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Morphological differences along a chronological gradient of urbanisation in an endemic insectivorous bird of New Zealand

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Abstract

Urbanisation constitutes one of the most rapid human-induced environmental changes, developing at the expense of natural and semi-natural habitats. It often implies alterations of many abiotic and biotic factors and contributes to create new environmental conditions, including temperature, food resources, competition and predation. Despite increasing empirical evidence of intra-specific divergence in phenotypic traits (e.g., physiological, behavioural or morphological) between urban and rural individuals, such patterns have often remained disconnected from the underlying mechanisms involved. In the current study, we tested for divergence in functional morphological traits that are related to feeding ecology (i.e., bill morphology, body mass and condition) and/or to the locomotory performance in escaping from predators (i.e., wing, tarsus and tail morphology, body mass and condition) along a chronological gradient of urbanisation (old urban, recent urban and rural areas), using the New Zealand fantail, an endemic insectivorous passerine species. We found divergences in phenotypic traits related to bill morphology along the urban–rural gradient: birds inhabiting the old urban area had stubbier bills (i.e., shorter, deeper and wider bills) than those inhabiting the recent urban and rural areas. We did not detect any difference in locomotion-related morphological traits. Our results suggest the urbanisation-induced alteration in food resources may drive morphological divergence in bird populations. We emphasized the need for mechanistic and experimental studies, with a particular focus on resource-based mechanisms, to identify more precisely the morphological responses of urban populations to changes in food composition, and the resulting implications for communities in urban ecosystems.

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Data availability

The dataset analysed during the current study is available in the Open Science Framework repository, https://doi.org/10.17605/osf.io/BF2TZ.

References

  • Aguilar GD, Farnworth MJ (2013) Distribution characteristics of unmanaged cat colonies over a 20 year period in Auckland, New Zealand. Appl Geogr 37:160–167

    Article  Google Scholar 

  • Alberti M, Marzluff J, Hunt VM (2017) Urban driven phenotypic changes: empirical observations and theoretical implications for eco-evolutionary feedback. Philos Trans R Soc B: Biol Sci 372:20160029

    Article  Google Scholar 

  • Amiot C, Lorvelec O, Mandon-Dalger I et al (2007) Rapid morphological divergence of introduced red-whiskered Bulbuls Pycnonotus jocosus in contrasting environments. Ibis 149:482–489

    Article  Google Scholar 

  • Auckland Regional Council (2010a) A brief history of Auckland’s urban form. Auckland Regional Council, Auckland

    Google Scholar 

  • Auckland Regional Council (2010b) Regional Parks Management Plan. Auckland Regional Council, Auckland

    Google Scholar 

  • Auer SK, Martin TE (2013) Climate change has indirect effects on resource use and overlap among coexisting bird species with negative consequences for their reproductive success. Glob Change Biol 19:411–419

    Article  Google Scholar 

  • Badyaev AV, Young RL, Oh KP, Addison C (2008) Evolution on a local scale: developmental, functional, and genetic bases of divergence in bill form and associated changes in song structure between adjacent habitats. Evol Int J Org Evol 62:1951–1964

    Article  Google Scholar 

  • Benkman CW (1993) Adaptation to single resources and the evolution of crossbill (Loxia) diversity. Ecol Monogr 63:305–325

    Article  Google Scholar 

  • Bitton PP, Graham BA (2015) Change in wing morphology of the European starling during and after colonization of North America. J Zool 295:254–260

    Article  Google Scholar 

  • Burns JG, Ydenberg RC (2002) The effects of wing loading and gender on the escape flights of least sandpipers (Calidris minutilla) and western sandpipers (Calidris mauri). Behav Ecol Sociobiol 52:128–136

    Article  Google Scholar 

  • Caizergues AE, Grégoire A, Charmantier A (2018) Urban versus forest ecotypes are not explained by divergent reproductive selection. Proc R Soc b Biol Sci 285:20180261

    Article  Google Scholar 

  • Chace JF, Walsh JJ (2006) Urban effects on native avifauna: a review. Landsc Urban Plan 74:46–69

    Article  Google Scholar 

  • Chamberlain DE, Cannon AR, Toms MP et al (2009) Avian productivity in urban landscapes: a review and meta-analysis. Ibis 151:1–18

    Article  Google Scholar 

  • Chastel O, Kersten M (2002) Brood size and body condition in the House Sparrow Passer domesticus: the influence of brooding behaviour. Ibis 144:284–292

    Article  Google Scholar 

  • Corbin CE (2008) Foraging ecomorphology within North American flycatchers and a test of concordance with southern African species. J Ornithol 149:83–95

    Article  Google Scholar 

  • Cuthill IC, Witter M, Clarke L (1992) The function of bill-wiping. Anim Behav 43:103–115

    Article  Google Scholar 

  • Cuthill IC, Maddocks SA, Weall CV, Jones EKM (2000) Body mass regulation in response to changes in feeding predictability and overnight energy expenditure. Behav Ecol 11:189–195

    Article  Google Scholar 

  • Darimont CT, Carlson SM, Kinnison MT, Paquet PC, Reimchen TE, Wilmers CC (2009) Human predators outpace other agents of trait change in the wild. Proc Natl Acad Sci 106:952–954

  • Demeyrier V, Charmantier A, Lambrechts MM, Grégoire A (2017) Disentangling drivers of reproductive performance in urban great tits: a food supplementation experiment. J Exp Biol 220:4195–4203

    PubMed  Google Scholar 

  • Dietz MW, Piersma T, Hedenström A, Brugge M (2007) Intraspecific variation in avian pectoral muscle mass: constraints on maintaining manoeuvrability with increasing body mass. Funct Ecol 21:317–326

    Article  Google Scholar 

  • Dulisz B, Nowakowski JJ, Górnik J (2016) Differences in biometry and body condition of the House Sparrow (Passer domesticus) in urban and rural population during breeding season. Urban Ecosystems 19:1307–1324

    Article  Google Scholar 

  • Duncan RP, Young JR (2000) Determinants of plant extinction and rarity 145 years after European settlement of Auckland, New Zealand. Ecology 81:3048–3061

  • Durell SLVD, Goss-Custard JD, Caldow RWG (1993) Sex-related differences in diet and feeding method in the oystercatcher Haematopus ostralegus. J Anim Ecol 62:205–215

    Article  Google Scholar 

  • Evans KL, Gaston KJ, Sharp SP et al (2009) The effect of urbanisation on avian morphology and latitudinal gradients in body size. Oikos 118:251–259

    Article  Google Scholar 

  • Evans KL, Hatchwell BJ, Parnell M, Gaston KJ (2010) A conceptual framework for the colonisation of urban areas: the blackbird Turdus merula as a case study. Biol Rev 85:643–667

    PubMed  Google Scholar 

  • Fischer JD, Cleeton SH, Lyons TP, Miller JR (2012) Urbanization and the predation paradox: the role of trophic dynamics in structuring vertebrate communities. Bioscience 62:809–818

    Article  Google Scholar 

  • Frid A, Dill L (2002) Human-caused disturbance stimuli as a form of predation risk. Conserv Ecol 6:11–26

    Google Scholar 

  • Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121

    Article  Google Scholar 

  • Fuller RA, Warren PH, Armsworth PR et al (2008) Garden bird feeding predicts the structure of urban avian assemblages. Divers Distrib 14:131–137

    Article  Google Scholar 

  • Galbraith JA, Beggs JR, Jones DN, Stanley MC (2015) Supplementary feeding restructures urban bird communities. Proc Natl Acad Sci 112:E2648–E2657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaynor KM, Hojnowski CE, Carter NH, Brashares JS (2018) The influence of human disturbance on wildlife nocturnality. Science 360:1232–1235

  • Geslin T, Chastel O, Eybert MC (2004) Sex-specific patterns in body condition and testosterone level changes in a territorial migratory bird: the Bluethroat Luscinia svecica. Ibis 146:632–641

    Article  Google Scholar 

  • Gil D, Brumm H (2014) Avian urban ecology. Oxford University Press, Oxford

    Google Scholar 

  • Gill BJ (1980) Abundance, feeding, and morphology of passerine birds at Kowhai Bush, Kaikoura, New Zealand. N Z J Zool 7:235–246

    Article  Google Scholar 

  • Gill BJ, Powlesland RG, Powlesland MH (1983) Laying seasons of three insectivorous song-birds at Kowhai Bush, Kaikoura. Notornis 30:81–85

    Google Scholar 

  • Gosler AG, Greenwood JJ, Perrins C (1995) Predation risk and the cost of being fat. Nature 377:621–623

    Article  CAS  Google Scholar 

  • Grimes A, Mitchell I, Smith V (2006) Housing supply in the Auckland Region 2000–2005. Centre for Housing Research Aotearoa New Zealand, Wellington. http://www.hnzc.co.nz/chr/pdfs/housing-supply-in-the-auckland-region-2000–2005.pdf

  • Hendry AP, Farrugia TJ, Kinnison MT (2008) Human influences on rates of phenotypic change in wild animal populations. Mol Ecol 17:20–29

  • Herrel A, Podos J, Huber SK, Hendry AP (2005) Bite performance and morphology in a population of Darwin’s finches: implications for the evolution of beak shape. Funct Ecol 19:43–48

    Article  Google Scholar 

  • Hulscher JB, Ens BJ (1991) Is the bill of the male Oystercatcher a better tool for attacking mussels than the bill of the female? Neth J Zool 42:85–100

    Article  Google Scholar 

  • Jakob EM, Marshall SD, Uetz GW (1996) Estimating fitness: a comparison of body condition indices. Oikos 77:61–67

    Article  Google Scholar 

  • Kleindorfer SM, Chapman TW, Winkler H, Sulloway F (2006) Adaptive divergence in contiguous populations of Darwin’s small ground finch (Geospiza fuliginosa). Evol Ecol Res 8:357–372

    Google Scholar 

  • Kowarik I (2011) Novel urban ecosystems, biodiversity, and conservation. Environ Pollut 159:1974–1983

    Article  CAS  PubMed  Google Scholar 

  • Kullberg C, Fransson T, Jakobsson S (1996) Impaired predator evasion in fat blackcaps (Sylvia atricapilla). Proc R Soc Lond B 263:1671–1675

    Article  Google Scholar 

  • LaBarbera K, Hayes KR, Marsh KJ, Lacey EA (2017) Complex relationships among environmental conditions and bill morphology in a generalist songbird. Evol Ecol 31:707–724

    Article  Google Scholar 

  • Land Information New Zealand (2019). https://www.linz.govt.nz. Accessed 1 May 2020

  • Lawrence C, Paris D, Briskie JV, Massaro M (2017) When the neighbourhood goes bad: can endangered black robins adjust nest-site selection in response to the risk of an invasive predator? Anim Conserv 20:321–330

    Article  Google Scholar 

  • Liker A, Papp Z, Bókony V, Lendvai ÁZ (2008) Lean birds in the city: body size and condition of house sparrows along the urbanization gradient. J Anim Ecol 77:789–795

    Article  CAS  PubMed  Google Scholar 

  • Lindström KM, Van der Veen IT, Legault BA, Lundström JO (2003) Activity and predator escape performance of common greenfinches Carduelis chloris infected with sindbis virus. Ardea 91:103–111

    Google Scholar 

  • Lowe EC, Wilder SM, Hochuli DF (2014) Urbanisation at multiple scales is associated with larger size and higher fecundity of an orb-weaving spider. PLoS One 9(8):e105480 

    Article  PubMed  PubMed Central  Google Scholar 

  • MacLeod R, Barnett P, Clark J, Cresswell W (2006) Mass-dependent predation risk as a mechanism for house sparrow declines? Biol Lett 2:43–46

    Article  PubMed  Google Scholar 

  • Marzluff JM (2017) A decadal review of urban ornithology and a prospectus for the future. Ibis 159:1–13

    Article  Google Scholar 

  • Marzluff JM, Bowman R, Donnelly R (2001) Avian ecology and conservation in an urbanizing world. Kluwer Academic Publishers, Norwell

    Book  Google Scholar 

  • Massaro M, Starling-Windhof A, Briskie JV, Martin TE (2008) Introduced mammalian predators induce behavioural changes in parental care in an endemic New Zealand bird. PLoS One 3(6):e2331

  • Maxwell SL, Fuller RA, Brooks TM, Watson JE (2016) Biodiversity: the ravages of guns, nets and bulldozers. Nature 536:143–145

    Article  CAS  PubMed  Google Scholar 

  • Mayfield H (1961) Nesting success calculated from exposure. Wilson Bullet 73:255–261

    Google Scholar 

  • Mennechez G, Clergeau P (2001) Settlement of breeding European Starlings in urban areas: Importance of lawns vs. anthropogenic wastes. In: Marzluff JM, Bowman R, Donnelly R (eds) Avian ecology and conservation in an urbanizing world. Kluwer Academic Publishers, Norwell, pp 275–287

    Chapter  Google Scholar 

  • Møller AP (2009) Successful city dwellers: a comparative study of the ecological characteristics of urban birds in the Western Palearctic. Oecologia 159:849–858

    Article  PubMed  Google Scholar 

  • Møller AP (2015) Birds. In: Cooper WEJ, Blumstein DT (eds) Escaping from predators: an integrative view of escape decisions and refuge use. Cambridge University Press, Cambridge, pp 88–112

    Chapter  Google Scholar 

  • Møller AP, Ibáñez-Álamo JD (2012) Escape behaviour of birds provides evidence of predation being involved in urbanization. Anim Behav 84:341–348

    Article  Google Scholar 

  • Møller AP, Couderc G, Nielsen JT (2009) Viability selection on prey morphology by a generalist predator. J Evol Biol 22:1234–1241

    Article  PubMed  Google Scholar 

  • Møller AP, Vágási CI, Pap PL (2013) Risk-taking and the evolution of mechanisms for rapid escape from predators. J Evol Biol 26:1143–1150

    Article  PubMed  Google Scholar 

  • Myers S (2005) North Shore City Ecological Survey—a survey of sites of ecological significance in Tamaki and Rodney Ecological Districts. Auckland Regional Council, Auckland

    Google Scholar 

  • Nathan R, Getz WM, Revilla E et al (2008) A movement ecology paradigm for unifying organismal movement research. Proc Natl Acad Sci 105:19052–19059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira Hagen E, Hagen O, Ibáñez-Álamo JD et al (2017) Impacts of urban areas and their characteristics on avian functional diversity. Front Ecol Evol 5:1–15

    Article  Google Scholar 

  • Pithon JA, Duflot R, Beaujouan V et al (2021) Grasslands provide diverse opportunities for bird species along an urban–rural gradient. Urban Ecosyst 28:1–14

    Google Scholar 

  • R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Ramalho CE, Hobbs RJ (2012) Time for a change: dynamic urban ecology. Trends Ecol Evol 27:179–188

    Article  PubMed  Google Scholar 

  • Robertson CJR (2007) Atlas of bird distribution in New Zealand 1999–2004. The Ornithological Society of New Zealand, Wellington

    Google Scholar 

  • Salleh Hudin N, Strubbe D, Teyssier A et al (2016) Predictable food supplies induce plastic shifts in avian scaled body mass. Behav Ecol 27:1833–1840

    Google Scholar 

  • Sanderson EW, Jaiteh M, Levy MA et al (2002) The human footprint and the last of the wild: the human footprint is a global map of human influence on the land surface, which suggests that human beings are stewards of nature, whether we like it or not. Bioscience 52:891–904

    Article  Google Scholar 

  • Scott P, Duncan P, Green JA (2015) Food preference of the Black-headed Gull Chroicocephalus ridibundus differs along a rural–urban gradient. Bird Study 62:56–63

    Article  Google Scholar 

  • Sepp T, McGraw KJ, Kaasik A, Giraudeau M (2018) A review of urban impacts on avian life-history evolution: does city living lead to slower pace of life? Glob Change Biol 24:1452–1469

    Article  Google Scholar 

  • Seress G, Liker A (2015) Habitat urbanization and its effects on birds. Acta Zool Acad Sci H 61:373–408

    Article  Google Scholar 

  • Shochat E (2004) Credit or debit? Resource input changes population dynamics of city-slicker birds. Oikos 106:622–626

    Article  Google Scholar 

  • Shochat E, Warren PS, Faeth SH et al (2006) From patterns to emerging processes in mechanistic urban ecology. Trends Ecol Evol 21:186–191

    Article  PubMed  Google Scholar 

  • Sih A, Bolnick DI, Luttbeg B et al (2010) Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos 119:610–621

    Article  Google Scholar 

  • Sih A, Ferrari MCO, Harris DJ (2011) Evolution and behavioural responses to human-induced rapid environmental change. Evol Appl 4:367–387

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith TB, Girman DJ (2000) Reaching new adaptive peaks: evolution of alternative bill forms in an African finch. In: Mousseau TA, Sinervo B, Endler J (eds) Adaptive genetic variation in the wild. Oxford University Press, New York, pp 139–156

    Google Scholar 

  • Sol D, Lapiedra O, González-Lagos C (2013) Behavioural adjustments for a life in the city. Anim Behav 85:1101–1112

    Article  Google Scholar 

  • Sol D, Maspons J, Gonzalez-Voyer A et al (2018) Risk-taking behavior, urbanization and the pace of life in birds. Behav Ecol Sociobiol 72:59

    Article  Google Scholar 

  • Steffen W, Sanderson RA, Tyson PD et al (2005) Global change and the earth system: a planet under pressure. Springer-Verlag, Berlin/Heidelberg

    Book  Google Scholar 

  • Swaddle JP, Lockwood R (1998) Morphological adaptations to predation risk in passerines. J Avian Biol 29:172–176

    Article  Google Scholar 

  • Swaddle JP, Lockwood R (2003) Wingtip shape and flight performance in the European Starling Sturnus vulgaris. Ibis 145:457–464

    Article  Google Scholar 

  • Thomas AL, Balmford A (1995) How natural selection shapes birds’ tails. Am Nat 146:848–868

    Article  Google Scholar 

  • Thompson JN (1998) Rapid evolution as an ecological process. Trends Ecol Evol 13:329–332

    Article  CAS  PubMed  Google Scholar 

  • Toft RJ, Ford DE, Sullivan JJ, Stewart GH (2019) Invertebrates of an urban old growth forest are different from forest restoration and garden communities. N Z J Ecol 43:1–10

    Google Scholar 

  • van den Hout PJ, Mathot KJ, Maas LRM, Piersma T (2010) Predator escape tactics in birds: linking ecology and aerodynamics. Behav Ecol 21:16–25

    Article  Google Scholar 

  • van der Veen IT, Lindström KM (2000) Escape flights of yellowhammers and greenfinches: more than just physics. Anim Behav 59:593–601

    Article  PubMed  Google Scholar 

  • van Heezik Y, Ludwig K, Whitwell S, McLean IG (2008) Nest survival of birds in an urban environment in New Zealand. N Z J Ecol 32:155–165

    Google Scholar 

  • van Heezik Y, Smyth A, Adams A, Gordon J (2010) Do domestic cats impose an unsustainable harvest on urban bird populations? Biol Conserv 143:121–130

    Article  Google Scholar 

  • Venter O, Sanderson EW, Magrach A et al (2016) Sixteen years of change in the global terrestrial human footprint and implications for biodiversity conservation. Nat Commun 7:1–11

    Article  CAS  Google Scholar 

  • Witter MS, Cuthill IC, Bonser RHC (1994) Experimental investigations of mass-dependent predation risk in the European starling, Sturnus vulgaris. Anim Behav 48:201–222

    Article  Google Scholar 

  • Yeh PJ (2004) Rapid evolution of a sexually selected trait following population establishment in a novel habitat. Evolution 58:166–174

    PubMed  Google Scholar 

  • Yom-Tov Y, Yom-Tov S, Wright J et al (2006) Recent changes in body weight and wing length among some British passerine birds. Oikos 112:91–101

    Article  Google Scholar 

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Acknowledgements

We thank the anonymous reviewers and editors for their valuable comments on the manuscript.

Funding

This project was supported by the Institute of Natural and Mathematical Sciences of Massey University.

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  1. Christophe Amiot and Clément Harmange share authorship

Authors and Affiliations

  1. LETG-Angers, UMR 6554 CNRS, Université d’Angers, 2 Bd Lavoisier, 49045, Angers, France

    Christophe Amiot & Clément Harmange

  2. REHABS International Research Laboratory, CNRS-Université Lyon 1-Nelson Mandela University, George Campus, Madiba Drive, George, 6531, South Africa

    Christophe Amiot & Clément Harmange

  3. Institute of Natural and Mathematical Sciences, Massey University, Auckland, New Zealand

    Christophe Amiot & Weihong Ji

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  1. Christophe Amiot
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  2. Clément Harmange
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Contributions

CA and WJ contributed to the study conception and design. Data collection was performed by CA. Data analysis was conducted by CA and CH. The first draft of the manuscript was written by CH and all authors commented and amended on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Christophe Amiot.

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Ethics approval

The study was conducted with clearance from the Massey University Animal Ethics Committee (10/102), Auckland Council and Department of Conservation (AK-29598-FAU), who gave the permission to handle the study birds. The study thus adheres to the ethical use of animals in research and to the legal requirements of New Zealand in which the work has been carried out.

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The authors have no conflicts of interest to declare that are relevant to the content of this article.

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Amiot, C., Harmange, C. & Ji, W. Morphological differences along a chronological gradient of urbanisation in an endemic insectivorous bird of New Zealand. Urban Ecosyst 25, 465–475 (2022). https://doi.org/10.1007/s11252-021-01156-w

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