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

Biological Invasions volume 17, pages 3275–3288 (2015)Cite this article

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.

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References

  • Bailey RE (1952) The incubation patch of passerine birds. Condor 54:121–136

    Article  Google Scholar 

  • Baker JR, Ranson R (1938) The breeding seasons of southern hemisphere birds in the northern hemisphere. Proc Zool Soc Lond 1:101–141

    Google Scholar 

  • Ball GF, Ketterson ED (2008) Sex differences in the response to environmental cues regulating seasonal reproduction in birds. Philos Trans R Soc B 363:231–246

    Article  Google Scholar 

  • Blackburn TM, Duncan RP (2001) Determinants of establishment success in introduced birds. Nature 414:195–197

    CAS  Article  PubMed  Google Scholar 

  • Blackburn TM, Lockwood JL, Cassey PB (2009) Avian invasions: the ecology and evolution of exotic birds. Oxford University Press, Oxford

    Book  Google Scholar 

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

    Google Scholar 

  • Carrete M, Tella JL (2008) Wild-bird trade and exotic invasions: a new link of conservation concern? Front Ecol Environ 6:207–211

    Article  Google Scholar 

  • Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15:22–40

    Article  Google Scholar 

  • Clement P, Harris A, Davis J (2010) Finches and sparrows. Christopher Helm, London

    Google Scholar 

  • 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 York

    Google Scholar 

  • 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 392–407

    Google Scholar 

  • Dawson A, King VM, Bentley GE, Ball GF (2001) Photoperiodic control of seasonality in birds. J Biol Rhythms 16:365–380

    CAS  Article  PubMed  Google Scholar 

  • Elith J, Leathwick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annu Rev Ecol Evol Syst 40:677–697

    Article  Google Scholar 

  • Evans K, Duncan R, Blackburn T, Crick H (2005) Investigating geographic variation in clutch size using a natural experiment. Funct Ecol 19:616–624

    Article  Google Scholar 

  • Fry CH, Keith S, Woodcock M, Willis I (2004) The birds of Africa. Vol. 7, Sparrows to buntings. Christopher Helm, London

    Google Scholar 

  • García-Novo G, Marín C (2005) Doñana, water and biosphere. Confederación Hidrográfica del Guadalquivir, Ministerio de Medio Ambiente, Madrid

    Google Scholar 

  • 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 156:355–365

    Article  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 R Soc B 363:267–286

    Article  Google Scholar 

  • 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 39–80

    Chapter  Google Scholar 

  • Hau M, Perfito N, Moore IT (2008) Timing of breeding in tropical birds: mechanisms and evolutionary implications. Ornitol Neotrop 19:39–59

    Google Scholar 

  • 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

  • Helm B, Schwabl I, Gwinner E (2009) Circannual basis of geographically distinct bird schedules. J Exp Biol 212:1259–1269

    Article  PubMed  Google Scholar 

  • Hengeveld R (1994) Small-step invasion research. Trends Ecol Evol 9:339–342

    CAS  Article  PubMed  Google Scholar 

  • 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:e100593

    PubMed Central  Article  PubMed  Google Scholar 

  • Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485

    CAS  Article  PubMed  Google Scholar 

  • Lack DL (1968) Ecological adaptations for breeding in birds. Methuen, London

    Google Scholar 

  • Larson ER, Olden JD, Usio N (2010) Decoupled conservatism of Grinnellian and Eltonian niches in an invasive arthropod. Ecosphere 1(6):art 16

  • Levin DA (2003) Ecological speciation: lessons from invasive species. Syst Bot 28:643–650

    Google Scholar 

  • Lockwood J, Hoopes M, Marchetti M (2007) Invasion ecology. Blackwell, Oxford

    Google Scholar 

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

    Article  Google Scholar 

  • Miller AH (1965) Capacity for photoperiodic response and endogenous factors in the reproductive cycles of an equatorial sparrow. Proc Natl Acad Sci USA 54:97–101

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • 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

  • Murton RK, Westwood N (1977) Avian breeding cycles. Clarendon Press, Oxford

    Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • 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 51:390–398

    Article  Google Scholar 

  • Peterson AT (2003) Predicting the geography of species’ invasions via ecological niche modeling. Q Rev Biol 78:419–433

    Article  PubMed  Google Scholar 

  • Price T, Kirkpatrick M, Arnold SJ (1998) Directional selection and the evolution of breeding date in birds. Science 240:798–899

    Article  Google Scholar 

  • Rasmussen PC, Anderton JC, Arlott N (2005) Birds of south Asia: the Ripley guide. Smithsonian Institution and Lynx Edicions, Washington and Barcelona

    Google Scholar 

  • 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 9:461–472

    Article  Google Scholar 

  • 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:e110019

    PubMed Central  Article  PubMed  Google Scholar 

  • Sax DF, Stachowicz JJ, Gaines SD (2005) Species invasions: insights into ecology, evolution and biogeography. Sinauer Associates, Sunderland

    Google Scholar 

  • Soberón J (2007) Grinnellian and Eltonian niches and geographic distributions of species. Ecol Lett 10:1115–1123

    Article  PubMed  Google Scholar 

  • Sol D, Timmermans S, Lefebvre L (2002) Behavioural flexibility and invasion success in birds. Anim Behav 63:495–502

    Article  Google Scholar 

  • Sol D, Bartomeus I, Griffin AS (2012a) The paradox of invasion in birds: competitive superiority or ecological opportunism? Oecologia 169:553–564

    Article  PubMed  Google Scholar 

  • 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 337:580–583

    CAS  Article  PubMed  Google Scholar 

  • 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 22:962–970

    Article  Google Scholar 

  • 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 291:2598–2600

    CAS  Article  PubMed  Google Scholar 

  • Tilman D (2004) Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. Proc Natl Acad Sci USA 101:10854–10861

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • 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 22:481–488

    Article  PubMed  Google Scholar 

  • Visser ME (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc R Soc Lond Ser B 275:649–659

    Article  Google Scholar 

  • 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 365:3113–3127

    CAS  Article  Google Scholar 

  • 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 13:1310–1324

    Article  PubMed  Google Scholar 

  • Williams GC (2008) Adaptation and natural selection: a critique of some current evolutionary thought. Princeton University Press, Princeton

    Book  Google Scholar 

  • Wolkovich EM, Cleland EE (2010) The phenology of plant invasions: a community ecology perspective. Front Ecol Environ 9:287–294

    Article  Google Scholar 

  • Zuur A, Ieno EN, Walker N et al (2009) Mixed effects models and extensions in ecology with R. Springer, Berlin

    Book  Google Scholar 

Download references

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).

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Authors and Affiliations

  1. Estación Biológica de Doñana (CSIC), Américo Vespucio s/n, 41092, Seville, Spain

    Ana Sanz-Aguilar, Martina Carrete, Pim Edelaar, Jaime Potti & José L. Tella

  2. Instituto Mediterráneo de Estudios Avanzados, IMEDEA (CSIC-UIB), Miquel Marqués 21, 07190, Esporles, Islas Baleares, Spain

    Ana Sanz-Aguilar

  3. Universidad Pablo de Olavide, Ctra Utrera km 1, 41013, Seville, Spain

    Martina Carrete & Pim Edelaar

Authors
  1. Ana Sanz-Aguilar
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  2. Martina Carrete
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  4. Jaime Potti
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  5. José L. Tella
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Correspondence to Ana Sanz-Aguilar.

Appendix

Appendix

See Tables 3, 4 and 5.

Table 3 Family, migratory habit, diet and mean body mass of the species considered in this study
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Table 4 Total number of individuals (and breeding individuals) captured by species and month
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Table 5 Models (GAM) to explain the probability of finding a female with an active brood patch among native and exotic (status) birds along time (month)
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Sanz-Aguilar, A., Carrete, M., Edelaar, P. et al. The empty temporal niche: breeding phenology differs between coexisting native and invasive birds. Biol Invasions 17, 3275–3288 (2015). https://doi.org/10.1007/s10530-015-0952-x

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  • DOI: https://doi.org/10.1007/s10530-015-0952-x

Keywords

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