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Population density mediates induced immune response, but not physiological condition in a well-adapted urban bird

  • Marzluff, J. M. Worldwide urbanization and its effects on birds. In Avian Ecology and Conservation in an Urbanizing World (eds Marzluff, J. et al.) 19–47 (Springer, Boston, 2001).

    Chapter 

    Google Scholar 

  • McKinney, M. L. Effects of urbanization on species richness: A review of plants and animals. Urban Ecosyst. 11, 161–176 (2008).

    Article 

    Google Scholar 

  • Luniak, M. Synurbization–adaptation of animal wildlife to urban development in Proceedings 4th international urban wildlife symposium (eds. Shaw, W., Harris, L.,Vandruff, L.) 50–55 (University of Arizona, Tucson, ARI, 2004).

  • Isaksson, C. Impact of urbanization on birds in Bird Species how they arise, modify and vanish (ed. Tietze D. T.) 235–257 (Springer, 2018).

  • Minias, P. Successful colonization of a novel urban environment is associated with an urban behavioural syndrome in a reed-nesting waterbird. Ethology 121, 1178–1190 (2015).

    Article 

    Google Scholar 

  • Møller, A. P. et al. Urban habitats and feeders both contribute to flight initiation distance reduction in birds. Behav. Ecol. 26, 861–865 (2015).

    Article 

    Google Scholar 

  • Jokimäki, J. & Suhonen, J. Distribution and habitat selection of wintering birds in urban environments. Landsc. Urban Plan. 39, 253–263 (1998).

    Article 

    Google Scholar 

  • Francis, R. A. & Chadwick, M. A. What makes a species synurbic?. Appl. Geogr. 32, 514–521 (2012).

    Article 

    Google Scholar 

  • Møller, A. P. et al. High urban population density of birds reflects their timing of urbanization. Oecologia 170, 867–875 (2012).

    PubMed 
    Article 
    ADS 

    Google Scholar 

  • Tella, J. L. et al. Offspring body condition and immunocompetence are negatively affected by high breeding densities in a colonial seabird: A multiscale approach. Proc. R. Soc. B 268, 1455–1461 (2001).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Savoca, M. S., Bonter, D. N., Zuckerberg, B., Dickinson, J. L. & Ellis, J. C. Nesting density is an important factor affecting chick growth and survival in the Herring Gull. Condor 113, 565–571 (2011).

    Article 

    Google Scholar 

  • Minias, P., Włodarczyk, R. & Janiszewski, T. Opposing selective pressures may act on the colony size in a waterbird species. Evol. Ecol. 29, 283–297 (2015).

    Article 

    Google Scholar 

  • Kamiński, M. et al. Density-dependence of nestling immune function and physiological condition in semi-precocial colonial bird: A cross-fostering experiment. Front. Zool. 18, 7 (2021).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Ward, P. & Zahavi, A. The importance of certain assemblages of birds as “information-centres” for food-finding. Ibis 115, 517–534 (1973).

    Article 

    Google Scholar 

  • Danchin, E. & Wagner, R. H. The evolution of coloniality: The emergence of new perspectives. Trends Ecol. Evol. 12, 342–347 (1997).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Brown, C. R. & Brown, M. B. Coloniality in the Cliff Swallow: The Effect of Group Size on Social Behavior (University of Chicago Press, 1996).

    Google Scholar 

  • Evans, J. C., Votier, S. C. & Dall, S. R. Information use in colonial living. Biol. Rev. 91, 658–672 (2016).

    PubMed 
    Article 

    Google Scholar 

  • Brown, C. R. & Brown, M. B. Avian coloniality. In Current Ornithology (eds Brown, C. R. & Brown, M. B.) 1–82 (Springer, Boston, 2001).

    Google Scholar 

  • Coulson, J. C., Duncan, N. & Thomas, C. Changes in the breeding biology of the herring gull (Larus argentatus) induced by reduction in the size and density of the colony. J. Anim. Ecol. 51, 739–756 (1982).

    Article 

    Google Scholar 

  • Ots, I. & Horak, P. Great tits Parus major trade health for reproduction. Proc. R. Soc. B. 263, 1443–1447 (1996).

    CAS 
    PubMed 
    Article 
    ADS 

    Google Scholar 

  • Richner, H. & Tripet, F. Ectoparasitism and the trade-off between current and future reproduction. Oikos 86, 535–538 (1999).

    Article 

    Google Scholar 

  • Fokkema, R. W., Ubels, R. & Tinbergen, J. M. Great tits trade off future competitive advantage for current reproduction. Behav. Ecol. 27, 1656–1664 (2016).

    Google Scholar 

  • Horak, P. & Leberton, J. D. Survival of adult Great Tits Parus major in relation to sex and habitat; a comparison of urban and rural populations. Ibis 140, 205–209 (1998).

    Article 

    Google Scholar 

  • Stracey, C. M. & Robinson, S. K. Are urban habitats ecological traps for a native songbird? Season-long productivity, apparent survival, and site fidelity in urban and rural habitats. J. Avian Biol. 43, 50–60 (2012).

    Article 

    Google Scholar 

  • Sepp, T., McGraw, K. J., Kaasik, A. & Giraudeau, M. 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 (2018).

    Article 
    ADS 

    Google Scholar 

  • Phillips, J. N., Gentry, K. E., Luther, D. A. & Derryberry, E. P. Surviving in the city: Higher apparent survival for urban birds but worse condition on noisy territories. Ecosphere 9, e02440 (2018).

    Article 

    Google Scholar 

  • Johnston, R. F. & Janiga, M. Feral Pigeons (Oxford University Press on Demand, 1995).

    Google Scholar 

  • Giunchi, D., Mucci, N., Bigi, D., Mengoni, C. & Baldaccini, N. E. Feral pigeon populations: Their gene pool and links with local domestic breeds. Zoology 142, 125817 (2020).

    PubMed 
    Article 

    Google Scholar 

  • Sol, D. Artificial selection, naturalization, and fitness: Darwin’s pigeons revisited. Biol. J. Linn. Soc. 93, 657–665 (2008).

    Article 

    Google Scholar 

  • Giunchi, D., Albores-Barajas, Y. V., Baldaccini, N. E., Vanni, L. & Soldatini, C. Feral pigeons: Problems, dynamics and control methods. In Integrated Pest Management and Pest Control. Current and Future Tactics (eds Soloneski, S. & Larramendy, M.) 215–240 (InTechOpen, London, 2012).

    Google Scholar 

  • Senar, J. C., Navalpotro, H., Pascual, J. & Montalvo, T. Nicarbazin has no effect on reducing feral pigeon populations in Barcelona. Pest Manag. Sci. 77, 131–137 (2021).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Rose, E., Nagel, P. & Haag-Wackernagel, D. Spatio-temporal use of the urban habitat by feral pigeons (Columba livia). Behav. Ecol. Sociobiol. 60, 242–254 (2006).

    Article 

    Google Scholar 

  • Corbel, H. et al. Stress response varies with plumage colour and local habitat in feral pigeons. J. Ornithol. 157, 825–837 (2016).

    Article 

    Google Scholar 

  • Møller, A. P., Merino, S., Brown, C. R. & Robertson, R. J. Immune defense and host sociality: A comparative study of swallows and martins. Am. Nat. 158, 136–145 (2001).

    PubMed 
    Article 

    Google Scholar 

  • Drzewińska-Chańko, J. et al. Immunocompetent birds choose larger breeding colonies. J. Anim. Ecol. https://doi.org/10.1111/1365-2656.13540 (2021).

    Article 
    PubMed 

    Google Scholar 

  • Saino, N., Suffritti, C., Martinelli, R., Rubolini, D. & Møller, A. P. Immune response covaries with corticosterone plasma levels under experimentally stressful conditions in nestling barn swallows (Hirundo rustica). Behav. Ecol. 14, 318–325 (2003).

    Article 

    Google Scholar 

  • Goutte, A. et al. Long-term survival effect of corticosterone manipulation in black-legged kittiwakes. Gen. Comp. Endocrinol. 167, 246–251 (2010).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Møller, A. P., Christe, P., Erritzøe, J. & Mavarez, J. Condition, disease and immune defence. Oikos 83, 301–306 (1998).

    Article 

    Google Scholar 

  • Navarro, C., Marzal, A., De Lope, F. & Møller, A. P. Dynamics of an immune response in house sparrows Passer domesticus in relation to time of day, body condition and blood parasite infection. Oikos 101, 291–298 (2003).

    Article 

    Google Scholar 

  • Toïgo, C., Gaillard, J. M., Van Laere, G., Hewison, M. & Morellet, N. How does environmental variation influence body mass, body size, and body condition? Roe deer as a case study. Ecography 29, 301–308 (2006).

    Article 

    Google Scholar 

  • Jacquin, L. et al. A potential role for parasites in the maintenance of color polymorphism in urban birds. Oecologia 173, 1089–1099 (2013).

    CAS 
    PubMed 
    Article 
    ADS 

    Google Scholar 

  • Meillère, A., Brischoux, F., Parenteau, C. & Angelier, F. Influence of urbanization on body size, condition, and physiology in an urban exploiter: A multi-component approach. PLoS ONE https://doi.org/10.1371/journal.pone.0135685 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Peig, J. & Green, A. J. New perspectives for estimating body condition from mass/length data: The scaled mass index as an alternative method. Oikos 118, 1883–1891 (2009).

    Article 

    Google Scholar 

  • Jacquin, L. et al. Melanin-based coloration is related to parasite intensity and cellular immune response in an urban free living bird: The feral pigeon Columba livia. J. Avian Biol. 42, 11–15 (2011).

    Article 

    Google Scholar 

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

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Audet, J. N., Ducatez, S. & Lefebvre, L. The town bird and the country bird: Problem solving and immunocompetence vary with urbanization. Behav. Ecol. 27, 637–644 (2016).

    Article 

    Google Scholar 

  • Kurucz, K., Purger, J. J. & Batáry, P. Urbanization shapes bird communities and nest survival, but not their food quantity. Glob. Ecol. Conserv. 26, e01475 (2021).

    Article 

    Google Scholar 

  • Partecke, J., Schwabl, I. & Gwinner, E. Stress and the city: Urbanization and its effects on the stress physiology in European blackbirds. Ecology 87, 1945–1952 (2006).

    PubMed 
    Article 

    Google Scholar 

  • Bailly, J. et al. Negative impact of urban habitat on immunity in the great tit Parus major. Oecologia 182, 1053–1062 (2016).

    PubMed 
    Article 
    ADS 

    Google Scholar 

  • Glądalski, M. et al. Differences in use of bryophyte species in tit nests between two contrasting habitats: An urban park and a forest. Eur. Zool. J. 88, 807–815 (2021).

    Article 

    Google Scholar 

  • Tella, J. L., Scheuerlein, A. & Ricklefs, R. E. Is cell–mediated immunity related to the evolution of life-history strategies in birds?. Proc. R. Soc. B 269, 1059–1066 (2002).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Brown, C. R. & Brown, M. B. Empirical measurement of parasite transmission between groups in a colonial bird. Ecology 85, 1619–1626 (2004).

    Article 

    Google Scholar 

  • O’Brien, V. A. & Brown, C. R. Group size and nest spacing affect Buggy Creek virus (Togaviridae: Alphavirus) infection in nestling house sparrows. PLoS ONE 6, e25521 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar 

  • Wilcoxen, T. E. et al. Effects of bird-feeding activities on the health of wild birds. Conserv. Physiol. 3, cov058 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Moyers, S. C., Adelman, J. S., Farine, D. R., Thomason, C. A. & Hawley, D. M. Feeder density enhances house finch disease transmission in experimental epidemics. Philos. Trans. R. Soc. B 373, 20170090 (2018).

    Article 
    CAS 

    Google Scholar 

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

    PubMed 
    Article 
    ADS 

    Google Scholar 

  • Watson, H., Videvall, E., Andersson, M. N. & Isaksson, C. Transcriptome analysis of a wild bird reveals physiological responses to the urban environment. Sci. Rep. 7, 44180 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar 

  • Hasselquist, D. & Nilsson, J. Å. Physiological mechanisms mediating costs of immune responses: What can we learn from studies of birds?. Anim. Behav. 83, 1303–1312 (2012).

    Article 

    Google Scholar 

  • Biard, C., Monceau, K., Motreuil, S. & Moreau, J. Interpreting immunological indices: The importance of taking parasite community into account. An example in blackbirds Turdus merula. Methods Ecol. Evol. 6, 960–972 (2015).

    Article 

    Google Scholar 

  • Leclaire, S., Czirják, G. Á., Hammouda, A. & Gasparini, J. Feather bacterial load shapes the trade-off between preening and immunity in pigeons. BMC Evol. Biol. 15, 60 (2015).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Vinkler, M., Adelman, J. S. & Ardia, D. R. Evolutionary and ecological immunology. In Avian Immunology 3rd edn (eds Kaspers, B. et al.) 519–558 (Academic Press, London, 2021).

    Google Scholar 

  • Davis, A. K., Maney, D. L. & Maerz, J. C. The use of leukocyte profiles to measure stress in vertebrates: A review for ecologists. Funct. Ecol. 22, 760–772 (2008).

    Article 

    Google Scholar 

  • Indykiewicz, P., Podlaszczuk, P., Kamiński, M., Włodarczyk, R. & Minias, P. Central–periphery gradient of individual quality within a colony of Black-headed Gulls. Ibis 161, 744–758 (2019).

    Article 

    Google Scholar 

  • Vleck, C. M., Vertalino, N., Vleck, D. & Bucher, T. L. Stress, corticosterone, and heterophil to lymphocyte ratios in free-living Adélie penguins. Condor 102, 392–400 (2000).

    Article 

    Google Scholar 

  • Davis, A. K., Cook, K. C. & Altizer, S. Leukocyte profiles in wild house finches with and without mycoplasmal conjunctivitis, a recently emerged bacterial disease. EcoHealth 1, 362–373 (2004).

    Article 

    Google Scholar 

  • Lobato, E., Moreno, J., Merino, S., Sanz, J. J. & Arriero, E. Haematological variables are good predictors of recruitment in nestling pied flycatchers (Ficedula hypoleuca). Ecoscience 12, 27–34 (2005).

    Article 

    Google Scholar 

  • Bobby Fokidis, H., Greiner, E. C. & Deviche, P. Interspecific variation in avian blood parasites and haematology associated with urbanization in a desert habitat. J. Avian Biol. 39, 300–310 (2008).

    Article 

    Google Scholar 

  • Padgett, D. A. & Glaser, R. How stress influences the immune response. Trends Immunol. 24, 444–448 (2003).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Dimitrov, S. et al. Cortisol and epinephrine control opposing circadian rhythms in T cell subsets. Blood 113, 5134–5143 (2009).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Ilmonen, P., Hasselquist, D., Langefors, Å. & Wiehn, J. Stress, immunocompetence and leukocyte profiles of pied flycatchers in relation to brood size manipulation. Oecologia 136, 148–154 (2003).

    PubMed 
    Article 
    ADS 

    Google Scholar 

  • Minias, P., Gach, K., Włodarczyk, R. & Janiszewski, T. Colony size affects nestling immune function: A cross-fostering experiment in a colonial waterbird. Oecologia 190, 333–341 (2019).

    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar 

  • Cyr, N. E., Earle, K., Tam, C. & Romero, L. M. The effect of chronic psychological stress on corticosterone, plasma metabolites, and immune responsiveness in European starlings. Gen. Comp. Endocrinol. 154, 59–66 (2007).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Schoech, S. J., Bowman, R. & Reynolds, S. J. Food supplementation and possible mechanisms underlying early breeding in the Florida Scrub-Jay (Aphelocoma coerulescens). Horm. Behav. 46, 565–573 (2004).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Ibáñez-Álamo, J. D. et al. Physiological stress does not increase with urbanization in European blackbirds: Evidence from hormonal, immunological and cellular indicators. Sci. Total Environ. 721, 137332 (2020).

    PubMed 
    Article 
    ADS 
    CAS 

    Google Scholar 

  • Bonier, F. Hormones in the city: Endocrine ecology of urban birds. Horm. Behav. 61, 763–772 (2012).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Valdebenito, J. O. et al. Seasonal variation in sex-specific immunity in wild birds. Sci. Rep. 11, 1349 (2021).

    CAS 
    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar 

  • Hetmański, T. Timing of breeding in the Feral Pigeon Columba livia f. domestica in Słupsk (NW Poland). Acta Ornithol. 39, 105–110 (2004).

    Article 

    Google Scholar 

  • Dijkstra, C. et al. An adaptive annual rhythm in the sex of first pigeon eggs. Behav. Ecol. Sociobiol. 64, 1393–1402 (2010).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Swanson, D. L. Seasonal variation of vascular oxygen transport in the dark-eyed junco. Condor 92, 62–66 (1990).

    Article 

    Google Scholar 

  • Niedojadlo, J., Bury, A., Cichoń, M., Sadowska, E. T. & Bauchinger, U. Lower haematocrit, haemoglobin and red blood cell number in zebra finches acclimated to cold compared to thermoneutral temperature. J. Avian Biol. 49, e01596 (2018).

    Article 

    Google Scholar 

  • Roulin, A. Condition-dependence, pleiotropy and the handicap principle of sexual selection in melanin-based colouration. Biol. Rev. 91, 328–348 (2016).

    PubMed 
    Article 

    Google Scholar 

  • Statistics Poland. https://stat.gov.pl/en/ (2021).

  • Sol, D. & Senar, J. C. Urban pigeon populations: Stability, home range, and the effect of removing individuals. Can. J. Zool. 73, 1154–1160 (1995).

    Article 

    Google Scholar 

  • Minias, P. Reproduction and survival in the city: Which fitness components drive urban colonization in a reed-nesting waterbird?. Curr. Zool. 62, 79–87 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Meissner, W. & Fischer, I. Sexing of common gull, Larus canus, using linear measurements. Folia Zool. 66, 183–188 (2017).

    Article 

    Google Scholar 

  • Haag-Wackernagel, D., Heeb, P. & Leiss, A. Phenotype-dependent selection of juvenile urban feral pigeons Columba livia. Bird Study 53, 163–170 (2006).

    Article 

    Google Scholar 

  • Harter, T. S., Reichert, M., Brauner, C. J. & Milsom, W. K. Validation of the i-STAT and HemoCue systems for the analysis of blood parameters in the bar-headed goose, Anser indicus. Conserv. Physiol. 3, cov021 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Minias, P. The use of haemoglobin concentrations to assess physiological condition in birds: A review. Conserv. Physiol. 3, cov007 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Martin, L. B. et al. Phytohemagglutinin-induced skin swelling in birds: Histological support for a classic immunoecological technique. Funct. Ecol. 20, 290–299 (2006).

    Article 

    Google Scholar 

  • Brown, G. P., Shilton, C. M. & Shine, R. Measuring amphibian immunocompetence: Validation of the phytohemagglutinin skin-swelling assay in the cane toad, Rhinella marina. Methods Ecol. Evol. 2, 341–348 (2011).

    Article 

    Google Scholar 

  • Kennedy, M. W. & Nager, R. G. The perils and prospects of using phytohaemagglutinin in evolutionary ecology. Trends Ecol. Evol. 21, 653–655 (2006).

    PubMed 
    Article 

    Google Scholar 

  • Vinkler, M., Bainová, H. & Albrecht, T. Functional analysis of the skin-swelling response to phytohaemagglutinin. Funct. Ecol. 24, 1081–1086 (2010).

    Article 

    Google Scholar 

  • Turmelle, A. S., Ellison, J. A., Mendonça, M. T. & McCracken, G. F. Histological assessment of cellular immune response to the phytohemagglutinin skin test in Brazilian free-tailed bats (Tadarida brasiliensis). J. Comp. Physiol. B 180, 1155–1164 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Griffiths, R., Double, M. C., Orr, K. & Dawson, R. J. A DNA test to sex most birds. Mol. Ecol. 7, 1071–1075 (1998).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Çakmak, E., Akın Pekşen, Ç. & Bilgin, C. C. Comparison of three different primer sets for sexing birds. J. Vet. Diagn. Investig. 29, 59–63 (2017).

    Article 
    CAS 

    Google Scholar 

  • Kaiser, H. F. The application of electronic computers to factor analysis. Educ. Psychol. Meas. 20, 141–151 (1960).

    Article 

    Google Scholar 

  • Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Article 

    Google Scholar 

  • Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest package: Tests in linear mixed effects models. J. Stat. Softw. 82, 1–26 (2017).

    Article 

    Google Scholar 

  • Jaeger, B. C., Edwards, L. J., Das, K. & Sen, P. K. An R 2 statistic for fixed effects in the generalized linear mixed model. J. Appl. Stat. 44, 1086–1105 (2017).

    MathSciNet 
    MATH 
    Article 

    Google Scholar 

  • Johnson, P. C. Extension of Nakagawa & Schielzeth’s R2GLMM to random slopes models. Methods Ecol. Evol. 5, 944–946 (2014).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Bartoń, K. MuMIn: Multi-model inference. R package ver. 1.43.17. CRAN: The Comprehensive R Archive Network, Berkeley, CA, USA. https://CRAN.R-project.org/package=MuMIn (2020).

  • Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).

    MATH 
    Book 

    Google Scholar 

  • Kahle, D. J. & Wickham, H. ggmap: Spatial visualization with ggplot2. R J. 5, 144–161 (2013).

    Article 

    Google Scholar 


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