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Background

Ecological functions and processes in urban ecosystems are governed by various human activities. City-adapted and city-exploiting animal species are expected to present certain specific behavioral and physiological traits in comparison to city-avoiders or conspecific individual frequenting less urbanized or rural environments. A trait of high importance, the plumage color polymorphism has been selected as the main study model and was correlated with different morphological and physiological parameters to highlight its importance in determining the possible health status of urban Feral Pigeons (Columba livia) in North African urban habitats.

Methods

Different body morphometrics, hematological and hemoparasitic parameters were quantified on free-living Feral Pigeons in urban environments of northern Algeria. Moreover, plumage melanin-based coloration (MBC) was measured and the data collected at the individual scale was correlated with the previous parameters using linear and non-linear modeling approaches.

Results

Plumage MBC scores of the sampled Feral Pigeons ranged between 0.3% and 74.8%. Among the 12 morphological traits measured, body weight, tail length and total length were deemed to be positively correlated with MBC. Darker morphs appeared to have more hemoparasites compared to lighter pigeons. Quite the same observation goes with the immunity but with non-linear trends. The number of monocytes and granulocytes increased with the increase in MBC levels in lighter morphs, while pigeons with high MBC scores exhibited negative relationships between MBC levels and the number of white blood cells.

Conclusions

Despite the existence of a number of studies demonstrating phenotypic directional selection, further studies are undoubtedly necessary to understand in detail the underlying mechanisms in species life-history strategies between differently colored individuals. Findings of this correlative study open exciting perspectives revealing that MBC can be considered a good indicator of and health status and adaptation strategies to changes in urban environments.


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Does melanin-based plumage coloration reflect health status of free-living birds in urban environments?

Show Author's information Hani Amir Aouissi1,2Mostefa Ababsa1Aissam Gaagai1Zihad Bouslama2,3Yassine Farhi1Haroun Chenchouni4,5 ( )
Scientific and Technical Research Center on Arid Regions (CRSTRA), 07000, Biskra, Algeria
Faculty of Sciences, Department of Biology, Badji-Mokhtar Annaba University, 23000, Annaba, Algeria
Environmental Research Center (CRE), Badji-Mokhtar Annaba University, 23000, Annaba, Algeria
Department of Nature and Life Sciences, Faculty of Exact Sciences and Nature and Life Sciences, University of Larbi Tebessi, 12002, Tebessa, Algeria
Laboratory of Natural Resources and Management of Sensitive Environments 'RNAMS', University of Larbi Ben M'hidi, 04000, Oum-El-Bouaghi, Algeria

Abstract

Background

Ecological functions and processes in urban ecosystems are governed by various human activities. City-adapted and city-exploiting animal species are expected to present certain specific behavioral and physiological traits in comparison to city-avoiders or conspecific individual frequenting less urbanized or rural environments. A trait of high importance, the plumage color polymorphism has been selected as the main study model and was correlated with different morphological and physiological parameters to highlight its importance in determining the possible health status of urban Feral Pigeons (Columba livia) in North African urban habitats.

Methods

Different body morphometrics, hematological and hemoparasitic parameters were quantified on free-living Feral Pigeons in urban environments of northern Algeria. Moreover, plumage melanin-based coloration (MBC) was measured and the data collected at the individual scale was correlated with the previous parameters using linear and non-linear modeling approaches.

Results

Plumage MBC scores of the sampled Feral Pigeons ranged between 0.3% and 74.8%. Among the 12 morphological traits measured, body weight, tail length and total length were deemed to be positively correlated with MBC. Darker morphs appeared to have more hemoparasites compared to lighter pigeons. Quite the same observation goes with the immunity but with non-linear trends. The number of monocytes and granulocytes increased with the increase in MBC levels in lighter morphs, while pigeons with high MBC scores exhibited negative relationships between MBC levels and the number of white blood cells.

Conclusions

Despite the existence of a number of studies demonstrating phenotypic directional selection, further studies are undoubtedly necessary to understand in detail the underlying mechanisms in species life-history strategies between differently colored individuals. Findings of this correlative study open exciting perspectives revealing that MBC can be considered a good indicator of and health status and adaptation strategies to changes in urban environments.

Keywords: Urbanization, Columba livia , Feather color polymorphism, Feral birds, Hematological indicators, Hemoparasitism, Immune ecophysiology, Urban ornithology

References(140)

Almasi B, Jenni L, Jenni-Eiermann S, Roulin A. Regulation of stress response is heritable and functionally linked to melanin-based coloration. J Evol Biol. 2010;23: 987–96.

Aouissi HA, Belabed AI, Bouslama Z. Doves' mapping and inventory into the urban sites of Annaba (Northeastern of Algeria). Adv Environ Biol. 2015;12: 328–38.

Aouissi HA, Gasparini J, Belabed AI, Bouslama Z. Impact of greenspaces in city on avian species richness and abundance in Northern Africa. CR Biol. 2017;340: 394–400.

Aouissi HA, Petrişor AI, Ababsa M, Boştenaru-Dan M, Tourki M, Bouslama Z. Influence of land use on avian diversity in North African urban environments. Land. 2021;10: 434.

Aouissi HA. Écologie des espèces aviaires dans le tissu urbain de la ville de Annaba. Doctoral Thesis. Annaba: University of Annaba; 2016.

Barber I, Dingemanse NJ. Parasitism and the evolutionary ecology of animal personality. Philos Trans R Soc B. 2010;365: 4077–88.

Barcia JJ. The Giemsa stain: its history and applications. Int J Surg Pathol. 2007;15: 292–6.

Belabed AI, Aouissi HA, Zediri H, Djemadi I, Driss K, Houhamdi M, et al. The effect of urbanization on the phenotype of the Collared Dove (Streptopelia decaocto) in northeastern Algeria. Bull Inst Sci Rabat. 2013;35: 155–64.

Belabed BE, Meddour A, Samraoui B, Chenchouni H. Modeling seasonal and spatial contamination of surface waters and upper sediments with trace metal elements across industrialized urban areas of the Seybouse watershed in North Africa. Environ Monit Assess. 2017;189: 265.

Bendjoudi D, Chenchouni H, Doumandji S, Voisin JF. Bird species diversity of the Mitidja Plain (Northern Algeria) with emphasis on the dynamics of invasive and expanding species. Acrocephalus. 2013;34: 13–26.

Bendjoudi D, Voisin JF, Doumandji S, Merabet A, Benyounes N, Chenchouni H. Rapid increase in numbers and change of land-use in two expanding Columbidae species (Columba palumbus and Streptopelia decaocto) in Algeria. Avian Res. 2015;6: 18.

Berry JL. Urbanization. The earth as transformed by human action. In: Turner II BL, Clark WC, Kates RW, Richards JF, Mathews JT, Meyer WB, editors. The earth as transformed by human action: global and regional changes in the biosphere over the past 300 years. Cambridge: Cambridge University Press, UK; 1990. p. 103–19.

Blair R. The effects of urban sprawl on birds at multiple levels of biological organization. Ecol Soc. 2004;9: 2.

Blanchet S, Méjean L, Bourque JF, Lek S, Thomas F, Marcogliese DJ, et al. Why do parasitized hosts look different? Resolving the "chicken-egg" dilemma. Oecologia. 2009;160: 37.

Borras A, Pascual J, Senar JC. What do different bill measures measure and what is the best method to use in granivorous birds? J Field Ornithol. 2000;71: 606–11.https://doi.org/10.1648/0273-8570-71.4.606
DOI

Bradley CA, Altizer S. Urbanization and the ecology of wildlife diseases. Trends Ecol Evol. 2007;22: 95–102.

Brazil M. Birds of east Asia: China, Taiwan, Korea, Japan, and Russia. Princeton, New Jersey: Princeton University Press; 2009.
Campbell TW. Avian hematology and cytology. 2nd ed. Ames, IA: Iowa State University Press; 1995.

Chakarov N, Boerner M, Krüger O. Fitness in common buzzards at the cross-point of opposite melanin–parasite interactions. Funct Ecol. 2008;22: 1062–9.

Chanarin I. Hematology: principles and procedures. J Clin Pathol. 1984;37: 1419.

Chatelain M, Gasparini J, Frantz A. Do trace metals select for darker birds in urban areas? An experimental exposure to lead and zinc. Glob Chang Biol. 2016;22: 2380–91.

Chatelain M, Gasparini J, Jacquin L, Frantz A. The adaptive function of melanin-based plumage coloration to trace metals. Biol Lett. 2014;10: 20140164.

Chatelain M, Pessato A, Frantz A, Gasparini J, Leclaire S. Do trace metals influence visual signals? Effects of trace metals on iridescent and melanic feather colouration in the feral pigeon. Oikos. 2017;126: 1542–53.

Chedad A, Bendjoudi D, Beladis I, Guezoul O, Chenchouni H. A comprehensive monograph on the ecology and distribution of the House bunting (Emberiza sahari) in Algeria. Front Biogeogr. 2021;13: e47727.

Chenchouni H. Contribution à l'étude de la bio-écologie de la Cigogne blanche (Ciconia ciconia) dans la région de Batna (Nord-est algérien). Doctoral Thesis. Algeria: University of Batna; 2017a.

Chenchouni H. Variation in White Stork (Ciconia ciconia) diet along a climatic gradient and across rural-to-urban landscapes in North Africa. Int J Biometeorol. 2017;61: 549–64.

Clavel J, Julliard R, Devictor V. Worldwide decline of specialist species: toward a global functional homogenization? Front Ecol Environ. 2011;9: 222–8.

Combes C. Parasitism: the ecology and evolution of intimate interactions. Chicago: University of Chicago Press; 2001.

Comer JA, Paddock CD, Childs JE. Urban zoonoses caused by Bartonella, Coxiella, Ehrlichia, and Rickettsia species. Vector Borne Zoonotic Dis. 2001;1: 91–118.

Corbel H, Legros A, Haussy C, Jacquin L, Gasparini J, Karimi B, Frantz A. Stress response varies with plumage colour and local habitat in feral pigeons. J Ornithol. 2016;157: 825–37.

Côte J, Boniface A, Blanchet S, Hendry AP, Gasparini J, Jacquin L. Melanin-based coloration and host–parasite interactions under global change. Proc R Soc Lond B Biol. 2018;285: 20180285.

Davey JW, Cezard T, Fuentes-Utrilla P, Eland C, Gharbi K, Blaxter ML. Special features of RAD Sequencing data: implications for genotyping. Mol Ecol. 2013;22: 3151–64.

Davidsohn I, Henry JB. Clinical diagnosis by laboratory methods. 15th ed. Philadelphia, Pa: W. B. Saunders Co; 1974.

Davis AK, Maney DL, Maerz JC. The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol. 2008;22: 760–72.

de Godoi FSL, Nishi SM, de Jesus Pena HF, Gennari SM. Toxoplasma gondii: diagnosis of experimental and natural infection in pigeons (Columba livia) by serological, biological and molecular techniques. Rev Bras Parasitol Vet. 2010;19: 238–43.

Devictor V, Julliard R, Clavel J, Jiguet F, Lee A, Couvet D. Functional biotic homogenization of bird communities in disturbed landscapes. Glob Ecol Biogeogr. 2008a;17: 252–61.

Devictor V, Julliard R, Couvet D, Lee A, Jiguet F. Functional homogenization effect of urbanization on bird communities. Conserv Biol. 2007;21: 741–51.

Devictor V, Julliard R, Jiguet F. Distribution of specialist and generalist species along spatial gradients of habitat disturbance and fragmentation. Oikos. 2008b;117: 507–14.

Dreiss A, Henry I, Ruppli C, Almasi B, Roulin A. Darker eumelanic barn owls better withstand food depletion through resistance to food deprivation and lower appetite. Oecologia. 2010;164: 65–71.

Ducatez S, Giraudeau M, Thébaud C, Jacquin L. Colour polymorphism is associated with lower extinction risk in birds. Glob Chang Biol. 2017;23: 3030–9.

Ducrest AL, Keller L, Roulin A. Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol. 2008;23: 502–10.

Eck S, Fiebig J, Fiedler W, Heynen I, Nicolai B, Töpfer T, et al. Measuring birds/vögel vermessen. Germany: Deutsche Ornithologen-Gesellschaft; 2011.

Emaresi G, Henry I, Gonzalez E, Roulin A, Bize P. Sexand melanism-specific variations in the oxidative status of adult tawny owls in response to manipulated reproductive effort. J Exp Biol. 2016;219: 73–9.

Ermert D, Niemiec MJ, Röhm M, Glenthøj A, Borregaard N, Urban CF. Candida albicans escapes from mouse neutrophils. J Leukocyte Biol. 2013;94: 223–36.

Evans KL, Gaston KJ, Sharp SP, McGowan A, Simeoni M, Hatchwell BJ. Effects of urbanisation on disease prevalence and age structure in blackbird Turdus merula populations. Oikos. 2009;118: 774–82.

Fallon SM, Ricklefs RE. Parasitemia in PCR-detected Plasmodium and Haemoproteus infections in birds. J Avian Biol. 2008;39: 514–22.

Farhi Y, Aouissi HA, Nouidjem Y, Belhamra M. Spur-winged Lapwing at Djamaa, Algeria, in June 2011. Dutch Birding. 2020;42: 186–7.

Fokidis HB, Greiner EC, Deviche P. Interspecific variation in avian blood parasites and haematology associated with urbanization in a desert habitat. J Avian Biol. 2008;39: 300–10.

French SS, Fokidis HB, Moore MC. Variation in stress and innate immunity in the tree lizard (Urosaurus ornatus) across an urban–rural gradient. J Comp Physiol B. 2008;178: 997–1005.

Gaagai A, Boudoukha A, Boumezbeur A, Benaabidate L. Hydrochemical characterization of surface water in the Babar watershed (Algeria) using environmetric techniques and time series analysis. Int J River Basin Manag. 2017;15: 361–72.

Galeotti P, Sacchi R. Differential parasitaemia in the tawny owl (Strix aluco): effects of colour morph and habitat. J Zool. 2003;261: 91–9.

Galván I, Solano F. Melanin chemistry and the ecology of stress. Physiol Biochem Zool. 2015;88: 352–5.

Galván I, Solano F. The evolution of euand pheomelanic traits may respond to an economy of pigments related to environmental oxidative stress. Pigment Cell Melanoma Res. 2009;22: 339–42.

Gasparini J, Bize P, Piault R, Wakamatsu K, Blount JD, Ducrest AL, et al. Strength and cost of an induced immune response are associated with a heritable melanin-based colour trait in female tawny owls. J Anim Ecol. 2009;78: 608–16.

George EL, Panos A. Does a high WBC count signal infection? Nursing. 2005;35: 20–1.https://doi.org/10.1097/00152193-200501000-00014
DOI

Germaine SS, Rosenstock SS, Schweinsburg RE, Richardson WS. Relationships among breeding birds, habitat, and residential development in greater Tucson, Arizona. Ecol Appl. 1998;8: 680–91.

Gilot-Fromont E, Jégo M, Bonenfant C, Gibert P, Rannou B, Klein F, et al. Immune phenotype and body condition in roe deer: individuals with high body condition have different, not stronger immunity. PLoS ONE. 2012;7: e45576.

Godfrey PS, Toone BK, Carney MW, Flynn TG, Bottiglieri T, Laundy M, et al. Enhancement of recovery from psychiatric illness by methylfolate. Lancet. 1990;336: 392–5.

Graczyk TK, Cranfield MR, Shiff CJ. Extraction of Haemoproteus columbae (Haemosporina: Haemoproteidae) antigen from rock dove pigeons (Columba livia) and its use in an antibody ELISA. J Parasitol. 1994;80: 713–8.

Gregoire A, Faivre B, Heeb P, Cezilly F. A comparison of infestation patterns by Ixodes ticks in urban and rural populations of the Common Blackbird Turdus merula. Ibis. 2002;144: 640–5.

Grimm NB, Grove JG, Pickett ST, Redman CL. Integrated approaches to long-term studies of urban ecological systems. Bioscience. 2000;50: 571–84.

Haase E, Ito S, Sell A, Wakamatsu K. Melanin concentrations in feathers from wild and domestic pigeons. J Hered. 1992;83: 64–7.

Hanson HE, Koussayer B, Kilvitis HJ, Schrey AW, Maddox JD, Martin LB. Epigenetic potential in native and introduced populations of house sparrows (Passer domesticus). Integr Comp Biol. 2020;60: 1458–68.

Hart BL. Behavioural defence. In: Clayton DH, Moore J, editors. Host-parasite evolution: general principle and avian models. Oxford: Oxford University Press; 1997. p. 59–77.
Hawkey CM, Dennett TB. A colour atlas of comparative veterinary haematology. London: Wolfe Publishing; 1989.https://doi.org/10.1111/j.1939-165X.1989.tb00532.x
DOI
Hill GE, McGraw KJ. Bird colouration: function and evolution. Cambridge: Harvard University Press; 2006.

Ishtiaq F, Rao M, Huang X, Bensch S. Estimating prevalence of avian haemosporidians in natural populations: a comparative study on screening protocols. Parasite Vectors. 2017;10: 127.

Jacquin L, Haussy C, Bertin C, Laroucau K, Gasparini J. Darker female pigeons transmit more specific antibodies to their eggs than do paler ones. Biol J Linn Soc. 2013a;108: 647–57.

Jacquin L, Lenouvel P, Haussy C, Ducatez S, Gasparini J. 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. 2011;42: 11–5.

Jacquin L, Récapet C, Bouche P, Leboucher G, Gasparini J. Melanin-based coloration reflects alternative strategies to cope with food limitation in pigeons. Behav Ecol. 2012;23: 907–15.

Jacquin L, Récapet C, Prévot-Julliard AC, Leboucher G, Lenouvel P, Erin N, et al. A potential role for parasites in the maintenance of color polymorphism in urban birds. Oecologia. 2013b;173: 1089–99.

Jacquin L. Coloration mélanique et stratégies d'histoire de vie chez le pigeon biset urbain. Doctoral Thesis. University of Paris 6; 2011.
Jarry G, Baillon F. Hivernage de la tourterelle des bois (Streptopelia turtur) au Sénégal: étude d'une population dans la région de Nianing. Paris: Report of CRBPO; 1991.

Jiguet F, Sunnen L, Prévot AC, Princé K. Urban pigeons losing toes due to human activities. Biol Conserv. 2019;240: 108241.

Johnston RF, Janiga M. Feral pigeons. Vol. 4. Oxford: Oxford University Press; 1995.

Karell P, Ahola K, Karstinen T, Kolunen H, Siitari H, Brommer JE. Blood parasites mediate morph-specific maintenance costs in a colour polymorphic wild bird. J Evol Biol. 2011;24: 1783–92.

Kark S, Iwaniuk A, Schalimtzek A, Banker E. Living in the city: can anyone become an 'urban exploiter'? J Biogeogr. 2007;34: 638–51.https://doi.org/10.1111/j.1365-2699.2006.01638.x
DOI

Kilvitis HJ, Hanson H, Schrey AW, Martin LB. Epigenetic potential as a mechanism of phenotypic plasticity in vertebrate range expansions. Integr Comp Biol. 2017;57: 385–95.

Kittilsen S, Schjolden J, Beitnes-Johansen I, Shaw JC, Pottinger TG, Sørensen C, et al. Melanin-based skin spots reflect stress responsiveness in salmonid fish. Horm Behav. 2009;56: 292–8.

Kolomak IO, Berdnyk VP, Kyrychko OB, Nedosekov VV. Analysis of ultrastructural morphometric changes of pigeon kidneys affected by colibacteriosis. Transl Res Vet Sci. 2019;2: 37–49.

Kramar DE, Carstensen B, Prisley S, Campbell J. Mercury concentrations in blood and feathers of nestling Bald Eagles in coastal and inland Virginia. Avian Res. 2019;10: 3.

Krause ET, Krüger O, Hoffman JI. The influence of inherited plumage colour morph on morphometric traits and breeding investment in zebra finches (Taeniopygia guttata). PLoS ONE. 2017;12: e0188582.

Krüger O, Lindström J. Lifetime reproductive success in common buzzard, Buteo buteo: from individual variation to population demography. Oikos. 2001;93: 260–73.

Law GRJ. Blood samples from jugular vein of turkeys. Poult Sci. 1960;39: 1450–2.

Le Viol I, Jiguet F, Brotons L, Herrando S, LindströmPearce-Higgins ÅJW, et al. More and more generalists: two decades of changes in the European avifauna. Biol Lett. 2012;8: 780–2.

Leclaire S, Chatelain M, Pessato A, Buatois B, Frantz A, Gasparini J. Pigeon odor varies with experimental exposure to trace metal pollution. Ecotoxicology. 2019;28: 76–85.

Luniak M. Synurbization – adaptation of animal wildlife to urban development. In: Shaw WW, Harris K, Vandruff L, editors. Proceedings of the 4th international symposium on urban wildlife conservation. Tucson, Arizona: University of Arizona; 2004. p. 50–5.
Madans JH, Webster KM. Health surveys. In: Wright JD, editor. International encyclopedia of the social and behavioral sciences. 2nd ed. Orlando: University of Central Florida; 2015. p. 725–30.https://doi.org/10.1016/B978-0-08-097086-8.14031-0
DOI

Martin LB. Stress and immunity in wild vertebrates: timing is everything. Gen Comp Endocrinol. 2009;163: 70–6.

Martínez J, Vásquez RA, Venegas C, Merino S. Molecular characterisation of haemoparasites in forest birds from Robinson Crusoe Island: is the Austral Thrush a potential threat to endemic birds? Bird Conserv Int. 2015;25: 139–52.

Martinossi-Allibert I, Clavel J, Ducatez S, Viol IL, Teplitsky C. Does habitat specialization shape the evolutionary potential of wild bird populations? J Avian Biol. 2017;48: 1158–65.

Marzluff JM. Worldwide urbanization and its effects on birds. In: Marzluff JM, Bowman R, Donnelly R, editors. Avian ecology and conservation in an urbanizing world. Boston: Springer; 2001. p. 19–47.https://doi.org/10.1007/978-1-4615-1531-9_2
DOI

McCarren S, Sumasgutner P, Tate G, Koeslag A, Amar A. Clinal variation in the polymorphic Black Sparrowhawk Accipiter melanoleucus is unrelated to infection by the blood parasite Haemoproteus nisi. J Ornithol. 2021;162: 231–41.

Miller LK, Brooks R. The effects of genotype, age, and social environment on male ornamentation, mating behavior, and attractiveness. Evolution. 2005;59: 2414–25.

Møller AP. Interspecific variation in fear responses predicts urbanization in birds. Behav Ecol. 2010;21: 365–71.

Møller AP. Successful city dwellers: a comparative study of the ecological characteristics of urban birds in the Western Palearctic. Oecologia. 2009;159: 849–58.

Moreno J, Møller AP. Are melanin ornaments signals of antioxydant and immune capacity in birds? Acta Zool Sin. 2006;52: 202–8.

Nebel C, Harl J, Pajot A, Weissenböck H, Amar A, Sumasgutner P. High prevalence and genetic diversity of Haemoproteus columbae (Haemosporida: Haemoproteidae) in feral pigeons Columbae livia in Cape Town. South Africa Parasitol Res. 2020;119: 447–63.

Obukhova NY. Geographic variation of color in the synanthropic Blue Rock Pigeon. Russ J Genet. 2001;37: 649–58.

Ouali N, Belabed BE, Chenchouni H. Modelling environment contamination with heavy metals in flathead grey mullet Mugil cephalus and upper sediments from north African coasts of the Mediterranean Sea. Sci Total Environ. 2018;639: 156–74.

Oxnard CE. One biologist's view of morphometrics. Annu Rev Ecol Evol Syst. 1978;9: 219–41.

Pal M, Pop P, Mahapatra A, Bhagat R, Hore U. Diversity and structure of bird assemblages along urban-rural gradient in Kolkata, India. Urban Forest Urban Green. 2019;38: 84–96.

Parmesan C, Yohe G. A globally coherent fingerprint of climate change impacts across natural systems. Nature. 2003;421: 37–42.

Pellegrino I, Cucco M, Calà E, Boano G, Pavia M. Plumage coloration and morphometrics of the Little Owl Athene noctua in the Western Palearctic. J Ornithol. 2020;161: 1071–81.

Pérez JE, Nirchio M, Alfonsi C, Muñoz C. The biology of invasions: the genetic adaptation paradox. Biol Invas. 2006;8: 1115–21.

Périquet JC. Le Pigeon: races, élevage et utilisation, reproduction, hygiène et santé. Collection Les cahiers de l'élevage, Ed. Rustica, Paris; 1998.

Pickett ST, Cadenasso ML, Grove JM, Boone CG, Groffman PM, Irwin E, et al. Urban ecological systems: scientific foundations and a decade of progress. J Environ Manage. 2011;92: 331–62.

Pinheiro J, Bates D, DebRoy S, Sarkar D and R Core Team. nlme: linear and nonlinear mixed effects models. R package version 3.1–131. 2017. https://cran.r-project.org/package=nlme.

Pollack L, Ondrasek NR, Calisi R. Urban health and ecology: the promise of an avian biomonitoring tool. Curr Zool. 2017;63: 205–12.

Quesada J, Senar JC. The role of melaninand carotenoid-based plumage coloration in nest defence in the Great Tit. Ethology. 2007;113: 640–7.

R Core Team. R: a language and environment for statistical computing. R foundation for statistical computing. 2020. https://www.R-project.org/.
Rasmussen PC, Anderton JC. Birds of south Asia: the Ripley guide: attributes and status. 1st Edn, Vol. 2. Washington and Barcelona: Smithsonian Institution and Lynx Edicions; 2005.

Récapet C, Dauphin L, Jacquin L, Gasparini J, Prévot-Julliard AC. Eumelanin-based colouration reflects local survival of juvenile feral pigeons in an urban pigeon house. J Avian Biol. 2013;44: 583–90.

Reyer HU, Fischer W, Steck P, Nabulon T, Kessler P. Sex-specific nest defense in house sparrows (Passer domesticus) varies with badge size of males. Behav Ecol Sociobiol. 1998;42: 93–9.

Roulin A, Almasi B, MeichtryStier KS, Jenni L. Eumelaninand pheomelanin-based colour advertise resistance to oxidative stress in opposite ways. J Evol Biol. 2011;24: 2241–7.

Roulin A, Altwegg R, Jensen H, Steinsland I, Schaub M. Sex-dependent selection on an autosomal melanic female ornament promotes the evolution of sex ratio bias. Ecol Lett. 2010;13: 616–26.

Roulin A, Altwegg R. Breeding rate is associated with pheomelanism in male and with eumelanism in female barn owls. Behav Ecol. 2007;18: 563–70.

Roulin A, Gasparini J, Bize P, Ritschard M, Richner H. Melanin-based colorations signal strategies to cope with poor and rich environments. Behav Ecol Sociobiol. 2008;62: 507–19.

Roulin A, Jungi TW, Pfister H, Dijkstra C. Female barn owls (Tyto alba) advertise good genes. Proc R Soc Lond B Biol. 2000;267: 937–41.

Roulin A, Riols C, Dijkstra C, Ducrest AL. Female plumage spottiness signals parasite resistance in the barn owl (Tyto alba). Behav Ecol. 2001;12: 103–10.

Roulin A. The evolution, maintenance and adaptive function of genetic colour polymorphism in birds. Biol Rev. 2004;79: 815–48.

Rumsfeld JS. Health status and clinical practice: when will they meet? Circulation. 2002;106: 5–7.

Saino N, Romano M, Rubolini D, Ambrosini R, Caprioli M, Milzani A, et al. Viability is associated with melanin-based coloration in the barn swallow (Hirundo rustica). PLoS ONE. 2013;8: e60426.

Samuel MD, Woodworth BL, Atkinson CT, Hart PJ, LaPointe DA. Avian malaria in Hawaiian forest birds: infection and population impacts across species and elevations. Ecosphere. 2015;6: 104.

Schultz PW, Gouveia VV, Cameron LD, Tankha G, Schmuck P, Franěk M. Values and their relationship to environmental concern and conservation behavior. J Cross-Cult Psychol. 2005;36: 457–75.

Shochat E, Warren PS, Faeth SH, McIntyre NE, Hope D. From patterns to emerging processes in mechanistic urban ecology. Trend Ecol Evol. 2006;21: 186–91.

Sol D, Jovani R, Torres J. Geographical variation in blood parasites in feral pigeons: the role of vectors. Ecography. 2000;23: 307–14.

Stevens RWC, Ridgway GJ. A technique for bleeding chickens from the jugular vein. Poultry Sci. 1966;45: 204–5.

Stone KD, Prussin C, Metcalfe DD. IgE, mast cells, basophils, and eosinophils. J Allergy Clin Immunol. 2010;125: S73-80.

Stöppler MC, Shiel WC, Credo Reference (Firm), WebMD (Firm). Webster's new world medical dictionary, 3rd ed.; Redo Reference: Boston, MA, USA; Wiley: Hoboken, NJ, USA. 2014; 480 p.

Sumasgutner P, Rose S, Koeslag A, Amar A. Exploring the influence of urbanization on morph distribution and morph-specific breeding performance in a polymorphic African raptor. J Raptor Res. 2018;52: 19–30.

The GIMP team. GIMP 2.8.10. 2014. www.gimp.org.

Tostes R, Vashist U, Scopel KKG, Massard CL, Daemon E, D'Agosto M. Plasmodium spp. and Haemoproteus spp. infection in birds of the Brazilian Atlantic Forest detected by microscopy and polymerase chain reaction. Pesq Vet Bras. 2015;35: 67–74.

Uhm TG, Kim BS, Chung IY. Eosinophil development, regulation of eosinophil-specific genes, and role of eosinophils in the pathogenesis of asthma. Allergy Asthma Immunol Res. 2012;4: 68–79.

Valkiūnas G, Palinauskas V, Ilgūnas M, Bukauskaitė D, Dimitrov D, Bernotienė R, et al. Molecular characterization of five widespread avian haemosporidian parasites (Haemosporida), with perspectives on the PCR-based detection of haemosporidians in wildlife. Parasitol Res. 2014;113: 2251–63.

Van den Brink V, Dreiss AN, Roulin A. Melanin-based coloration predicts natal dispersal in the barn owl Tyto Alba. Anim Behav. 2012;84: 805–12.

Vignieri SN, Larson JG, Hoekstra HE. The selective advantage of crypsis in mice. Evolution. 2010;64: 2153–8.

Vlahov D, Freudenberg N, Proietti F, Ompad D, Quinn A, Nandi V, et al. Urban as a determinant of health. J Urban Health. 2007;84: 16–26.

Wei T, Simko V. R package "corrplot": Visualization of a Correlation Matrix (Version 0.84). 2017. https://github.com/taiyun/corrplot.

Yeh PJ. Rapid evolution of a sexually selected trait following population establishment in a novel habitat. Evolution. 2004;58: 166–74.

Publication history
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Acknowledgements
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Publication history

Received: 19 October 2020
Accepted: 02 September 2021
Published: 14 September 2021
Issue date: January 2021

Copyright

© The Author(s) 2021.

Acknowledgements

Acknowledgements

Many thanks are addressed to Pr. Julien Gasparini and the IEES – UPMC (Paris) for providing good working conditions to HAA. Mrs. Warda Aouissi and Mr. Salah-Eddine Aouissi helped conducting this study. Dr. Ibrahim Belabed and Mr. Walid Makrouf assisted in field work with specimen handling. Dr. Saifi Merdas helped with drawing the map of the study area. The anonymous reviewers' comments improved the manuscript.

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