Section: Ecology
Topic: Biology of interactions, Ecology, Evolution

Cities as parasitic amplifiers? Malaria prevalence and diversity in great tits along an urbanization gradient

10.24072/pcjournal.405 - Peer Community Journal, Volume 4 (2024), article no. e38.

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Urbanization is a worldwide phenomenon that modifies the environment. By affecting the reservoirs of pathogens and the body and immune conditions of hosts, urbanization alters the epidemiological dynamics and diversity of diseases. Cities could act as areas of pathogen dilution or amplification, depending on whether urban features have positive or negative effects on vectors and hosts. In this study, we focused on a host species and investigated the prevalence and diversity of avian malaria parasites (Plasmodium/Haemoproteus sp. and Leucocytozoon sp.) in great tits (Parus major) living across an urbanization gradient. In general, we observed high prevalence in adult birds (from 95% to 100%), yet lower prevalence in fledglings (from 0% to 38%). We found a slight tendency for increased Plasmodium sp. prevalence with increasing urbanization in adults. Urban nestlings had higher Plasmodium sp. infection rates than non-urban nestlings. We found evidence of higher diversity of parasites in the most natural urban park; however, parasite diversity was similar across other urbanization levels (e.g. from a little artificialized park to a highly anthropized industrial area). Parasite lineages were not habitat specific. Only one Plasmodium sp. lineage (YWT4) was associated with urban areas and some rare lineages (e.g., AFR065) were present only in a zoo area, perhaps because of the presence of African birds. This study suggests that urbanization can lead to a parasite amplification effect and can favor different avian malaria lineages.

Published online:
DOI: 10.24072/pcjournal.405
Type: Research article
Caizergues, Aude E. 1, 2; Robira, Benjamin 3; Perrier, Charles 4; Jeanneau, Mélanie 1; Berthomieu, Arnaud 1; Perret, Samuel 1; Gandon, Sylvain 1; Charmantier, Anne 1

1 CEFE, Univ Montpellier, CNRS, EPHE, IRD, Montpellier, France
2 Department of Biology, University of Toronto Mississauga; Mississauga, ON, Canada
3 Animal Ecology Unit, Research and Innovation Centre, Fondazione Edmund Mach, San Michele all’Adige, TN, Italy
4 UMR CBGP, INRAE, CIRAD, IRD, Institut Agro, Université Montpellier, Montpellier, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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     title = {Cities as parasitic amplifiers? {Malaria} prevalence and diversity in great tits along an urbanization gradient},
     journal = {Peer Community Journal},
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Caizergues, Aude E.; Robira, Benjamin; Perrier, Charles; Jeanneau, Mélanie; Berthomieu, Arnaud; Perret, Samuel; Gandon, Sylvain; Charmantier, Anne. Cities as parasitic amplifiers? Malaria prevalence and diversity in great tits along an urbanization gradient. Peer Community Journal, Volume 4 (2024), article  no. e38. doi : 10.24072/pcjournal.405. https://peercommunityjournal.org/articles/10.24072/pcjournal.405/

Peer reviewed and recommended by PCI : 10.24072/pci.ecology.100587

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Asghar, M.; Hasselquist, D.; Bensch, S.; Asghar, M.; Hasselquist, D.; Bensch, S. Are chronic avian haemosporidian infections costly in wild birds?, Journal of Avian Biology, Volume 42 (2011) no. 6, pp. 530-537 | DOI

[2] Bailly, J.; Scheifler, R.; Belvalette, M.; Garnier, S.; Boissier, E.; Clément-Demange, V.-A.; Gète, M.; Leblond, M.; Pasteur, B.; Piget, Q.; Sage, M.; Faivre, B. Negative impact of urban habitat on immunity in the great tit Parus major, Oecologia, Volume 182 (2016) no. 4, pp. 1053-1062 | DOI

[3] Bates, D.; Mächler, M.; Bolker, B.; Walker, S. Fitting Linear Mixed-Effects Models Using lme4, Journal of Statistical Software, Volume 67 (2015) no. 1 | DOI

[4] Becker, D. J.; Streicker, D. G.; Altizer, S. Linking anthropogenic resources to wildlife–pathogen dynamics: a review and meta-analysis, Ecology Letters, Volume 18 (2015) no. 5, pp. 483-495 | DOI

[5] Belo, N. O.; Pinheiro, R. T.; Reis, E. S.; Ricklefs, R. E.; Braga, É. M. Prevalence and Lineage Diversity of Avian Haemosporidians from Three Distinct Cerrado Habitats in Brazil, PLoS ONE, Volume 6 (2011) no. 3 | DOI

[6] Bensch, S.; Hellgren, O.; PÉrez-Tris, J. MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages, Molecular Ecology Resources, Volume 9 (2009) no. 5, pp. 1353-1358 | DOI

[7] Bichet, C.; Scheifler, R.; Cœurdassier, M.; Julliard, R.; Sorci, G.; Loiseau, C. Urbanization, Trace Metal Pollution, and Malaria Prevalence in the House Sparrow, PLoS ONE, Volume 8 (2013) no. 1 | DOI

[8] Bradley, C. A.; Altizer, S. Urbanization and the ecology of wildlife diseases, Trends in Ecology & Evolution, Volume 22 (2007) no. 2, pp. 95-102 | DOI

[9] Caizergues, A. E. AudeCaizergues/Malaria_Great_Tits: Second release, Zenodo, 2024 | DOI

[10] Caizergues, A. E.; Charmantier, A.; Lambrechts, M. M.; Perret, S.; Demeyrier, V.; Lucas, A.; Grégoire, A. An avian urban morphotype: how the city environment shapes great tit morphology at different life stages, Urban Ecosystems (2021), pp. 1-13 | DOI

[11] Calegaro-Marques, C.; Amato, S. B. Urbanization Breaks Up Host-Parasite Interactions: A Case Study on Parasite Community Ecology of Rufous-Bellied Thrushes (Turdus rufiventris) along a Rural-Urban Gradient, PLOS ONE, Volume 9 (2014) no. 7 | DOI

[12] Capilla-Lasheras, P.; Dominoni, D. M.; Babayan, S. A.; O'Shaughnessy, P. J.; Mladenova, M.; Woodford, L.; Pollock, C. J.; Barr, T.; Baldini, F.; Helm, B. Elevated Immune Gene Expression Is Associated with Poor Reproductive Success of Urban Blue Tits, Frontiers in Ecology and Evolution, Volume 5 (2017) | DOI

[13] Carbó-Ramírez, P.; Zuria, I.; Schaefer, H.; Santiago-Alarcon, D. Avian haemosporidians at three environmentally contrasting urban greenspaces, Journal of Urban Ecology, Volume 3 (2017) no. 1 | DOI

[14] Charmantier, A.; Demeyrier, V.; Lambrechts, M.; Perret, S.; Grégoire, A. Urbanization Is Associated with Divergence in Pace-of-Life in Great Tits, Frontiers in Ecology and Evolution, Volume 5 (2017) | DOI

[15] Charmantier, A.; Demeyrier, V.; Lambrechts, M.; Perret, S.; Grégoire, A. Urbanization Is Associated with Divergence in Pace-of-Life in Great Tits, Frontiers in Ecology and Evolution, Volume 5 (2017) | DOI

[16] Christe, P.; Glaizot, O.; Strepparava, N.; Devevey, G.; Fumagalli, L. Twofold cost of reproduction: an increase in parental effort leads to higher malarial parasitaemia and to a decrease in resistance to oxidative stress, Proceedings of the Royal Society B: Biological Sciences, Volume 279 (2011) no. 1731, pp. 1142-1149 | DOI

[17] Coene, J. Malaria in urban and rural Kinshasa: the entomological input, Medical and Veterinary Entomology, Volume 7 (1993) no. 2, pp. 127-137 | DOI

[18] Cohen, J. Statistical Power Analysis for the Behavioral Sciences, Academic Press; Routledge, 2013 | DOI

[19] Cosgrove, C. L.; Knowles, S. C. L.; Day, K. P.; Sheldon, B. C. No evidence for avian malaria infection during the nestling phase in a passerine bird, Journal of Parasitology, Volume 92 (2006) no. 6, pp. 1302-1304 | DOI

[20] Delgado-V., C. A.; French, K. Parasite–bird interactions in urban areas: Current evidence and emerging questions, Landscape and Urban Planning, Volume 105 (2012) no. 1-2, pp. 5-14 | DOI

[21] Demeyrier, V.; Lambrechts, M. M.; Perret, P.; Grégoire, A. Experimental demonstration of an ecological trap for a wild bird in a human-transformed environment, Animal Behaviour, Volume 118 (2016), pp. 181-190 | DOI

[22] Diaz, A. Exploring the Impact of Urbanization on Avian Malaria Dynamics in Great Tits: Insights from a Study Across Urban and Non-Urban Environments, Peer Community in Ecology (2024) | DOI

[23] Dyrcz, A.; Wink, M.; Kruszewicz, A.; Leisler, B. Male Reproductive Success is Correlated With Blood Parasite Levels and Body Condition in the Promiscuous Aquatic Warbler (Acrocephalus Paludicola), The Auk, Volume 122 (2005) no. 2, pp. 558-565 | DOI

[24] Evans, K. L.; Gaston, K. J.; Sharp, S. P.; McGowan, A.; Simeoni, M.; Hatchwell, B. J. Effects of urbanisation on disease prevalence and age structure in blackbird Turdus merula populations, Oikos, Volume 118 (2009) no. 5, pp. 774-782 | DOI

[25] Faeth, S. H.; Bang, C.; Saari, S. Urban biodiversity: Patterns and mechanisms, Annals of the New York Academy of Sciences, Volume 1223 (2011) no. 1, pp. 69-81 | DOI

[26] Ferraguti, M.; Hernández-Lara, C.; Sehgal, R. N. M.; Santiago-Alarcon, D. Anthropogenic Effects on Avian Haemosporidians and Their Vectors, Avian Malaria and Related Parasites in the Tropics: Ecology, Evolution and Systematics, Springer International Publishing, Cham, 2020, pp. 451-485 | DOI

[27] Ferrer, E. S.; García-Navas, V.; Sanz, J. J.; Ortego, J. Molecular characterization of avian malaria parasites in three Mediterranean blue tit (Cyanistes caeruleus) populations, Parasitology Research, Volume 111 (2012) no. 5, pp. 2137-2142 | DOI

[28] Fink, D.; Auer, T.; Johnston, A.; Strimas-Mackey, M.; Robinson, O.; Ligocki, S.; Hochachka, W.; Jaromczyk, L.; Rodewald, A.; Wood, C.; Davies, I.; Spencer, A. eBird Status and Trends, eBird, 2022 | DOI

[29] Forman, R. T. T.; Godron, M. Landscape Ecology, John Wiley and Sons, New York, 1986

[30] French, S. S.; Fokidis, H. B.; Moore, M. C. Variation in stress and innate immunity in the tree lizard (Urosaurus ornatus) across an urban–rural gradient, Journal of Comparative Physiology B, Volume 178 (2008) no. 8, pp. 997-1005 | DOI

[31] Gaston, K. J.; Visser, M. E.; Hölker, F. The biological impacts of artificial light at night: the research challenge, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 370 (2015) no. 1667 | DOI

[32] Geue, D.; Partecke, J. Reduced parasite infestation in urban Eurasian blackbirds (Turdus merula): A factor favoring urbanization?, Canadian Journal of Zoology, Volume 86 (2008) no. 12, pp. 1419-1425 | DOI

[33] Giraudeau, M.; Mousel, M.; Earl, S.; McGraw, K. Parasites in the City: Degree of Urbanization Predicts Poxvirus and Coccidian Infections in House Finches (Haemorhous mexicanus), PLoS ONE, Volume 9 (2014) no. 2 | DOI

[34] Glaizot, O.; Fumagalli, L.; Iritano, K.; Lalubin, F.; Van Rooyen, J.; Christe, P. High Prevalence and Lineage Diversity of Avian Malaria in Wild Populations of Great Tits (Parus major) and Mosquitoes (Culex pipiens), PLoS ONE, Volume 7 (2012) no. 4 | DOI

[35] Hellgren, O.; Waldenström, J.; Bensch, S. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood, Journal of Parasitology, Volume 90 (2004) no. 4, pp. 797-802 | DOI

[36] Hõrak, P.; Ots, I.; Vellau, H.; Spottiswoode, C.; Møller, A. P. Carotenoid-based plumage coloration reflects hemoparasite infection and local survival in breeding great tits, Oecologia, Volume 126 (2001) no. 2, pp. 166-173 | DOI

[37] Inci, A.; Yildirim, A.; Njabo, K. Y.; Duzlu, O.; Biskin, Z.; Ciloglu, A. Detection and molecular characterization of avian Plasmodium from mosquitoes in central Turkey, Veterinary parasitology, Volume 188 (2012) no. 1-2, pp. 179-184 | DOI

[38] Jansen, C. C.; Webb, C. E.; Graham, G. C.; Craig, S. B.; Zborowski, P.; Ritchie, S. A.; Russell, R. C.; Van Den Hurk, A. F. Blood sources of mosquitoes collected from urban and peri-urban environments in eastern Australia with species-specific molecular analysis of avian blood meals, The American journal of tropical medicine and hygiene, Volume 81 (2009) no. 5, pp. 849-857 | DOI

[39] Jiménez-Peñuela, J.; Ferraguti, M.; Martínez-de la Puente, J.; Soriguer, R. C.; Figuerola, J. Urbanization effects on temporal variations of avian haemosporidian infections, Environmental Research, Volume 199 (2021) | DOI

[40] Lachish, S.; Knowles, S. C.; Alves, R.; Wood, M. J.; Sheldon, B. C. Fitness effects of endemic malaria infections in a wild bird population: the importance of ecological structure, Journal of Animal Ecology, Volume 80 (2011) no. 6, pp. 1196-1206 | DOI

[41] Lepczyk, C. A.; Aronson, M. F.; Evans, K. L.; Goddard, M. A.; Lerman, S. B.; Macivor, J. S. Biodiversity in the City: Fundamental Questions for Understanding the Ecology of Urban Green Spaces for Biodiversity Conservation, BioScience, Volume 67 (2017) no. 9, pp. 799-807 | DOI

[42] Lutz, H. L.; Hochachka, W. M.; Engel, J. I.; Bell, J. A.; Tkach, V. V.; Bates, J. M.; Hackett, S. J.; Weckstein, J. D. Parasite Prevalence Corresponds to Host Life History in a Diverse Assemblage of Afrotropical Birds and Haemosporidian Parasites, PLOS ONE, Volume 10 (2015) no. 4 | DOI

[43] Martin, L. B.; Boruta, M. The impacts of urbanization on avian disease transmission and emergence, Avian Urban Ecology, Oxford University Press, 2013, pp. 116-128 | DOI

[44] Martínez-De La Puente, J.; Martínez, J.; Rivero-De-Aguilar, J.; Del Cerro, S.; Merino, S. Vector abundance determines Trypanosoma prevalence in nestling blue tits, Parasitology, Volume 140 (2013) no. 8, pp. 1009-1015 | DOI

[45] Marzal, A.; De Lope, F.; Navarro, C.; Møller, A. P. Malarial parasites decrease reproductive success: An experimental study in a passerine bird, Oecologia, Volume 142 (2005) no. 4, pp. 541-545 | DOI

[46] Marzluff, J. M. Worldwide urbanization and its effects on birds, Avian Ecology and Conservation in an Urbanizing World, Springer US, Boston, MA, 2001, pp. 19-47 | DOI

[47] McKinney, M. L. Effects of urbanization on species richness: A review of plants and animals, Urban Ecosystems, Volume 11 (2008) no. 2, pp. 161-176 | DOI

[48] Nagendra, H. Opposite trends in response for the Shannon and Simpson indices of landscape diversity, Applied Geography, Volume 22 (2002) no. 2, pp. 175-186 | DOI

[49] Neiderud, C.-J. How urbanization affects the epidemiology of emerging infectious diseases, Infection Ecology & Epidemiology, Volume 5 (2015) no. 1 | DOI

[50] Nielsen, A. B.; van den Bosch, M.; Maruthaveeran, S.; van den Bosch, C. K. Species richness in urban parks and its drivers: A review of empirical evidence, Urban Ecosystems, Volume 17 (2013) no. 1, pp. 305-327 | DOI

[51] Ots, I.; Hõrak, P. Health impact of blood parasites in breeding great tits, Oecologia, Volume 116 (1998) no. 4, pp. 441-448 | DOI

[52] Partecke, J.; Hegyi, G.; Fitze, P. S.; Gasparini, J.; Schwabl, H. Maternal effects and urbanization: Variation of yolk androgens and immunoglobulin in city and forest blackbirds, Ecology and Evolution, Volume 10 (2020) no. 4, pp. 2213-2224 | DOI

[53] Paz, S.; Albersheim, I. Influence of warming tendency on Culex pipiens population abundance and on the probability of West Nile fever outbreaks (Israeli case study: 2001-2005), EcoHealth, Volume 5 (2008) no. 1, pp. 40-48 | DOI

[54] Perrier, C.; Lozano del Campo, A.; Szulkin, M.; Demeyrier, V.; Gregoire, A.; Charmantier, A. Great tits and the city: Distribution of genomic diversity and gene–environment associations along an urbanization gradient, Evolutionary Applications, Volume 11 (2018) no. 5, pp. 593-613 | DOI

[55] Perrins, C. M. British tits, London, UK, 1979

[56] 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, Volume 9 (2018) no. 9 | DOI

[57] Pigeault, R.; Cozzarolo, C. S.; Choquet, R.; Strehler, M.; Jenkins, T.; Delhaye, J.; Bovet, L.; Wassef, J.; Glaizot, O.; Christe, P. Haemosporidian infection and co-infection affect host survival and reproduction in wild populations of great tits, International Journal for Parasitology, Volume 48 (2018) no. 14, pp. 1079-1087 | DOI

[58] R Core Team R: A language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, 2018 (https://www.R-project.org)

[59] Rivero, A.; Gandon, S. Evolutionary Ecology of Avian Malaria: Past to Present, Trends in Parasitology, Volume 34 (2018) no. 8, pp. 712-726 | DOI

[60] Rooyen, J. v.; Lalubin, F.; Glaizot, O.; Christe, P. Altitudinal variation in haemosporidian parasite distribution in great tit populations, Parasites and Vectors, Volume 6 (2013) no. 1, pp. 1-10 | DOI

[61] Santiago-Alarcon, D.; Carbó-Ramírez, P.; Macgregor-Fors, I.; Chávez-Zichinelli, C. A.; Yeh, P. J. The prevalence of avian haemosporidian parasites in an invasive bird is lower in urban than in non-urban environments, Ibis, Volume 162 (2020) no. 1, pp. 201-214 | DOI

[62] Santiago-Alarcon, D.; Havelka, P.; Schaefer, H. M.; Segelbacher, G. Bloodmeal Analysis Reveals Avian Plasmodium Infections and Broad Host Preferences of Culicoides (Diptera: Ceratopogonidae) Vectors, PLoS ONE, Volume 7 (2012) no. 2 | DOI

[63] Santiago-Alarcon, D.; MacGregor-Fors, I.; Kühnert, K.; Segelbacher, G.; Schaefer, H. M. Avian haemosporidian parasites in an urban forest and their relationship to bird size and abundance, Urban Ecosystems, Volume 19 (2016) no. 1, pp. 331-346 | DOI

[64] Shochat, E.; Warren, P. S.; Faeth, S. H.; McIntyre, N. E.; Hope, D. From patterns to emerging processes in mechanistic urban ecology, Trends in Ecology & Evolution, Volume 21 (2006) no. 4, pp. 186-191 | DOI

[65] Valkiunas, G. Avian Malaria Parasites and other Haemosporidia, CRC Press, 2004 | DOI

[66] Valkiunas, G.; Iezhova, T. A. Keys to the avian malaria parasites, Malaria Journal, Volume 17 (2018) no. 1, pp. 1-24 | DOI

[67] Ventim, R.; Ramos, J. A.; Osório, H.; Lopes, R. J.; Pérez-Tris, J.; Mendes, L. Avian malaria infections in western European mosquitoes, Parasitology research, Volume 111 (2012) no. 2, pp. 637-645 | DOI

[68] Wood, M. J.; Cosgrove, C. L.; Wilkin, T. A.; Knowles, S. C.; Day, K. P.; Sheldon, B. C. Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus, Molecular Ecology, Volume 16 (2007) no. 15, pp. 3263-3273 | DOI

[69] Zélé, F.; Vézilier, J.; L’Ambert, G.; Nicot, A.; Gandon, S.; Rivero, A.; Duron, O. Dynamics of prevalence and diversity of avian malaria infections in wild Culex pipiens mosquitoes: the effects of Wolbachia, filarial nematodes and insecticide resistance, Parasites & Vectors, Volume 7 (2014) no. 1 | DOI

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