Intensity of Haemoproteus spp. blood infection differs between wild birds captured using different trapping methods
DOI:
https://doi.org/10.21638/spbu03.2024.307Abstract
Infection with haemoparasites (Haemosporida spp.) is common within wild birds’ populations and has been associated with adverse effects on birds’ fitness and life performance. Existing literature suggests a hypothesis that birds infected with haemosporidians and exhibiting high parasitemia levels may demonstrate reduced activity, potentially leading to their underrepresentation in captures which use stationary traps, such as mist nets. However, there are limited studies demonstrating this phenomenon in wild birds. To study the possible under representation of highly parasitized birds, captured with commonly used stationary mist nets, we compared parasitemia levels of haemosporidian parasites in wild birds captured during spring migration using both actively startling of birds and birds trapped passively into the mist nets. Utilizing cumulative link mixed models, we assessed the influence of trapping methods on parasitemia scores, controlling for factors such as species identity, season progression, and migration distance. Our dataset comprised 1815 individuals of 60 species, including 142 actively captured and 1673 passively captured ones. Although the number of infected individuals was higher in passively caught birds (24 % in active vs 43 % in passive), the study revealed a significant difference between infected birds within two capture methods: despite challenges in balancing sample sizes, and trapping dates, the findings affirm the underestimation of birds having high parasitemia levels with prevalent mist net techniques. We highlight the importance of considering potential biases in trapping methods when studying haemosporidian parasites in avian hosts during migration.
Keywords:
avian haemosporidiosis, Haemoproteus, parasitemia, spring migration, chronic haemosporidiosis
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References
Altizer, S., Bartel, R., and Han, B. A. 2011. Animal migration and infectious disease risk. Science 331(6015):296–302. https://doi.org/10.1126/science.1194694
Applegate, J. and Beaudoin, R. 1970. Mechanism of spring relapse in avian malaria: effect of gonadotropin and corticosterone. Journal of Wildlife Diseases 6(4):443–447. https://doi.org/10.7589/0090-3558-6.4.443
Asghar, M., Hasselquist, D., and Bensch, S. 2011. Are chronic avian haemosporidian infections costly in wild birds? Journal of Avian Biology 42(6):530–537. https://doi.org/10.1111/j.1600-048X.2011.05281.x
Asghar, M., Westerdahl, H., Zehtindjiev, P., Ilieva, M., Hasselquist, D., and Bensch, S. 2012. Primary peak and chronic malaria infection levels are correlated in experimentally infected great reed warblers. Parasitology 139(10)(10):1246–1252. https://doi.org/10.1017/S0031182012000510
Atkinson, C. T. and Van Riper III, C. 1991. Pathogenicity and epizootiology of avian haematozoa: Plasmodium, leucocytozoon, and haemoproteus; pp. 19–48 in Loye, J. E. and Zuk, M. (eds), Bird-parasite interactions, ecology, evolution and behavior. Oxford University Press, New York. https://doi.org/10.1093/oso/9780198577386.003.0002
Atkinson, C. T., Thomas, N. J., and Hunter, D. B. (eds). 2008. Parasitic Diseases of Wild Birds. Wiley-Blackwell. Ames, Iowa. https://doi.org/10.1002/9780813804620
Bates, D., Mächler, M., Bolker, B., and Walker, S. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67(1):1–48. https://doi.org/10.18637/jss.v067.i01
Bennett, G., Peirce, M., and Ashford, R. 1993. Avian haematozoa: mortality and pathogenicity. Journal of Natural History 27(5):993–1001. https://doi.org/10.1080/00222939300770621
Bensch, S., Waldenström, J., Jonzán, N., Westerdahl, H., Hansson, B., Sejberg, D., and Hasselquist, D. 2007. Temporal dynamics and diversity of avian malaria parasites in a single host species. Journal of Animal Ecology 112–122. https://doi.org/10.1111/j.1365-2656.2006.01176.x
Byrd, A. J., Talbott, K. M., Smiley, T. M., Verrett, T. B., Gross, M., Hladik, M. L., Ketterson, E. D., and Becker, D. 2023. Determinants of spring migration departure dates in a New World sparrow: Weather variables reign supreme. bioRxiv:2023.2011.2017.567563. https://doi.org/10.1101/2023.11.17.567563
Christensen, R. H. B. 2022. Regression models for ordinal data [R package ordinal version 2022.11–16].
Cornet, S., Nicot, A., Rivero, A., and Gandon, S. 2014. Evolution of plastic transmission strategies in avian malaria. Plos Pathogens 10(9):e1004308. https://doi.org/10.1371/journal.ppat.1004308
Duc, M., Ilgūnas, M., Kubiliūnaitė, M., and Valkiūnas, G. 2021. First report of Haemoproteus (Haemosporida, Haemoproteidae) megalomeronts in the brain of an avian host, with description of megalomerogony of Haemoproteus pastoris, the blood parasite of the common starling. Animals 11(10):2824. https://doi.org/https://doi.org/10.3390/ani11102824
Duc, M., Himmel, T., Ilgūnas, M., Eigirdas, V., Weissenböck, H., and Valkiūnas, G. 2023. Exo-erythrocytic development of two Haemoproteus species (Haemosporida, Haemoproteidae), with description of Haemoproteus dumbbellus, a new blood parasite of bunting birds (Emberizidae). International Journal for Parasitology 53(10)531–543. https://doi.org/10.1016/j.ijpara.2023.02.009
Emmenegger, T., Bauer, S., Hahn, S., Müller, S. B., Spina, F., and Jenni, L. 2018. Blood parasites prevalence of migrating passerines increases over the spring passage period. Journal of Zoology 306(1):23–27. https://doi.org/10.1111/jzo.12565
Emmenegger, T., Riello, S., Schmid, R., Serra, L., Spina, F., and Hahn, S. 2023. Avian haemosporidians infecting short-and long-distance migratory old world flycatcher species and the variation in parasitaemia after endurance flights. Acta Parasitologica 1–8. https://doi.org/10.1007/s11686-023-00710-0
Emmenegger, T., Bensch, S., Hahn, S., Kishkinev, D., Procházka, P., Zehtindjiev, P., and Bauer, S. 2021. Effects of blood parasite infections on spatio-temporal migration patterns and activity budgets in a long‐distance migratory passerine. Ecology and evolution 11(2):753–762. https://doi.org/10.1002/ece3.7030
Hernández-Lara, C., Duc, M., Ilgūnas, M., and Valkiūnas, G. 2021. Massive infection of lungs with exo-erythrocytic meronts in European Robin Erithacus rubecula during natural Haemoproteus attenuatus haemoproteosis. Animals 11(11):3273. https://doi.org/10.3390/ani11113273
Holmstad, P. R., Jensen, K. H., and Skorping, A. 2006. Vector-borne parasites decrease host mobility: A field test of freeze or flee behaviour of willow ptarmigan. International journal for parasitology 36(7):735–740. https://doi.org/10.1016/j.ijpara.2006.02.015
Ilgūnas, M., Romeiro Fernandes Chagas, C., Bukauskaitė, D., Bernotienė, R., Iezhova, T., and Valkiūnas, G. 2019. The life-cycle of the avian haemosporidian parasite Haemoproteus majoris, with emphasis on the exoerythrocytic and sporogonic development. Parasites and Vectors 12:1–15. https://doi.org/10.1186/s13071-019-3773-4
López, G., Muñoz, J., Soriguer, R., and Figuerola, J. 2013. Increased endoparasite infection in late-arriving individuals of a trans-Saharan passerine migrant bird. PloS One 8(12):e81898. https://doi.org/10.1371/journal.pone.0081898
Merino, S., Moreno, J., Sanz, J. J., and Arriero, E. 2000. Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proceedings of the Royal Society of London. Series B: Biological Sciences 267(1461):2507–2510. https://doi.org/10.1098/rspb.2000.1312
Møller, A. P. and Nielsen, J. T. 2007. Malaria and risk of predation: a comparative study of birds. Ecology 88(4):871–881. https://doi.org/10.1890/06-0747
Møller, A. P., de Lope, F., and Saino, N. 2004. Parasitism, immunity, and arrival date in a migratory bird, the barn swallow. Ecology 85(1):206–219. https://doi.org/https://doi.org/10.1890/02-0451
Mukhin, A., Palinauskas, V., Platonova, E., Kobylkov, D., Vakoliuk, I., and Valkiūnas, G. 2016. The strategy to survive primary malaria infection: An experimental study on behavioural changes in parasitized birds. Plos One 11(7):e0159216. https://doi.org/10.1371/journal.pone.0159216
Nilsson, E., Taubert, H., Hellgren, O., Huang, X., Palinauskas, V., Markovets, M., Valkiūnas, G., and Bensch, S. 2016. Multiple cryptic species of sympatric generalists within the avian blood parasite Haemoproteus majoris. Journal of Evolutionary Biology 29(9):1812–1826. https://doi.org/10.1111/jeb.12911
Ortiz-Catedral, L., Brunton, D., Stidworthy, M. F., Elsheikha, H. M., Pennycott, T., Schulze, C., Braun, M., Wink, M., Gerlach, H., and Pendl, H. 2019. Haemoproteus minutus is highly virulent for Australasian and South American parrots. Parasites and Vectors 12(1):1–10. https://doi.org/10.1186/s13071-018-3255-0
Palinauskas, V., Žiegytė, R., Šengaut, J., and Bernotienė, R. 2018. Different paths–the same virulence: Experimental study on avian single and co-infections with Plasmodium relictum and Plasmodium elongatum. International Journal for Parasitology 48(14):1089–1096. https://doi.org/10.1016/j.ijpara.2018.08.003
Peirce, M. and Mead, C. 1978. Haematozoa of British birds: III. Spring incidence of blood parasites of birds from Hertfordshire, especially returning migrants. Journal of Natural History 12(3):337–340. https://doi.org/10.1080/00222937800770181
Pigeault, R., Cozzarolo, C.-S., Choquet, R., Strehler, M., Jenkins, T., Delhaye, J., Bovet, L., Wassef, J., Glaizot, O., and Christe, P. 2018. Haemosporidian infection and co-infection affect host survival and reproduction in wild populations of great tits. International Journal for Parasitology 48(14):1079–1087. https://doi.org/10.1016/j.ijpara.2018.06.007
Poulin, R. and de Angeli Dutra, D. 2021. Animal migrations and parasitism: Reciprocal effects within a unified framework. Biological Reviews 96(4):1331–1348. https://doi.org/10.1111/brv.12704
Puente, J. M.-d. l., Merino, S., Tomás, G., Moreno, J., Morales, J., Lobato, E., García-Fraile, S., and Belda, E. J. 2010. The blood parasite Haemoproteus reduces survival in a wild bird: A medication experiment. Biology Letters 6(5):663–665. https://doi.org/10.1098/rsbl.2010.0046
R Core Team. 2022. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.R-project.org/.
Sorensen, M. C., Asghar, M., Bensch, S., Fairhurst, G. D., Jenni‐Eiermann, S., and Spottiswoode, C. N. 2016. A rare study from the wintering grounds provides insight into the costs of malaria infection for migratory birds. Journal of Avian Biology 47(4):575–582. https://doi.org/10.1111/jav.00870
Sorensen, M. C., Dixit, T., Kardynal, K. J., Newton, J., Hobson, K. A., Bensch, S., Jenni‐Eiermann, S., and Spottiswoode, C. N. 2019. Migration distance does not predict blood parasitism in a migratory songbird. Ecology and Evolution 9(14):8294–8304. https://doi.org/10.1002/ece3.5404
Valkiūnas, G. 2005. Avian malaria parasites and other haemosporidia. Boca Raton, USA: CRC press. https://doi.org/10.1201/9780203643792
Valkiūnas, G. and Iezhova, T. A. 2017. Exo-erythrocytic development of avian malaria and related haemosporidian parasites. Malaria Journal 16:1–24. https://doi.org/10.1186/s12936-017-1746-7
Valkiūnas, G., Iezhova, T. A., Križanauskienė, A., Palinauskas, V., Sehgal, R. N., and Bensch, S. 2008. A comparative analysis of microscopy and PCR-based detection methods for blood parasites. Journal of Parasitology 94(6):1395–1401. https://doi.org/10.1645/GE-1570.1
Videvall, E., Cornwallis, C. K., Ahrén, D., Palinauskas, V., Valkiūnas, G., and Hellgren, O. 2017. The transcriptome of the avian malaria parasite Plasmodium ashfordi displays host‐specific gene expression. Molecular Ecology 26(11):2939–2958. https://doi.org/10.1111/mec.14085
Waldenström, J., Bensch, S., Kiboi, S., Hasselquist, D., and Ottosson, U. 2002. Cross‐species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Ecology 11(8):1545–1554. https://doi.org/10.1046/j.1365-294X.2002.01523.x
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Published
2024-12-06
How to Cite
Erokhina, M., Bushuev, A., Palinauskas, V., Platonova, E., & Mukhin, A. (2024). Intensity of <em>Haemoproteus</em> spp. blood infection differs between wild birds captured using different trapping methods. Biological Communications, 69(3), 192–199. https://doi.org/10.21638/spbu03.2024.307
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Articles of Biological Communications are open access distributed under the terms of the License Agreement with Saint Petersburg State University, which permits to the authors unrestricted distribution and self-archiving free of charge.
