Skip to main content

Advertisement

Log in

From eggs to fledging: negative impact of urban habitat on reproduction in two tit species

  • Original Article
  • Published:
Journal of Ornithology Aims and scope Submit manuscript

Abstract

The exploration of the effects of urbanization on bird demography has attracted much attention, and several studies found lower reproductive success in towns, which suggested strong environmental constraints. Here, we conducted a 3-year study to explore the consequences of urbanization on the breeding success of two species that originated in forests, the Blue Tit Cyanistes caeruleus and the Great Tit Parus major. In two replicates of urban and forest habitats, we studied the components of reproductive success. In one replicate of each habitat, we quantified nestling growth over the three breeding seasons, and we collected data on egg quality during one breeding season. The general picture that emerges from our finding is that in urban sites breeding success was lower with smaller clutch sizes, higher clutch, higher brood failure rates and lower survival rates. Our results also showed reduced growth in urban habitats, at the embryonic and nestling stages, with potential adverse consequences on fitness. Crucial ecological factors could explain the observed contrasts between the habitats, and food limitation is among the most likely. Overall, we demonstrated the negative effects of urbanization on the reproductive success of forest birds, and our results were consistent between species and geographic areas for these negative effects. Our results suggest a mismatch between urban environments and the habitat exploitation abilities that birds have evolved in their native forest ecosystems.

Zusammenfassung

Vom Ei zum flüggen Jungvogel: negativer Einfluss von urbanem Lebensraum auf die Reproduktion bei zwei Meisenarten

Die Erforschung der Effekte von Urbanisierung auf Vogeldemografie hat viel Aufmerksamkeit auf sich gezogen und einige Studien haben einen niedrigeren Reproduktionserfolg innerhalb von Städten gefunden. Dies weist auf starke Umwelteinflüsse hin. In unserer dreijährigen Studie haben wir die Folgen der Urbanisierung auf den Bruterfolg von Blaumeisen C. caeruleus und Kohlmeisen P. major, welche beide ursprünglich in Wäldern vorkamen, erforscht. Auf je zwei Untersuchungsflächen je Lebensraum haben wir Komponenten des Reproduktionserfolgs untersucht. In einem Gebiet pro Brutsaison haben wir über je drei Jahre das Kükenwachstum aufgenommen, zudem in einem Jahr die Eiqualität untersucht. Das generelle Bild ist, dass in urbanem Gelände Bruterfolg und Gelegegröße geringer, Gelegeverluste und Brutverluste höher und die Überlebensraten geringer waren. Zudem war die Wachstumsrate in urbanen Lebensräumen während der embryonalen Phase und der Nestlingsphase geringer, was potentiell negative Auswirkungen auf die Fitness hat. Die beobachteten Unterschiede zwischen den Lebensräumen könnten von wichtigen ökologischen Faktoren erklärt werden, wobei Nahrungsbegrenzung vermutlich einer der wahrscheinlichsten ist. Wir haben den negativen Einfluss von Urbanisierung auf den Reproduktionserfolg von Waldvögeln gezeigt. Diese negativen Effekte stimmten zwischen den Arten und den geografischen Gebieten überein. Unsere Ergebnisse zeigen eine Diskrepanz zwischen urbaner Umwelt und den Fähigkeiten der Vögel, diesen Lebensraum zu nutzen, welche die welche Vögel in ihren ursprünglichen Lebensräumen evolviert haben.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alonso-Alvarez C, Bertrand S, Devevey G et al (2004) An experimental test of the dose-dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity. Am Nat 164:651–659. doi:10.1086/424971

    Article  PubMed  Google Scholar 

  • Arnold KE, Ramsay SL, Henderson L et al (2010) Seasonal variation in diet quality: antioxidants, invertebrates and Blue Titis Cyanistes caeruleus. Biol J Linn Soc 99:708–717

    Article  Google Scholar 

  • Bańbura M, Sulikowska-Drozd A, Kaliński A et al (2010) Egg size variation in Blue Tits Cyanistes caeruleus and Great Tits Parus major in relation to habitat differences in snail abundance. Acta Ornithol 45:121–129. doi:10.3161/000164510X551264

    Article  Google Scholar 

  • Bates D (2010) lme4: Mixed-effects modeling with R. http//lme4.r-forge.r-project.Org/b. Accessed 27 Sept 2013

  • Battin J (2007) When good animals love bad habitats: ecological traps and the conservation of animal populations. Conserv Biol 18:1482–1491

    Article  Google Scholar 

  • Biard C, Surai PF, Møller AP (2005) Effects of carotenoid availability during laying on reproduction in the Blue Tit. Oecologia 144:32–44. doi:10.1007/s00442-005-0048-x

    Article  PubMed  Google Scholar 

  • Blondel J (2007) Coping with habitat heterogeneity: the story of Mediterranean Blue Tits. J Ornithol 148:3–15. doi:10.1007/s10336-007-0161-1

    Article  Google Scholar 

  • Blount JD, Houston DC, Moller AP (2000) Why egg yolk is yellow. Trends Ecol Evol 15:47–49

    Article  PubMed  Google Scholar 

  • Blount JD, Surai PF, Nager RG et al (2002) Carotenoids and egg quality in the Lesser blackbacked gull Larus fuscus: a supplemental feeding study of maternal effects. Proc R Soc Lond B 269:29–36. doi:10.1098/rspb.2001.1840

    Article  CAS  Google Scholar 

  • Both C, Visser ME (2003) Density dependence, territoriality, and divisibility of resources: from optimality models to population processes. Am Nat 161:326–336. doi:10.1086/346098

    Article  PubMed  Google Scholar 

  • Chace JF, Walsh JJ (2006) Urban effects on native avifauna: a review. Landsc Urban Plan 74:46–69. doi:10.1016/j.landurbplan.2004.08.007

    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. doi:10.1111/j.1474-919X.2008.00899.x

    Article  Google Scholar 

  • Christians JK (2002) Avian egg size: variation within species and inflexibility within individuals. Biol Rev Camb Philos Soc 77:1–26

    Article  PubMed  Google Scholar 

  • Cleasby IR, Nakagawa S, Gillespie DOS, Burke T (2010) The influence of sex and body size on nestling survival and recruitment in the House sparrow. Biol J Linn Soc 101:680–688. doi:10.1111/j.1095-8312.2010.01515.x

    Article  Google Scholar 

  • Cramp S, Perrins CM, Brooks DJ (1993) The birds of western Palearctic—volume VII. Handbook of the birds of Europe, the Middle East and North Africa. Oxford University Press, New York, pp 225–281

    Google Scholar 

  • Cresswell W, McCleery RH (2003) How Great Tits maintain synchronization of their hatch date with food supply in response to long-term variability in temperature. J Anim Ecol 72:356–366. doi:10.1046/j.1365-2656.2003.00701.x

    Article  Google Scholar 

  • Dominoni D, Quetting M, Partecke J (2013) Artificial light at night advances avian reproductive physiology. Proc R Soc Lond B 280:20123017

    Article  Google Scholar 

  • Drent PJ, Woldendorp JW (1989) Acid rain and eggshells. Nature 339:431

    Article  Google Scholar 

  • Eeva T, Lehikoinen E, Nurmi J (1994) Effects of ectoparasites on breeding success of Great Tits (Parus major) and Pied flycatchers (Ficedula hypoleuca) in an air pollution gradient. Can J Zool 72:624–635. doi:10.1139/z94-085

    Article  Google Scholar 

  • Eising C, Pavlova D, Groothuis T (2008) Maternal yolk androgens in European Starlings: affected by social environment or individual traits of the mother? Behaviour 145:51–72

    Article  Google Scholar 

  • Faivre B, Préault M, Théry M et al (2001) Breeding strategy and morphological characters in an urban population of Blackbirds, Turdus merula. Anim Behav 61:969–974. doi:10.1006/anbe.2000.1669

    Article  Google Scholar 

  • Farnsworth G, Simons T, Brawn J (2001) How many baskets? Clutch sizes that maximize annual fecundity of multiple-brooded birds. Auk 118:973–982

    Article  Google Scholar 

  • Fontaine JJ, Martin TE (2006) Parent birds assess nest predation risk and adjust their reproductive strategies. Ecol Lett 9:428–434. doi:10.1111/j.1461-0248.2006.00892.x

    Article  CAS  PubMed  Google Scholar 

  • Geue D, Partecke J (2008) Reduced parasite infestation in urban Eurasian Blackbirds (Turdus merula): a factor favoring urbanization? Can J Zool 86:1419–1425. doi:10.1139/Z08-129

    Article  Google Scholar 

  • Graveland J, Berends AE (1997) Timing of the calcium intake and effect of calcium deficiency on behaviour and egg laying in captive Great Tits, Parus major. Physiol Zool 70:74–84

    Article  CAS  PubMed  Google Scholar 

  • Grégoire A (2003) Démographie et différenciation chez le Merle Noir Turdus merula: lien avec l’habitat et les relations hôtes-parasites. Doctoral thesis, University of Bourgogne, Dijon

  • Grimm NB, Faeth SH, Golubiewski NE et al (2008) Global change and the ecology of cities. Science 319:756–760. doi:10.1126/science.1150195

    Article  CAS  PubMed  Google Scholar 

  • Groothuis TGG, Schwabl H (2008) Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Philos Trans R Soc Lond B 363:1647–1661. doi:10.1098/rstb.2007.0007

    Article  CAS  Google Scholar 

  • Groothuis TGG, Müller W, von Engelhardt N et al (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 29:329–352. doi:10.1016/j.neubiorev.2004.12.002

    Article  CAS  PubMed  Google Scholar 

  • Hargitai R, Matus Z, Hegyi G et al (2006) Antioxidants in the egg yolk of a wild passerine: differences between breeding seasons. Comp Biochem Physiol B 143:145–152. doi:10.1016/j.cbpb.2005.11.001

    Article  PubMed  Google Scholar 

  • Hõrak P (1993) Low fledging success of urban Great Tits. Ornis Fenn 70:168–172

    Google Scholar 

  • Hõrak P, Jenni-Eiermann S, Ots I (1999) Do Great Tits (Parus major) starve to reproduce? Oecologia 119:293–299

    Article  Google Scholar 

  • Hõrak P, Vellau H, Ots I, Møller a P (2000) Growth conditions affect carotenoid-based plumage coloration of Great Tit nestlings. Naturwissenschaften 87:460–464

    Article  PubMed  Google Scholar 

  • Hõrak P, Surai P, Moller A (2002) Fat-soluble antioxidants in the eggs of Great Tits Parus major in relation to breeding habitat and laying sequence. Avian Sci 2:123–130

    Google Scholar 

  • Isaksson C (2009) The chemical pathway of arotenoids: from plants to birds. Ardea 97:125–128

    Article  Google Scholar 

  • Isaksson C, Andersson S (2007) Carotenoid diet and nestling provisioning in urban and rural Great Tits Parus major. J Avian Biol 38:564–572. doi:10.1111/j.2007.0908-8857.04030.x

    Article  Google Scholar 

  • Isaksson C, Johansson A, Andersson S (2008) Egg yolk carotenoids in relation to habitat and reproductive investment in the Great Tit Parus major. Physiol Biochem Zool 81:112–118. doi:10.1086/522650

    Article  CAS  PubMed  Google Scholar 

  • Kaliński A, Wawrzyniak J, Bańbura M et al (2009) Haemoglobin concentration and body condition of nestling Great Tits Parus major: a comparison of first and second broods in two contrasting seasons. Ibis 151:667–676. doi:10.1111/j.1474-919X.2009.00959.x

    Article  Google Scholar 

  • Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53:983–997. doi:10.2307/2533558

    Article  CAS  PubMed  Google Scholar 

  • Kilgas P, Tilgar V, Mänd R (2007) Physiological condition of incubating and brood rearing female Great Tits Parus major in two contrasting habitats. Acta Ornithol 42:129–136

    Article  Google Scholar 

  • Koutsos EA, Clifford AJ, Calvert CC, Klasing KC (2003) Maternal carotenoid status modifies the incorporation of dietary carotenoids into immune tissues of growing chickens (Gallus gallus domesticus). J Nutr 133:1132–1138

    CAS  PubMed  Google Scholar 

  • Krist M (2011) Egg size and offspring quality: a meta-analysis in birds. Biol Rev Camb Philos Soc 86:692–716. doi:10.1111/j.1469-185X.2010.00166.x

    Article  PubMed  Google Scholar 

  • Lambrechts MM, Rieux A, Galan M-J et al (2008) Double-brooded Great Tits (Parus major) in Mediterranean oak habitats: do first broods always perform better than second broods? Russ J Ecol 39:516–522. doi:10.1134/S1067413608070084

    Article  Google Scholar 

  • Luniak M (2004) Synurbization–adaptation of animal wildlife to urban development. In: Shaw WW, Harris LK, Vandruff L (eds) Proceedings of 4th international symposium urban wildlife conservation, Tucson, pp 50–55

  • Marciniak B, Nadolski J, Nowakowska M et al (2007) Habitat and annual variation in arthropod abundance affects Blue Tit Cyanistes caeruleus reproduction. Acta Ornithol 42:53–62

    Article  Google Scholar 

  • Marri V, Richner H (2014) Yolk carotenoids increase fledging success in Great Tit nestlings. Oecologia 176:371–377. doi:10.1007/s00442-014-3051-2

    Article  PubMed  Google Scholar 

  • Martin T (1987) Food as a limit on breeding birds: a life-history perspective. Annu Rev Ecol Syst 18:453–487

    Article  Google Scholar 

  • Marzal A, de Lope F, Navarro C, Møller AP (2005) Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142:541–545. doi:10.1007/s00442-004-1757-2

    Article  PubMed  Google Scholar 

  • Marzluff J (2001) Worldwide urbanization and its effects on birds. In: Marzluff JM, Bowman R, Donnelly R (eds) Avian ecology and conservation in an urbanizing world. Springer, New York, pp 19–47

    Chapter  Google Scholar 

  • McGraw KJ, Adkins-Regan E, Parker RS (2005) Maternally derived carotenoid pigments affect offspring survival, sex ratio, and sexual attractiveness in a colorful songbird. Naturwissenschaften 92:375–380. doi:10.1007/s00114-005-0003-z

    Article  CAS  PubMed  Google Scholar 

  • McKinney M, Lockwood J (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14:450–453

    Article  PubMed  Google Scholar 

  • Mennechez G, Clergeau P (2006) Effect of urbanisation on habitat generalists: starlings not so flexible? Acta Oecol 30:182–191. doi:10.1016/j.actao.2006.03.002

    Article  Google Scholar 

  • Monrós J, Belda E, Barba E (1998) Delays of the hatching dates in Great Tits Parus major: effects on breeding performance. Ardea 86:213–220

    Google Scholar 

  • Naef-Daenzer L, Nager R, Keller LF, Naef-Daenzer B (2004) Are hatching delays a cost or a benefit for Great Tit Parus major parents? Ardea 92:229–238

    Google Scholar 

  • Nilsson J, Stjernman M, Nilsson J (2008) Experimental reduction of incubation temperature affects both nestling and adult Blue Tits Cyanistes caeruleus. J Avian Biol 39:553–559. doi:10.1111/j.2008.0908-8857.04199.x

    Article  Google Scholar 

  • Ouyang JQ, Quetting M, Hau M (2012) Corticosterone and brood abandonment in a passerine bird. Anim Behav 84:261–268. doi:10.1016/j.anbehav.2012.05.006

    Article  Google Scholar 

  • Parejo D, Danchin E (2006) Brood size manipulation affects frequency of second clutches in the Blue Tit. Behav Ecol Sociobiol 60:184–194. doi:10.1007/s00265-005-0155-z

    Article  Google Scholar 

  • Peach WJ, Vincent KE, Fowler JA, Grice PV (2008) Reproductive success of House sparrows along an urban gradient. Anim Conserv 11:493–503. doi:10.1111/j.1469-1795.2008.00209.x

    Article  Google Scholar 

  • Porlier M, Charmantier A, Bourgault P et al (2012) Variation in phenotypic plasticity and selection patterns in Blue Tit breeding time: between-and within-population comparisons. J Anim Ecol 81:1041–1051. doi:10.1111/j.1365-2656.2012.01996.x

    Article  PubMed  Google Scholar 

  • Ratcliffe DA (1970) Changes attributable to pesticides in egg breakage frequency and eggshell thickness in some British birds. J Appl Ecol 7:67–115

    Article  Google Scholar 

  • Richner H (1989) Habitat-specific growth and fitness in Carrion crows (Corvus corone corone). J Anim Ecol 58:427–440

    Article  Google Scholar 

  • Richner H, Oppliger A, Christe P (1993) Effect of an ectoparasite on reproduction in Great Tits. J Anim Ecol 62:703–710

    Article  Google Scholar 

  • Safran RJ, McGraw KJ, Pilz KM, Correa SM (2010) Egg-yolk androgen and carotenoid deposition as a function of maternal social environment in Barn swallows Hirundo rustica. J Avian Biol 41:470–478. doi:10.1111/j.1600-048X.2010.04962.x

    Article  Google Scholar 

  • Saino N, Bertacche V, Ferrari RP et al (2002) Carotenoid concentration in Barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proc R Soc Lond B 269:1729–1733. doi:10.1098/rspb.2002.2088

    Article  CAS  Google Scholar 

  • Sanz J, García-Navas V, Ruiz-Peinado J (2010) Habitat type and nest-site characteristics on the breeding performance of Great and Blue Tits (Parus major and P. caeruleus) in a Mediterranean landscape. Ornis Fenn 87:1–11

    Google Scholar 

  • Schew W, Ricklefs R (1998) Developmental plasticity. In: Starck JM, Ricklefs RE (eds) Avian growth and development. Oxford University Press, New York, pp 288–304

    Google Scholar 

  • Seress G, Bókony V, Pipoly I et al (2012) Urbanization, nestling growth and reproductive success in a moderately declining House sparrow population. J Avian Biol 43:403–414. doi:10.1111/j.1600-048X.2012.05527.x

    Article  Google Scholar 

  • Slabbekoorn H (2013) Songs of the city: noise-dependent spectral plasticity in the acoustic phenotype of urban birds. Anim Behav 85:1089–1099. doi:10.1016/j.anbehav.2013.01.021

    Article  Google Scholar 

  • Solonen T (2001) Breeding of the Great Tit and Blue Tit in urban and rural habitats in southern Finland. Ornis Fenn 78:49–60

    Google Scholar 

  • Starck JM, Ricklefs RE (1998) Avian growth and development: evolution within the altricial-precocial spectrum. Oxford University Press, New York

    Google Scholar 

  • Stracey CM, Robinson SK (2011) Are urban habitats ecological traps for a native songbird? Seson-long productivity, apparent survival, and site fidelity in urban and rural habitats. J Avian Biol 43:50–60

    Article  Google Scholar 

  • Styrsky JD, Eckerle KP, Thompson CF (1999) Fitness-related consequences of egg mass in nestling House wrens. Proc R Soc Lond B 266:1253. doi:10.1098/rspb.1999.0771

    Article  Google Scholar 

  • Surai PF, Speake BK (1998) Distribution of carotenoids from the yolk to the tissues of the chick embryo. J Nutr Biochem 9:645–651. doi:10.1016/S0955-2863(98)00068-0

    Article  CAS  Google Scholar 

  • Surai P, Speake B, Sparks N (2001) Carotenoids in avian nutrition and embryonic development. 2. Antioxidant properties and discrimination in embryonic tissues. J Poult Sci 38:117–145

    Article  CAS  Google Scholar 

  • Van Balen JH (1973) A comparative study of the breeding ecology of the Great tit, Parus major, in different habitats. Ardea 61:1–93

    Google Scholar 

  • Verhulst S, Nilsson J-A (2008) The timing of birds’ breeding seasons: a review of experiments that manipulated timing of breeding. Philos Trans R Soc Lond B 363:399–410. doi:10.1098/rstb.2007.2146

    Article  Google Scholar 

  • Visser ME, Holleman LJM, Gienapp P (2006) Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird. Oecologia 147:164–172. doi:10.1007/s00442-005-0299-6

    Article  PubMed  Google Scholar 

  • Warton D, Hui F (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10

    Article  PubMed  Google Scholar 

  • Weggler M (2006) Constraints on, and determinants of, the annual number of breeding attempts in the multi-brooded Black redstart Phoenicurus ochruros. Ibis 148:273–284. doi:10.1111/j.1474-919X.2006.00527.x

    Article  Google Scholar 

  • Williams TD (1994) Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biol Rev Camb Philos Soc 69:35–59. doi:10.1111/j.1469-185X.1994.tb01485.x

    Article  CAS  PubMed  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ et al (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgments

The Regional Council of Burgundy and the Center for Research and Higher Education provided financial support for this work. The study site in Franche-Comté belongs to the Long Term Ecological Research (LTER) Network “Zone Atelier Arc Jurassien” (http://zaaj.univ-fcomte.fr/). We thank S. Garnier who helped with the fieldwork. We thank G. Sorci, P. Christ, A. Grégoire, S. Cornet and M. Galipaud for statistical analyses and their comments on the results. Many thanks to I. Stewart for his comments on an earlier version of this manuscript. The authors also greatly thank D. Dominoni and the anonymous reviewer for their helpful comments on this paper. The study conforms to the legal requirements of France.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Juliette Bailly.

Additional information

Communicated by F. Bairlein.

Electronic supplementary material

Meteorological conditions during the tit reproduction season (March–June) in Burgundy and Franche-Comté for the 3 years of study (2012–2014): minimum and maximum monthly temperatures (°C); cumulative rainfall per month (mm); cumulative sunshine per month (h). Meteorological stations used were Dijon-Longvic for Burgundy sites (47°27N, 5°09E) and Besançon-Thise for Franche-Comté sites (47°25N, 5°99E). Data obtained with permission from http://www.infoclimat.fr (all rights reserved).

Supplementary information (PDF 431 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bailly, J., Scheifler, R., Berthe, S. et al. From eggs to fledging: negative impact of urban habitat on reproduction in two tit species. J Ornithol 157, 377–392 (2016). https://doi.org/10.1007/s10336-015-1293-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10336-015-1293-3

Keywords

Navigation