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Biological Invasions

, Volume 17, Issue 11, pp 3275–3288 | Cite as

The empty temporal niche: breeding phenology differs between coexisting native and invasive birds

  • Ana Sanz-AguilarEmail author
  • Martina Carrete
  • Pim Edelaar
  • Jaime Potti
  • José L. Tella
Original Paper

Abstract

Invasive species face new environmental conditions in their areas of introduction. A correct timing of reproduction is crucial for the successful adjustment of individuals to their environments, yet the temporal aspects of the niche are a neglected subject in the study of biological invasions. When introduced, exotic species could successfully invade new habitats by making use of ecological opportunities, e.g. empty temporal Eltonian niches. Specifically, they may achieve this via conservatism of their native reproductive phenology and/or via plasticity in their reproductive timing. Here we compare the reproductive phenology of a marshland passerine community composed of five successfully established tropical exotic species and twelve coexisting Mediterranean native species along four consecutive years. Both groups showed large differences in their phenology, with exotics reproducing along more months and later in the year than natives. One exotic species even breeds only in late summer and early autumn, when virtually all natives have ceased breeding and when overall bird abundance as well as primary production in cultivated areas (rice fields) were highest. Nonetheless, estimates of population sizes and juvenile survival rates in the study area suggest that late breeding is not maladaptive but instead highly successful. The striking difference in reproductive timing suggests that the exotics may be taking advantage of a vacant Eltonian temporal niche, possibly generated by high resource availability in human-transformed habitats (rice fields and other croplands) in the study area. This study highlights the need to also consider the temporal aspects of the niche when studying invasions.

Keywords

Timing of reproduction Temporal niche Biological invasions Grinnellian and Eltonian niche Niche conservatism Weaver 

Notes

Acknowledgments

We thank J. Ayala, A. Jurado, M. Vázquez, D. Serrano and J. Blas for their field assistance. Logistical support and primary production data were provided by the Laboratorio de SIG y Teledetección, Estación Biológica de Doñana, CSIC (LAST-EBD). Fundación Repsol, two Projects of Excellence from the Junta de Andalucía (P07-RNM-02918 and P08-RNM-4014), and the Spanish Ministry of Economy and Competitiveness (Projects JCI-2011-09085, RYC-2009-04860, RYC-2011-07889 and CGL2012-35232) funded this research, with the support from the ERDF and the Project EBD-Severo Ochoa (SEV-2012-0262).

References

  1. Bailey RE (1952) The incubation patch of passerine birds. Condor 54:121–136CrossRefGoogle Scholar
  2. Baker JR, Ranson R (1938) The breeding seasons of southern hemisphere birds in the northern hemisphere. Proc Zool Soc Lond 1:101–141Google Scholar
  3. Ball GF, Ketterson ED (2008) Sex differences in the response to environmental cues regulating seasonal reproduction in birds. Philos Trans R Soc B 363:231–246CrossRefGoogle Scholar
  4. Blackburn TM, Duncan RP (2001) Determinants of establishment success in introduced birds. Nature 414:195–197CrossRefPubMedGoogle Scholar
  5. Blackburn TM, Lockwood JL, Cassey PB (2009) Avian invasions: the ecology and evolution of exotic birds. Oxford University Press, OxfordCrossRefGoogle Scholar
  6. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  7. Carrete M, Tella JL (2008) Wild-bird trade and exotic invasions: a new link of conservation concern? Front Ecol Environ 6:207–211CrossRefGoogle Scholar
  8. Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15:22–40CrossRefGoogle Scholar
  9. Clement P, Harris A, Davis J (2010) Finches and sparrows. Christopher Helm, LondonGoogle Scholar
  10. Cramp S, Simmons K (1977) Birds of the western Palearctic: handbook of the birds of Europe, the Middle East and North Africa. Oxford University Press, New YorkGoogle Scholar
  11. Daan S, Dijkstra C, Drent R, Meijer T (1988) Food supply and the annual timing of avian reproduction. In: Ouellet H (ed) Acta XIX Congressus Internationalis Ornithologici. University of Ottawa Press, Ottawa, pp 392–407Google Scholar
  12. Dawson A, King VM, Bentley GE, Ball GF (2001) Photoperiodic control of seasonality in birds. J Biol Rhythms 16:365–380CrossRefPubMedGoogle Scholar
  13. Elith J, Leathwick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annu Rev Ecol Evol Syst 40:677–697CrossRefGoogle Scholar
  14. Evans K, Duncan R, Blackburn T, Crick H (2005) Investigating geographic variation in clutch size using a natural experiment. Funct Ecol 19:616–624CrossRefGoogle Scholar
  15. Fry CH, Keith S, Woodcock M, Willis I (2004) The birds of Africa. Vol. 7, Sparrows to buntings. Christopher Helm, LondonGoogle Scholar
  16. García-Novo G, Marín C (2005) Doñana, water and biosphere. Confederación Hidrográfica del Guadalquivir, Ministerio de Medio Ambiente, MadridGoogle Scholar
  17. Grundy JP, Franco A, Sullivan MJ (2014) Testing multiple pathways for impacts of the non-native black-headed weaver Ploceus melanocephalus on native birds in Iberia in the early phase of invasion. Ibis 156:355–365CrossRefGoogle Scholar
  18. Hahn TP, MacDougall-Shackleton SA (2008) Adaptive specialization, conditional plasticity and phylogenetic history in the reproductive cue response systems of birds. Philos Trans R Soc B 363:267–286CrossRefGoogle Scholar
  19. Hahn TP, Boswell T, Wingfield JC, Ball GF (1997) Temporal flexibility in avian reproduction. In: Nolan VJ, Ketterson ED (eds) Current ornithology. Plenum, New York, pp 39–80CrossRefGoogle Scholar
  20. Hau M, Perfito N, Moore IT (2008) Timing of breeding in tropical birds: mechanisms and evolutionary implications. Ornitol Neotrop 19:39–59Google Scholar
  21. Heinsch FA, Reeves M, Votava P, Kang S, Milesi C, Zhao M, Glassy J, Jolly WM, Loehman R, Bowker CF, Kimball JS, Nemani RR, Running SW (2003) GPP and NPP (MOD17A2/A3) products NASA MODIS land algorithm. www.ntsg.umt.edu/modis/MOD17UsersGuide.pdf
  22. Helm B, Schwabl I, Gwinner E (2009) Circannual basis of geographically distinct bird schedules. J Exp Biol 212:1259–1269CrossRefPubMedGoogle Scholar
  23. Hengeveld R (1994) Small-step invasion research. Trends Ecol Evol 9:339–342CrossRefPubMedGoogle Scholar
  24. Hernández-Brito D, Carrete M, Popa-Lisseanu AG, Ibáñez C, Tella JL (2014) Crowding in the city: losing and winning competitors of an invasive bird. PLoS ONE 9:e100593PubMedCentralCrossRefPubMedGoogle Scholar
  25. Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485CrossRefPubMedGoogle Scholar
  26. Lack DL (1968) Ecological adaptations for breeding in birds. Methuen, LondonGoogle Scholar
  27. Larson ER, Olden JD, Usio N (2010) Decoupled conservatism of Grinnellian and Eltonian niches in an invasive arthropod. Ecosphere 1(6):art 16Google Scholar
  28. Levin DA (2003) Ecological speciation: lessons from invasive species. Syst Bot 28:643–650Google Scholar
  29. Lockwood J, Hoopes M, Marchetti M (2007) Invasion ecology. Blackwell, OxfordGoogle Scholar
  30. Martin TE (1987) Food as a limit on breeding birds: a life-history perspective. Annu Rev Ecol Evol Syst 18:453–487CrossRefGoogle Scholar
  31. Miller AH (1965) Capacity for photoperiodic response and endogenous factors in the reproductive cycles of an equatorial sparrow. Proc Natl Acad Sci USA 54:97–101PubMedCentralCrossRefPubMedGoogle Scholar
  32. Molina B, Bermejo A (2003) Amandava amandava. Atlas de las Aves Reproductoras de España. Ministerio de Agricultura, Alimentación y Medio Ambiente. http://www.magrama.gob.es/es/biodiversidad
  33. Murton RK, Westwood N (1977) Avian breeding cycles. Clarendon Press, OxfordGoogle Scholar
  34. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669CrossRefGoogle Scholar
  35. Penteriani V, del Delgado M, Lokki H (2014) Global warming may depress avian population fecundity by selecting against early-breeding, high-quality individuals in northern populations of single-brooded, long-lived species. Ann Zool Fenn 51:390–398CrossRefGoogle Scholar
  36. Peterson AT (2003) Predicting the geography of species’ invasions via ecological niche modeling. Q Rev Biol 78:419–433CrossRefPubMedGoogle Scholar
  37. Price T, Kirkpatrick M, Arnold SJ (1998) Directional selection and the evolution of breeding date in birds. Science 240:798–899CrossRefGoogle Scholar
  38. Rasmussen PC, Anderton JC, Arlott N (2005) Birds of south Asia: the Ripley guide. Smithsonian Institution and Lynx Edicions, Washington and BarcelonaGoogle Scholar
  39. Sanz JJ, Potti J, Moreno J, Merino S, Frías O (2003) Climate change and fitness components of a migratory bird breeding in the Mediterranean region. Glob Change Biol 9:461–472CrossRefGoogle Scholar
  40. Sanz-Aguilar A, Anadón JD, Edelaar P, Carrete M, Tella JL (2014) Can establishment success be determined through demographic parameters? A case study on five introduced bird species. PLoS ONE 9:e110019PubMedCentralCrossRefPubMedGoogle Scholar
  41. Sax DF, Stachowicz JJ, Gaines SD (2005) Species invasions: insights into ecology, evolution and biogeography. Sinauer Associates, SunderlandGoogle Scholar
  42. Soberón J (2007) Grinnellian and Eltonian niches and geographic distributions of species. Ecol Lett 10:1115–1123CrossRefPubMedGoogle Scholar
  43. Sol D, Timmermans S, Lefebvre L (2002) Behavioural flexibility and invasion success in birds. Anim Behav 63:495–502CrossRefGoogle Scholar
  44. Sol D, Bartomeus I, Griffin AS (2012a) The paradox of invasion in birds: competitive superiority or ecological opportunism? Oecologia 169:553–564CrossRefPubMedGoogle Scholar
  45. Sol D, Maspons J, Vall-Llosera M, Bartomeus I, García-Peña GE, Piñol J, Freckleton RP (2012b) Unraveling the life history of successful invaders. Science 337:580–583CrossRefPubMedGoogle Scholar
  46. Strubbe D, Broennimann O, Chiron F, Matthysen E (2013) Niche conservatism in non-native birds in Europe: niche unfilling rather than niche expansion. Glob Ecol Biogeogr 22:962–970CrossRefGoogle Scholar
  47. Thomas DW, Blondel J, Perret P, Lambrechts MM, Speakman JR (2001) Energetic and fitness costs of mismatching resource supply and demand in seasonally breeding birds. Science 291:2598–2600CrossRefPubMedGoogle Scholar
  48. Tilman D (2004) Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. Proc Natl Acad Sci USA 101:10854–10861PubMedCentralCrossRefPubMedGoogle Scholar
  49. Vellend M, Harmon LJ, Lockwood JL, Mayfield MM, Hughes AR, Wares JP, Sax DF (2007) Effects of exotic species on evolutionary diversification. Trends Ecol Evol 22:481–488CrossRefPubMedGoogle Scholar
  50. Visser ME (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc R Soc Lond Ser B 275:649–659CrossRefGoogle Scholar
  51. Visser ME, Caro SP, Van Oers K, Schaper SV, Helm B (2010) Phenology, seasonal timing and circannual rhythms: towards a unified framework. Philos Trans R Soc B 365:3113–3127CrossRefGoogle Scholar
  52. Wiens JJ, Ackerly DD, Allen AP, Anacker BL, Buckley LB, Cornell HV, Damschen EI, Jonathan Davies T, Grytnes JA, Harrison SP, Hawkins BA, Holt RD, McCain CM, Stephens PR (2010) Niche conservatism as an emerging principle in ecology and conservation biology. Ecol Lett 13:1310–1324CrossRefPubMedGoogle Scholar
  53. Williams GC (2008) Adaptation and natural selection: a critique of some current evolutionary thought. Princeton University Press, PrincetonCrossRefGoogle Scholar
  54. Wolkovich EM, Cleland EE (2010) The phenology of plant invasions: a community ecology perspective. Front Ecol Environ 9:287–294CrossRefGoogle Scholar
  55. Zuur A, Ieno EN, Walker N et al (2009) Mixed effects models and extensions in ecology with R. Springer, BerlinCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Ana Sanz-Aguilar
    • 1
    • 2
    Email author
  • Martina Carrete
    • 1
    • 3
  • Pim Edelaar
    • 1
    • 3
  • Jaime Potti
    • 1
  • José L. Tella
    • 1
  1. 1.Estación Biológica de Doñana (CSIC)SevilleSpain
  2. 2.Instituto Mediterráneo de Estudios Avanzados, IMEDEA (CSIC-UIB)EsporlesSpain
  3. 3.Universidad Pablo de OlavideSevilleSpain

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