Immune status of the Collared dove Streptopelia decaocto in northeastern Algeria

Authors

  • Hassiba Zediri Department of Biology, Faculty of Sciences, University of Badji MOKHTAR, Annaba, Algeria. https://orcid.org/0000-0002-0171-9039
  • Adnène Belabed Department of Biology, Faculty of Sciences, University of Badji MOKHTAR, Annaba, Algeria. https://orcid.org/0000-0002-3272-5204
  • Zihad Bouslama Department of Biology, Faculty of Sciences, University of Badji MOKHTAR, Annaba, Algeria.

DOI:

https://doi.org/10.5281/zenodo.11181067

Keywords:

Collared dove, Streptopelia decaocto, Annaba, health status, bursa of Fabricius

Abstract

Since its initial sighting in Algeria in 1994, the Eurasian Collared dove (Streptopelia decaocto) has exhibited invasive behavior, expanding its range gradually and consistently to the country's extreme south. An inventory of its health status has emerged, trying to respond more accurately to the question: does the immune status play a role in this invasion? Our investigation into the health of both nestlings and adults included identification and quantification of blood cells in nestlings before fledging, focusing on the evolution of total red blood cells (RBC) and white blood cells (WBC); Analysis of the bursal index and microscopic examination of the bursa. The study involved collecting blood smears from nestlings at different ages (5 days, 10 days, 15 days), and euthanizing individuals from each age group (5 days, 10 days, 15 days, 18-20 days, and adults), to extract the bursa for histological examination. This process aimed to ascertain the immune status of the species in Annaba (Northeastern Algeria). Our findings indicate a decline in immune competence with age, starting from an "Excellent" status in early life, deteriorating to "Poor" in later stages, and finally reaching "Bad" in adulthood. Although our results do not definitively confirm a compromised health status in the Eurasian Collared dove population studied, they suggest the need for further research to substantiate these preliminary findings.

References

Aerts, J. (2018). Quantification of a Glucocorticoid Profile in Non-pooled Samples Is Pivotal in Stress Research Across Vertebrates. Frontiers in Endocrinology, 9, 635. *https://doi.org/10.3389/fendo.2018.00635

Al-Tememy, H. A. S., Hussein, J. S., & Rasool, B. S. (2011). Histological study on bursa of Fabricius of quail birds (Coturnix coturnix japonica). Egyptian Poultry Science Journal, 31(3), 613-620.

Alloui, N., Sellaoui, S., Bennoune, O., & Ayachi, A. (2020). Relation between the bursa of Fabricius evolution and the weight of broiler chickens in intensive poultry flocks in Algeria. Livestock Research for Rural Development, 32(8), 124.

Andrews, I. J. (1995). The Birds of the Hashemite Kingdom of Jordan. Musselburgh 185 pp.

Bańbura, J., Skwarska, J., Bańbura, M., Glądalski, M., Holysz, M., Kaliński, A., Markowski, M., Wawrzyniak, J., & Zielinski, P. (2013). Spatial and Temporal Variation in Heterophil-to-Lymphocyte Ratios of Nestling Passerine Birds: Comparison of Blue Tits and Great Tits. PLoS ONE, 8(9), e74226. *https://doi.org/10.1371/journal.pone.0074226

Beaumont, A., & Cassier, P. (1987). Biologie animale. Les Cordés, anatomie comparée des Vertébrés 6ème édition revue et corrigée. Préface de Marcel Prenant. Dunod.

Belabed, A., Draidi, K., Djemadi, I., Zediri, H., Eraud, C., & Bouslama, Z. (2012). Deux nouvelles espèces de tourterelles nicheuses Streptopelia turtur arenicola et Streptopelia senegalensis phoenicophila dans la ville d’Annaba (Nord-est algérien). Alauda, 80(4), 299-300.

Belabed, A., Djemadi, I., Zediri, H., Eraud, C., & Bouslama, Z. (2013a). Étude de l’investissement parental chez la Tourterelle turque (Streptopelia decaocto) dans le nord-est algérien. European Journal of Scientific Research, 94(4), 421-436.

Belabed, A. I., Aouissi, H. A., Zediri, H., Djemadi, I., Driss, K., Houhamdi, M., Eraud, C., & Bouslama, Z. (2013b). L’effet de l’urbanisation sur le phénotype de la Tourterelle turque (Streptopelia decaocto) dans le Nord-Est algérien. Bulletin de l’Institut Scientifique, Rabat, Section Sciences de la Vie, 35, 110-119.

Belabed, A. I., Zediri, H., Shehab, A., & Bouslama, Z. (2015). The effect of altitude on seasonal dynamics of Ticks (Acari: Ixodidae) in Northeastern Algeria. Advances in Environmental Biology, 9(14), 169-184.

Bendjoudi, D., Voisin, J. F., Doumandji, S., Merabet, A., Benyounes, N., & Chenchouni, H. (2015). Rapid increase in numbers and change of land-use in two expanding Columbidae species (Columba palumbus and Streptopelia decaocto) in Algeria. Avian Research, 6, 18. *https://doi.org/10.1186/s40657-015-0027-9

Bennett, C. (2002). How to score bursa size in broiler chicken flocks. University of Saskatchewan.

Benyacoub, S. (1998). La tourterelle turque Streptopelia decaocto en Algérie. Alauda, 66, 251-253.

van den Berg, T. P., Eterradossi, N., Toquin, D., & Meulemans, G. (2000). Infectious bursal disease (Gumboro disease). Revue Scientifique et Technique, 19(2), 509-543.

Bergier, P., Franchimont, J., & Thévenot, M. (1999). Implantation et expansion de deux espèces de Columbidés au Maroc : la Tourterelle turque Streptopelia decaocto et la Tourterelle maillée Streptopelia senegalensis. Alauda, 67, 23-36.

Biard, C., Monceau, K., Motreuil, S., & Moreau, J. (2015). Interpreting immunological indices: The importance of taking parasite community into account. An example in blackbirds Turdus merula. Methods in Ecology and Evolution, 6, 960-972. *https://doi.org/10.1111/2041-210X.12371

Bódi, I., Felföldi, B., Minkó, K., Benyeda, Z., Nagy, N., Kiss, A. L., Palya, V., & Oláh, I. (2019). Effect of IBDV infection on the interfollicular epithelium of chicken bursa of Fabricius. Poultry Science, 98: 3464-3470. *https://doi.org/10.3382/ps/pey512

Boross, N., Markó, G., Laczi, M., Garamszegi, L. Zs., Hegyi, G., Herényi, M., Kiss, D., Nagy, G., Rosivall, B., Szöllősi, E., & Török, J. (2012). Sources of variation in haematocrit in the Collared Flycatcher (Ficedula albicollis). Ornis Hungarica, 20(2), 64-72. *https://doi.org/10.2478/orhu-2013-0008

Boulinier, T., McCoy, K., & Sorci, G. (2001). Dispersal and parasitism. In: Dispersal (J. Clobert, J.D. Nichols, E. Danchin and A. Dhondt, eds), pp. 169-179. Oxford University Press, Oxford, UK.

Campbell, T. W. (2015). Exotic Animal Hematology and Cytology. 4th Edition. Blackwell Publishing, Oxford. 395p.

Chatterjee, S., Clark, C. E., Lugli, E., Roederer, M., & Nutman, T. B. (2015). Filarial infection modulates the immune response to mycobacterium tuberculosis through expansion of CD4+ IL‐4 memory T cells. The Journal of Immunology, 194, 2706-2714. *https://doi.org/10.4049/jimmunol.1402718

Ciriaco, E., Muglia, U., & Germana, G. (1989). An ultrastructural study of pigeon bursa of Fabricius during involution. Anatomischer Anzeiger, 169, 67-73.

Ciriaco, E., Píñera, P. P., Díaz-Esnal, B., & Laurá, R. (2003). Age-Related Changes in the Avian Primary Lymphoid Organs (Thymus and Bursa of Fabricius). Microscopy Research and Technique, 62, 482-487. *https://doi.org/10.1002/jemt.10416

Clark, P., Boardman, W. S. J., & Raidal, S. R. (2009). Atlas of Clinical Avian Hematology. Wiley-Blackwell, Oxford. 200 Pages.

Clark, N. J., Wells, K., Dimitrov, D., & Clegg, S. M. (2016). Co-infections and environmental conditions drive the distributions of blood parasites in wild birds. Journal of Animal Ecology, 85, 1461-1470. *https://doi.org/10.1111/1365-2656.12578

Clark, P. (2015). Observed variation in the heterophil to lymphocyte ratio values of birds undergoing investigation of health status. Comparative Clinical Pathology, 24, 1151-1157. *https://doi.org/10.1007/s00580-014-2052-1

Crooks, J. A., & Soule, M. E. (1999). Lag times in population explosions of invasive species: causes and implications. In Sandland, O. T., Schei, P. J., Viken, A. (eds) Invasive Species and Biodiversity Management, 103-125. Dordrecht: Kluwer Academic Publishers.

Davis, A. K., Maney, D. L., & Maerz, J. C. (2008). The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Functional Ecology, 22, 760-772. *https://doi.org/10.1111/j.1365-2435.2008.01467.x

Dunn, J. C., Stockdale, J. E., Bradford, E. L., McCubbin, A., Morris, A. J., Grice, P. V., Goodman, S. J., & Hamer, K. C. (2017). High rates of infection by blood parasites during the nestling phase in UK Columbids with notes on ecological associations. Parasitology, 144(5), 622-628. *https://doi.org/10.1017/S0031182016002274

El Lethey, H., Huber-Eicher, B., & Jungi, T. W. (2003). Exploration of stress-induced immunosuppression in chickens reveals both stress-resistant and stress-susceptible antigen responses. Veterinary Immunology and Immunopathology, 95, 91-101. *https://doi.org/10.1016/s0165-2427(02)00308-2

Eraud, C., Boutin, J-M., Roux, D., Belabed, A. I., & Lormée, H. (2011). La tourterelle turque : histoire et dynamique d’une expansion. Faune Sauvage, 293(4), 32-33.

Ewenson, E. L., Zann, R. A., & Flannery, G. R. (2001). Body condition and immune response in wild zebra finches: effects of capture, confinement and captive-rearing. Naturwissenschaften, 88, 391-394. *https://doi.org/10.1007/s001140100250

Fair, J., Whitaker, S., & Pearson, B. (2007). Sources of variation in haematocrit in birds. Ibis, 149(3), 535-552. *https://doi.org/10.1111/j.1474-919X.2007.00680.x

Figuerola, J., Munoz, E., Gutierrez, R., & Ferrer, D. (1999). Blood parasites, leucocytes and plumage brightness in the Cirl Bunting, Emberiza cirlus. Functional Ecology, 13, 594-601. *https://doi.org/10.1046/j.1365-2435.1999.00354.x

Fokidis, H. B., Greiner, E.C., & Deviche, P. (2008). Interspecific variation in avian blood parasites and haematology associated with urbanization in a desert habitat. Journal of Avian Biology, 39, 300-310. *https://doi.org/10.1111/j.0908-8857.2008.04248.x

Franchimont, J. (1987). À propos de l’installation de la tourterelle turque (Streptopelia decaocto) au Magreb. Aves, 24(3), 150-151.

Fujisaki, I., Pearlstine, E. V., & Mazzotti, F. J. (2010). The rapid spread of invasive Eurasian Collared Doves Streptopelia decaocto in the continental USA follows human-altered habitats. Ibis, 152, 622-632. *https://doi.org/10.1111/j.1474-919X.2010.01038.x

Gallego, M., Del Cacho, E., Felices, C., Varas, A., & Bascuas, J. A. (1996). Distribution of bursal secretory dendritic cells in the chicken. The Anatomical Record, 246, 372-376. *https://doi.org/10.1002/(SICI)1097-0185(199611)246:3%3C372::AID-AR8%3E3.0.CO;2-%23

Genovese, K. J., He, H., Swaggerty, C. L., & Kogut, M. H. (2013). The avian heterophil. Developmental and Comparative Immunology, 41, 334-340. *https://doi.org/10.1016/j.dci.2013.03.021

Gibbons, D. W., Reid, J. B., & Chapman, R. A. (1993). The New Atlas of Breeding Birds in Britain and Ireland: 1988-1991. London: T. and A.D. Poyser.

Helin, A. (2020). Eco-immunological studies of innate immunity in Mallards (Anas platyrhynchos), Linnaeus University Dissertation No 376/2020, 64pp.

Hofmann, T., Schmucker, S. S., Bessei, W., Grashorn, M., & Stefanski, V. (2020). Impact of Housing Environment on the Immune System in Chickens: A Review. Animals (Basel), 10(7), 1138. *https://doi.org/10.3390/ani10071138

Ifrah, M. E., Perelman, B., Finger, A., & Uni, Z. (2017). The role of the bursa of Fabricius in the immune response to vaccinal antigens and the development of immune tolerance in chicks (Gallus domesticus) vaccinated at a very young age. Poultry Science, 96(1), 51-57. *https://doi.org/10.3382/ps/pew232

Johnstone, C. P., Reina, R. D., & Lill, A. (2012). Interpreting indices of physiological stress in free-living vertebrates. Journal of Comparative Physiology B, 182, 861-879. *https://doi.org/10.1007/s00360-012-0656-9

Khenenou, T., Melizi, M., & Benzaoui, H. (2012). Morpho-histological Study of the Bursa of Fabricius of Broiler Chickens during Post-hashing Age. World Academy of Science, Engineering and Technology International Journal of Animal and Veterinary Sciences, 6(12), 1131-1133.

Kita, H. (2011) Eosinophils: Multifaceted biologic properties and roles in health and disease. Immunological Reviews, 242(1), 161-177. *https://doi.org/10.1111/j.1600-065X.2011.01026.x

Koonpaew, S., Teeravechyan, S., Frantz, P. N., Chailangkarn, T., & Jongkaewwattana, A. (2019). PEDV and PDCoV pathogenesis: The interplay between host innate immune responses and porcine enteric coronaviruses. Frontiers Veterinary Science, 6, 34. *https://doi.org/10.3389/fvets.2019.00034

Krams, I., Vrublevska, J., Cirule, D., Kivleniece, I., Krama, T., Rantala, M. J., Sild, E., & Hõrak, P. (2012). Heterophil/lymphocyte ratios predict the magnitude of humoral immune response to a novel antigen in great tits (Parus major). Comparative Biochemistry and Physiology Part A, 161, 422-428. *https://doi.org/10.1016/j.cbpa.2011.12.018

Lashev, L., Hubenov, H., Nikolov, Y., Lasheva, V., & Mihailov, R. (2009). Comparison of some haematological parameters between three bird species from the Columbidae family. Veterinarski Arhiv, 79(4), 409-414.

Lill, A., Rajchl, K., Yachou-Wos, L., & Johnstone, C. P. (2013). Are haematocrit and haemoglobin concentration reliable body condition indicators in nestlings: the Welcome Swallow as a case study. Avian Biology Research, 6(1), 57-66. *https://doi.org/10.3184/175815513X1357899690660

Løken, O. M., Bjørgen, H., Hordvik, I., & Koppang, E. O. (2019). A teleost structural analogue to the avian bursa of Fabricius. Journal of Anatomy, 236(5), 798-808. *https://doi.org/10.1111/joa.13147

MacColl, E., Vanesky, K., Buck, J. A., Dudek, B. M., Eagles-Smith, C. A., Heath, J. A., Herring, G., Vennum, C., & Downs, C. J. (2017). Correlates of immune defenses in golden eagle nestlings. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 327(5), 243-253. *https://doi.org/10.1002/jez.2081

Male, D., Brostoff, J., Roth, D., & Roitt, I. (2012). Immunology, 8th Edition. New York: Elsevier. 482pp.

Martin, T. E., Møller, A. P., Merino, S., & Clobert, J. (2001). Does clutch size evolve in response to parasites and immunocompetence? Proceedings of the National Academy of Sciences of the United States of America, 98, 2071-2076. *https://doi.org/10.1073/pnas.98.4.2071

Meeusen, E. N. T., & Balic, A. (2000). Do eosinophils have a role in the killing of helminth parasites? Parasitology Today, 16, 95-101. *https://doi.org/10.1016/s0169-4758(99)01607-5

Mešťanová, V., & Varga, I. (2016). Morphological view on the evolution of the immunity and lymphoid organs of vertebrates, focused on thymus. Biologia, 71(10), 1080-1097. *https://doi.org/10.1515/biolog-2016-0137

Minias, P. (2019). Evolution of heterophil/lymphocyte ratios in response to ecological and life-history traits: A comparative analysis across the avian tree of life. Journal of Animal Ecology, 288, 554-565. *https://doi.org/10.1111/1365-2656.12941

Møller, A. P., & Erritzøe, J. (2001). Dispersal, vaccination and regression of immune defence organs. Ecology Letters, 4, 484-490. *https://doi.org/10.1046/j.1461-0248.2001.00259.x

Møller, A. P., Martín-Vivaldi, M., & Soler, J. J. (2004). Parasitism, host immune defence and dispersal. Journal of Evolutionary Biology, 17, 603-612. *https://doi.org/10.1111/j.1420-9101.2004.00694.x

Møller, A. P. (2008). Flight distance of urban birds, predation and selection for urban life. Behavioral Ecology and Sociobiology, 63, 63-75. *https://doi.org/10.1007/s00265-008-0636-y

Müller, C., Jenni-Eiermann, S., & Jenni, L. (2011). Heterophils/Lymphocytes-ratio and circulating corticosterone do not indicate the same stress imposed on Eurasian kestrel nestlings. Functional Ecology, 25, 566-576. *https://doi.org/10.1111/j.1365-2435.2010.01816.x

Nagy, N., & Oláh, I. (2010). Experimental evidence for the ectodermal origin of the epithelial anlage of the chicken bursa of Fabricius. Development, 137, 3019-3023. *https://doi.org/10.1242/dev.055194

Norris, K., & Evans, M. R. (2000). Ecological immunology: life history trade-offs and immune defense in birds. Behavioral Ecology, 11, 19-26. *https://doi.org/10.1093/beheco/11.1.19

Norte, A. C., Araujo, P. M., Sampaio, H. L., Sousa, J. P., & Ramos, J. A. (2009). Haematozoa infections in a great tit Parus major population in Central Portugal: relationships with breeding effort and health. Ibis, 151, 677-688. *https://doi.org/10.1111/j.1474-919X.2009.00960.x

O’Dell, D. A., Carlo, M. A., Kimmitt, A., Bikowski, E., Morris, K. R., & Dolby, A. (2014). A Comparison of Techniques Measuring Stress in Birds. Virginia Journal of Science, 65, 133-149. *https://doi.org/10.25778/5h4z-5938

Oláh, I., & Vervelde, L. (2008). Structure of the avian lymphoid system. Academic Press, London.

Peinado, V. I., Polo, F. J., Celdrán, J. F., Viscor, G., & Palomeque, J. (1992). Hematology and Plasma Chemistry in Endangered Pigeons. Journal of Zoo and Wildlife Medicine, 23, 65-71.

Romagosa, C. M., & Labisky, R. F. (2000). Establishment and dispersal of the Eurasian Collared-dove in Florida. Journal of Field Ornithology, 71, 159-166. *https://doi.org/10.1648/0273-8570-71.1.159

Ruhs, E. C., Martin, L. B., & Downs, C. J. (2020). The impacts of body mass on immune cell concentrations in birds. Proceedings of the Royal Society B: Biological Sciences, 287, 20200655. *https://doi.org/10.1098/rspb.2020.0655

Schat, K. A., Kaspers, B., & Kaiser, P. (2013). Avian immunology 2nd Ed. Elsevier Science.

Schoenle, L. A., Downs, C. J., & Martin, L. B. (2018). An Introduction to Ecoimmunology. Advances in Comparative Immunology, 10, 901-932. *https://doi.org/10.1007/978-3-319-76768-0_26

Schultz, D. J. (2003). Columbiformes (pigeons, doves). In: Fowler, M.E., Miller, R.E. (Eds.), Zoo and Wild Animal Medicine, fifth ed. Saunders, St. Louis, MO, pp. 180-187.

Sinan, Th. A. (2014). Effect of probiotics addition into diet and drinking water in Collared Dove (Streptopelia decaocto) on certain physiological and biochemical parameters. Iraqi Journal of Veterinary Sciences, 28(2), 127-131.

Sinan, Th. A. (2017). Effects of Probiotic and Antibiotic Supplementation on some Blood Parameters in Collared Dove (Streptopelia decaocto). Rafidain Journal of Science, 26(1), 25-31. *https://doi.org/10.33899/rjs.2017.138957

Sinan, Th. A. (2019). Impact of Collared Dove Pigeons (Streptopelia decaocto) Age on some Hematological and Biochemical Parameters in Mosul City. Rafidain Journal of Science, 28(4), 8-12. *https://doi.org/10.33899/rjs.2019.163291

Small, M. F., Baccus, J. T., Mink, J. N., & Roberson, J. A. (2005). Hematologic responses in captive white-winged doves (Zenaida asiatica), induced by various radio transmitter attachments. Journal of Wildlife Diseases, 41, 387-394. *https://doi.org/10.7589/0090-3558-41.2.387

Stenkewitz, U., Nielsen, Ó. K., Skírnisson, K., & Stefánsson, G. (2015). The relationship between parasites and spleen and bursa mass in the Icelandic Rock Ptarmigan Lagopus muta. Journal of Ornithology, 156(2), 429-440. *https://doi.org/10.1007/s10336-014-1141-x

Vinkler, M., Schnitzer, J., Munclinger, P., Votýpka, J., & Albrecht T. (2010). Haematological health assessment in a passerine with extremely high proportion of basophils in peripheral blood. Journal of Ornithology, 151, 841-849. *https://doi.org/10.1007/s10336-010-0521-0

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Published

2024-05-12

How to Cite

Zediri, H., Belabed, A., & Bouslama, Z. (2024). Immune status of the Collared dove Streptopelia decaocto in northeastern Algeria. Journal of Wildlife and Biodiversity, 8(3), 1–26. https://doi.org/10.5281/zenodo.11181067