Bird Community Composition, Migration, and Environmental Factors Jointly Influence the Global Distribution of Avian Haemosporidian Lineages

Abstract

Parasite distributions are under the influence of host occurrence and tolerable environmental conditions. In vector-borne disease systems, including avian malaria, they are further constrained by the environmental niche of the vectors. The fact that avian haemosporidians occur in a large number of migratory and non-migratory species means the role of bird migration in the global distribution of avian haemosporidians is an open question. Because avian haemosporidians refer to a large number of genetic lineages that are well characterized in terms of host and geographic range, we introduce an ecoregion pairwise analysis that sets out to explain the similarity in lineages in pairs of ecoregions as a function of the pair's similarity in migratory and non-migratory bird communities, as well as environmental conditions. We identify important roles for each of these factors in explaining the overall geographic distribution of lineages, including strong support for the role of migratory birds in moving lineages between environmentally dissimilar ecoregions.

Keywords

disease ecology / malaria / migratory species / parasite distribution / parasite sharing

References

[1] Altizer, S., R. Bartel, and B. A. Han. 2011. “Animal Migration and Infectious Disease Risk.” Science (New York, N.Y.) 331, no. 6015: 296–302.

[2] Beadell, J. S., F. Ishtiaq, R. Covas, et al. 2006. “Global Phylogeographic Limits of Hawaii's Avian Malaria.” Proceedings of the Royal Society B: Biological Sciences 273, no. 1604: 2935–2944.

[3] Beaudoin, R. L., J. E. Applegate, D. E. Davis, and R. G. Mclean. 1971. “A Model for the Ecology of Avian Malaria.” Journal of Wildlife Diseases 7, no. 1: 5–13.

[4] Bennett, G. F., M. A. Peirce, and R. W Ashford. 1993. “Avian Haematozoa: Mortality and Pathogenicity.” Journal of Natural History 27, no. 5: 993–1001.

[5] Benning, T. L., D. Lapointe, C. T. Atkinson, and P. M. Vitousek. 2002. “Interactions of Climate Change with Biological Invasions and Land Use in the Hawaiian Islands: Modeling the Fate of Endemic Birds Using a Geographic Information System.” Proceedings of the National Academy of Sciences of the United States of America 99, no. 22: 14246–14249.

[6] Bensch, S., O. Hellgren, and J. Pérez-Tris. 2009. “MalAvi: A Public Database of Malaria Parasites and Related Haemosporidians in Avian Hosts Based on Mitochondrial Cytochrome B Lineages.” Molecular Ecology Resources 9, no. 5: 1353–1358.

[7] BirdLife International and Handbook of the Birds of the World. 2021. " Bird Species Distribution Maps of the World." Version 2021.1. http://datazone.birdlife.org/species/requestdis.

[8] Both, C., S. Bouwhuis, C. M. Lessells, and M. E. Visser. 2006. “Climate Change and Population Declines in a Long-Distance Migratory Bird.” Nature 441, no. 7089: 81–83.

[9] Brown, J. J., M. Pascual, M. C. Wimberly, L. R. Johnson, and C. C. Murdock. 2023. “Humidity—The Overlooked Variable in the Thermal Biology of Mosquito-Borne Disease.” Ecology Letters 26, no. 7: 1029–1049.

[10] Byers, J. E., J. P. Schmidt, P. Pappalardo, S. E. Haas, and P. R. Stephens. 2019. “What Factors Explain the Geographical Range of Mammalian Parasites?” Proceedings of the Royal Society B: Biological Sciences 286, no. 1903: 20190673.

[11] Caminade, C., K. M. McIntyre, and A. E. Jones. 2019. “Impact of Recent and Future Climate Change on Vector-Borne Diseases: Climate Change and Vector-Borne Diseases.” Annals of the New York Academy of Sciences 1436, no. 1: 157–173.

[12] Cizauskas, C. A., C. J. Carlson, K. R. Burgio, et al. 2017. “Parasite Vulnerability to Climate Change: An Evidence-Based Functional Trait Approach.” Royal Society Open Science 4, no. 1: 160535.

[13] Clark, N. J., S. M. Clegg, and M. Klaassen. 2016. “Migration Strategy and Pathogen Risk: Non-Breeding Distribution Drives Malaria Prevalence in Migratory Waders.” Oikos (Copenhagen, Denmark) 125, no. 9: 1358–1368.

[14] Cleveland, C. A., T. A. Dallas, S. Vigil, D. G. Mead, J. L. Corn, and A. W. Park. 2023. “Vector Communities Under Global Change May Exacerbate and Redistribute Infectious Disease Risk.” Parasitology Research 122, no. 4: 963–972.

[15] Cooper, N., R. Griffin, M. Franz, M. Omotayo, and C. L. Nunn. 2012. “Phylogenetic Host Specificity and Understanding Parasite Sharing in Primates.” Ecology Letters 15, no. 12: 1370–1377.

[16] Davies, T. J., and A. B. Pedersen. 2008. “Phylogeny and Geography Predict Pathogen Community Similarity in Wild Primates and Humans.” Proceedings of the Royal Society B: Biological Sciences 275, no. 1643: 1695–1701.

[17] de Angeli Dutra, D., R. Poulin, and F. C. Ferreira. 2022. “Evolutionary Consequences of Vector-Borne Transmission: How Using Vectors Shapes Host, Vector and Pathogen Evolution.” Parasitology 149, no. 13: 1667–1678.

[18] Dharmarajan, G., P. Gupta, C. K. Vishnudas, and V. V. Robin. 2021. “Anthropogenic Disturbance Favours Generalist over Specialist Parasites in Bird Communities: Implications for Risk of Disease Emergence.” Ecology Letters 24, no. 9: 1859–1868.

[19] Dufour, P., C. De Franceschi, P. Doniol-Valcroze, et al. 2021. “A New Westward Migration Route in an Asian Passerine Bird.” Current Biology 31, no. 24: 5590–5596.e4.

[20] Ellis, V. A., E. H. R. Sari, D. R. Rubenstein, R. C. Dickerson, S. Bensch, and R. E. Ricklefs. 2019. “The Global Biogeography of Avian Haemosporidian Parasites Is Characterized by Local Diversification and Intercontinental Dispersal.” Parasitology 146, no. 2: 213–219.

[21] Fecchio, A., N. J. Clark, J. A. Bell, et al. 2021. “Global Drivers of Avian Haemosporidian Infections Vary Across Zoogeographical Regions.” Global Ecology and Biogeography: A Journal of Macroecology 30, no. 12: 2393–2406.

[22] Fecchio, A., K. Wells, J. A. Bell, et al. 2019. “Climate Variation Influences Host Specificity in Avian Malaria Parasites.” Ecology Letters 22, no. 3: 547–557.

[23] Fick, S. E., and R. J. Hijmans. 2017. “WorldClim 2: New 1-km Spatial Resolution Climate Surfaces for Global Land Areas: New Climate Surfaces for Global Land Areas.” International Journal of Climatology: A Journal of the Royal Meteorological Society 37, no. 12: 4302–4315.

[24] Freeman, M. T., B. Coulson, J. C. Short, C. A. Ngcamphalala, M. O. Makola, and A. E. Mckechnie. 2024. “Evolution of Avian Heat Tolerance: The Role of Atmospheric Humidity.” Ecology 105, no. 5: e4279.

[25] Gage, K. L., T. R. Burkot, R. J. Eisen, and E. B. Hayes. 2008. “Climate and Vectorborne Diseases.” American Journal of Preventive Medicine 35, no. 5: 436–450.

[26] Gager, A. B., J. Del Rosario Loaiza, D. C. Dearborn, and E. Bermingham. 2008. “Do Mosquitoes Filter the Access of Plasmodium Cytochrome B Lineages to an Avian Host?” Molecular Ecology 17, no. 10: 2552–2561.

[27] Galen, S. C., J. Borner, E. S. Martinsen, et al. 2018. “The Polyphyly of Plasmodium: Comprehensive Phylogenetic Analyses of the Malaria Parasites (Order Haemosporida) Reveal Widespread Taxonomic Conflict.” Royal Society Open Science 5, no. 5: 171780.

[28] Galen, S. C., S. Ray, M. Henry, and J. D. Weckstein. 2022. “Parasite-Associated Mortality in Birds: The Roles of Specialist Parasites and Host Evolutionary Distance.” Biology Letters 18, no. 4: 20210575.

[29] Gangoso, L., C. Santamaría-Cervantes, J. Martínez-De La Puente, M. J. Ruiz López, and J. Figuerola. 2024. “Does Malaria Infection Increase the Risk of Predation-Related Mortality During Bird Migration?” iScience 27, no. 12: 111358.

[30] Gatewood, A. G., K. A. Liebman, G. Vourc'h, et al. 2009. “Climate and Tick Seasonality Are Predictors of Borrelia burgdorferi Genotype Distribution.” Applied and Environmental Microbiology 75, no. 8: 2476–2483.

[31] Glaizot, O., L. Fumagalli, K. Iritano, F. Lalubin, J. Van Rooyen, and P. Christe. 2012. “High Prevalence and Lineage Diversity of Avian Malaria in Wild Populations of Great Tits (Parus major) and Mosquitoes (Culex pipiens).” PLoS ONE 7, no. 4: e34964.

[32] Guisan, A., T. C. Edwards Jr, and T. Hastie. 2002. “Generalized Linear and Generalized Additive Models in Studies of Species Distributions: Setting the Scene.” Ecological Modelling 157, no. 2-3: 89–100.

[33] Huang, S., O. R. P. Bininda-Emonds, P. R. Stephens, J. L. Gittleman, and S. Altizer. 2013. “Phylogenetically Related and Ecologically Similar Carnivores Harbour Similar Parasite Assemblages.” The Journal of Animal Ecology83, no. 3: 671–680. https://doi.org/10.1111/1365-2656.12160.

[34] Huntley, B., Y. C. Collingham, R. E. Green, G. M. Hilton, C. Rahbek, and S. G. Willis. 2006. “Potential Impacts of Climatic Change Upon Geographical Distributions of Birds.” Ibis 148: 8–28.

[35] Ishtiaq, F., E. Gering, J. H. Rappole, et al. 2007. “Prevalence and Diversity of Avian Hematozoan Parasites in Asia: A Regional Survey.” Journal of Wildlife Diseases 43, no. 3: 382–398.

[36] IUCN. 2021. The IUCN Red List of Threatened Species. Accessed 2021. http://www.iucnredlist.org/.

[37] Kilpatrick, A. M., and S. E. Randolph. 2012. “Drivers, Dynamics, and Control of Emerging Vector-Borne Zoonotic Diseases.” Lancet 380, no. 9857: 1946–1955.

[38] Lapointe, D. A., C. T. Atkinson, and M. D. Samuel. 2012. “Ecology and Conservation Biology of Avian Malaria: Ecology of Avian Malaria.” Annals of the New York Academy of Sciences 1249, no. 1: 211–226.

[39] Lawrence, K. B., C. R. Barlow, K. Bensusan, C. Perez, and S. G. Willis. 2022. “Phenological Trends in the Pre- and Post-Breeding Migration of Long-Distance Migratory Birds.” Global Change Biology 28, no. 2: 375–389.

[40] Li, N., Z. Wang, Y. Cai, and L. Zhang. 2020. “Importance of Microhabitat Selection by Birds for the Early Recruitment of Endangered Trees in a Fragmented Forest.” Avian Research 11: 46.

[41] Lima, M. R., and J. Pérez-Tris. 2020. “Host Specialization and Dispersal in Avian Haemosporidians.” In Avian Malaria and Related Parasites in the Tropics: Ecology, Evolution and Systematics, edited by D. Santiago-Alarcon and A. Marzal, 379–400. Springer International Publishing.

[42] Lymbery, A. J. 2015. “Niche Construction: Evolutionary Implications for Parasites and Hosts.” Trends in Parasitology 31, no. 4: 134–141.

[43] Miranda Paez, A., K. Chalkowski, S. Zohdy, and J. R. Willough. 2022. “Management of Avian Malaria in Populations of High Conservation Concern.” Parasites & Vectors 15, no. 1: 208.

[44] Mordecai, E. A., K. P. Paaijmans, L. R. Johnson, et al. 2013. “Optimal Temperature for Malaria Transmission Is Dramatically Lower Than Previously Predicted.” Ecology Letters 16, no. 1: 22–30.

[45] Moyer, B. R., D. M. Drown, and D. H. Clayton. 2002. “Low Humidity Reduces Ectoparasite Pressure: Implications for Host Life History Evolution.” Oikos (Copenhagen, Denmark) 97, no. 2: 223–228.

[46] Mukhin, A., V. Palinauskas, E. Platonova, D. Kobylkov, I. Vakoliuk, and G. Valkiūnas. 2016. “The Strategy to Survive Primary Malaria Infection: An Experimental Study on Behavioural Changes in Parasitized Birds.” PLoS ONE 11, no. 7: e0159216.

[47] O'Brien, R. M. 2007. “A Caution Regarding Rules of Thumb for Variance Inflation Factors.” Quality & Quantity 41, no. 5: 673–690.

[48] Olson, D. M., and E. Dinerstein. 1998. “The Global 200: A Representation Approach to Conserving the Earth's Most Biologically Valuable Ecoregions.” Conservation Biology: The Journal of the Society for Conservation Biology 12, no. 3: 502–515.

[49] Pacheco, M. A., A. S. Cepeda, R. Bernotienė, et al. 2018. “Primers Targeting Mitochondrial Genes of Avian Haemosporidians: PCR Detection and Differential DNA Amplification of Parasites Belonging to Different Genera.” International Journal for Parasitology 48, no. 8: 657–670.

[50] Pebesma, E. 2018. “Simple Features for R: Standardized Support for Spatial Vector Data.” The R Journal 10, no. 1: 439–446. https://doi.org/10.32614/RJ-2018-009.

[51] Perrin, A., O. Glaizot, and P. Christe. 2025. “Migratory Birds Spread Their Haemosporidian Parasites Along the World's Major Migratory Flyways.” Oikos (Copenhagen, Denmark)e11012.

[52] Pulgarín-R, P. C., C. Gómez, N. J. Bayly, et al. 2019. “Migratory Birds as Vehicles for Parasite Dispersal? Infection by Avian Haemosporidians over the Year and Throughout the Range of a Long-Distance Migrant.” Journal of Biogeography 46, no. 1: 83–96.

[53] Ramón-Martínez, D., and J. Seoane. 2024. “Changes in Thermal Niche Position and Breadth of Bird Assemblages in Spain in Relation to Increasing Temperatures.” Journal of Biogeography 51, no. 5: 783–796.

[54] Reisen, W. K. 2010. “Landscape Epidemiology of Vector-Borne Diseases.” Annual Review of Entomology 55, no. 1: 461–483.

[55] Ricklefs, R. E., M. Medeiros, V. A. Ellis, et al. 2017. “Avian Migration and the Distribution of Malaria Parasites in New World Passerine Birds.” Journal of Biogeography 44, no. 5: 1113–1123.

[56] Rivero, A., and S. Gandon. 2018. “Evolutionary Ecology of Avian Malaria: Past to Present.” Trends in Parasitology 34, no. 8: 712–726.

[57] Rozen-Rechels, D., A. Dupoué, O. Lourdais, et al. 2019. “When Water Interacts with Temperature: Ecological and Evolutionary Implications of Thermo-Hydroregulation in Terrestrial Ectotherms.” Ecology and Evolution 9, no. 17: 10029–10043.

[58] Santiago-Alarcon, D., and A. Marzal. 2020. “Research on Avian Haemosporidian Parasites in the Tropics Before the Year 2000.” In Avian Malaria and Related Parasites in the Tropics, 1–44. Springer International Publishing.

[59] Sauer, F. G., J. Grave, R. Lühken, and E. Kiel. 2021. “Habitat and Microclimate Affect the Resting Site Selection of Mosquitoes.” Medical and Veterinary Entomology 35, no. 3: 379–388.

[60] Schatz, A. M., and A. W. Park. 2021. “Host and Parasite Traits Predict Cross-Species Parasite Acquisition by Introduced Mammals.” Proceedings of the Royal Society B: Biological Sciences 288, no. 1950: 20210341.

[61] Schatz, A. M., and A. W. Park. 2023. “Patterns of Host-Parasite Coinvasion Promote Enemy Release and Specialist Parasite Spillover.” The Journal of Animal Ecology 92: 1029–1041. http://doi.org/10.1111/1365-2656.13910.

[62] Schatz, A. M., and A. W. Park. 2025. “Evidence for the Vacated Niche Hypothesis in Parasites of Invasive Mammals.” Ecology and Evolution 15, no. 2: e70959.

[63] Şekercioğlu, Ç. H., R. B. Primack, and J. Wormworth. 2012. “The Effects of Climate Change on Tropical Birds.” Biological Conservation 148, no. 1: 1–18.

[64] Smith, D. L., K. E. Battle, S. I. Hay, C. M. Barker, T. W. Scott, and F. E. Mckenzie. 2012. “Ross, Macdonald, and a Theory for the Dynamics and Control of Mosquito-Transmitted Pathogens.” PLoS Pathogens 8, no. 4: e1002588.

[65] Soares, L., S. C. Latta, and R. E. Ricklefs. 2020. “Neotropical Migratory and Resident Birds Occurring in Sympatry During Winter Have Distinct Haemosporidian Parasite Assemblages.” Journal of Biogeography 47, no. 3: 748–759.

[66] Stephens, P. R., S. Altizer, V. O. Ezenwa, et al. 2019. “Parasite Sharing in Wild Ungulates and Their Predators: Effects of Phylogeny, Range Overlap, and Trophic Links.” The Journal of Animal Ecology 88, no. 7: 1017–1028.

[67] Tomás, G., S. Merino, J. Martínez-De La Puente, J. Moreno, J. Morales, and E. Lobato. 2008. “A Simple Trapping Method to Estimate Abundances of Blood-Sucking Flying Insects in Avian Nests.” Animal Behaviour 75, no. 2: 723–729.

[68] Visser, M. E., and P. Gienapp. 2019. “Evolutionary and Demographic Consequences of Phenological Mismatches.” Nature Ecology & Evolution 3, no. 6: 879–885.

[69] Wood, S. N. 2011. “Fast Stable Restricted Maximum Likelihood and Marginal Likelihood Estimation of Semiparametric Generalized Linear Models: Estimation of Semiparametric Generalized Linear Models.” Journal of the Royal Statistical Society Series B: Statistical Methodology 73, no. 1: 3–36.

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