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Reproductive timing as a constraint on invasion success in the Ring-necked parakeet (Psittacula krameri)

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Abstract

Climate similarity favors biological invasion, but a match between seasonality in the novel range and the timing of life cycle events of the invader also influences the outcome of species introduction. Yet, phenology effects on invasion success have generally been neglected. Here we study whether a phenological mismatch limits the non-native range of a globally successful invader, the Ring-necked parakeet, in Europe. Given the latitudes at which parakeets have established across Europe, they breed earlier than expected based on breeding dates from the native Asian range. Moreover, comparing the breeding dates of European populations to those of parakeets in the native Asian range, to five native breeding bird species in Europe and to the start of the growing season of four native European trees shows that the discrepancy between expected and actual breeding phenology is greater in northern Europe. In northern European populations, this temporal mismatch appears to have negative effects on hatching success, and on population growth rates in years that are colder than average in the first six months. Phenological mismatch also can explain why parakeets from African populations (that are more likely to breed in autumn) have been poor invaders compared to parakeets from Asia. These lines of evidence support the hypothesis that the reproductive phenology of the Ring-necked parakeet can be a limiting factor for establishment and range expansion in colder climates. Our results provide growing support for the hypothesis that the match between climate seasonality and timing of reproduction (or other important life cycle events) can affect the establishment success, invasive potential and distribution range of introduced non-native species, beyond the mere effect of climate similarity.

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References

  • Araújo MB, Peterson AT (2012) Uses and misuses of bioclimatic envelope modeling. Ecology 93:1527–1539

    Article  PubMed  Google Scholar 

  • Both C, te Marvelde L (2007) Climate change and timing of avian breeding and migration throughout Europe. Clim Res 35:93–105

    Article  Google Scholar 

  • Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81–83

    Article  CAS  PubMed  Google Scholar 

  • Both C, Bijlsma RG, Foppen RPB, Siepel H, Van Strien AJ, Van Turnhout CAM (2010) Avian population consequences of climate change are most severe for long-distance migrants in seasonal habitats. Proc R Soc B 277:1259–1266

    Article  PubMed  Google Scholar 

  • Braun M (2004) Alien species in urban habitats: ecology and niche expansion of Ring-necked Parakeets (Psittacula krameri SCOPOLI, 1769). M.Sc. Thesis, University of Marburg, Germany

  • Braun MP (2007) Welchen Einfluss hat die Gebäudedämnung im Rahmen des EU-Klimaschutzes auf die Brutbiologie tropischer Halsbandsittiche (Psittacula krameri) im gemässigten Mitteleuropa? Ornithol Jh Bad-Württ 23:39–56

    Google Scholar 

  • Braun MP, Wink M (2013) Nestling development of ring-necked parakeets (Psittacula krameri) in a nest box population. Open Ornithol J 6:9–24

    Article  Google Scholar 

  • Butler CJ (2003) Population biology of the introduced rose ringed parakeet (Psittacula krameri) in the U.K. Ph.D. Thesis, Department of Zoology, Edward Grey Institute of Field Ornithology

  • Butler CJ, Gosler A (2004) Sexing and ageing rose-ringed parakeets (Psittacula krameri) in Britain. Ringing Migr 22:7–12

    Article  Google Scholar 

  • Cardador L, Carrete M, Gallardo B, Tella JL (2016) Combining trade data and niche modeling improves predictions of the origin and distribution of non-native European populations of a globally invasive species. J Biogeogr 43:967–978

    Article  Google Scholar 

  • Chmielewski F-M, Rötzer T (2001) Response of tree phenology to climate change across Europe. Agr For Meteorol 108:101–112

    Article  Google Scholar 

  • Chmielewski FM, Heider S, Moryson S, Bruns E (2013) International phenological observation networks—concept of IPG and GPM (chapter 8). In: Schwartz MD (ed) Phenology: an integrative environmental science, 2nd edn. Springer, Dordrecht, pp 137–153

    Chapter  Google Scholar 

  • Clergeau P, Vergnes A (2011) Bird feeders may sustain feral Rose-ringed parakeets (Psittacula krameri) in temperate Europe. Wildl Biol 17:248–252

    Article  Google Scholar 

  • Cramp S, Perrins SM (1993) Handbook of the birds of Europe, the Middle East, and North Africa. Flycatchers to Shrikes, vol 7, p 242

  • Cramp S, Brooks DJ, Perrins SM (1994) Handbook of the birds of Europe, the Middle East, and North Africa. Crows to Finches, vol 8

  • DAISIE (Delivering Alien Invasive Species in Europe) European Invasive Alien Species Gateway 2008. Psittacula krameri. http://www.europe-aliens.org/speciesFactsheet.do?speciesId=50460

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

    Article  CAS  PubMed  Google Scholar 

  • Dodaro G, Battista C (2014) Rose -ringed parakeet (Psittacula krameri) and starling (Sturnus vulgaris) syntopics in a Mediterranean urban park: evidence for competition in nest-site selection? Belg J Zool 144:5–14

    Google Scholar 

  • Edelaar P, Avery ML, Carrete M, Gonçalves da Silva A, Hobson EA, Roques S, Russello MA, Senar JC, Tella JL, Wright TF (2015) Shared genetic diversity across the global invasive range of the Monk parakeet suggests a common restricted geographic origin and the possibility of convergent selection. Mol Ecol 24:2164–2176

    Article  PubMed  Google Scholar 

  • FERA (2010) Impact of ring-necked parakeets on native birds. Research project WC0732. Final report to DEFRA, United Kingdom. Www.envirobase.info/PDF/RES17285_executive_summary.pdf

  • Franz D, Dietzen C (2016) Halsbandsittich Psittacula krameri (Scopoli, 1789). In: Dietzen C et al (eds) Die Vogelwelt von Rheinland-Pfalz. Band 3: Greifvögel bis Spechtvögel (Accipitriformes–Piciformes). Landau, Germany, pp 601–613

  • Godoy O, Levine JM (2014) Phenology effects on invasion success: insights from coupling field experiments to coexistence theory. Ecology 95:726–736

    Article  PubMed  Google Scholar 

  • Gurvich DE, Díaz S, Tecco PA (2005) Plant invasions in undisturbed ecosystems: the triggering attribute approach. J Veg Sci 16:723–728

    Article  Google Scholar 

  • Hernández-Brito D, Carrete M, Ibáñez C, Popa-Lisseanu AG, Tella JL (2014) Crowding in the city: losing and winning competitors of an invasive bird. PLoS ONE 9:e100593

    Article  PubMed  PubMed Central  Google Scholar 

  • Jackson H, Groombridge JJ, Matthysen E, Prys-Jones R, Strubbe D, Tollington S (2015) Ancestral origins and invasion pathways in a globally invasive bird correlate with climate and influences from bird trade. Mol Ecol 24:4269–4285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeschke JM (2014) General hypotheses in invasion ecology. Divers Distrib 20:1229–1234

    Article  Google Scholar 

  • Juniper T, Parr M (1998) Parrots: a guide to the parrots of the world. Christopher Helm, London

    Google Scholar 

  • Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204

    Article  PubMed  Google Scholar 

  • Krishnaprasadan TN, Haase E, Kotak VC, Schmedemann R, Sharp PJ (1988) Environmental and hormonal factors in seasonal breeding in free-living male indian rose-ringed parakeets (Psittacula krameri). Horm Behav 22:488–496

    Article  CAS  PubMed  Google Scholar 

  • Lambrechts MM, Visser ME (1999) Proximate aspects of the timing of the reproduction. In: Adams NJ, Slotow RH (eds) Proceeding of the 22th international ornithology congress, Durban. Birdlife South Africa, Johannesburg, pp 231–233

  • Le Gros A, Samadi S, Zuccon D, Cornette R, Braun MP, Senar JC, Clergeau P (2016) Rapid morphological changes, admixture and invasive success in populations of Ring-necked parakeets (Psittacula krameri) established in Europe. Biol Invasions 18:1581–1598

    Article  Google Scholar 

  • Lowe S, Boudjelas S, Browne M, De Poorter M (2000) 100 of the world’s worst invasive alien species: a selection from the global invasive species database. In: The Invasive Species Specialist Group (ISSG), a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN), Aliens, December 2000, p 12

  • Mack RN, Bazzaz FA, Clout M, Evans H, Lonsdale WM, Simberloff D (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • Maitra SK, Dey M (1992) Importance of photoperiods in determining temporal pattern of annual testicular events in Rose-ringed parakeet (Psittacula krameri). J Biol Rhythms 7:13–25

    Article  CAS  PubMed  Google Scholar 

  • Menchetti M, Mori E (2014) Worldwide impact of alien parrots (Aves Psittaciformes) on native biodiversity and environment: a review. Ethol Ecol Evol 26:172–194

    Article  Google Scholar 

  • Orchan Y, Chiron F, Kark S, Shwartz A (2013) The complex interaction network among multiple invasive bird species in a cavity-nesting community. Biol Invasions 15:429–445

    Article  Google Scholar 

  • Oro D, Fowler MS, Genovart M, Martínez-Abraín A, Tavecchia G (2013) Ecological and evolutionary implications of food subsidies from humans. Ecol Lett 16:1501–1514

    Article  PubMed  Google Scholar 

  • Paini DR, Cook DC, De Barro PJ, Sheppard AW, Thomas MB, Worner SP (2016) Global threat to agriculture from invasive species. P Natl Acad Sci USA 113:7575–7579

    Article  CAS  Google Scholar 

  • Panicker KN (1980) Ecology of hole nesting birds. J Bombay Nat Hist Soc 75:1227–1237

    Google Scholar 

  • Pârâu LG, Albayrak T, Ancillotto L, Braun MP, Clergeau P, Franz D, Hernández-Brito D, Kleunen AV, Luna A, Menchetti M, Mori E, Le Louarn M, Schroeder J, Strubbe D, White RL, Wink M (2016) Rose-ringed Parakeet Psittacula krameri populations and numbers in Europe: a complete overview. Open Ornithol J 9:1–13

    Article  Google Scholar 

  • Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Change Biol 13:1860–1872

    Article  Google Scholar 

  • Pearman PB, D’Amen M, Graham CH, Thuiller W, Zimmermann NE (2010) Within-taxon niche structure: niche conservatism, divergence and predicted effects of climate change. Ecography 33:990–1003

    Article  Google Scholar 

  • Pollheimer M, Pollheimer J, Föger M, Pack I (2006) Vorkommen und entstandsentwicklung des Halsbandsittichs Psittacula krameri in Innsbruck/Tirol/Österreich 1978 bis 2006. Monticola 9:366–371

    Google Scholar 

  • Pyle P (2013) Evolutionary implications of synapomorphic wing-molt sequences among falcons (Falconiformes) and parrots (Psittaciformes). Condor 115:593–602

    Article  Google Scholar 

  • Robb GN, Bearhop S, Chamberlain DE, McDonald RA (2008) Food for thought: supplementary feeding as a driver of ecological change in avian populations. Front Earth Sci 6:476–484

    Google Scholar 

  • Rötzer T, Chmielewski FM (2001) Phenological maps of Europe. Clim Res 18:249–257

    Article  Google Scholar 

  • Sailaja R, Haase E, Kotak VC, Schmedemann R, Sharp PJ (1988) Environmental, dietary, and hormonal factors in the regulation of seasonal breeding in free-living female indian rose-ringed parakeets (Psittacula krameri). Horm Behav 22:518–527

    Article  CAS  PubMed  Google Scholar 

  • Sala OE, Armesto JJ, Berlow E, Bloomfield J, Chapin FS III, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774

    Article  CAS  PubMed  Google Scholar 

  • Sanz JJ (1998) Effects of geographic location and habitat on breeding parameters of Great Tits. Auk 115:1034–1051

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Scharlemann JPW (2001) Museum egg collections as stores of long-term phenological data. Int J Biometerol 45:208–211

    Article  CAS  Google Scholar 

  • Schürmann A (1981) Deutschland—deine Papageien. Kosmos 8:42–49

    Google Scholar 

  • Shwartz A, Butler CJ, Kark S, Matthysen E, Strubbe D (2009) The effect of enemy-release and climate conditions on invasive birds: a regional test using the rose-ringed parakeet (Psittacula krameri) as a case study. Divers Distrib 15:310–318

    Article  Google Scholar 

  • Strubbe D, Matthysen E (2009a) Establishment success of invasive ring-necked and monk parakeets in Europe. J Biogeogr 36:2264–2278

    Article  Google Scholar 

  • Strubbe D, Matthysen E (2009b) Experimental evidence for nest-site competition between invasive Ring-necked parakeets (Psittacula krameri) and native nuthatches (Sitta europaea). Biol Conserv 142:1588–1594

    Article  Google Scholar 

  • Strubbe D, Matthysen E (2011) A radiotelemetry study of habitat use by the exotic Ring-necked Parakeet Psittacula krameri in Belgium. Ibis 153:180–184

    Article  Google Scholar 

  • Strubbe D, Jackson H, Groombridge J, Matthysen E (2015) Invasion success of a global avian invader is explained by within-taxon niche structure and association with humans in the native range. Divers Distrib 21:675–685

    Article  Google Scholar 

  • Temara K, Arnhem R (1996) Perruches à collier (Psittacula krameri) victimes des conditions climatiques en region Bruxelloise. Aves 33:128–129

    Google Scholar 

  • Thabethe V, Brown M, Downs CT, Hart LA, Thompson LJ (2013) Seasonal effects on the thermoregulation of invasive rose-ringed parakeets (Psittacula krameri). J Therm Biol 38:553–559

    Article  Google Scholar 

  • Thomas DW, Blondel J, Lambrechts MM, Perret P, Speakman JR (2001) Energetic and fitness costs of mismatching resource supply and demand in seasonally breeding birds. Science 291:2598–2600

    Article  CAS  PubMed  Google Scholar 

  • Verhulst S, Nilsson J-Å (2008) The timing of birds’ breeding seasons: a review of experiments that manipulated timing of breeding. Phil Trans R Soc B 363:399–410

    Article  PubMed  Google Scholar 

  • Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478

    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 

  • Zingel D (1997) Zum Verhalten von Halsbandsittich und Alexandersittich Psittacula krameri und Psittacula eupatria im Schlosspark Wiesbaden-Biebrich und in ihren Heimatländern. Ornithologischen Mitteilungen 49:143–165

    Google Scholar 

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Acknowledgements

We thank Marco van Wieringen for carrying out roost counts in Haarlem, Christopher Rhodes for collecting nesting data in London, NPA rangers for help with roost counts in Israel, and D. Brito, I. Brito and D. Hernández for help with obtaining feather samples on Tenerife. We would like to acknowledge all natural history collections that gave access to their egg collections online or in private, and especially Iris Heynen (Staatliches Museum für Naturkunde, Stuttgart, Germany) and the National Museum of Scotland. We thank the staff of María Luisa Park for access. The work in London was funded by The Department for Environment, Food and Rural Affairs (Defra). DS is funded by a Marie Skłodowska-Curie Action under the Horizon 2020 call (H2020-MSCA-IF-2015, Grant Number 706318), and acknowledges the Danish National Research Foundation for support to the Center for Macroecology, Evolution and Climate (Grant Number DNRF96). PE was supported by the Spanish Ministry of Economy and Competitiveness through grants RYC-2011-07889, CGL-2012-35232, CGL2013-49460-EXP and CGL2016-79483-P, with support from the European Regional Development Fund. We further acknowledge the financial support by COST Action ES1304 (‘ParrotNet’) that facilitated collaboration between the authors. The contents of this manuscript are the authors’ responsibility and neither COST nor any person acting on its behalf is responsible for the use which might be made of the information contained in it.

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Authors and Affiliations

  1. Department Molecular Biology, University Pablo de Olavide, Seville, Spain

    Alvaro Luna, Dailos Hernández-Brito & Pim Edelaar

  2. Department of Conservation Biology, Estación Biológica de Doñana, Seville, Spain

    Alvaro Luna

  3. Bruchstrasse 15, 55263, Wackernheim, Germany

    Detlev Franz

  4. Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark

    Diederik Strubbe

  5. Evolutionary Ecology Group, University of Antwerp, Antwerp, Belgium

    Diederik Strubbe

  6. Terrestrial Ecology Unit, Ghent University, KL Ledeganckstraat 32, 9000, Ghent, Belgium

    Diederik Strubbe

  7. Faculty of Architecture and Town Plaining, Technion, Haifa, Israel

    Assaf Shwartz

  8. Department of Biology, Institute of Pharmacy and Molecular Biotechnology, University of Heidelberg, Im Neuenheimer Feld 364, 69120, Heidelberg, Germany

    Michael P. Braun

  9. Israel Nature and Park Authority, Rosh Haayin, Israel

    Yariv Malihi & Asaf Kaplan

  10. Dipartimento di Scienze della Vita, Università degli Studi di Siena, Siena, Italy

    Emiliano Mori

  11. Department of Biology, University of Florence, Florence, Italy

    Mattia Menchetti

  12. Sovon Dutch Centre for Field Ornithology, PO Box 6521, 6503 GA, Nijmegen, The Netherlands

    Chris A. M. van Turnhout

  13. Department of Animal Ecology and Ecophysiology, Institute for Water and Wetland Research, Radboud University, PO Box 9010, 6500 GL, Nijmegen, The Netherlands

    Chris A. M. van Turnhout

  14. National Wildlife Management Centre, Animal and Plant Health Agency, York, UK

    Dave Parrott

  15. Albrecht Daniel Thaer-Institute, Humboldt-University of Berlin, Albrecht-Thaer-Weg 5, 14195, Berlin, Germany

    Frank-M. Chmielewski

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  1. Alvaro Luna
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  2. Detlev Franz
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  3. Diederik Strubbe
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Luna, A., Franz, D., Strubbe, D. et al. Reproductive timing as a constraint on invasion success in the Ring-necked parakeet (Psittacula krameri). Biol Invasions 19, 2247–2259 (2017). https://doi.org/10.1007/s10530-017-1436-y

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