Survey on Avian Malaria Parasites in Village Chickens (Gallus gallus domesticus) in Gombe Local Government Area, Gombe State, Nigeria

Authors

  • Jallailudeen Rabana Lawal Department of Veterinary Medicine, Faculty of Veterinary Medicine, University of Maiduguri, P.M.B. 1069, Maiduguri, Borno State, Nigeria
  • Umar Isa IBRAHIM Department of Veterinary Medicine, Faculty of Veterinary Medicine, University of Maiduguri, P.M.B. 1069, Maiduguri, Borno State, Nigeria
  • Abdullahi Abubakar BIU Department of Veterinary Parasitology and Entomology, Faculty of Veterinary Medicine, University of Maiduguri, P.M.B. 1069, Maiduguri, Borno State, Nigeria
  • Hassan Ismail MUSA Department of Veterinary Public Health and Preventive Medicine, Faculty of Veterinary Medicine, University of Maiduguri, P.M.B. 1069, Maiduguri, Borno State, Nigeria

DOI:

https://doi.org/10.30564/vsr.v3i2.4127

Abstract

Reports of avian malaria parasites in village chicken in Nigeria generally remain fragmentary and scarce. The study was conducted in Gombe Local Government Area of Gombe State, Nigeria to investigate avian malaria parasites in Village Chickens (Gallus gallus domesticus) and to determine the risk factors associated with the prevalence of the haemoparasites. A total of 530 village chickens blood samples were obtained from apparently healthy village chickens' brachial veins using sterile 2mls syringes and 23 gauge needles. Thin blood smear was made from each blood sample, and Giemsa stained and examined for the presence of avian haemoparasites under an electro-microscope. The result indicates 23.8% overall prevalence rate of three species of avian malaria parasites consisting of Plasmodium, Haemoproteus and Leucocytozoon species.Plasmodium spp. has the highest prevalent rate of 13.0% followed by Haemoproteus spp. (5.1%), mixed Plasmodium spp. + Haemoproteus spp. (4.9%) infection and Leucocytozoon spp. (0.8%). Prevalence of avian malaria parasites was significantly higher in cocks compared to hens (p < 0.05), as well as higher in adults compared to growers chickens (p < 0.05). This study also showed a higher prevalence of avian malaria parasites during the rainy season compared to the dry season of the study period. It was concluded that haemoparasites of Plasmodium, Haemoproteus and Leucocytozoon species that occur in both single and mixed infections are prevalent among village chickens that are apparently healthy in Gombe Local Government Area of Gombe State, Nigeria.

Keywords:

Avian Malaria, Haemoproteus, Leucocytozoon, Plasmodium, Village chickens

References

[1] Dessie, T., Dana, N., Ayalew, W. and Hanotte, O., 2012. Current state of knowledge on indigenous

[2] chicken genetic resources of the tropics: domestication, distribution and documentation of information

[3] on the genetic resources. World's Poultry Science Journal, 68 (1): 11-20. DOI:https://doi.org/10.1017/S0043933912000025

[4] Alders, R. G. and Pym, R. A. E., 2009. Village poultry: still important to millions eight thousand years after domestication. World’s Poult Sci J., 65 (2): 181- 190. DOI:https://doi.org/10.1017/S0043933909000117

[5] Food and Agriculture Organization (FAO), 2012. How can animal health systems support small-scale poultry producers and traders? Reflections on experience with Highly Pathogenic Avian Influenza (HPAI). Food and Agriculture Organization of the United Nations, Animal Production and Health Working Paper. No. 10. Rome.

[6] Hamer, G. L., Anderson, T. K., Berry, G. E., Makohon-Moore, A. P., Crafton, J. C., Brawn, J. D., Dolinski, A. C., Krebs, B. L., Ruiz, M. O., Muzzall, P. M., Goldberg, T. L. and Walker, E. D., 2013. Prevalence of filarioid nematodes and trypanosomes in American robins and house sparrows in Chicago. Int J Parasitol Parasites Wildl., 2, 42-49. DOI: https://doi.org/10.1016/j.ijppaw.2012.11.005, PMID: 24533314.

[7] Sehgal, R. N. M., 2015. Manifold habitat effects on the prevalence and diversity of avian blood parasites Intern J Parasitol Paras Wldlife, 4: 421-430. DOI:https://doi.org/10.1016/j.ijppaw.2015.09.001, PMID: 26835250.

[8] Bush, S. E., and Clayton, D. H., 2018. Anti-parasite behaviour of birds. Philos Trans R Soc Lond B Biol Sci., 373(1751), 20170196. DOI:https://doi.org/10.1098/rstb.2017.0196, PMID: 29866911.

[9] Tostes, R., Vashist, U., Scopel, K. K. G., Massard, C. L., Daemon, E. and D’Agosto, M., 2015. Plasmodium spp. and Haemoproteus spp. infection in birds of the Brazilian Atlantic Forest detected by microscopy and polymerase chain reaction. Pesq Veta Brasil. 35(1): 67-74. DOI:http://dx.doi.org/10.1590/S0100-736X2015000 100014, ISSN: 1678-5150.

[10] Valkiūnas, G., Palinauskas, V., Ilgūnas, M., Bukauskaitė, D., Dimitrov, D., Bernotienė, R., Zehtindjiev, P., Ilieva, M. and Iezhova, T. A., 2014. Molecular characterization of five widespread avian haemosporidian parasites (Haemosporida), with perspectives on the PCR-based detection of haemosporidians in wildlife. Parasitol. Res. 113: 2251-2263. DOI:https://doi.org/10.1007/s00436-014-3880-2, PMID: 24728557.

[11] Valkiūnas, G., 2005. Avian malaria parasites and other haemosporidia, CRC Press, Boca Raton, Florida, pp. 946. ISBN 9780415300971.

[12] Iezhova, T. A., Dodge, M., Sehgal, R. N. M., Smith, T. B. and Valkiūnas, G., 2011. New avian Haemoproteus species (Haemosporida: Haemoproteidae) from African birds, with a critique of the use of host taxonomic information in hemoproteid classification. J Parasitol. 97: 682-694. DOI:https://doi.org/10.1645/ge-2709.1, PMID: 21506819

[13] Žiegytė, R. and Valkiūnas, G., 2014. Recent advances in vector studies of avian haemosporidian parasites. Ekologija, 60 (4): 73-83. DOI: https://doi.org/10.6001/ekologija.v60i4.3042.

[14] Garamszegi, L. Z., 2011. Climate change increases the risk of malaria in birds. Glob Chan Biol. 17: 1751-1759. DOI:https://doi.org/10.1111/j.1365-2486.2010.02346.x

[15] Chasar, A., Loiseau, C., Valkiūnas, G., Iezhova, T. and Smith, T. B., 2009. Prevalence and diversity patterns of avian blood parasites in degraded African rainforest habitats. J Mol Ecol. (18): 4121-4133. DOI:https://doi.org/10.1111/j.1365-294X.2009. 04346.x, PMID: 19754513.

[16] Hellgren, O. and Perez-Tris, J., 2009. A public database of avian malaria and related haemosporidian parasites based on mitochondrial cytochrome b lineages. Mol Eco Res. 9: 1353-1358. DOI:https://doi.org/10.1111/j.1755-0998.2009.02692.x, PMID: 21564906.

[17] Zamora-Vilchis, I., Williams, S. E. and Johnson, C. N., 2012. Environmental temperature affects prevalence of blood parasites of birds on an elevation gradient: implications for disease in a warming climate. PLoS One, 7(6): e39208. DOI:https://doi.org/10.1371/journal.pone.0039208, PMID: 22723966

[18] Zehtindjiev, P., Krizanauskiene, A., Bensch, S., Palinauskas, V., Asghar, M., Dimitrov, D., Scebba, S. and Valkiunas, G., 2012. A new morphologically distinct avian malaria parasite that fails detection by established polymerase chain reaction-based protocols for amplification of the cytochrome b gene. J Parasitol. 98, 657-665. 19 Veterinary Science Research | Volume 03 | Issue 02 | December 2021 DOI:https://doi.org/10.1645/GE-3006.1, PMID: 22288487

[19] Dimitrov, D., Zehtindjiev P., Bensch, S., Ilieva, M., Iezhova, T. and 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. Syst. Parasitol. 87: 135-151. DOI:https://doi.org/10.1007/s11230-013-9464-1, PMID: 24474037

[20] Zhang, Y., Wu, Y., Zhang, Q., Su, D. and Zou, F., 2014. Prevalence patterns of avian

[21] Plasmodium and Haemoproteus parasites and the influence of host relative abundance in southern China. PloS one, 9(6), e99501. DOI:https://doi.org/10.1371/journal.pone.0099501, PMID: 24911323.

[22] Braga, E. M., Silveira, P., Belo, N. O. and Valkiūnas, G., 2011. Recent advances in the study of avian malaria: an overview with an emphasis on the distribution of Plasmodium spp in Brazil. Mem Inst Oswaldo Cruz., 106: 3-11. DOI:https://doi.org/10.1590/s0074-027620110009 00002, PMID: 21881752.

[23] Igbokwe, I. O., Hassan, S. U.., Faive, Z. T., Iliya, Y., Dagare, M. J., Rabo, J. S., Mohammed, A. and Igbokwe, N. A., 2008. Effect of Plasmodium species infections on packed cell volume of domestic chickens and helmeted guinea fowls in North eastern Nigeria. Anim Res Inter. 5(3): 892-895. DOI:http://dx.doi.org/10.4314/ari.v5i3.48756

[24] Opara, M. N., Ogbuewu, I. P., Iwuji, C. T., Njoku, L., Ihesie, E. K. and Etuk, I. F., 2012. Blood characteristics, microbial and gastrointestinal parasites of street pigeons (Columba Livia) in Owerri Imo State, Nigeria. Scientific J Anim Sci. 1(1): 14-21. ISSN : 2322- 1704 https://www.civilica.com/Paper-JR_SJAS-JR_ SJAS-1-1_003.html COI code: JR_SJAS-1-1_003.

[25] Sabuni, Z. A., 2009. Prevalence, Intensity and Pathology of Ecto and Haemoparasites Infections in Indigenous Chickens in Eastern Province of Kenya, MSc thesis. Department of Veterinary Pathology, Microbiology and Parasitology, Faculty of Veterinary Medicine University of Nairobi. pp. 132.

[26] Sabuni, Z. A., Mbuthia, P. G., Maingi, N., Nyaga, P. N., Njagi, L. W., Bebora, L.C. and Michieka, J. N., 2011. Prevalence of haemoparasites infection in indigenous chicken in Eastern Province of Kenya. Livestock R Dev. 23 (11): 2011. Article #238. Retrieved April 6, 2019, from http://www.lrrd.org/ lrrd23/11/sabu23238.htm

[27] Cornet, S., Nicot, A., Rivero, A. and Gandon, S., 2013. Malaria infection increases bird attractiveness to uninfected mosquitoes. Ecol. Lett. 16, 323-329. DOI:https://doi.org/10.1111/ele.12041, PMID: 23205903.

[28] Taroda, A., Barros, L. D., Seixas, M., Cardim, S. T., Sasse, J. P., Minutti, A. F., Vidotto, O. and Garcia, J. L., 2020. First molecular detection of Haemoproteus spp. and Plasmodium spp. in eared doves (Zenaida auriculata) in Brazil. Brazilian Journal of Veterinary Parasitology, 29(3): e000920.

[29] Anonymous, 2009. Gombe State, Wikipedia free encyclopedia. http://en.wikipedia.org/wiki/Gombe_ State retrieved 2018-11-13.

[30] Adene, D. F. and Oguntade, A. E., 2006. The structure and importance of the commercial and village based poultry industry in Nigeria. Poultry production systems. J. Poult. Sci., 7(12): 1216-1218.

[31] Zajac, A. M. and Conboy, G. A., 2012. Veterinary Clinical Parasitology. 8th edition. Wiley- blackwell.A john wiley and Sons. Inc. publication, pp. 186.

[32] Taylor, M. A., Coop, R. L. and Wall, R. L., 2007. Veterinary Parasitology. 3rd edition, Blackwell Publishing, Oxford. pp. 586-593.

[33] Bush, A. O., Fernandez, J. C., Esch, G. W. and Seed, J. R., 2001. The diversity and ecology of animal parasites. Cambridge University press, UK, 531 pp. ISBN 0 521 66278 8.

[34] Elston, R. C. and Johnson, W. D., 2008. Basic biostatistics for geneticists and epidemiologists. A practical approach. John Willey and Sons Ltd. United Kingdom, 1st edn. pp. 233-246.

[35] Ogbaje, C. I., Jerry A. Okpe, J. A. and Oke, P, 2019. Haemoparasites and Haematological Parameters of Nigerian Indigenous (local) and Exotic (broiler) Chickens Slaughtered in Makurdi Major Markets, Benue State, Nigeria. Alexandria J. Vet. Sci., 63 (2): 90 - 96. DOI:https://doi.org/10.5455/ajvs.53637

[36] Walther, E.L., Valkiūnas, G., González, A.D., Matta, N.E., Ricklefs, R.E., Cornel, A. and Sehgal, R.N., 2014. Description, molecular characterization, and patterns of distribution of a widespread New World avian malaria parasite (Haemosporida: Plasmodiidae), Plasmodium (Novyella) homopolare sp. nov. Parasitol. Res. 113, 3319-3332. DOI:https://doi.org/10.1007/s00436-014-3995-5, PMID: 24974962

[37] Nourani, L., Aliabadian, M., Mirshamsi, O. and Dinparast-Djadid, N., 2018. Molecular detection and genetic diversity of avian haemosporidian parasites 20 Veterinary Science Research | Volume 03 | Issue 02 | December 2021 in Iran. PLoS ONE 13(11): e0206638. DOI:https://doi.org/10.1371/journal.pone.0206638

[38] Gimba, F. I., Zakaria, A., Mugok, L. B., Siong, H. C., Jaafar, N., Moktar, M., A., Rahman, A. R. A., Amzah, A., Abu, J., Sani, R. A., Amin-babjee., S. M. and Reuben, S. K. S., 2014. Haemoparasites of Domestic Poultry and Wild Birds in Selangor, Malaysia. Malay J Vet Res. 5(1): 43-51.

[39] Hasson, R. H., 2015. Haemosporidians parasites of Gallus domesticus, poultry in Iraq. Inter J Adv Res. 3 (8): 1046-1054. ISSN 2320-5407.

[40] Lutz, H. L., Hochachka, W. M., Engel, J. I., Bell, J. A., Tkach, V. V., Bates, J. M., Hackett, S. J. and Weckstein, J. D., 2015. Parasite prevalence corresponds to host life history in a diverse assemblage of afrotropical birds and haemosporidian. PLoS One 10(4): e0121254. DOI:https://doi.org/10.1371/journal.pone.0121254, PMID: 25853491.

[41] Nath, T.C. and Bhuiyan, M. J. U., 2017. Haemoprotozoa infection of domestic birds in hilly Areas of Bangladesh. Indep J Manag Prod, 8: 82. DOI:https://doi.org/10.14807/ijmp.v8i1.520

[42] Naqvi, M. A., Khan, M. K., Iqbal, Z., Rizwan, H. M., Khan, M. N., Naqvi, S. Z., Zafar, A., Sindhu, Z. U. D., Abbas, R. Z. and Abbas, A., 2017. Prevalence and associated risk factors of haemoparasites, and their effects on hematological profile in domesticated chickens in District Layyah, Punjab, Pakistan. Prev Vet Med. 1: 143:49-53. DOI:https://doi.org/10.1016/j.prevetmed.2017. 05.001, PMID: 28622791.

[43] Usmana, M., Fabiyia, J. P., Mohammeda, A. A., Merab, U. M., Mahmudaa, A., Alayandea, M. O., Lawala, M. D. and Danmaigoro, A., 2012. Ectoparasites and haemoparasites of chickens in sokoto, northwestern Nigeria. Scient J Zool. 1(3): 74-78. DOI:https://doi.org/10.14196/sjz.v1i3.344

[44] Opara, M. N., Osowa, D. K. and Maxwell, J. A., 2014. Blood and Gastrointestinal Parasites of Chickens and Turkeys Reared in the Tropical Rainforest Zone of Southeastern Nigeria. Open J Vet Med. 4, 308-313. DOI:https://doi.org/10.4236/ojvm.2014.412037

[45] Opara, N. M., Okereke, E. R., Olayemi, O. D. and Jegede, O. C., 2016. Haemoparasitism of Local and Exotic Chickens Reared in the Tropical Rainforest Zone of Owerri Nigeria. Alexandria J Vet Sci. 51 (1): 84-89. DOI:https://doi.org/10.5455/ajvs.224788

[46] Karamba, K. I., Kawo, A. H., Dabo, N. T and Mukhtar, M. D., 2012. A survey of avian malaria parasite in Kano State, Northern Nigeria. Inter J Biotech Mol Biol Res. 3(1): 8-14. DOI:https://doi.org/10.5897/IJBMBR11.035, ISSN 2141-2154.

[47] Lawal, J. R., Bello, A. M., Balami, S. Y., Dauda, J., Malgwi, K. D., Ezema, K. U., Kasim, M. and Biu, A. A., 2016. Prevalence of Haemoparasites in village chickens (Gallus gallus domesticus) slaughtered at poultry markets in Maiduguri, Northeastern Nigeria. J Anim Sci Vet Med. 1: 39-45. DOI:https://doi.org/10.31248/JASVM2016.013, ISSN 2536-7099.

[48] Permin, A., Esmann, J. B., Hoj, C. H., Hove, T. and Mukatirwa, S., 2002. Ecto, Endo and Haemoparasites in free range chicken in the Goromonzi District in Zimbabwe. Prev Vet Med. 54: 213-224. DOI:https://doi.org/10.1016/s0167-5877(02)00024- 7, PMID: 12114010.

[49] Etisa, E., Chanie, M. and Tolossa, Y. H., 2017. Prevalence of Haemoparasites Infections in Scavenging Indigenous Chickens in and Around Bishoftu. World Appl Sci J. 35 (2): 302-309. DOI:https://doi.org/10.5829/idosi.wasj.2017.302.309

[50] Poulsen, J., Permin, A., Hindsho, O., Yelifari, L., Nansen, P. and Bloch, P., 2000. Prevalence and distribution of gastro-intestinal helminths and haemoparasites in young scavenging chickens in upper eastern region of Ghana, West Africa. Prev Vet Med. 45: 237-245. DOI:https://doi.org/10.1016/s0167-5877(00)00125- 2, PMID: 10821963.

[51] Njunga, G. R., 2003. Ecto- and haemoparasites of chicken in Malawi with emphasis on the effects of the chicken louse, Menacanthus cornutus. MSc Thesis. Department of Veterinary Microbiology and Network for Smallholder Poultry Development, The Royal Veterinary and Agriculture University, Dyrlæ- gevej, Frederiksberg C., Denmark, pp. 4 - 21.

[52] Hasan, A. M., Hossain, M. S., Anita Rani Dey, A. R. and Alam, M. Z., 2017. Prevalence of malaria parasites in indigenous chickens and ducks in selected districts of Bangladesh. J Bang Agric Uni. 15 (2): 260-265. DOI:https://doi.org/10.3329/jbau.v15i2.35072

[53] Bell, J. A., Weckstein, J. D., Fecchio, A. and Tkach, V. V., 2015. A new real-time PCR protocol for detection of avian haemosporidians. Parasites and Vectors. 8:383. DOI: https://doi.org/10.1186/s13071-015-0993-0.21 Veterinary Science Research | Volume 03 | Issue 02 | December 2021

[54] Biu, A. A., Agbede, R. I. and Peace, P., 2007. Studies on ectoparasites of poultry in Maiduguri, Nigeria. Nig J Para. 28:1117-1145. DOI: https://doi.org/10.4314/njpar.v28i2.37866, ISSN: 1117-4145.

[55] Sadiq, N. A., Adejinmi, J.O., Adedokun, O.A., Fashanu, S. O., Alimi, A. A. and Sofunmade, Y. T., 2003. Ectoparasites and haemoparasites of indigenous chicken (Gallus domesticus) in Ibadan and environs. Trop Vet. (21): 187-191. DOI: https://doi.org/10.4314/tv.v21i4.4541

[56] Shadan, H. A., 2013. Prevalence of Blood Parasites in Local Chickens in Qaradagh District, Sulaimani - Iraq. Iraqi J Vet Med. 37(1): 17-21. ISSN-P:1609-5693 ISSN-E:2410-7409), Retrieved from http://jcovm.uobaghdad.edu.iq/index.php/Iraqijvm/article/view/321

[57] Mbuthia, P. G., Sabuni, Z. A., Maingi, N., Nyaga, P. N. and Michieka, J. N., 2011. Prevalence of haemoparasites infection in indigenous chicken in Eastern Province of Kenya. Livestock Res for R Devel. (23): 11-19. http://www.lrrd.org/lrrd23/11/sabu23238.htm

[58] Islam, A., Anisuzzaman, Rabbi, A. K. M. A., Rahman, A., Islam, M. A. and Rahman, M. H., 2013. Haemoproteus spp. infection of domestic poultry of Bangladesh. VETSCAN, 7(2), 85-88. ISSN 0973- 6980.

[59] Sehgal, R. N. M., Valkiunas, G., Iezhova, T.A. and Smith, T. B., 2006. Blood parasites of chickens in Uganda and Cameroon with molecular descriptions of Leucocytozoon schoutedeni and Trypanosoma gallinarum, J Parasitol. 92, 1336-1343. DOI:https://doi.org/10.1645/GE-927R.1, PMID: 17304817.

[60] Legowo, D. Khotimah, S. H. and Suwanti, L. T., 2017. Blood Parasite Infection Prevalence in Kampong Chicken Breeder’s Group in Garut. The Veterinary Medicine International Conference (VMIC) Dec. 2017. KnE Life Sci. [S.l.], 308-315. DOI:https://doi.org/10.18502/kls.v3i6.1139

[61] Valkiūnas, G., Anwar, A. M., Atkinson, C. T., Greiner, E. C., Paperna, I. and Peirce, M. A., 2005. What distinguishes malaria parasites from other pigmented haemosporidians? Trends Parasitol. 21(8): 357-358. DOI:https://doi.org/10.1016/j.pt.2005.06.005, PMID:15967726.

[62] Palinauskas, V., Valkiūnas, G., Bolshakov, C. V. and Bensch, S., 2011. Plasmodium relictum (lineage SGS1) and Plasmodium ashfordi (lineage GRW2): The effects of the co-infection on experimentally infected passerine birds. Experimental Parasitol. 127: 527-533. DOI:https://doi.org/10.1016/j.exppara.2010.10.007, PMID: 21050849.

[63] Palinauskas, V., Valkiūnas, G., Križanauskiené, A., Bensch, S. and Bolshakov C. V., 2009. Plasmodium relictum (lineage P- SGS1): further observation of effects on experimentally infected passeriform birds, with remarks on treatment with Malarone™. Experimental Parasitol. 123:134-139. DOI:https://doi.org/10.1016/j.exppara.2009.06.012

[64] Palinauskas, V., Ziegyte, R., Ilgunas, M., Iezhova, T.A., Bernotiene, R., Bolshakov, C. and Valkiunas, G., 2015. Description of the first cryptic avian malaria parasite, Plasmodium homocircumflexum n. sp., with experimental data on its virulence and development in avian hosts and mosquitoes. Inter J Parasitol. 45, 51-62. DOI:https://doi.org/10.1016/j.ijpara.2014.08.012, PMID: 25449950.

[65] Sehgal, R. N. M., Buermann, W., Harrigan, R. J., Bonneaud, C., Loiseau, C., Chasar, A., Sepil, L., Valkiūnas, G., Iezhova, T. A., Saatchi, S. and Smith, T. B., 2011. Spatially explicit predictions of blood parasites in a widely distributed African rainforest bird. Proc R Soc B. 278: 1025-1033. DOI:https://doi.org/10.1098/rspb.2010.1720, PMID: 20880888

[66] Njabo, K. Y., Cornel, A. J., Bonneaud, C., Toffelmier, E., Sehgal, R. N. M., Valkiūnas, G., Russell, A. F. and Smith, T. B., 2011. Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest. Mol Ecol. 20: 1049-1061. DOI:https://doi.org/10.1111/j.1365-294X.2010. 04904.x, PMID: 21134011.

[67] Elahi, R., Islam, A., Hossain, M. S., Mohiuddin, K., Mikolon, A., Paul,S. K., Hosseini, P. R., Daszak, P. and Alam M. S., 2014. Prevalence and Diversity of Avian Haematozoan Parasites in Wetlands of Bangladesh. J Paras Res. vol. 2014, Hindawi Publishing Corporation, Article ID 493754, 12 pages. DOI:https://doi.org/10.1155/2014/493754, PMID: 24587896.

[68] Soulsby, E. J. L., 1982. Helminth, Arthropods and Protozoa of Domesticated Animals. 7th edition. Baillire, Tindall. 1982, Pp. 35-740. DOI:https://doi.org/10.1016/0035-9203(84)90110-X

[69] Samani, A. D., Kheirabadi, K. P. and Samani, A. D., 2013. Prevalence and rate of parasitemia of Haemoproteus columbae in Columba iiviadomestica in southwest of Iran. Iranian J Parasitol. 8 (4): 641-644. PMID: 25516748.22 Veterinary Science Research | Volume 03 | Issue 02 | December 2021

[70] Momin, M. A., Begum, N., Dey, A. R., Paran, M. S. and Alam, M. Z., 2014. Prevalence of blood protozoa in poultry in Tangail, Bangladesh. Sch J Agric Vet Sci. 7: 55-60. DOI:https://doi.org/10.9790/2380-07735560

[71] Sehgal, R. N., Hull, A. C., Anderson, N. L., Valkiunas, G., Markovets, M. J., Kawamura, S. and Tell, L. A., 2006. Evidence for cryptic speciation of Leucocytozoon spp. (Haemosporida, Leucocytozoidae) in diurnal raptors. J Parasitol. 92, 375-379. DOI:https://doi.org/10.1645/GE-656R.1

[72] Okanga, S., Cumming, G. S. and Hockey P. A. R., 2013. Avian malaria prevalence and mosquito abundance in the Western Cape, South Africa. Malar J. 12: 370. DOI: https://doi.org/10.1186/1475-2875-12-370

[73] Smith, M. M. and Ramey, A. M., 2015. Prevalence and genetic diversity of haematozoa in South American waterfowl and evidence for intercontinental redistribution of parasites by migratory birds. Inter J Parasitol: Paras Wildl. 4: 22-28. DOI:https://doi.org/10.1016/j.ijppaw.2014.12.007, PMID: 25830104.

[74] Adriano, E. A. and Cordeiro, N. S., 2001. Prevalence and Intensity of Haemoproteus columbae in three species of wild doves from Brazil. Mem Inst Oswaldo Cruz, 96: 175-178. DOI:https://doi.org/10.1590/S0074-02762001000200007

[75] Lafferty, K. D., 2009. The ecology of climate change and infectious diseases. Ecol. 12: 888-900. DOI:https://doi.org/10.1890/08-0079.1

[76] Schrader, M. S., Walters, E. L., James, F. C. and Greiner, E. C., 2003. Seasonal prevalence of a haematozoan parasite of red-bellied woodpeckers (Melanerpes carolinus) and its association with host condition and overwinter survival. Auk., 120 (1): 130- 137. DOI:https://doi.org/10.1093/auk/120.1.130

[77] Cosgrove, C. L., Wood, M. J., Day, K. P. and Sheldon, B. C., 2008. Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. J Anim Ecol. 12: 540-548. DOI:https://doi.org/10.1111/j.1365-2656.2008.01370.x, PMID: 18312339.

[78] Zhao, W., Cai, B., Qi, Y., Liu, S., Hong, L., Lu, M., Chen, X., Qiu, C., Peng, W., Jian Li, J. and Su, X., 2014. Multi-strain infections and 'relapse' of Leucocytozoon sabrazesi gametocytes in domestic chickens in southern China. PLoS One. 2014; 9(4):e94877. Epub2014/04/15. DOI:https://doi.org/10.1371/journal.pone.0094877, PMID: 24728499.

[79] Zhao, W., Pang, Q., Xu, R., Liu, J., Liu, S., Li, J. and Su, X., 2016. Monitoring the Prevalence of Leucocytozoon sabrazesi in Southern China and Testing Tricyclic Compounds against Gametocytes. PLoS ONE 11(8): e0161869. DOI:https://doi.org/10.1371/journal.pone.0161869, PMID: 27571513.

Downloads

Issue

Vol. 3 , Iss. 2 (December 2021)

Article Type

Articles

License

Copyright © 2021 Jallailudeen Rabana Lawal, Umar Isa IBRAHIM, Abdullahi Abubakar BIU, Hassan Ismail MUSA

Creative Commons License

This is an open access article under the Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0) License.

Copyright and Licensing

The authors shall retain the copyright of their work but allow the Publisher to publish, copy, distribute, and convey the work.

Veterinary Science Research publishes accepted manuscripts under Creative Commons Attribution-NonCommercial 4.0 International License (CC BY-NC 4.0). Authors who submit their papers for publication by Veterinary Science Research agree to have the CC BY-NC 4.0 license applied to their work, and that anyone is allowed to reuse the article or part of it free of charge for non-commercial use. As long as you follow the license terms and original source is properly cited, anyone may copy, redistribute the material in any medium or format, remix, transform, and build upon the material.

License Policy for Reuse of Third-Party Materials

If a manuscript submitted to the journal contains the materials which are held in copyright by a third-party, authors are responsible for obtaining permissions from the copyright holder to reuse or republish any previously published figures, illustrations, charts, tables, photographs, and text excerpts, etc. When submitting a manuscript, official written proof of permission must be provided and clearly stated in the cover letter.
The editorial office of the journal has the right to reject/retract articles that reuse third-party materials without permission.

Journal Policies on Data Sharing

We encourage authors to share articles published in our journal to other data platforms, but only if it is noted that it has been published in this journal.