Abstract
The establishment of an introduced species is an important step of the invasion pathway. Often species become established because of their superior competitiveness over the native community or by occupying empty niches. Recently, the red-billed leiothrix Leiothrix lutea has become established in some European natural-woods, which can be quite relevant for nature conservation considering its position among the seven exotic bird species with highest negative impact in bird communities. We assessed which European-native species are more likely to compete with the leiothrix (i.e. potential competitors) based on their structural size and diet composition. Also, we evaluated the competitive advantages of the leiothrix, relatively to its potential competitors, that may allow its successful establishment, considering two approaches: exploratory behaviour and foraging morphology. Two species showed great similarity in structural size with the leiothrix, and also presented great similarity in diet composition, which makes them potential competitors: the robin Erithacus rubecula and the blackcap Sylvia atricapilla. The exploratory behaviour of the leiothrix did not differ from those of its potential competitors. However, the leiothrix presented more efficient foraging morphology than their potential competitors. Our results support the hypothesis of an establishment process by competitive advantage over native species rather than an opportunistic occupation of an empty ecological niche. The establishment of the leiothrix in European natural-habitats, and not in highly disturbed habitats as other invasive species, may constitute a new challenge for conservation.
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References
Amano HE, Eguchi K (2002) Foraging niches of introduced Red-billed Leiothrix and native species in Japan. Ornithol Sci 1:123–131
Andrade P, Rodrigues P, Lopes RJ, Ramos JA, Cunha RTD, Gonçalves D (2015) Ecomorphological patterns in the Blackcap Sylvia atricapilla: insular versus mainland populations. Bird Study 62:498–507
Azzurro E, Tuset VM, Lombarte A, Maynou F, Simberloff D, Rodríguez-Pérez A, Solé RV (2014) External morphology explains the success of biological invasions. Ecol Lett 17:1455–1463
Batalha HR, Ramos JA, Cardoso GC (2013) A successful avian invasion occupies a marginal ecological niche. Acta Oecol 49:92–98
Carnicer J, Jordano P, Melián CJ (2009) The temporal dynamics of resource use by frugivorous birds: a network approach. Ecology 90:1958–1970
Catry P, Costa H, Elias G, Matias R (2010) Aves de Portugal: Ornitologia do território continental. Assírio & Alvim, Lisboa
Chapple DG, Simmonds SM, Wong BB (2012) Can behavioral and personality traits influence the success of unintentional species introductions? Trends Ecol Evol 27:57–64
Cordier J (2007) Reproduction dans les Pyrénées-Atlantiques du Léiothrix Jaune Leiothrix lutea. Alauda 70:260–262
Corlett RT (1998) Frugivory and seed dispersal by birds in Hong Kong shrubland. Forktail 13:23–28
Cramp S, Perrins CM (1994) The birds of the Western Palearctic. Oxford University Press, Oxford
Dawson A (2005) The scaling of primary flight feather length and mass in relation to wing shape, function and habitat. Ibis 147:283–292
Dingemanse NJ, Both C, Drent PJ, Van Oers K, Van Noordwijk AJ (2002) Repeatability and heritability of exploratory behaviour in great tits from the wild. Anim Behav 64:929–938
Dubois PJ, Cugnasse J-M (2015) Les populations d’oiseaux allochtones en France en 2014 (3e enquête nationale). Ornithos 22:72–91
Duncan RP (1997) The role of competition and introduction effort in the success of passeriform birds introduced to New Zealand. Am Nat 149:903–915
Duncan RP, Blackburn TM, Sol D (2003) The ecology of bird introductions. Annu Rev Ecol Evol Syst 34:71–98
Farina A, Pieretti N, Morganti N (2013) Acoustic patterns of an invasive species: the Red-billed Leiothrix (Leiothrix lutea Scopoli 1786) in a Mediterranean shrubland. Bioacoustics 22:175–194
Fernández-González S, De la Hera I, Pérez-Rodríguez A, Pérez-Tris J (2013) Divergent host phenotypes create opportunities and constraints on the distribution of two wing-dwelling feather mites. Oikos 122:1227–1237
Fisher HI, Baldwin PH (1947) Notes on the Red-billed Leiothrix in Hawaii. Pac Sci 1:45–51
Forstmeier W, Keßler A (2001) Morphology and foraging behaviour of Siberian Phylloscopus warblers. J Avian Biol 32:127–138
Foster JT, Robinson SK (2007) Introduced birds and the fate of Hawaiian rainforests. Conserv Biol 21:1248–1257
Fuentes M (1994) Diets of fruit-eating birds: what are the causes of interspecific differences? Oecologia 97:134–142
Gaston A (1974) Adaptation in the genus Phylloscopus. Ibis 116:432–450
Herrando S, Llimona F, Brotons L, Quesada J (2010) A new exotic bird in Europe: recent spread and potential range of Red-billed Leiothrix Leiothrix lutea in Catalonia (northeast Iberian Peninsula). Bird Study 57:226–235
Herrando S, Brotons L, Estrada J, Guallar S, Anton M (2011) Atles dels ocells de Catalunya a l’hivern 2006–2009: Catalan winter bird atlas 2006–2009. Institut Catalá d’Ornitologia y Lynx Edicions, Barcelona
Herrera CM (1984) A study of avian frugivores, bird-dispersed plants, and their interaction in Mediterranean scrublands. Ecol Monogr 54:1–23
Herrera CM (1998) Long-term dynamics of mediterranean frugivorous birds and fleshy fruits: a 12-year study. Ecol Monogr 68:511–538
Holway DA (1999) Competitive mechanisms underlying the displacement of native ants by the invasive Argentine ant. Ecology 80:238–251
Jordano P (1982) Migrant birds are the main seed dispersers of blackberries in southern Spain. Oikos 38:183–193
Kaboli M, Aliabadian M, Guillaumet A, Roselaar CS, Prodon R (2007) Ecomorphology of the wheatears (genus Oenanthe). Ibis 149:792–805
Keast A (1996) Wing shape in insectivorous passerines inhabiting New Guinea and Australian rain forests and eucalypt forest/eucalypt woodlands. The Auk 113:94–104
Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18
Lenth RV (2013) lsmeans: least-squares means. R package Version 1.06-05. http://cran.r-project.org/package=lsmeans
Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion ecology. Wiley, Malden
Male TD, Fancy SG, Ralph CJ (1998) The red-billed leiothrix. In: Poole A, Gill F (eds) The birds of north America. Birds of North America, Incorporated, Philadelphia
Martin-Albarracin VL, Amico GC, Simberloff D, Nuñez MA (2015) Impact of non-native birds on native ecosystems: a global analysis. PLoS ONE. doi:10.1371/journal.pone.0143070
Matias R (2010) Aves exóticas em Portugal: anos de 2005–2008. Anu Ornitol 7:95–108
Morrison ML (1982) The structure of western warbler assemblages: ecomorphological analysis of the Black-throated Gray and Hermit Warblers. Auk 99:503–513
Nentwig W (2007) Biological invasions, vol 193. Springer, Berlin
Palmeirim J, Gorchoy D, Stoleson S (1989) Trophic structure of a neotropical frugivore community: is there competition between birds and bats? Oecologia 79:403–411
Parker IM et al (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19
Peiró IG, Robledano F, Esteve MA (2006) The effect of age and sex on wing morphology and body size of the Bearded Tit Panurus biarmicus in relation to complete moult. Ring Migr 23:101–106
Pejchar L (2015) Introduced birds incompletely replace seed dispersal by a native frugivore. AoB Plants. doi:10.1093/aobpla/plv072
Petren K, Case TJ (1996) An experimental demonstration of exploitation competition in an ongoing invasion. Ecology 77:118–132
Piet GJ (1998) Ecomorphology of a size-structured tropical freshwater fish community. Environ Biol Fishes 51:67–86
Puglisi L, Bosi E, Corsi I, Del Sere M, Pezzo F, Sposimo P, Verducci D (2009) Usignolo del Giappone, bengalino & Co: alieni in Toscana. Alula 16:426–431
R-Core-Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
Rehage JS, Sih A (2004) Dispersal behavior, boldness, and the link to invasiveness: a comparison of four Gambusia species. Biol Invasions 6:379–391
Rey PJ, Gutiérrez JE (1996) Pecking of olives by frugivorous birds: a shift in feeding behaviour to overcome gape limitation. J Avian Biol 27:327–333
Rey P, Gutiérrez J, Alcántara J, Valera F (1997) Fruit size in wild olives: implications for avian seed dispersal. Funct Ecol 11:611–618
Sanz-Aguilar A, Carrete M, Edelaar P, Potti J, Tella JL (2015) The empty temporal niche: breeding phenology differs between coexisting native and invasive birds. Biol Invasions 17:3275–3288
Schoener TW (1983) Field experiments on interspecific competition. Am Nat 123:240–285
Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176
Sol D (2008) Do successful invaders exist? Pre-adaptations to novel environments in terrestrial vertebrates. In: Czeschlik D (ed) Biological invasions. Springer, Heidelberg, pp 127–141
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 (2012) The paradox of invasion in birds: competitive superiority or ecological opportunism? Oecologia 169:553–564
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
Svensson L (1992) Identification guide to European Passerines. Märstatryck, Stockholm
Swaddle J, Lockwood R (1998) Morphological adaptations to predation risk in passerines. J Avian Biol 29:172–176
Swaddle JP, Lockwood R (2003) Wingtip shape and flight performance in the European Starling Sturnus vulgaris. Ibis 145:457–464
Vall-llosera M, Llimona F, de Cáceres M, Sales S, Sol D (2016) Competition, niche opportunities and the successful invasion of natural habitats. Biol Invasions 18:3535–3546
Yong W, Moore FR (1994) Flight morphology, energetic condition, and the stopover biology of migrating thrushes. The Auk 111:683–692
Acknowledgements
P. F. P. was supported by a doctoral grant (SFRH/BD/87340/2012), C.G. by a doctoral grant (SFRH/BD/81602/2011) and R. L. by a post-doctoral grant (SFRH/BPD/78241/2011) from Fundação para a Ciência e a Tecnologia (Portugal POPH/QREN). We also thank all team members who helped in the field work, particularly Helder Cardoso, Luísa Catarino, Pedro Salgueiro and Liliana Almeida. We thank an anonymous reviewer for its many comments, which contributed to improve previous versions of the manuscript.
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Pereira, P.F., Godinho, C., Vila-Viçosa, M.J. et al. Competitive advantages of the red-billed leiothrix (Leiothrix lutea) invading a passerine community in Europe. Biol Invasions 19, 1421–1430 (2017). https://doi.org/10.1007/s10530-016-1364-2
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DOI: https://doi.org/10.1007/s10530-016-1364-2