Haemosporidian Parasites in Domestic and Wild Birds

Isra’a M. Essa

doi:10.37899/journallalifesci.v6i1.1838

Isra’a M. Essa Department of Public Health, College of Veterinary Medicine, University of Basrah, Basra, Iraq https://orcid.org/0000-0002-7379-7503

DOI: https://doi.org/10.37899/journallalifesci.v6i1.1838

Keywords: Blood parasites of birds, Haemoproteus, Plasmodium, Leucocytozoon

Abstract

This study aims to provide brief information about the role of haemosporidian parasites in birds and significant implications for avian health, population dynamics, and control efforts. Haemosporidian parasites, belonging to the phylum Apicomplexa, are a diverse group of protozoan organisms that infect a wide range of vertebrate hosts, including birds. These parasites have a complex life cycle, with both sexual and asexual stages, and are transmitted by blood-feeding insects such as mosquitoes, midges, and blackflies. The potential impact of these parasites include a wide range of health issues in infected birds, including anemia, decreased body condition, and reduced reproductive success. Additionally, the distribution of parasitic populations within individual hosts can lead to complex interactions between the host and its parasites, which can influence the overall population structure and dynamics of both the host and the parasite. The prevalence and genetic diversity of haemosporidian parasites can also vary depending on various factors, such as the migratory patterns of birds, availability of suitable vectors, and environmental conditions in different regions. In conclusion, haemosporidian parasites play a crucial role in the dynamics of bird populations, influencing their health, fitness, and population structure. Understanding the complex interactions between these parasites and their avian hosts is essential for developing effective strategies for the conservation and management of bird populations.

References

Ajaj, E. A., Mohammad, H. A., & Gharban, H. A. (2021). First molecular confirmation of Coenurus cerebralis in sheep and goats with neurological behaviors in Iraq. Veterinary World, 14(6), 1420–1425. https://doi.org/10.14202/vetworld.2021.1420-1425

Al-Abedi, G. J., Sray, A. H., Hussein, A. J., & Gharban, H. A. (2020). Detection and bloody profiles evaluation of naturally infected camels with subclinical Trypanosoma evansi, Iraq. Annals of Tropical Medicine and Public Health, 23, 232–243. https://doi.org/10.36295/ASRO.2020.232243

Alkefari, O. A., Al-Gharban, H. A., & Ahmed, T. H. (2017). Microscopic, serological and molecular detection of Babesia bigemina in buffaloes (Bubalus bubalis) in Wasit province, Iraq. Al-Qadisiyah Journal of Veterinary Medicine Sciences, 16(1), 123–130. https://doi.org/10.29079/vol16iss1art48

Al-Shaeli, S. J., Ethaeb, A. M., & Gharban, H. A. (2020). Molecular and histopathological identification of ovine neosporosis (Neospora caninum) in aborted ewes in Iraq. Veterinary World, 13(3), 597–603. https://doi.org/10.14202/vetworld.2020.597-603

Álvarez-Mendizábal, P., Villalobos, F., Rodríguez-Hernández, K., Hernández-Lara, C., Rico-Chávez, O., Suzán, G., & Santiago-Alarcon, D. (2021). Metacommunity structure reveals that temperature affects the landscape compositional patterns of avian malaria and related haemosporidian parasites across elevations. Acta Oecologica, 113, 103789. https://doi.org/10.1016/j.actao.2021.103789

Antonelli, L. R., Junqueira, C., Vinetz, J. M., Golenbock, D. T., Ferreira, M. U., & Gazzinelli, R. T. (2020). The immunology of Plasmodium vivax malaria. Immunological Reviews, 293(1), 163–189. https://doi.org/10.1111/imr.12816

Atkinson, C. T. (2023). Avian malaria and the extinction of Hawaiian forest birds. In D. A. Jessup & R. W. Radcliffe (Eds.), Wildlife Disease and Health in Conservation (pp. 326–347). Johns Hopkins University Press. https://doi.org/10.56021/9781421446745

Atkinson, C. T., & Van Riper, C. (1991). Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In J. E. Loye & M. Zuk (Eds.), Bird–Parasite Interactions (pp. 19–48). Oxford University Press. https://doi.org/10.1093/oso/9780198577445.003.0002

Bensch, S., & Hellgren, O. (2020). The use of molecular methods in studies of avian haemosporidians. In D. Santiago-Alarcon & A. Marzal (Eds.), Avian Malaria and Related Parasites in the Tropics: Ecology, Evolution and Systematics (pp. 113–135). Springer. https://doi.org/10.1007/978-3-030-51633-8_4

Bonneaud, C., Sepil, I., Milá, B., Buermann, W., Pollinger, J., Sehgal, R. N., & Smith, T. B. (2009). The prevalence of avian Plasmodium is higher in undisturbed tropical forests of Cameroon. Journal of Tropical Ecology, 25(4), 439–447. https://doi.org/10.1017/S0266467409006178

Boonchuay, K., Thomrongsuwannakij, T., Chagas, C. R. F., & Pornpanom, P. (2023). Prevalence and diversity of blood parasites (Plasmodium, Leucocytozoon, and Trypanosoma) in backyard chickens (Gallus gallus domesticus) raised in Southern Thailand. Animals, 13(17), 2798. https://doi.org/10.3390/ani13172798

Brown, M. (2000). Gene regulation and the structure and function of cytoskeletal molecules and polymers, in relation to signal transduction mechanisms, in the apicomplexan parasite, Eimeria tenella. The University of Manchester.

Burkot, T. R., & Graves, P. M. (2000). Malaria, babesiosis, theileriosis, and related diseases. In Medical Entomology: A Textbook on Public Health and Veterinary Problems Caused by Arthropods (pp. 187-230). Springer Netherlands. https://doi.org/10.1007/978-94-015-9423-2_9

Chapa-Vargas, L., Matta, N. E., & Merino, S. (2020). Effects of ecological gradients on tropical avian hemoparasites. In Avian malaria and related parasites in the tropics: Ecology, evolution, and systematics (pp. 349-377). http://dx.doi.org/10.1007/978-3-030-51633-8_10

Chapman, H. D., & Rathinam, T. (2022). Focused review: The role of drug combinations for the control of coccidiosis in commercially reared chickens. International Journal for Parasitology: Drugs and Drug Resistance, 18, 32-42. https://doi.org/10.1016/j.ijpddr.2022.02.001

Clark, N. J., Clegg, S. M., & Lima, M. R. (2014). A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): New insights from molecular data. International Journal for Parasitology, 44(5), 329-338. https://doi.org/10.1016/j.ijpara.2014.01.002

Cornet, S., Bichet, C., Larcombe, S., Faivre, B., & Sorci, G. (2014). Impact of host nutritional status on infection dynamics and parasite virulence in a bird-malaria system. Journal of Animal Ecology, 83(1), 256-265. https://doi.org/10.1111/1365-2656.12116

Cornet, S., Nicot, A., Rivero, A., & Gandon, S. (2019). Avian malaria alters the dynamics of blood feeding in Culex pipiens mosquitoes. Malaria Journal, 18, 1-6. https://doi.org/10.1186/s12936-019-2667-z

Cortez-Maya, S., Moreno-Herrera, A., Palos, I., & Rivera, G. (2020). Old antiprotozoal drugs: Are they still viable options for parasitic infections or new options for other diseases?. Current Medicinal Chemistry, 27(32), 5403-5428. https://doi.org/10.2174/0929867327666200309101549

de Wit, J. S., & Montiel, E. (2022). Practical aspects of poultry vaccination. In K. A. Schat, B. Kaspers, & P. Kaiser (Eds.), Avian Immunology (pp. 469–488). Academic Press. https://doi.org/10.1016/B978-0-12-818708-1.00012-9

Delhaye, J., Glaizot, O., & Christe, P. (2018). The effect of dietary antioxidant supplementation in a vertebrate host on the infection dynamics and transmission of avian malaria to the vector. Parasitology Research, 117, 2043–2052. https://doi.org/10.1007/s00436-018-5869-8

Delves, M., Plouffe, D., Scheurer, C., Meister, S., Wittlin, S., Winzeler, E. A., & Leroy, D. (2012). The activities of current antimalarial drugs on the life cycle stages of Plasmodium: A comparative study with human and rodent parasites. PLoS Medicine, 9(2), e1001169. https://doi.org/10.1371/journal.pmed.1001169

Desser, S. S. (2012). The Haemogregarinidae. In J. P. Kreier (Ed.), Parasitic Protozoa (2nd ed., Vol. 2, pp. 247–272). Academic Press. https://doi.org/10.1016/B978-0-12-397722-9.00010-0

Dimitrov, D., Zehtindjiev, P., Bensch, S., Ilieva, M., Iezhova, T., & Valkiūnas, G. (2014). Two new species of Haemoproteus Kruse, 1890 (Haemosporida, Haemoproteidae) from European birds, with emphasis on DNA barcoding for detection of haemosporidians in wildlife. Systematic Parasitology, 87, 135–151. https://doi.org/10.1007/s11230-014-9503-9

Dimitrov, D., Palinauskas, V., Iezhova, T. A., Bernotienė, R., Ilgūnas, M., Bukauskaitė, D., & Valkiūnas, G. (2015). Plasmodium spp.: An experimental study on vertebrate host susceptibility to avian malaria. Experimental Parasitology, 148, 1–16. https://doi.org/10.1016/j.exppara.2014.10.002

Donovan, T. A., Schrenzel, M., Tucker, T. A., Pessier, A. P., & Stalis, I. H. (2008). Hepatic hemorrhage, hemocoelom, and sudden death due to Haemoproteus infection in passerine birds: Eleven cases. Journal of Veterinary Diagnostic Investigation, 20(3), 304–313. https://doi.org/10.1177/104063870802000307

Duc, M. Y. L. (2023). Exo-erythrocytic stages of Haemoproteus (Apicomplexa, Haemosporida) parasites in wild birds: Insights into developmental patterns (Doctoral dissertation, Vilniaus universitetas). https://doi.org/10.15388/Dissertation.2023.12

Duc, M., Himmel, T., Ilgūnas, M., Eigirdas, V., Weissenböck, H., & Valkiūnas, G. (2023). Chromogenic in situ hybridization in avian haemosporidian research: How it further strengthens the research on tissue stages. In The COINS 2023: International Conference of Life Sciences: Book of Abstracts. https://doi.org/10.15388/Proceedings.2023.12

El-Ghany, W. A. A. (2023). Avian haemosporidian parasites: An updated review. Archives of Veterinary Science, 28(2), 1–16. https://doi.org/10.5380/avs.v28i2.100000

Ellis, V. A., Fecchio, A., & Ricklefs, R. E. (2020). Haemosporidian parasites of Neotropical birds: Causes and consequences of infection. The Auk, 137(4), ukaa055. https://doi.org/10.1093/auk/ukaa055

Emmenegger, T. (2018). Avian malaria on the move: The potential causes and cascading consequences of blood parasite infections in migratory birds (Doctoral dissertation, ETH Zurich). https://doi.org/10.3929/ethz-b-000309394

Escalante, A. A., Cepeda, A. S., & Pacheco, M. A. (2022). Why Plasmodium vivax and Plasmodium falciparum are so different? A tale of two clades and their species diversities. Malaria Journal, 21(1), 139. https://doi.org/10.1186/s12936-022-04130-9

Esteban Henao, M. C. (2019). Are blood parasite infections associated with the immune and energetic condition of a migratory passerine bird? (Bachelor's thesis, Universidad de los Andes, Colombia).

Ewbank, A. C. (2016). Morphometric evaluation of hepatic hemosiderosis and necrosis in Magellanic penguins (Spheniscus magellanicus) naturally infected by Plasmodium spp. (Doctoral dissertation, Universidade de São Paulo).

Ferraguti, M., Hernández-Lara, C., Sehgal, R. N., & Santiago-Alarcon, D. (2020). Anthropogenic effects on avian haemosporidians and their vectors. In D. Santiago-Alarcon & A. Marzal (Eds.), Avian malaria and related parasites in the tropics: Ecology, evolution and systematics (pp. 451–485). Springer. http://dx.doi.org/10.1007/978-3-030-51633-8_14

Ferreira Junior, F. C., Rodrigues, R. A., Ellis, V. A., Leite, L. O., Borges, M. A., & Braga, E. M. (2017). Habitat modification and seasonality influence avian haemosporidian parasite distributions in southeastern Brazil. PLoS ONE, 12(6), e0178791. https://doi.org/10.1371/journal.pone.0178791

Florin-Christensen, M., Schnittger, L., Bastos, R. G., Rathinasamy, V. A., Cooke, B. M., Alzan, H. F., & Suarez, C. E. (2021). Pursuing effective vaccines against cattle diseases caused by apicomplexan protozoa. CABI Reviews. https://doi.org/10.1079/PAVSNNR202116004

Galen, S. C., Natarajan, C., Moriyama, H., Weber, R. E., Fago, A., Benham, P. M., & Witt, C. C. (2015). Contribution of a mutational hot spot to hemoglobin adaptation in high-altitude Andean house wrens. Proceedings of the National Academy of Sciences, 112(45), 13958–13963. https://doi.org/10.1073/pnas.1507300112

Ganser, C., Monadjem, A., McCleery, R. A., Ndlela, T., & Wisely, S. M. (2020). Is it best on the nest? Effects of avian life-history on haemosporidian parasitism. International Journal for Parasitology: Parasites and Wildlife, 13, 62–71. https://doi.org/10.1016/j.ijppaw.2020.07.007

García-Longoria, L., Magallanes, S., González-Blázquez, M., Refollo, Y., de Lope, F., & Marzal, A. (2016). New approaches for an old disease: Studies on avian malaria parasites for the twenty-first century challenges. In M. M. Rodriguez (Ed.), Current topics in malaria. IntechOpen. https://doi.org/10.5772/64154

Gharban, H. A., Al-Ghuraibawi, H. N., Al-Rubaye, Z. A., Jahlol, H. A., Al-Zergany, A. A., & Al-Abedi, G. J. (2023). Most clinically detected viral diseases in field animals of Wasit Province, Iraq. Annals of the Romanian Society for Cell Biology, 27(1), 154–168.

Gharban, H. A., & Al-Kaabi, M. A. (2022). Molecular and seroprevalence of toxoplasmosis in goats' blood and milk in Iraq. Archives of Razi Institute, 77(5), 1749–1755. https://doi.org/10.22092/ari.2022.357809.2106

Gozalo, A. S., Robinson, C. K., Holdridge, J., Mahecha, O. F. L., & Elkins, W. R. (2024). Overview of Plasmodium spp. and animal models in malaria research. Comparative Medicine, 74(4), 205–230. https://doi.org/10.30802/AALAS-CM-23-000015

Gupta, S. (2024). Darwin review: The evolution of virulence in human pathogens. Proceedings of the Royal Society B: Biological Sciences, 291(2016), 20232043. https://doi.org/10.1098/rspb.2023.2043

Hahn, S., Bauer, S., Dimitrov, D., Emmenegger, T., Ivanova, K., Zehtindjiev, P., & Buttemer, W. A. (2018). Low-intensity blood parasite infections do not reduce the aerobic performance of migratory birds. Proceedings of the Royal Society B: Biological Sciences, 285(1871), 20172307. https://doi.org/10.1098/rspb.2017.2307

Harl, J., Himmel, T., Valkiūnas, G., Ilgūnas, M., Bakonyi, T., & Weissenböck, H. (2020). Geographic and host distribution of haemosporidian parasite lineages from birds of the family Turdidae. Malaria Journal, 19, 1–35. https://doi.org/10.1186/s12936-020-03488-9

Himmel, T., Harl, J., Matt, J., Nedorost, N., Lunardi, M., Ilgūnas, M., & Weissenböck, H. (2024). Co-infecting Haemoproteus species (Haemosporida, Apicomplexa) show different host tissue tropism during exo-erythrocytic development in Fringilla coelebs (Fringillidae). International Journal for Parasitology, 54(1), 1–22. https://doi.org/10.1016/j.ijpara.2023.10.001

Huang, X. (2021). Assessment of associations between malaria parasites and avian hosts—a combination of classic system and modern molecular approach. Biology, 10(7), 636. https://doi.org/10.3390/biology10070636

Ilgūnas, M., Bukauskaitė, D., Palinauskas, V., Iezhova, T. A., Dinhopl, N., Nedorost, N., & Valkiūnas, G. (2016). Mortality and pathology in birds due to Plasmodium (Giovannolaia) homocircumflexum infection, with emphasis on the exoerythrocytic development of avian malaria parasites. Malaria Journal, 15, 256. https://doi.org/10.1186/s12936-016-1310-x

Ings, K., & Denk, D. (2022). Avian malaria in penguins: Diagnostics and future direction in the context of climate change. Animals, 12(5), 600. https://doi.org/10.3390/ani12050600

Ishtiaq, F., Rao, M., Huang, X., & Bensch, S. (2017). Estimating prevalence of avian haemosporidians in natural populations: A comparative study on screening protocols. Parasites & Vectors, 10, 127. https://doi.org/10.1186/s13071-017-2010-1

Ivanova, K., Zehtindjiev, P., Mariaux, J., Dimitrov, D., & Georgiev, B. B. (2018). Avian haemosporidians from rain forests in Madagascar: Molecular and morphological data of the genera Plasmodium, Haemoproteus, and Leucocytozoon. Infection, Genetics and Evolution, 58, 115–124. https://doi.org/10.1016/j.meegid.2018.01.015

Jhun, H. (2018). Probing lipoylation in Plasmodium (Doctoral dissertation, Johns Hopkins University).

Knowles, S. C. L., Palinauskas, V., & Sheldon, B. C. (2010). Chronic malaria infections increase family inequalities and reduce parental fitness: Experimental evidence from a wild bird population. Journal of Evolutionary Biology, 23(3), 557–569. https://doi.org/10.1111/j.1420-9101.2009.01920.x

Krama, T., Krams, R., Cīrule, D., Moore, F. R., Rantala, M. J., & Krams, I. A. (2015). Intensity of haemosporidian infection of parids positively correlates with proximity to water bodies, but negatively with host survival. Journal of Ornithology, 156, 1075–1084. https://doi.org/10.1007/s10336-015-1235-4

Lumsden, W. H. R., & Bertram, D. S. (1940). Observations on the biology of Plasmodium gallinaceum Brumpt, 1935, in the domestic fowl, with special reference to the production of gametocytes and their development in Aedes aegypti (L.). Annals of Tropical Medicine & Parasitology, 34(2), 135–160. https://doi.org/10.1080/00034983.1940.11685062

Lutz, H. L., Patterson, B. D., Peterhans, J. C. K., Stanley, W. T., Webala, P. W., Gnoske, T. P., & Stanhope, M. J. (2016). Diverse sampling of East African haemosporidians reveals chiropteran origin of malaria parasites in primates and rodents. Molecular Phylogenetics and Evolution, 99, 7–15. https://doi.org/10.1016/j.ympev.2016.02.015

Martinez, C., Marzec, T., Smith, C. D., Tell, L. A., & Sehgal, R. N. (2013). Identification and expression of maebl, an erythrocyte-binding gene, in Plasmodium gallinaceum. Parasitology Research, 112, 945–954. https://doi.org/10.1007/s00436-012-3211-0

Marzal, A., de Lope, F., Navarro, C., & Møller, A. P. (2005). Malarial parasites decrease reproductive success: An experimental study in a passerine bird. Oecologia, 142, 541–545. https://doi.org/10.1007/s00442-004-1757-2

Marzal, A. (2012). Recent advances in studies on avian malaria parasites. Malaria Parasites, 30, 135-158. https://doi.org/10.1007/s00436-012-2926-3

Mora-Rubio, C., Ferraguti, M., Magallanes, S., Bravo-Barriga, D., Hernandez-Caballero, I., Marzal, A., & de Lope, F. (2023). Unravelling the mosquito-haemosporidian parasite-bird host network in the southwestern Iberian Peninsula: Insights into malaria infections, mosquito community and feeding preferences. Parasites and Vectors, 16(1), 395. https://doi.org/10.1186/s13071-023-05548-3

Mordecai, E. A., Paaijmans, K. P., Johnson, L. R., Balzer, C., Ben‐Horin, T., de Moor, E., & Lafferty, K. D. (2013). Optimal temperature for malaria transmission is dramatically lower than previously predicted. Ecology Letters, 16(1), 22-30. https://doi.org/10.1111/ele.12015

Musa, S. (2023). Mitochondrial genome amplification of avian haemosporidian parasites from single-infected wildlife samples using a novel nested PCR approach. Parasitology Research, 122(12), 2967-2975. https://doi.org/10.1007/s00436-023-07476-x

Norrie, P. (2016). A history of disease in ancient times: More lethal than war. Springer.

Nourani, L., Aliabadian, M., Mirshamsi, O., & Dinparast Djadid, N. (2018). Molecular detection and genetic diversity of avian haemosporidian parasites in Iran. PLOS ONE, 13(11), e0206638. https://doi.org/10.1371/journal.pone.0206638

O'Donoghue, P. (2017). Haemoprotozoa: making biological sense of molecular phylogenies. International Journal for Parasitology: Parasites and Wildlife, 6(3), 241-256. https://doi.org/10.1016/j.ijppaw.2017.08.007

Ouologuem, D. T. (2014). Dynamics and fate of the inner membrane complex in apicomplexan parasites. University of Pennsylvania.

Padilla, D. P., Illera, J. C., Gonzalez-Quevedo, C., Villalba, M., & Richardson, D. S. (2017). Factors affecting the distribution of haemosporidian parasites within an oceanic island. International Journal for Parasitology, 47(4), 225-235. https://doi.org/10.1016/j.ijpara.2016.11.008

Palatnik-de-Sousa, C. B., & Nico, D. (2020). The delay in the licensing of protozoal vaccines: a comparative history. Frontiers in Immunology, 11, 204. https://doi.org/10.3389/fimmu.2020.00204

Perkins, S. L. (2014). Malaria's many mates: past, present, and future of the systematics of the order Haemosporida. Journal of Parasitology, 100(1), 11-25. https://doi.org/10.1645/13-362.1

Pigeault, R., Cozzarolo, C. S., Choquet, R., Strehler, M., Jenkins, T., Delhaye, J., & 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

Pigeault, R., Cozzarolo, C. S., Glaizot, O., & Christe, P. (2020). Effect of age, haemosporidian infection and body condition on pair composition and reproductive success in Great Tits Parus major. Ibis, 162(3), 613-626. https://doi.org/10.1111/ibi.12774

Poblete, Y., Contreras, C., Ávila, M., Carmona, M. P., Fernández, C., Flores, C. R., & Sabat, P. (2024). Haemosporidian Infection Is Associated with the Oxidative Status in a Neotropical Bird. Birds, 5(3), 604-615. https://doi.org/10.3390/birds5030040

Power, B. J. (2019). Epigenomics and gametocytogenesis in the rodent malaria model, Plasmodium berghei (Doctoral dissertation, University of Glasgow).

Pugliese, N., Samarelli, R., Lombardi, R., Schiavone, A., Crescenzo, G., Circella, E., & Camarda, A. (2023). A Safe and Effective Atovaquone-Proguanil Therapeutic Protocol for the Treatment of Avian Malaria by Plasmodium relictum in Snowy Owl (Bubo scandiacus). Animals, 13(22), 3457. https://doi.org/10.3390/ani13223457

Rasidi, E. K., & Cornejo, J. (2021). Managing the health of captive flocks of birds. Vet. Clin. Exot. Anim. Pract, 24, 521-530. http://dx.doi.org/10.1016/j.cvex.2021.05.004

Richie, T. L., Billingsley, P. F., Sim, B. K. L., James, E. R., Chakravarty, S., Epstein, J. E., & Hoffman, S. L. (2015). Progress with Plasmodium falciparum sporozoite (PfSPZ)-based malaria vaccines. Vaccine, 33(52), 7452-7461. https://doi.org/10.1016/j.vaccine.2015.09.096

Rodrigues, R. A., Massara, R. L., Bailey, L. L., Pichorim, M., Moreira, P. A., & Braga, É. M. (2020). Using a multistate occupancy approach to determine molecular diagnostic accuracy and factors affecting avian haemosporidian infections. Scientific Reports, 10(1), 8480. https://www.nature.com/articles/s41598-020-65523-x

Rooyen, J. V., Lalubin, F., Glaizot, O., & Christe, P. (2013). Avian haemosporidian persistence and co-infection in great tits at the individual level. Malaria Journal, 12, 1-8. https://doi.org/10.1186/1475-2875-12-40

Santiago‐Alarcon, D., Palinauskas, V., & Schaefer, H. M. (2012). Diptera vectors of avian Haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biological Reviews, 87(4), 928-964. https://doi.org/10.1111/j.1469-185X.2012.00234.x

Santiago-Alarcon, D., MacGregor-Fors, I., Falfán, I., Lüdtke, B., Segelbacher, G., Schaefer, H. M., & Renner, S. (2019). Parasites in space and time: a case study of haemosporidian spatiotemporal prevalence in urban birds. International Journal for Parasitology, 49(3-4), 235-246. https://doi.org/10.1016/j.ijpara.2018.08.009

Santiago-Alarcon, D., & Marzal, A. (2020). Research on avian haemosporidian parasites in the tropics before the year 2000. Avian malaria and related parasites in the tropics: ecology, evolution and systematics, 1-44. http://dx.doi.org/10.1007/978-3-030-51633-8_1

Schumm, Y. R., Wecker, C., Marek, C., Wassmuth, M., Bentele, A., Willems, H., & Quillfeldt, P. (2019). Blood parasites in Passeriformes in central Germany: prevalence and lineage diversity of Haemosporida (Haemoproteus, Plasmodium and Leucocytozoon) in six common songbirds. PeerJ, 6, e6259. https://doi.org/10.7717/peerj.6259

Sehgal, R. N. (2015). Manifold habitat effects on the prevalence and diversity of avian blood parasites. International Journal for Parasitology: Parasites and Wildlife, 4(3), 421-430. https://doi.org/10.1016/j.ijppaw.2015.09.001

Simwela, N. V., & Waters, A. P. (2022). Current status of experimental models for the study of malaria. Parasitology, 149(6), 729-750. https://doi.org/10.1017/s0031182021002134

Sray, A., AL-SHabbani, A., & GHarban, H. (2019). Serological and molecular estimation of Theileria equi Infections in horses of Baghdad, Al-Qadisiyah, and Wasit Provinces. Iraq. J Res Lepid [Internet], 50(4), 391-404.

Tembe, D., Malatji, M. P., & Mukaratirwa, S. (2023). Occurrence, Prevalence, and Distribution of Haemoparasites of Poultry in Sub-Saharan Africa: A Scoping Review. Pathogens, 12(7), 945. https://doi.org/10.3390/pathogens12070945

Valkiūnas, G., Sehgal, R. N., Iezhova, T. A., & Hull, A. C. (2010). Identification of Leucocytozoon toddi group (Haemosporida: Leucocytozoidae), with remarks on the species taxonomy of leucocytozoids. Journal of Parasitology, 96(1), 170-177. https://doi.org/10.1645/ge-2109.1

Valkiūnas, G., Palinauskas, V., Ilgūnas, M., Bukauskaitė, D., Dimitrov, D., Bernotienė, R., & Iezhova, T. A. (2014). Molecular characterization of five widespread avian haemosporidian parasites (Haemosporida), with perspectives on the PCR-based detection of haemosporidians in wildlife. Parasitology research, 113, 2251-2263. https://doi.org/10.1007/s00436-014-3880-2

Valkiūnas, G., & 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. (2018). Keys to the avian malaria parasites. Malaria Journal, 17, 1-24. https://doi.org/10.1186/s12936-018-2359-5

Van Hemert, C., Meixell, B. W., Smith, M. M., & Handel, C. M. (2019). Prevalence and diversity of avian blood parasites in a resident northern passerine. Parasites and vectors, 12, 1-16. https://doi.org/10.1186/s13071-019-3545-1

van Hoesel, W., Santiago-Alarcon, D., Marzal, A., & Renner, S. C. (2020). Effects of forest structure on the interaction between avian hosts, dipteran vectors and haemosporidian parasites. BMC ecology, 20(1), 47. https://doi.org/10.1186/s12898-020-00315-5

Veiga, J., Garrido, M., Garrigós, M., Chagas, C. R., & Martínez-de la Puente, J. (2024). A Literature review on the role of the invasive Aedes albopictus in the transmission of avian malaria parasites. Animals, 14(14), 2019. https://doi.org/10.3390/ani14142019

Viljoen, G. J., Unger, H., Wijewardana, V., & Naletoski, I. (2021). Novel Developments and Next‐Generation Vaccines. Veterinary vaccines: principles and applications, 119-134. http://dx.doi.org/10.1002/9781119506287.ch10

Vinetz, J. M., Clain, J., Bounkeua, V., Eastman, R. T., & Fidock, D. (2011). Chemotherapy of malaria. The pharmacological basis of therapeutics, 12, 1383-418.

Yoshimoto, M., Ozawa, K., Kondo, H., Echigoya, Y., Shibuya, H., Sato, Y., & Sehgal, R. N. (2021). A fatal case of a captive snowy owl (Bubo scandiacus) with Haemoproteus infection in Japan. Parasitology Research, 120, 277-288. https://doi.org/10.1007/s00436-020-06972-1

Zhang, X., Meadows, S. N., Martin, T., Doran, A., Angles, R., Sander, S., & Witola, W. H. (2022). Plasmodium relictum MSP-1 capture antigen-based ELISA for detection of avian malaria antibodies in African penguins (Spheniscus demersus). International Journal for Parasitology: Parasites and Wildlife, 19, 89-95. https://doi.org/10.1016/j.ijppaw.2022.08.009