Abstract
Urbanization creates new habitats with novel benefits and challenges not found in natural systems. How a species fares in urban habitats is largely dependent on its life history, yet predicting the response of individual species to urbanization remains a challenge. While some species thrive in urban areas, others do poorly or are not present at all. Mountain chickadees (Poecile gambeli) are year-round residents of montane regions of western North America. Commonly found in higher-elevation coniferous forests, these birds can also be found in urban areas where they will regularly visit bird feeders and nest in nest boxes. We monitored mountain chickadees nesting along a habitat gradient, from natural habitat to suburban areas, to determine if the degree of urbanization was associated with: clutch size and success; nestling growth rates; or variation in parental size and age. Females nesting in urbanized areas initiated clutches earlier in the breeding season than those in natural areas, but neither fledging success nor the rate of nestling mass-change differed between habitats. Nestling feather growth-rate increased with later first egg dates in both habitats, and the magnitude of this increase was greatest in urban habitats. We found no difference in the proportion of first-time breeders versus experienced breeders between habitat types, nor any differences in male or female mass or size. Our results indicate no detriment to nesting in urban habitats, suggesting mountain chickadees are able to adapt to moderate urbanization much like other members of the Paridae family.
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References
Anderies J, Katti M, Shochat E (2007) Living in the city: resource availability, predation, and bird population dynamics in urban areas. J Theor Biol 247:36–49
Bailly J, Scheifler R, Berthe S, Clément-Demange V, Leblond M, Pasteur B, Faivre B (2016) From eggs to fledging: negative impact of urban habitat on reproduction in two tit species. J Ornithol 157:377–392
Baker P, Molony S, Stone E, Cuthill I, Harris S (2008) Cats about town: is predation by free-ranging pet cats Felis catus likely to affect urban bird populations? Ibis 150:86–99
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Beissinger S, Osborne D (1982) Effects of urbanization on avian community organization. Condor 84:75–83
Blair R (1996) Land use and avian species diversity along an urban gradient. Ecol Appl 6:506–519
Blancher P (2013) Estimated number of birds killed by house cats (Felis catus) in Canada. Avian Conserv Ecol 8:3
Blewett C, Marzluff J (2005) Effects of urban sprawl on snags and the abundance and productivity of cavity-nesting birds. Condor 107:678–693
Boag P (1987) Effects of nestling diet on growth and adult size of zebra finches (Poephila guttata). Auk 104:155–166
Borgmann K, Rodewald A (2004) Nest predation in an urbanizing landscape: the role of exotic shrubs. Ecol Appl 14:1757–1765
Burger J, Bowman R, Wooldenden G, Gochfeld M (2004) Metal and metalloid concentrations in the eggs of threatened Florida scrub-jays in suburban habitats from south-central Florida. Sci Total Environ 328:185–193
Chamberlain D, Cannon A, Toms M, Leech D, Hatchwell B, Gaston K (2009) Avian productivity in urban landscapes: a review and meta-analysis. Ibis 151:1–18
Croci S, Butet A, Clergeau P (2008) Does urbanization filter birds on the basis of their biological traits? Condor 110:223–240
Dahlsten DL, Cooper WA (1979) The use of nesting boxes to study the biology of the mountain chickadee (Parus gambeli) and its impact on selected forest insects. In: Dickson JG, Connor RN, Fleet RR, Jackson JA, Kroll JC (eds) The role of insectivorous birds in forest ecosystems. Academic Press, New York, pp 217–260
de la Hera I, Pérez-Tris J, Tellería J (2009) Migratory behaviour affects the trade-off between feather growth rate and feather quality in a passerine bird. Biol J Linn Soc 97:98–105
Dowling J, Luther D, Marra P (2012) Comparative effects of urban development and anthropogenic noise on bird songs. Behav Ecol 23:201–209
Gering J, Blair R (1999) Predation on artificial bird nests along an urban gradient: predatory risk or relaxation in urban environments? Ecography 22:532–541
Germain R, Schuster R, Delmore K, Arcese P (2015) Habitat preference facilitates successful early breeding in an open-cup nesting songbird. Funct Ecol 29:1522–1532
Gladąlski M, Bańburna M, Kaliński A, Markowski M, Skwarska J, Wawrzyniak J et al (2015) Inter-annual and inter-habitat variation in breeding performance of blue tits (Cyanistes caeruleus) in central Poland. Ornis Fennica 92:34–42
Google Inc (2012) Google Earth http://google.com/earth/
Issacs R, Tuell J, Fiedler A, Gardiner M, Landis D (2009) Maximizing arthropod-mediated ecosystem services in agricultural landscapes: the role of native plants. Front Ecol Environ 7:196–203
Kuznetsova A, Brockhoff P, Christensen R (2016) lmerTest: tests in linear mixed effects models. R package version 2.0-33
Lack D (1947) The significance of clutch-size. Ibis 89:302–352
LaZerte S, Otter K, Slabbekoorn H (2017) Mountain chickadees adjust songs, calls and chorus composition with increasing ambient and experimental anthropogenic noise. Urban Ecosys. doi:10.1007/s11252-017-0652-7
Lodjak J, Mägi M, Vallo T (2014) Insulin-like growth factor 1 and growth rate in nestlings of a wild passerine bird. Funct Ecol 28:159–166
Loss S, Will T, Marra P (2013) The impact of free-ranging domestic cats on wildlife of the United States. Nat Commun 4:1396. doi:10.1038/ncomms2380
Loyd K, Hernandez S, Carroll J, Abernathy K, Marshall G (2013) Quantifying free-roaming domestic cat predation using animal-borne video cameras. Biol Conserv 160:183–189
Marciniak B, Nadolski J, Nowakowska M, Loga B, Bańbura J (2007) Habitat and annual variation in arthropod abundance affects blue tit Cyanistes caeruleus reproduction. Acta Ornithologica 42:53–62
Marzluff J (2001) Worldwide urbanization and its effects on birds. In: Marzluff J, Bowman R, Donnelly R (eds) Avian ecology and conservation in an urbanizing world. Kluwer Academic Publishers, Springer, US, pp 19–38
McCallum DA, Grundel R, Dahlsten DL (1999) In: Poole A (ed) Mountain chickadee (Poecile gambeli), the birds of North America online. Cornell Lab of Ornithology, New York. doi:10.2173/bna.453
Morneau F, Lépine C, Décarie R, Villard M, Des Granges J (1995) Reproduction of American robin (Turdus migratorius) in a suburban environment. Landsc Urban Plan 32:55–62
Nager R, Monaghan P, Houston D, Genovart M (2000) Parental condition, brood sex ratio and differential young survival: an experimental study in gulls (Larus fuscus). Behav Ecol Sociobiol 48:452–457
Nowicki S, Searcy W, Peters S (2002) Brain development, song learning and mate choice in birds: a review and experimental test of the “nutritional stress hypothesis”. J Comp Physiol A 188:1003–1014
O’Connor R (1978) Structure in avian growth patterns: a multivariate study of passerine development. J Zool (Lond) 185:147–172
Otter K (ed) (2007) Ecology and behavior of chickadees and titmice: an integrated approach. Oxford University Press, New York
Pearson M, Healey M (2012) Species and risk and local government: a primer for BC. Stewardship Center of British Columbia, Courtenay (BC) http://www.speciesatrisk.bc.ca/node/8055
Penteriani V, 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
Perrins C (1970) The timing of birds’ breeding season. Ibis 112:242–255
Perrins C, McCleery R (1989) Laying dates and clutch size in the great tit. Wilson Bull 101:236–253
Preiszner B, Papp S, Pipoly I, Seress G, Vincze E, Liker A, Bókony V (2016) Problem-solving performance and reproductive success of great tits in urban and forest habitats. Anim Cogn. doi:10.1007/s10071-016-1008-z
Pyle P (1997) Identification guide to North American birds. Part 1. Slate Creek Press, Bolinas
R Core Team (2017) R: a language and environment for statistical computing. Version 3.3.3. R Foundation for Statistical Computing. Vienna. https://www.R-project.org/. Accessed 3 March 2017
Reudink MW, Marra PP, Kyser TK, Boag PT, Langin KM, Ratcliffe LM (2009) Non-breeding season events influence sexual selection in a long-distance migratory bird. Proc R Soc B 276:1619–1626
Ricklefs R (1968) Patterns of growth in birds. Ibis 110:419–451
Robb G, McDonald R, Chamberlain D, Bearhop S (2008) Food for thought: supplementary feeding as a driver of ecological change in avian populations. Front Ecol Environ 6:476–484
Rodewald A, Shustack D, Hitchcock L (2010) Exotic shrubs as ephemeral ecological traps for nesting birds. Biol Invasions 12:33–39
Rolando A, Maffei G, Pulcher C, Giuso A (1997) Avian community structure along an urbanization gradient. Ital J Zool 64:341–349
Rowse L, Rodewald A, Sullivan S (2014) Pathways and consequences of contaminant flux to Acadian flycatchers (Empidonax virescens) in urbanizing landscapes of Ohio, USA. Sci Total Environ 485-486:461–467
Rutz C (2008) The establishment of an urban bird population. J Anim Ecol 77:1008–1019
Saarikivi J, Herczeg G (2014) Do hole-nesting passerine birds fare well at artificial suburban forest edges? Ann Zool Fenn 51:488–494
Salmón P, Nilsson J, Nord A, Bensch S, Isaksson C (2016) Urban environment shortens telomere length in nestling great tits, Parus major. Biol Lett 12:20160155
SAS Institute (2015) JMP®, Version 12. SAS Institute Inc, Cary
Searcy W, Peters S, Nowicki S (2004) Effects of early nutrition on growth rate and adult size in song sparrow Melospiza melodia. J Avian Biol 35:269–279
Seress G, Liker A (2015) Habitat urbanization and its effects on birds. Acta Zool Acad Sci 61:373–408
Sherry D (1984) Food storage by black-capped chickadees: memory for the location and contents of caches. Anim Behav 32:451–464
Shochat E (2004) Credit or debit? Resource input changes population dynamics of city-slicker birds. Oikos 106:622–626
Slabbekoorn H (2013) Songs of the city: noise-dependent spectral plasticity in the acoustic phenotype of urban birds. Anim Behav 85:1089–1099
Slabbekoorn H, Ripmeester E (2008) Birdsong and anthropogenic noise: implications and applications for conservation. Mol Ecol 17:72–83
Southwood T (1961) The number of species of insect associated with various trees. J Anim Ecol 30:1–8
Stracey C, Robinson S (2012) Are urban habitats ecological traps for a native songbird? Seasonal productivity, apparent survival, and site fidelity in urban and rural habitats. J Avian Biol 43:50–60
Sullivan B, Wood C, Iliff M, Bonney R, Fink D, Kelling S (2009) eBird: a citizen-based bird observation network in the biological sciences. Biol Conserv 142:2282–2292
Sumasgutner P, Nemeth E, Tebb G, Krenn H, Gamauf A (2014) Hard times in the city – attractive nest sites but insufficient food supply leads to low reproductive success rates in a bird of prey. Front Zool 11:48–61
The GIMP Team (1997-2014) GIMP 2.8.10. https://www.gimp.org
Townsend A, Sillett T, Lany N, Kaiser S, Rodenhouse N, Webster M, Holmes R (2013) Warm springs, early lay dates, and double brooding in a North American migratory songbird, the black-throated blue warbler. PLoS One 8:e59467. doi:10.1371/journal.pone.0059467
Tremblay I, Thomas D, Blondel J, Perret P, Lambrechts M (2005) The effect of habitat quality on foraging patterns, provisioning rate and nestling growth in Corsican blue tits Parus caeruleus. Ibis 147:17–24
Tveraa T, Sether E, Aanes R, Erikstad K (1998) Regulation of food provisioning in the Antarctic petrel; the importance of parental body condition and chick body mass. J Anim Ecol 67:699–704
Van Noordwijk A, McCleery R, Perrins C (1995) Selection for the timing of great tit breeding in relation to caterpillar growth and temperature. J Anim Ecol 64:451–458
Verhulst S, Nilsson J (2008) The timing of birds’ breeding seasons: a review of experiments that manipulated timing of breeding. Philos Trans R Soc B 363:399–410
Vincze E, Seress G, Lagisz M, Nakagawa S, Dingemanse N, Sprau P (2017) Does urbanization affect predation of bird nests? A meta-analysis. Front Ecol Evol 5:29
Visser M, van Noordwijk A, Tinbergen J, Lessells C (1998) Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc R Soc Lond Biol 265:1867–1870. doi:10.1098/rspb.1998.0514
Wawrzyniak J, Kaliński A, Glądalski M, Bańbura M, Markowski M, Skwarska J et al (2015) Long-term variation in laying date and clutch size of the great tit Parus major in central Poland: a comparison between urban parkland and deciduous forest. Ardeola 62:311–322
Weldon A, Haddad N (2005) The effects of patch shape on indigo buntings: evidence for an ecological trap. Ecology 86:1422–1431
Wilson S, Arcese P (2003) El Niño drives timing of breeding but not population growth in the song sparrow (Melospiza melodia). Proc Natl Acad Sci U S A 100:1139–1142
Acknowledgements
The authors would like to thank S. Joly and members of the BEAC Lab at Thompson Rivers University for assisting with the capture and banding of chickadees, as well as all the field technicians who assisted with data collection and field work. Funding was provided by Natural Sciences and Engineering Research Council of Canada Discovery Grants to M.W.R. and K.A.O, and a Natural Sciences and Engineering Research Council of Canada Industrial Postgraduate Scholarship to K.L.D. Marini.
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Marini, K.L.D., Otter, K.A., LaZerte, S.E. et al. Urban environments are associated with earlier clutches and faster nestling feather growth compared to natural habitats. Urban Ecosyst 20, 1291–1300 (2017). https://doi.org/10.1007/s11252-017-0681-2
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DOI: https://doi.org/10.1007/s11252-017-0681-2