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Mass gained during breeding positively correlates with adult survival because both reflect life history adaptation to seasonal food availability

Abstract

Both mass (as a measure of body reserves) during breeding and adult survival should reflect variation in food availability. Those species that are adapted to less seasonally variable foraging niches and so where competition dominates during breeding, will tend to have a higher mass increase via an interrupted foraging response, because their foraging demands increase and so become more unpredictable. They will then produce few offspring per breeding attempt, but trade this off with higher adult survival. In contrast, those species that occupy a more seasonal niche will not gain mass because foraging remains predictable, as resources become superabundant during breeding. They can also produce more offspring per breeding attempt, but with a trade-off with reduced adult survival. We tested whether the then predicted positive correlation between levels of mass gained during seasonal breeding and adult survival was present across 40 species of tropical bird measured over a 10-year period in a West African savannah. We showed that species with a greater seasonal mass increase had higher adult survival, controlling for annual mass variation (i.e. annual variation in absolute food availability) and variation in the timing of peak mass (i.e. annual predictability of food availability), clutch size, body size, migratory status and phylogeny. Our results support the hypothesis that the degree of seasonal mass variation in birds is probably an indication of life history adaptation: across tropical bird species it may therefore be possible to use mass gain during breeding as an index of adult survival.

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References

  1. Allcorn RI et al (2012) Demography and breeding ecology of the critically endangered Montserrat oriole. Condor 114:227–235

    Article  Google Scholar 

  2. Bennett PM, Owens IPF (2002) Evolutionary ecology of birds: life histories, mating systems and extinction. Oxford University Press, Oxford

    Google Scholar 

  3. Boyce MS (1984) Restitution of r- and K-selection as a model of density-dependent natural selection. Annu Rev Ecol Syst 15:427–447

    Google Scholar 

  4. Brandt MJ (2007) Trade-offs between the risks of predation and starvation in subtropical granivorous finches. Ph.D. thesis, School of Biology, St Andrews

    Google Scholar 

  5. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  6. Cox DTC, Brandt MJ, McGregor R, Ottosson U, Stevens MC, Cresswell W (2011) Patterns of seasonal and yearly mass variation in West African tropical savannah birds. Ibis 153:672–683

    Article  Google Scholar 

  7. Cox DTC, Brandt M, McGregor RM, Ottosson U, Stevens M, Cresswell W (2013) The seasonality of breeding in savannah birds of West Africa assessed from brood patch and juvenile occurrence. J Ornithol 154:671–683

    Article  Google Scholar 

  8. Cresswell W, Clark JA, Macleod R (2009) How climate change might influence the starvation–predation risk trade-off response. Proc R Soc B Biol Sci 276:3553–3560

    CAS  Article  Google Scholar 

  9. Crowley G, Garnett S (1999) Seeds of the annual grasses Schizachyrium spp. as a food resource for tropical granivorous birds. Aust J Ecol 24:208–220

    Article  Google Scholar 

  10. Dingle H, Khamala CPM (1972) Seasonal-changes in insect abundance and biomass in an East African grassland with reference to breeding and migration in birds. Ardea 60:216–221

    Google Scholar 

  11. Fogden MPL (1972) The seasonality and population dynamics of equatorial birds in Sarawak. Ibis 114:307–343

    Article  Google Scholar 

  12. Fogden MPL, Fogden PM (1979) The role of fat and protein reserves in the annual cycle of the grey-backed Camaroptera in Uganda (Aves: Syhidae). J Zool 189:233–258

    Article  Google Scholar 

  13. Fry CH, Keith S, Urban EK (eds) (1992–2004) The birds of Africa, vols 3–7. Academic Press, London

    Google Scholar 

  14. Ghalambor CK, Martin TE (2001) Fecundity-survival trade-offs and parental risk-taking in birds. Science 292:494–497

    CAS  PubMed  Article  Google Scholar 

  15. Gibbs HL, Grant PR (1987) Adult survivorship in Darwin’s ground finch (Geospiza) populations in a variable environment. J Anim Ecol 56:797–813

    Article  Google Scholar 

  16. Gill SA, Haggerty TM (2012) A comparison of life-history and parental care in temperate and tropical wrens. J Avian Biol 43:461–471

    Article  Google Scholar 

  17. Gosler AG (1996) Environmental and social determinants of winter fat storage in the great tit Parus major. J Anim Ecol 65:1–17

    Article  Google Scholar 

  18. Grant PR, Grant BR, Keller LF, Petren K (2000) Effects of El Niño events on Darwin’s finch productivity. Ecology 81:2442–2457

    Google Scholar 

  19. Griebeler EM, Caprano T, Boehning-Gaese K (2010) Evolution of avian clutch size along latitudinal gradients: do seasonality, nest predation or breeding season length matter? J Evol Biol 23:888–901

    CAS  PubMed  Article  Google Scholar 

  20. Haftorn S (1989) Seasonal and diurnal body weight variations in titmice, based on analyses of individual birds. Wilson Bull 101:217–235

    Google Scholar 

  21. Hambly C, Markman S, Roxburgh L, Pinshow B (2007) Seasonal sex-specific energy expenditure in breeding and non-breeding palestine sunbirds Nectarinia osea. J Avian Biol 38:190–197

    Article  Google Scholar 

  22. Houston AI, McNamara JM (1993) A theoretical investigation of the fat reserves and mortality levels of small birds in winter. Ornis Scand 24:205–219

    Article  Google Scholar 

  23. Houston AI, McNamara JM, Hutchinson JMC (1993) General results concerning the trade-off between gaining energy and avoiding predation. Philos Trans Rs Soc B 341:375–397

    Article  Google Scholar 

  24. Lebreton JD, Burnham KP, Clobert J, Anderson DR (1992) Modelling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol Monogr 62:67–118

    Article  Google Scholar 

  25. Lima SL (1986) Predation risk and unpredictable feeding conditions: determinants of body-mass in birds. Ecology 67:377–385

    Article  Google Scholar 

  26. MacLeod R, Lind J, Clark J, Cresswell W (2007) Mass regulation in response to predation risk can indicate population declines. Ecol Lett 10:945–955

    PubMed  Article  Google Scholar 

  27. MacLeod R, Clark J, Cresswell W (2008) The starvation–predation risk trade-off, body mass and population status in the common starling Sturnus vulgaris. Ibis 150:199–208

    Article  Google Scholar 

  28. Markman S, Pinshow B, Wright J (2002) The manipulation of food resources reveals sex-specific trade-offs between parental self-feeding and offspring care. Proc R Soc B Biol Sci 269:1931–1938

    CAS  Article  Google Scholar 

  29. Martin TE (1987) Food as a limit on breeding birds: a life history perspective. Annu Rev Ecol Syst 18:453–487

    Article  Google Scholar 

  30. McNamara JM, Houston AI (1987) Starvation and predation as factors limiting population size. Ecology 68:1515–1519

    Article  Google Scholar 

  31. McNamara JM, Barta Z, Wikelski M, Houston AI (2008) A theoretical investigation of the effect of latitude on avian life histories. Am Nat 172:331–345

    PubMed  Article  Google Scholar 

  32. Molokwu MN, Olsson O, Nilsson JA, Ottosson U (2008) Seasonal variation in patch use in a tropical African environment. Oikos 117:892

    Article  Google Scholar 

  33. Molokwu MN, Nilsson JK, Ottosson U, Olsson O (2010) Effects of season, water and predation risk on patch use by birds on the African savannah. Oecologia 164:637–645

    PubMed  Article  Google Scholar 

  34. Norris K, Evans MR (2000) Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 11:19–26

    Article  Google Scholar 

  35. Peach WJ, Hanmer DB, Oatley TB (2001) Do Southern African songbirds live longer than their European counterparts? Oikos 93:235–249

    Article  Google Scholar 

  36. Perfito N, Zann RA, Bentley GE, Hau M (2007) Opportunism at work: habitat predictability affects reproductive readiness in free-living zebra finches. Funct Ecol 21:291–301

    Article  Google Scholar 

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

    Article  Google Scholar 

  38. Pinheiro J, Bates D, Debroy S, Sarkar D (2011) nlme: linear and nonlinear mixed effects models. R package version 3.1–102

  39. Poulin B, Lefebvre G, McNeil R (1992) Tropical avian phenology in relation to abundance and exploitation of food resources. Ecology 73:2295–2309

    Article  Google Scholar 

  40. R (Development Core Team 2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org

  41. Renton K, Salinas-Melgoza A (2004) Climatic variability, nest predation, and reproductive output of Lilac-crowned parrots (Amazona finschi) in tropical dry forest of western Mexico. Auk 121:1214–1225

    Google Scholar 

  42. Ricklefs RE (1980) Geographical variation in clutch size among passerine birds: Ashmole’s hypothesis. Auk 97:38–49

    Google Scholar 

  43. Roff DA (2002) Life history evolution. Sinauer, Sunderland

    Google Scholar 

  44. Rogers CM (1987) Predation risk and fasting capacity: do wintering birds maintain optimal body-mass? Ecology 68:1051–1061

    Article  Google Scholar 

  45. Rogers CM, Heath-Coss R (2003) Effect of experimentally altered food abundance on fat reserves of wintering birds. J Anim Ecol 72:822–830

    Article  Google Scholar 

  46. Rozman J, Runciman D, Zann RA (2003) Seasonal variation in body mass and fat of zebra finches in South-Eastern Australia. Emu 103:11–19

    Article  Google Scholar 

  47. Saether BE (1988) Pattern of covariation between life-history traits of European birds. Nature 331:616–617

    CAS  PubMed  Article  Google Scholar 

  48. Stevens MC, Ottosson U, McGregor R, Brandt M, Cresswell W (2013) Survival rates in West African savannah birds. Ostrich 84:11–25

    Article  Google Scholar 

  49. Sylla MB, Dell’Aquila A, Ruti PM, Giorgi F (2010) Simulation of the intra-seasonal and the interannual variability of rainfall over West Africa with RegCM3 during the monsoon period. Int J Climatol 30:1865–1883

    Google Scholar 

  50. Thiollay JM (1988) Comparative foraging success of insectivorous birds in tropical and temperate forests: ecological implications. Oikos 53:17–30

    Article  Google Scholar 

  51. Tokolyi J, McNamara JM, Houston AI, Barta Z (2012) Timing of avian reproduction in unpredictable environments. Evol Ecol 26:25–42

    Article  Google Scholar 

  52. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:S120–S139

    Article  Google Scholar 

  53. Witter MS, Cuthill IC (1993) The ecological costs of avian fat storage. Philos Trans R Soc B 340:73–92

    CAS  Article  Google Scholar 

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Acknowledgments

We would like to thank the A. P. Leventis Ornithological Research Institute for logistical support, and the many ringers who have contributed over the years to this long-term dataset. Thank you to the Leventis Conservation Foundation for funding this study. This is publication no. 72 from the A. P. Leventis Ornithological Research Institute.

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Correspondence to Daniel T. C. Cox.

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Communicated by Ola Olsson.

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Cox, D.T.C., Cresswell, W. Mass gained during breeding positively correlates with adult survival because both reflect life history adaptation to seasonal food availability. Oecologia 174, 1197–1204 (2014). https://doi.org/10.1007/s00442-013-2859-5

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Keywords

  • Fat
  • Interrupted foraging
  • Life history
  • Seasonality
  • Tropical birds