Prevalence and Genetic Diversity of Avian Blood Parasites (Apicomplexa: Haemosporidia) in Songbirds from the West of Iran

Document Type : Research articles

Authors

• Mohammad Aljehni ¹
• Omid Mirshamsi ²
• Mansour Aliabadian ²

¹ Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad 9177948974, Iran

² - Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad 9177948974, Iran. - Research Department of Zoological Innovations (RDZI), Institute of Applied Zoology, Faculty of Science, Ferdowsi University of

10.22067/ijab.2024.85290.1065

Abstract

Haemosporidian parasites, which encompass Haemoproteus, Plasmodium, and Leucocytozoon, are intracellular parasites commonly found in the blood and other tissues of birds worldwide. The prevalence of these parasites can vary depending on the bird species and the habitats they inhabit. Notably, the highest diversity of Haemosporidian parasites has been observed within the Passeriformes order of birds. In our study, we collected 145 blood samples from wild songbirds in the western region of Iran during the period from April to November 2021-2022. Blood smears were prepared using the push-slide method and subsequently stained with Giemsa. The stained smears were then examined under a light microscope, and all samples were screened using a nested PCR protocol that targeted a 479-base-pair segment of the mitochondrial cytochrome b (cytb) gene of Haemoproteus, Plasmodium, and Leucocytozoon species. Among the seven songbird families we sampled, we detected blood parasites in 31 individuals, representing an infection rate of 21.4% (95% CI: 0.1501 to 0.2896). These infected individuals belonged to five different families, and a total of 21 lineages were identified, including thirteen for Leucocytozoon spp, seven for Haemoproteus spp, and one for Plasmodium spp. Notably, the highest infection rates were observed in the Paridae family (9.7%, 95% CI: 0.0537 to 0.1567) and the Motacillidae family (4.8%, 95% CI: 0.0196 to 0.0970), while the lowest infection rates were recorded in the Corvidae family (1.4%, 95% CI: 0.0016 to 0.0490) and the Acrocephalidae family (1.4%, 95% CI: 0.0016 to 0.0490). Additionally, our study documented two new host species for Leucocytozoon spp. (Motacilla flava and Acrocephalus melanopogon), marking the first such observations globally. We also established five new host records (Motacilla flava, Pica pica, Acrocephalus melanopogon, Poecile lugubris, and Acrocephalus agricola) for avian haemosporidian parasites in the western region of Iran. These findings underscore the remarkable lineage diversity within the Leucocytozoon genus compared to other haemosporidian parasites in songbirds in western Iran, setting our study apart from previous research in Iran.

Keywords

• Haemoproteus
• haemosporidian parasites
• Plasmodium
• Leucocytozoon spp
• wild birds

Main Subjects

• Morphology
• Taxonomy

---

References

Bahrami, A. M., A. L. Monfared, and M. Razmjoo (2012), Pathological study of parasitism in racing
pigeons: An indication of its effects on community health, African Journal of Biotechnology, 11(59),
12364-12370.
Bennett, G., M. Peirce, and R. Ashford (1993), Avian haematozoa: mortality and pathogenicity, Journal
of Natural History, 27(5), 993-1001.
Bensch, S., M. Stjernman, D. Hasselquist, Ö. Örjan, B. Hannson, H. Westerdahl, and R. T. Pinheiro
(2000), Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus
mitochondrial DNA amplified from birds, Proceedings of the Royal Society of London. Series B:
Biological Sciences, 267(1452), 1583-1589.
Bruford, M. W., O. Hanotte, J. Brookfield, and T. Burke (1992), Single-locus and multilocus DNA
fingerprinting, Molecular genetic analysis of populations: a practical approach., 225-269.
Dezfoulian, O., M. Zibaei, H. Nayebzadeh, M. Haghgoo, A. Emami-Razavi, and K. Kiani (2013),
Leucocytozoonosis in domestic birds in southwestern iran: an ultrastructural study, Iranian journal of
parasitology, 8(1), 171.
Dimitrov, D., P. Zehtindjiev, and S. Bensch (2010), Genetic diversity of avian blood parasites in SE
Europe: Cytochrome b lineages of the genera Plasmodium and Haemoproteus (Haemosporida) from
Bulgaria, Acta Parasitologica, 55, 201-209.
Ghaemitalab, V., O. Mirshamsi, G. Valkiūnas, and M. Aliabadian (2021), Prevalence and genetic
diversity of avian haemosporidian parasites in southern Iran, Pathogens, 10(6), 645.
Gorji, S. F., B. Shemshadi, H. Habibi, S. Jalali, M. Davary, and M. Sepehri (2012), Survey on parasites in
sparrows of Amol (Mazandaran Province, Iran), Journal of Life Sciences, 6(7), 783.
Hellgren, O., J. Waldenström, and S. Bensch (2004), a new PCR assay for simultaneous studies of
Leucocytozoon, Plasmodium, and Haemoproteus from avain blood, Journal of Parasitology, 90(4), 797-
802.
PREVALENCE AND GENETIC DIVERSITY OF AVIAN BLOOD PARASITES 9
Himmel, T., J. Harl, J. Matt, and H. Weissenböck (2021), A citizen science-based survey of avian
mortality focusing on haemosporidian infections in wild passerine birds, Malaria Journal, 20, 1-13.
Jenkins, T., and I. P. Owens (2011), Biogeography of avian blood parasites (Leucocytozoon spp.) in two
resident hosts across Europe: phylogeographic structuring or the abundance–occupancy relationship?,
Molecular Ecology, 20(18), 3910-3920.
Marzal, A., F. d. Lope, C. Navarro, and A. P. Møller (2005), Malarial parasites decrease reproductive
success: an experimental study in a passerine bird, Oecologia, 142, 541-545.
Medeiros, M. C., G. L. Hamer, and R. E. Ricklefs (2013), Host compatibility rather than vector–host-
encounter rate determines the host range of avian Plasmodium parasites, Proceedings of the Royal Society
B: Biological Sciences, 280(1760), 20122947.
Nazifi, S., S. Razavi, F. Yavari, M. Rajaifar, E. Bazyar, and Z. Esmailnejad (2008), Evaluation of
hematological values in indigenous chickens infected with Plasmodium gallinaceum and Aegyptianella
pullorum, Comparative Clinical Pathology, 17, 145-148.
Nematollahi, A., M. Ebrahimi, A. Ahmadi, and M. Himan (2012), Prevalence of Haemoproteus columbae
and Trichomonas gallinae in pigeons (Columba domestica) in Isfahan, Iran, Journal of Parasitic Diseases,
36, 141-142.
Nourani, L., M. Aliabadian, N. Dinparast-Djadid, and O. Mirshamsi (2017a), New host records for
Haemoproteus spp.(Apicomplexa: Haemosporidiasina) in passeriformes from north-west of Iran, Journal
of arthropod-borne diseases, 11(2), 236.
Nourani, L., M. Aliabadian, O. Mirshamsi, and N. D. Djadid (2017b), Detection of the avian blood
parasites from northeast of Iran, paper presented at 1st International Congress on Vector-Borne Diseases
and Climate Change.
Nourani, L., M. Aliabadian, N. D. Djadid, and O. Mirshamsi (2018a), Occurrence of Haemoproteus
spp.(Haemosporida: Haemoproteidae) in new host records of passerine birds from the east of Iran, Iranian
Journal of Parasitology, 13(2), 267.
Nourani, L., M. Aliabadian, O. Mirshamsi, and N. Dinparast Djadid (2018b), Molecular detection and
genetic diversity of avian haemosporidian parasites in Iran, PloS One, 13(11), e0206638.
Nourani, L., M. Aliabadian, H. Amini, and O. Mirshamsi (2020), Prevalence of haemosporidian parasite
infections in raptors of Iran, Journal of Raptor Research, 54(4), 455-462.
Peirce, M. (1981), Distribution and host-parasite check-list of the haematozoa of birds in Western Europe,
Journal of Natural History, 15(3), 419-458.
Reiczigel, J., M. Marozzi, I. Fábián, and L. Rózsa (2019), Biostatistics for parasitologists–a primer to
quantitative parasitology, Trends in parasitology, 35(4), 277-281.
Rooyen, J. v., F. Lalubin, O. Glaizot, and P. Christe (2013), Avian haemosporidian persistence and co-
infection in great tits at the individual level, Malaria Journal, 12(1), 1-8.
10 IRANIAN JOURNAL OF ANIMAL BIOSYSTEMATICS Vol.20, No.1
Scheuerlein, A., and R. E. Ricklefs (2004), Prevalence of blood parasites in European passeriform birds,
Proceedings of the Royal Society of London. Series B: Biological Sciences, 271(1546), 1363-1370.
Seutin, G., B. N. White, and P. T. Boag (1991), Preservation of avian blood and tissue samples for DNA
analyses, Canadian journal of zoology, 69(1), 82-90.
Statistics, I. (2013), IBM Corp. Released 2013. IBM SPSS Statistics for Windows, Version 22.0.
Armonk, NY: IBM Corp, Google Search.
Valkiunas, G. (2004), Avian malaria parasites and other haemosporidia, CRC press.
Valkiūnas, G., A. M. Anwar, C. T. Atkinson, E. C. Greiner, I. Paperna, and M. A. Peirce (2005), What
distinguishes malaria parasites from other pigmented haemosporidians?, Trends in parasitology, 21(8),
357-358.
Valkiūnas, G., V. Palinauskas, M. Ilgūnas, D. Bukauskaitė, D. Dimitrov, R. Bernotienė, P. Zehtindjiev,
M. Ilieva, and T. A. Iezhova (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.
Van Riper III, C., S. G. Van Riper, M. L. Goff, and M. Laird (1986), The epizootiology and ecological
significance of malaria in Hawaiian land birds, Ecological monographs, 56(4), 327-344.
Wood, M. J., C. L. Cosgrove, T. A. Wilkin, S. C. Knowles, K. P. Day, and B. C. Sheldon (2007),
Within‐population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes
caeruleus, Molecular Ecology, 16(15), 3263-3273