation. Bioscience 50:783–792CrossRefGoogle Scholar
  28. Palomares F (2001) Comparison of 3 methods to estimate rabbit abundance in a Mediterranean environment. Wildl Soc Bull 29:578–585Google Scholar
  29. Seigel RA, Fitch HS (1985) Annual variation in reproduction in snakes in a fluctuating environment. J Anim Ecol 54:497–505CrossRefGoogle Scholar
  30. Sergio F, Marchesi L, Pedrini P (2003a) Adaptive selection of foraging and nesting habitat by black kites (Milvus migrans) and its implications for conservation: a multi-scale approach. Biol Conserv 112:351–362CrossRefGoogle Scholar
  31. Sergio F, Marchesi L, Pedrini P (2003b) Spatio-temporal shifts in gradients of habitat quality for an opportunistic avian predator. Ecography 26:243–255CrossRefGoogle Scholar
  32. Sergio F, Pedrini P, Marchesi L (2003c) Reconciling the dichotomy between single species and ecosystem conservation: black kites (Milvus migrans) and eutrophication in pre-Alpine lakes. Biol Conserv 110:101–111CrossRefGoogle Scholar
  33. Sergio F, Blas J, Forero MG, Fernández N, Donázar JA, Hiraldo F (2005) Preservation of wide-ranging top predators by site protection: black and red kites in Doñana National Park. Biol Conserv 125:11–21CrossRefGoogle Scholar
  34. Sergio F, Blas J, Forero MG, Donázar JA, Hiraldo F (2007) Sequential settlement and site-dependence in a migratory raptor. Behav Ecol 18:811–821CrossRefGoogle Scholar
  35. Sergio F, Blas J, Baos R, Forero MG, Donázar JA, Hiraldo F (2009a) Short and long-term consequences of individual and territory quality in a long-lived bird. Oecologia 160:507–514PubMedCrossRefGoogle Scholar
  36. Sergio F, Blas J, Hiraldo F (2009b) Predictors of floater status in a long-lived bird: a cross-sectional and longitudinal test of hypotheses. J Anim Ecol 78:109–118PubMedCrossRefGoogle Scholar
  37. Shine R, Brown GP (2008) Adapting to the unpredictable: reproductive biology of vertebrates in the Australian wet-dry tropics. Philos Trans R Soc B 363:363–373CrossRefGoogle Scholar
  38. Snyder NFR, Beissinger SR, Chandler RE (1989) Reproduction and demography of the Florida Everglade (Snail) Kite. Condor 91:300–316CrossRefGoogle Scholar
  39. Stearns SC (1999) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  40. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  41. Thomas DW, Blondel J, Perret P, Lambrechts MM, Speakman JR (2001) Energetic and fitness costs of mismatching resource supply and demand in a seasonally breeding bird. Science 291:2598–2600PubMedCrossRefGoogle Scholar
  42. Tryjanowski P, Sparks TH, Profus P (2009) Severe flooding causes a crash in production of white stork (Ciconia ciconia) chicks across Central and Eastern Europe. Basic Appl Ecol 10:387–392CrossRefGoogle Scholar
  43. Valkama J, Korpimäki E, Holm A, Hakkarainen H (2002) Hatching asynchrony and brood reduction in Tengmalm’s owl Aegolius funereus: the role of temporal and spatial variation in food abundance. Oecologia 133:334–341CrossRefGoogle Scholar
  44. Van Noordwijk AJ, McCleery RH, Perrins CM (1995) Selection for the timing of great tit breeding in relation to caterpillar growth and temperature. J Anim Ecol 64:451–458CrossRefGoogle Scholar
  45. Vargas FH, Barlow S, Jimenez-Uzcátegui G, Chavez J, Naranjo S, Macdonald DW (2008) Effects of climate variation on the abundance and distribution of flamingos in the Galápagos Islands. J Zool 276:252–265CrossRefGoogle Scholar
  46. Verhulst S, Nilsson J (2008) The timing of birds’ breeding seasons: a review of experiments that manipulated timing of breeding. Philos Trans R Soc B 363:399–410CrossRefGoogle Scholar
  47. Viñuela J (1999) Sibling aggression, hatching asynchrony, and nestling mortality in the black kite (Milvus migrans). Behav Ecol Sociobiol 45:33–45CrossRefGoogle Scholar
  48. Viñuela J (2000) Opposing selective pressures on hatching asynchrony: egg viability, brood reduction, and nestling growth. Behav Ecol Sociobiol 48:333–343CrossRefGoogle Scholar
  49. Viñuela J, Bustamante J (1992) Effect of growth and hatching asynchrony on the fledging age of black kites and red kites. Auk 109:748–757Google Scholar
  50. Viñuela J, Veiga JP (1992) Importance of rabbits in the diet and reproductive success of black kites in southwestern Spain. Ornis Scand 23:132–138CrossRefGoogle Scholar
  51. Viñuela J, Villafuerte R, De Le Court C (1994) Nesting dispersion of a black kite population in relation to location of rabbit warrens. Can J Zool 72:1680–1683CrossRefGoogle Scholar
  52. Wiebe KL, Bortolotti GR (1994) Food supply and hatching spans of birds: energy constraints or facultative manipulation? Ecology 75:813–823CrossRefGoogle Scholar
  53. Wingfield JC (2008) Organization of vertebrate annual cycles: implications for control mechanisms. Philos Trans R Soc B 363:425–441CrossRefGoogle Scholar
  54. Winne CT, Willson JD, Whitfield Gibbons J (2006) Income breeding allows an aquatic snake Seminatrix pygea to reproduce normally following prolonged drought-induced aestivation. J Anim Ecol 75:1352–1360PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Fabrizio Sergio
    • 1
    Email author
  • J. Blas
    • 1
  • L. López
    • 1
  • A. Tanferna
    • 1
    • 2
  • R. Díaz-Delgado
    • 1
  • J. A. Donázar
    • 1
  • F. Hiraldo
    • 1
  1. 1.Department of Conservation BiologyEstación Biológica de Doñana, CSICSevillaSpain
  2. 2.DISUAN, Department of Human, Environmental and Natural SciencesUniversity of UrbinoUrbinoItaly

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