Abstract
Interspecific competition is rarely assessed between exotic and distantly related native species, although these can compete for some ecological resources. Here, we assessed the occurrence of interspecific aggression resulting from direct competition between two European native songbird species (henceforth focal species), the robin Erithacus rubecula and the blackcap Sylvia atricapilla, which are potential competitors for feeding resources and behaviourally subordinate to the exotic red-billed leiothrix Leiothrix lutea. In central Portugal, this exotic species lives in sympatry with robins and blackcaps at least since 2007. We used interactive playbacks to measure the behavioural response of blackcaps and robins towards intrusions by leiothrix and a submissive, native competitor—great tit Parus major. The singing behaviour of both focal species was affected by leiothrix playback. Robins exhibited a longer latency to sing, and both species avoided singing near the loudspeaker after leiothrix playback compared with great tit playback, which generally suggests a subordinate behaviour. Regarding changes in song parameters during the playbacks, only the peak frequency of blackcaps was affected by the playback. We discuss different possibilities for the origin of such submissive behaviour in native species.
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References
Amarasekare P (2003) Competitive coexistence in spatially structured environments: a synthesis. Ecol Lett 6:1109–1122
Arnott G, Elwood RW (2008) Information gathering and decision making about resource value in animal contests. Anim Behav 76:529–542
Bibby CJ, Burgess ND, Hill DA, Mustoe SH (2000) Bird census techniques. Elsevier
Bleach IT, Beckmann C, Both C, Brown GP, Shine R (2015) Noisy neighbours at the frog pond: effects of invasive cane toads on the calling behaviour of native Australian frogs. Behav Ecol Sociobiol 69:675–683
Briefer E, Rybak F, Aubin T (2008) When to be a dear enemy: flexible acoustic relationships of neighbouring skylarks, Alauda arvensis. Anim Behav 76:1319–1325
Brindley EL (1991) Response of European robins to playback of song: neighbour recognition and overlapping. Anim Behav 41:503–512
Brumm H (2006) Signalling through acoustic windows: nightingales avoid interspecific competition by short-term adjustment of song timing. J Comp Physiol A 192:1279–1285
Cerato E, Fracasso G (2014) Uccelli Dei Colli Berici. Gruppo di studi naturalistici Nisoria, Provincia di Vicenza
Chajewski M (2009) Rela: scale item analysis. R package version, 4
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
Cody ML (1978) Habitat selection and interspecific territoriality among the sylviid warblers of England and Sweden. Ecol Monogr 48:351–396
Cramp S, Perrins CM (1994) The birds of the Western Palearctic. Oxford University Press, Oxford
Dabelsteen T, McGregor PK, Holland J, Tobias JA, Pedersen SB (1997) The signal function of overlapping singing in male robins. Anim Behav 53:249–256
Darolová A, Krištofík J, Knauer F, Hoi H (2020) Behavioural response of Eurasian blackcaps to acoustically simulated conspecific and heterospecific male intruders. J Ornithol 161:447–458
Doutrelant C, Blondel J, Perret P, Lambrechts MM (2000) Blue tit song repertoire size, male quality and interspecific competition. J Avian Biol 31:360–366
Dubois PJ, Maillard J-F, Cugnasse J-M (2016) Les populations d’oiseaux allochtones en France en 2015 (4 e enquête nationale). Ornithos 23:129–141
Ehlman SM, Trimmer PC, Sih A (2019) Prey responses to exotic predators: effects of old risks and new cues. Am Nat 193:575–587
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
Farina A, Pieretti N (2014) Acoustic codes in action in a soundscape context. Biosemiotics 7:321–328
Francis ML, Plummer KE, Lythgoe BA, Macallan C, Currie TE, Blount JD (2018) Effects of supplementary feeding on interspecific dominance hierarchies in garden birds. PLoS One 13:e0202152
Freed LA, Cann RL (2009) Negative effects of an introduced bird species on growth and survival in a native bird community. Curr Biol 19:1736–1740
Freeman BG (2016) Strong asymmetric interspecific aggression between two sympatric new Guinean robins. Ibis 158:75–81
Funghi C, Leitão AV, Ferreira AC, Mota PG, Cardoso GC (2015a) Social dominance in a gregarious bird is related to body size but not to standard personality assays. Ethology 121:84–93
Funghi C, Cardoso GC, Mota PG (2015b) Increased syllable rate during aggressive singing in a bird with complex and fast song. J Avian Biol 46:283–288
Gil D, Llusia D (2020) The bird Dawn chorus revisited. In Aubin T, Mathevon N (eds) Coding strategies in vertebrate acoustic communication (pp. 45-90). Springer, Cham
Goodwin SE, Podos J (2013) Shift of song frequencies in response to masking tones. Anim Behav 85:435–440
Grether GF, Losin N, Anderson CN, Okamoto K (2009) The role of interspecific interference competition in character displacement and the evolution of competitor recognition. Biol Rev 84:617–635
Grether GF, Peiman KS, Tobias JA, Robinson BW (2017) Causes and consequences of behavioral interference between species. Trends Ecol Evol 32:760–772
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
Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19:470–474
Halekoh U, Højsgaard S, Yan J (2006) The R package geepack for generalized estimating equations. J Stat Softw 15:1–11
Hau M, Dominoni D, Casagrande S, Buck CL, Wagner G, Hazlerigg D, Greives T, Hut RA (2017) Timing as a sexually selected trait: the right mate at the right moment. Philosophical Transactions of the Royal Society B: Biological Sciences 372:20160249
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
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
Hick KG, Doucet SM, Mennill DJ (2016) Tropical wrens rely more on acoustic signals than visual signals for inter-and intraspecific discrimination. Anim Behav 118:153–163
Hoi-Leitner M, Nechtelberger H, Hoi H (1995) Song rate as a signal for nest site quality in blackcaps (Sylvia atricapilla). Behav Ecol Sociobiol 37:399–405
Hudina S, Hock K (2014) The role of aggression in range expansion and biological invasions. Current Zoology 60:401–409
Husson F, Josse J, Le S, Mazet J, Husson MF (2019) Package ‘FactoMineR’. Package FactorMineR
Leach IH (1981) Wintering blackcaps in Britain and Ireland. Bird Study 28:5–14
Leedale AE, Collins SA, Kort SR (2015) Blackcaps (Sylvia atricapilla) increase the whistle part of their song in response to simulated territorial intrusion. Ethology 121:403–409
Losin N, Drury JP, Peiman KS, Storch C, Grether GF (2016) The ecological and evolutionary stability of interspecific territoriality. Ecol Lett 19:260–267
Lowe KA, Taylor CE, Major RE (2011) Do common mynas significantly compete with native birds in urban environments? J Ornithol 152:909–921
Malavasi R, Farina A (2013) Neighbours’ talk: interspecific choruses among songbirds. Bioacoustics 22:33–48
Martens J, Eck S (1995) Towards an ornithology of the Himalayas: systematics, ecology and vocalization of Nepal birds. Bonner Zoologische Monographien, vol 38
Martin-Albarracin VL, Amico GC, Simberloff D, Nuñez MA (2015) Impact of non-native birds on native ecosystems: a global analysis. PLoS One 10:e0143070
Martin PR, Fotheringham JR, Ratcliffe L, Robertson RJ (1996) Response of American redstarts (suborder Passeri) and least flycatchers (suborder Tyranni) to heterospecific playback: the role of song in aggressive interactions and interference competition. Behav Ecol Sociobiol 39:227–235
Mathevon N, Aubin T (2001) Sound-based species-specific recognition in the blackcap Sylvia atricapilla shows high tolerance to signal modifications. Behaviour 138:511–524
Matias R (2010) Aves exóticas em Portugal: anos de 2005-2008. Anuário Ornitológico 7:95–108
Matias R (2002) Aves exóticas que nidificam em Portugal continental. Instituto da Conservação da Natureza, Sociedade Portuguesa para o Estudo das Aves
Matyjasiak P (2005) Birds associate species-specific acoustic and visual cues: recognition of heterospecific rivals by male blackcaps. Behav Ecol 16:467–471
McEvoy J, Sinn DL, Wapstra E (2008) Know thy enemy: Behavioural response of a native mammal (Rattus lutreolus velutinus) to predators of different coexistence histories. Austral Ecology 33:922–931
McLaughlin KE, Kunc HP (2013) Experimentally increased noise levels change spatial and singing behaviour. Biol Lett 9:20120771
Miller ET, Bonter DN, Eldermire C, Freeman BG, Greig EI, Harmon LJ, Lisle C, Hochachka WM (2017) Fighting over food unites the birds of North America in a continental dominance hierarchy. Behav Ecol 28:1454–1463
Murray BG (1971) The ecological consequences of interspecific territorial behavior in birds. Ecology 52:414–423
Naguib M (2005) Singing interactions in songbirds: implications for social relations and territorial settlement. In McGregor PK (ed) Animal communication networks (pp. 300-319). Cambridge University press, Cambridge
Naguib M, Mennill DJ (2010) The signal value of birdsong: empirical evidence suggests song overlapping is a signal. Anim Behav 80:e11–e15
Naugler CT, Ratcliffe L (1994) Character release in bird song: a test of the acoustic competition hypothesis using American tree sparrows Spizella arborea. J Avian Biol 25:142–148
Ord TJ, King L, Young AR (2011) Contrasting theory with the empirical data of species recognition. Evolution 65:2572–2591
Peck HL, Pringle HE, Marshall HH, Owens IP, Lord AM (2014) Experimental evidence of impacts of an invasive parakeet on foraging behavior of native birds. Behav Ecol 25:582–590
Peiman K, Robinson B (2010) Ecology and evolution of resource-related heterospecific aggression. Q Rev Biol 85:133–158
Pagani-Núñez E, Renom M, Furquet C, Rodríguez J, Llimona F, Senar JC (2018) Isotopic niche overlap between the invasive leiothrix and potential native competitors. Anim Biodivers Conserv 41:427–434
Pekár S, Brabec M (2018) Generalized estimating equations: a pragmatic and flexible approach to the marginal GLM modelling of correlated data in the behavioural sciences. Ethology 124:86–93
Pereira PF, Godinho C, Vila-Viçosa MJ, Mota PG, Lourenço R (2017) Competitive advantages of the red-billed leiothrix (Leiothrix lutea) invading a passerine community in Europe. Biol Invasions 19:1421–1430
Pereira PF, Lourenço R, Mota PG (2018) Behavioural dominance of the invasive red-billed leiothrix (Leiothrix lutea) over European native passerine-birds in a feeding context. Behaviour 155:55–67
Pereira PF, Barbosa AM, Godinho C, Salgueiro PA, Silva RR, Lourenço R (2020) The spread of the red-billed leiothrix (Leiothrix lutea) in Europe: the conquest by an overlooked invader? Biol Invasions 22:709–722
Pérez-Tris J, Tellería JL (2002) Regional variation in seasonality affects migratory behaviour and life-history traits of two Mediterranean passerines. Acta Oecol 23:13–21
Pigot AL, Tobias JA (2013) Species interactions constrain geographic range expansion over evolutionary time. Ecol Lett 16:330–338
Planqué R, Slabbekoorn H (2008) Spectral overlap in songs and temporal avoidance in a Peruvian bird assemblage. Ethology 114:262–271
Qvarnström A, Haavie J, Saether SA, Eriksson D, Pärt T (2006) Song similarity predicts hybridization in flycatchers. J Evol Biol 19:1202–1209
Ramellini S (2017) L’usignolo del Giappone Leiothrix lutea nel Lazio: aggiornamento della distribuzione ed annotazioni eco-etologiche. Alula 24:95–108
Ramellini S, Simoncini A, Ficetola GF, Falaschi M (2020) Modelling the potential spread of the red-billed Leiothrix Leiothrix lutea in Italy. Bird Study DOI 66:550–560. https://doi.org/10.1080/00063657.2020.1732864
Revelle W, Revelle MW (2015) Package ‘psych’. The Comprehensive R Archive Network
Reif J, Jiran M, Reifová R, Vokurková J, Dolata PT, Petrusek A, Petrusková T (2015) Interspecific territoriality in two songbird species: potential role of song convergence in male aggressive interactions. Anim Behav 104:131–136
Ritschard M, van Oers K, Naguib M, Brumm H (2012) Song amplitude of rival males modulates the territorial behaviour of great tits during the fertile period of their mates. Ethology 118:197–202
Robinson SK, Terborgh J (1995) Interspecific aggression and habitat selection by Amazonian birds. J Anim Ecol 64:1–11
Searcy WA, Beecher MD (2009) Song as an aggressive signal in songbirds. Anim Behav 78:1281–1292
Sebastián-González E, van Aardt J, Sacca K, Barbosa JM, Kelbe D, Hart PJ (2018) Testing the acoustic adaptation hypothesis with native and introduced birds in Hawaiian forests. J Ornithol 159:827–838
Schumacker RE (2015) Using R with multivariate statistics. Sage Publications
Számadó S (2008) How threat displays work: species-specific fighting techniques, weaponry and proximity risk. Anim Behav 76:1455–1463
Tanner CJ, Adler FR (2009) To fight or not to fight: context-dependent interspecific aggression in competing ants. Anim Behav 77:297–305
Tchernichovski O, Nottebohm F, Ho CE, Pesaran B, Mitra PP (2000) A procedure for an automated measurement of song similarity. Anim Behav 59:1167–1176
Tennessen JB, Parks SE, Tennessen TP, Langkilde T (2016) Raising a racket: invasive species compete acoustically with native treefrogs. Anim Behav 114:53–61
Tobias JA, Planqué R, Cram DL, Seddon N (2014) Species interactions and the structure of complex communication networks. Proc Natl Acad Sci 111:1020–1025
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
Verzijden MN, Ripmeester EAP, Ohms VR, Snelderwaard P, Slabbekoorn H (2010) Immediate spectral flexibility in singing chiffchaffs during experimental exposure to highway noise. J Exp Biol 213:2575–2581
Waser PM, Wiley RH (1979) Mechanisms and evolution of spacing in animals. In Marler P, Vandenbergh JG (eds) Social behavior and communication (pp. 159-223). Springer, Boston, MA
Wheatcroft D, Price TD (2013) Learning and signal copying facilitate communication among bird species. Proc R Soc Lond B Biol Sci 280:20123070
Xia C, Lloyd H, Shi J, Wei C, Zhang Y (2018) Dawn singing of the brownish-flanked bush warbler influences dawn chorusing in a bird community. Ethology 124:400–409
Acknowledgements
We are grateful for the comments and suggestions of the associate editor Mylene M. Mariette and two anonymous reviewers who contributed to improve a previous version of the manuscript. We thank the LabOr (University of Évora) and CIBIO for logistical support.
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PFP was supported by a doctoral grant (SFRH/BD/87340/2012) and RL by a post-doctoral grant (SFRH/BPD/78241/2011) from Fundação para a Ciência e a Tecnologia (Portugal POPH/FSE).
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Pereira, P.F., Lourenço, R. & Mota, P.G. Two songbird species show subordinate responses to simulated territorial intrusions of an exotic competitor. acta ethol 23, 143–154 (2020). https://doi.org/10.1007/s10211-020-00347-6
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DOI: https://doi.org/10.1007/s10211-020-00347-6