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
Baker JR, Ranson R (1938) The breeding seasons of southern hemisphere birds in the northern hemisphere. Proc Zool Soc Lond 1:101–141
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
Blackburn TM, Duncan RP (2001) Determinants of establishment success in introduced birds. Nature 414:195–197
Blackburn TM, Lockwood JL, Cassey PB (2009) Avian invasions: the ecology and evolution of exotic birds. Oxford University Press, Oxford
Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer, New York
Carrete M, Tella JL (2008) Wild-bird trade and exotic invasions: a new link of conservation concern? Front Ecol Environ 6:207–211
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
Clement P, Harris A, Davis J (2010) Finches and sparrows. Christopher Helm, London
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
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
Dawson A, King VM, Bentley GE, Ball GF (2001) Photoperiodic control of seasonality in birds. J Biol Rhythms 16:365–380
Elith J, Leathwick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annu Rev Ecol Evol Syst 40:677–697
Evans K, Duncan R, Blackburn T, Crick H (2005) Investigating geographic variation in clutch size using a natural experiment. Funct Ecol 19:616–624
Fry CH, Keith S, Woodcock M, Willis I (2004) The birds of Africa. Vol. 7, Sparrows to buntings. Christopher Helm, London
García-Novo G, Marín C (2005) Doñana, water and biosphere. Confederación Hidrográfica del Guadalquivir, Ministerio de Medio Ambiente, Madrid
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
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
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
Hau M, Perfito N, Moore IT (2008) Timing of breeding in tropical birds: mechanisms and evolutionary implications. Ornitol Neotrop 19:39–59
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
Hengeveld R (1994) Small-step invasion research. Trends Ecol Evol 9:339–342
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
Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485
Lack DL (1968) Ecological adaptations for breeding in birds. Methuen, London
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
Lockwood J, Hoopes M, Marchetti M (2007) Invasion ecology. Blackwell, Oxford
Martin TE (1987) Food as a limit on breeding birds: a life-history perspective. Annu Rev Ecol Evol Syst 18:453–487
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
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
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669
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
Peterson AT (2003) Predicting the geography of species’ invasions via ecological niche modeling. Q Rev Biol 78:419–433
Price T, Kirkpatrick M, Arnold SJ (1998) Directional selection and the evolution of breeding date in birds. Science 240:798–899
Rasmussen PC, Anderton JC, Arlott N (2005) Birds of south Asia: the Ripley guide. Smithsonian Institution and Lynx Edicions, Washington and Barcelona
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
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
Sax DF, Stachowicz JJ, Gaines SD (2005) Species invasions: insights into ecology, evolution and biogeography. Sinauer Associates, Sunderland
Soberón J (2007) Grinnellian and Eltonian niches and geographic distributions of species. Ecol Lett 10:1115–1123
Sol D, Timmermans S, Lefebvre L (2002) Behavioural flexibility and invasion success in birds. Anim Behav 63:495–502
Sol D, Bartomeus I, Griffin AS (2012a) The paradox of invasion in birds: competitive superiority or ecological opportunism? Oecologia 169:553–564
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
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
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
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
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
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
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
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
Williams GC (2008) Adaptation and natural selection: a critique of some current evolutionary thought. Princeton University Press, Princeton
Wolkovich EM, Cleland EE (2010) The phenology of plant invasions: a community ecology perspective. Front Ecol Environ 9:287–294
Zuur A, Ieno EN, Walker N et al (2009) Mixed effects models and extensions in ecology with R. Springer, Berlin
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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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