Prevalência e parasitemia sanguínea de rolas de colar (Streptopelia decaocto) e rolas carpideiras (Zenaida macroura) em Durango, México
Palavras-chave:
Streptopelia decaocto, Zenaida macroura, variação sazonal, Haemoproteus, PlasmodiumResumo
O parasitismo do sangue nas aves no México é um fenómeno pouco estudado e a sua ocorrência em muitas espécies de aves é desconhecida. Neste estudo, comparámos a prevalência e parasitemia da hemosporidia nas épocas de reprodução (húmida) e não reprodutiva (seca) de rolas de colar (Streptopelia decaocto) e rolas carpideiras (Zenaida macroura) no norte de México. Foi analisado o sangue de 40 aves de cada espécie, recolhido entre 2013 e 2014. O diagnóstico de hemoparasitas foi realizado utilizando técnicas de microscopia e reacção em cadeia da polimerase (PCR). A prevalência de hemoparasitas foi de 87,5 % (95% IC=78,3-93,3). A parasitemia média foi de 7,03 (95 % IC= 5,68-9,04) hemoparasitas por 10.000 eritrócitos infectados. A prevalência e parasitemia eram mais elevadas para Haemoproteus sp do que para Plasmodium sp. e microfilariase. As taxas de prevalência não variaram entre espécies de aves, nem entre estações do ano. No entanto, a sazonalidade parece ser um factor importante na parasitemia. A espécie com maiores taxas de parasitemia era a Z. macoura. São necessários mais estudos para compreender os mecanismos que associam a parasitemia nesta espécie com outras espécies columbiformes.
e2021-45
Referências
BENSCH S, Stjernman M, Hasselquist D, Örjan Ö, Hannson B, Westerdahl H, Torres-Pinheiro R. 2000. Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society. 267(1452):1583–1589. ISSN: 0370-1662.
https://doi.org/10.1098/rspb.2000.1181
BENSCH S, Waldenström J, Jonzen N,Westerdahl H, Hansson B, Sejberg D, Hasselquist D. 2007. Temporal dynamics and diversity of avian malaria parasites in a single host species. Journal of Animal Ecology. 76(1):112–122. ISSN: 1365-2656. https://doi.org/10.1111/j.1365-2656.2006.01176.x
BORJI H, Moghaddas E, Razmi G, Heidarpour M, Mohri M, Azad M. 2011. Prevalence of pigeon haemosporidians and effect of infection on biochemical factors in Iran. Journal of Parasitic Diseases. 35: 199-201. ISSN: 0971-7196.
https://doi.org/10.1007/s12639-011-0056-1
CARDONA CJ, Ihejirika A, McClellan L. 2002. Haemoproteus lophortyx infection in bobwhite quail. Avian Dissease. 46(1):249–255. ISSN: 1090-2449.
https://doi.org/10.1637/0005-2086(2002)046[0249:hliibq]2.0.co;2
CARLSON J, Martínez-Gómez JE, Valkiūnas G, Loiseau C, Bell DA, Sehgal RN. 2013. Diversity and phylogenetic relationships of hemosporidian parasites in birds of Socorro Island,México and their role in the re-introduction of the Socorro Dove (Zenaida graysoni). Journal of Parasitology. 99(2):270–276. ISSN: 0022-3395.
https://doi.org/10.1645/GE-3206.1
CHAGAS CRF, de Oliveira-Guimarães L, Monteiro EF, Valkiūnas G, Katayama MV, Santos SV, Guida FJV, Simões RF, Kirchgatter K. 2016. Hemosporidian parasites of free-living birds in the São Paulo Zoo, Brazil. Parasitology Research. 115:1443–1452. ISSN: 1432-1955. https://doi.org/10.1007/s00436-015-4878-0
CLARK, GW, Swinehart, B. 1969. Avian haematozoa from the offshore islands of northern Mexico. Bulletin of the Wildlife Disease Association. 5(2):111-112. ISSN: 0098373x. https://bioone.org/journalArticle/Download?fullDOI=10.7589/0090-3558-5.2.111
DEBROCK S, Cohen E, Balasubramanian S, Marra PP, Hamer SA. 2021. Characterization of the Plasmodium and Haemoproteus parasite community in temperate-tropical birds during spring migration. International Journal for Parasitology: Parasites and Wildlife. 15:12–21. ISSN: 22132244.
https://doi.org/10.1016/j.ijppaw.2021.03.013
DEVICHE P., Parris J. 2006. Testosterone Treatment to Free-Ranging Male Dark-Eyed Juncos (Junco Hyemalis) Exacerbates Hemoparasitic Infection. The Auk. 123(2):548–562. ISSN: 2732-4613. https://doi.org/10.1093/auk/123.2.548
DUBIEC A, Podmoka E, Zagalska-Neubauer M, Drobniak SM, Arct A, Gustafsson L, Cichoń M .2016. Differential prevalence and diversity of haemosporidian parasites in two sympatric closely related non-migratory passerines. Parasitology. 143:1320–1329. ISSN: 0031-1820. https://doi.org/10.1017/S0031182016000779
DUNN JC, Stockdale JE, Bradford EL, McCubbin A, Morris AJ, Grice PV, Goodman SJ, Hamer KC. 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. ISSN: 0031-1820. https://doi.org/10.1017/S0031182016002274
EBIRD. 2021. eBird: An online database of bird distribution and abundance. eBird, Cornell Lab of Ornithology, Ithaca, New York. http://www.ebird.org
EL‐MANSI AA, El‐Bealy EA, Rady A M, Abumandour M A, El‐Badry DA. 2021. Macro‐and microstructures of the digestive tract in the Eurasian collared dove, Streptopelia decaocto (Frivaldszky 1838): Adaptive interplay between structure and dietary niche. Microscopy Research and Technique. ISSN: 1097-0029.
https://doi.org/10.1002/jemt.23843
FERREIRA L, Silva-Torres C, Torres J, Venette R. 2021. Potential displacement of the native Tenuisvalvae notata by the invasive Cryptolaemus montrouzieri in South America suggested by differences in climate suitability. Bulletin of Entomological Research. 1–11. ISSN: 1475-2670. https://doi.org/10.1017/S000748532100033X
FOKIDIS HB, Greiner EC, 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. ISSN: 1600-048X. https://doi.org/10.1111/j.0908-8857.2008.04248.x
FORONDA P, Valladares B, Rivera-Medina JA, Figueruelo E, Abreu N, Casanova JC. 2004. Parasites of Columba livia (Aves: Columbiformes) in Tenerife (Canary Islands) and their role in the conservation biology of the Laurel pigeons. Parasite. 11(3):311–316. ISSN: 1776-1042. https://doi.org/10.1051/parasite/2004113311
GODFREY RD, Fedynich AM, Pence DB. 1987. Quantification of hematozoa in blood smears. Journal of Wildlife Disease. 23:558–565. ISSN: 0090-3558.
https://doi.org/10.7589/0090-3558-23.4.558
GREEN AW, Sofaer HR, Otis DL, Van Lanen NJ. 2020. Co‐Occurrence and Occupancy of Mourning Doves and Eurasian Collared‐Doves. The Journal of Wildlife Management. 84(4):775-785. ISSN: 1937-2817. https://doi.org/10.1002/jwmg.21835
GUPTA DK, Jahan N, Gupta N. 2011. New records of Haemoproteus and Plasmodium (Sporozoa: Haemosporida) of rock pigeon (Columba livia) in India. Journal of Parasitic Diseases. 35:155–168. ISSN: 0975-0703. https://doi.org/10.1007/s12639-011-0044-5
HAM-DUEÑAS, JG., Chapa-Vargas L, Stracey CM, Huber-Sannwald E. 2017. Haemosporidian prevalence and parasitaemia in the Black-throated sparrow (Amphispiza bilineata) in central-Mexican dryland habitats. Parasitology Research. 116: 2527–2537. ISSN: 1432-1955. https://doi.org/10.1007/s00436-017-5562-3
HAWKINS S, Garner MM, Hartup BK. 2021. Neoplasia in captive cranes. Journal of Zoo and Wildlife Medicine. 52(2):689–697. ISSN: 1937-2825.
https://doi.org/10.1638/2020-0180
HELLARD E, Cumming GS, Caron A, Coe E, Peters JL. 2016. Testing epidemiological functional groups as predictors of avian haemosporidia patterns in southern Africa. Ecosphere. 7(4):1–17. ISSN: 2150-8925. https://doi.org/10.1002/ecs2.1225
HELLGREN O, Waldenstrom J, Bensch S. 2004. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. Journal of Parasitology. 90(4):797–802. ISSN: 0022-3395. https://doi.org/10.1645/ge-184r1
HERNANDEZ-COLINA A., Gonzalez-Olvera M, Lomax E, Townsend F, Maddox A, Hesson JC, Sherlock K, Ward D, Eckley L, Vercoe M, Lopez J, Baylis M. 2021. Blood-feeding ecology of mosquitoes in two zoological gardens in the United Kingdom. Parasites Vectors. 14(249). ISSN: 1756-3305. https://doi.org/10.1186/s13071-021-04735-0
HEYM EC, Kampen H, Krone O, Schäfer M, Werner D. 2019. Molecular detection of vector-borne pathogens from mosquitoes collected in two zoological gardens in Germany. Parasitology Research. 118(3):2097–2105. ISSN: 1432-1955.
https://doi.org/10.1007/s00436-019-06327-5
HUANG X, Huang D, Liang Y, Zhang L, Yang G, Peng Y, Deng W, Dong L. 2020. A new protocol for absolute quantification of haemosporidian parasites in raptors and comparison with current assays. Parasites Vectors. 13:354. ISSN: 1756-3305. https://doi.org/10.1186/s13071-020-04195-y
INUMARU M, Yamada A, Shimizu M, Ono A, Horinouchi M, Shimamoto T, Tsuda Y, Murata K, Sato Y. 2021. Vector incrimination and transmission of avian malaria at an aquarium in Japan: mismatch in parasite composition between mosquitoes and penguins. Malaria Journal. 20(136). ISSN: 14752875. https://doi.org/10.1186/s12936-021-03669-3
KNOWLES SCL, Palinauskas V, Sheldon BC. 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. ISSN: 1420-9101. https://doi.org/10.1111/j.1420-9101.2009.01920.x
KOENIG WD. 2020. What are the competitive effects of invasive species? Forty years of the Eurasian collared-dove in North America. Biological Invasions. 22:3645–3652. ISSN: 1573-1464. https://doi.org/10.1007/s10530-020-02350-1
LEE KA, Martin LB, Hasselquist D, Ricklefs RE, Wikelski M. 2006. Contrasting adaptive immune defenses and blood parasite prevalence in closely related Passer sparrows. Oecologia. 150:383–392. ISSN: 1432-1939. https://doi.org/10.1007/s00442-006-0537-6
LEGA J, Brown HE, Barrera R. 2017. Aedes aegypti (Diptera: Culicidae) abundance model improved with relative humidity and precipitation-driven egg hatching. Journal of medical entomology. ISSN: 00222585. 54(5):1375-1384.
https://doi.org/10.1093/jme/tjx077
LOISEAU C, Harrigan RJ, Cornel AJ, Guers SL, Dodge M, Marzec T, Carlson JS, Seppi B, Ravinder NM. 2012. First Evidence and Predictions of Plasmodium Transmission in Alaskan Bird Populations. Plos One. ISSN: 1932-6203.
https://dx.doi.org/10.1371%2Fjournal.pone.0044729
LONGMIRE JL, Lewis AK, Brown NC, Buckingham JM, Clark LM, Jones MD, Meincke LJ, Meyne J, Ratliff RL, Ray FA, Wagner RP, Moyzis RK. 1988. Isolation and molecular characterization of a highly polymorphic centromeric tandem repeat in the family Falconidae. Genomics. 2(1):14–24. ISSN: 0888-7543. https://doi.org/10.1016/0888-7543(88)90104-8
LYNTON‐JENKINS JG, Bründl AC, Cauchoix M, Lejeune LA, Sallé L, Thiney AC, Russell AF, Chaine AS, Bonneaud C. 2020. Contrasting the seasonal and elevational prevalence of generalist avian haemosporidia in co‐occurring host species. Ecology and evolution. 10(12):6097–6111. ISSN: 2045-7758.
https://doi.org/10.1002/ece3.6355
MARTÍNEZ-PÉREZ P, Hyndman TH, Fleming PA, Vaz PK, Ficorilli NP, Wilks CR. 2021. A widespread novel gammaherpesvirus in apparently healthy wild quokkas (Setonix brachyurus): a threatened and endemic wallaby of western Australia. Journal of Zoo and Wildlife Medicine. 52(2):592–603. ISSN: 1937-2825.
https://doi.org/10.1638/2020-0029
MURIEL, J. 2020. Evaluación ecofisiológica de las infecciones por hemosporidios sanguíneos en aves. Ecosistemas. 29(2):1979. ISSN: ISSN 1697-2473. https://doi.org/10.7818/ECOS.1979
NATH T, Bhuiyan M, Alam M. 2014. A study on the presence of leucocytozoonosis in pigeon and chicken of hilly districts of Bangladesh. Biological Sciences and Pharmaceutical Research. 2(2): 13–18. ISSN: 2350-1588.
https://journalissues.org/ibspr/wp-content/uploads/sites/6/2014/02/Nath-et-al.pdf
NEBEL C, Harl J, Pajot A, Weissenböck H, Amar A, Sumasgutner P. 2020. High prevalence and genetic diversity of Haemoproteus columbae (Haemosporida: Haemoproteidae) in feral pigeons Columba livia in Cape Town, South Africa. Parasitology Research. 119:447–463. ISSN: 1432-1955.
https://doi.org/10.1007/s00436-019-06558-6
NODEN, BH, Bradt, DL, Sanders, JD. 2021. Mosquito-borne parasites in the Great Plains: searching for vectors of nematodes and avian malaria parasites. Acta Tropica. 213:105735. ISSN:0001-706X.
https://doi.org/10.1016/j.actatropica.2020.105735
OTIS DL, Schulz JH, Miller D, Mirarchi RE, Baskett TS. 2020. Mourning Dove (Zenaida macroura), version 1.0. En Birds of the World (A. F. Poole, Editor). Cornell Lab of Ornithology, Ithaca, NY, USA. https://doi.org/10.2173/bow.moudov.01
PALINAUSKAS V, Valkunias G, Bolshakov CV, Bensch S. 2011. Plasmodium relictum (lineage SGS1) and Plasmodium ashfordi (lineage GRW2): The effects of the co-infection on experimentally infected passerine birds. Experimental Parasitology. 127(2):527–33. ISSN: 00144894. https://doi.org/10.1016/j.exppara.2010.10.007
PATERSON S, Lello J .2003. Mixed models: getting the best use of parasitological data. Trends in Parasitology. 19:370–375. ISSN: 1471-5007.
https://doi.org/10.1016/s1471-4922(03)00149-1
QUIAGEN. 2021. DNeasy Blood & Tissue Kits Handbook. https://www.qiagen.com/us/resources/resourcedetail?id=68f29296-5a9f-40fa-8b3d-1c148d0b3030&lang=en
R CORE TEAM (4.0.5). 2021. [Software]. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/
REICZIGEL J, Marozzi M, Fábián I, Rózsa L. 2019. Biostatistics for parasitologists – a primer to Quantitative Parasitology. Trends in Parasitology. 35(4)277–281. ISSN: 1471-5007. https://doi.org/10.1016/j.pt.2019.01.003
REINOSO-PÉREZ MT, Canales-Delgadillo JC, Chapa-Vargas L, Riego-Ruiz L .2016. Haemosporidian parasite prevalence, parasitemia, and diversity in three resident bird species at a shrubland dominated landscape of the Mexican highland plateau. Parasites Vectors. 9:307. ISSN: 1756-3305.
https://doi.org/10.1186/s13071-016-1569-3
ROCHA SL, Guimarães JP, Barbosa De Oliveira, CY, Nader C. 2021. Current status of Brazilian scientific production on non-native species. Ethology Ecology & Evolution. ISSN: 0394-9370. https://doi.org/10.1080/03949370.2020.1870570
RÓZSA L, Reiczigel J, Majoros G. 2000. Quantifying parasites in samples of hosts. Journal of Parasitology. 86:228–232. ISSN: 0022-3395. https://doi.org/10.1645/0022-3395(2000)086[0228:qpisoh]2.0.co;2
SALAZAR-BORUNDA MA, Martínez-Guerrero JH, Pereda-Solís ME, Delgado-León T, Sierra-Franco D. 2019. Phenotypic variation in eurasian collared dove (Streptopelia decaocto Frivaldszky) in Durango, Mexico. AgroProductividad. 12(10). ISSN: 2594-0252. http://dx.doi.org/10.32854/agrop.vi0.1461
SANTIAGO-ALARCÓN D, Carbó-Ramírez P. 2015. Parásitos sanguíneos de malaria y géneros relacionados (Orden: Haemosporida) en aves de México: recomendaciones metodológicas para campo y laboratorio. Ornitología Neotropical. 26(1):59–77. ISSN 1075–4377. https://journals.sfu.ca/ornneo/index.php/ornneo/article/view/13
SCHUMM, YR, Bakaloudis D, Barboutis C, Cecere JG, Eraud C, Fischer D, Hering J, Hillerich K, Lormée H, Mader V, Masello JF, Metzger B, Rocha G, Spina F, Quillfeldt, P. 2021. Prevalence and genetic diversity of avian haemosporidian parasites in wild bird species of the order Columbiformes. Parasitology Research. 120(4):1405-1420. ISSN: 1432-1955. https://doi.org/10.1007/s00436-021-07053-7
STARKLOFF NC, Turner WC, FitzGerald AM, Oftedal MC, Martinsen ES, Kirchman JJ. 2021. Disentangling the effects of host relatedness and elevation on haemosporidian parasite turnover in a clade of songbirds. Ecosphere. 12(5): e03497. ISSN: 2150-8925.
https://doi.org/10.1002/ecs2.3497 https://doi.org/10.1002/ecs2.3497
STILMMELMAYR R, Stefani LM, Thrall MA, Landers K, Revan F, Miller A, Beckstead R, Gerhold R. 2012. Trichomonosis in free-ranging Eurasian collared doves (Streptopelia decaocto) and African collared dove hybrids (Streptopelia risoria) in the Caribbean and description of ITS -1 region genotypes. Avian Diseases. 56(2):451–455. ISSN: 0005-2086. https://doi.org/10.1637/9905-082311-case.1
TAVASSOLI M, Esmaeilnejad B, Malekifard F, Mardani K. 2018. PCR-RFLP detection of Haemoproteus spp. (Haemosporida: Haemoproteidae) in pigeon blood samples from Iran. Bulgarian Journal of Veterinarian Medicine. 21(4):429–435. ISSN: 1311-1477. https://doi.org/10.15547/bjvm.2014
VALKIŪNAS G, Iezhova TA. 2017. Exo-erythrocytic development of avian malaria and related haemosporidian parasites. Malaria Journal. 16(1):1–24. ISSN: 14752875. https://doi.org/10.1186/s12936-017-1746-7
VALKIŪNAS G, Iezhova TA. 2018. Keys to the avian malaria parasites. Malaria Journal. 17(1):1-24. ISSN: 1475-2875. https://doi.org/10.1186/s12936-018-2359-5
VENABLES WN, Ripley BD. 2002. Modern Applied Statistics with S, Fourth edition. Springer, New York. ISBN 0-387-95457-0. https://www.stats.ox.ac.uk/pub/MASS4/
VILLALVA-PASILLAS D, Medina JP, Soriano-Vargas E, Martínez-Hernández DA, García-Conejo M, Galindo-Sánchez KP, Sánchez-Jasso JM, Martín-Talavera-Rojas M, Salgado-Miranda C. 2020. Haemoparasites in endemic and non-endemic passerine birds from central Mexico highlands. International Journal for Parasitology: Parasites and Wildlife. 11:88–92. ISSN: 2213-2244.
https://doi.org/10.1016/j.ijppaw.2019.12.007
WHITE EM, Greiner EC, Bennett GF, Herman CM. 1978. Distribution of hematozoa of Neotropical birds. Revista de Biología Tropical. 1: 43–102. ISSN: 0034-7744.
https://pubmed.ncbi.nlm.nih.gov/108771/
WILEY-BLACKWELL, New York. USA. ISBN: 978-1-444-31619-3. https://www.wiley.com/en-us/Atlas+of+Clinical+Avian+Hematology-p-9781444316193
WOOD MJ, Cosgrove CL, Wilkin TA, Sknowles C, Day KP, Sheldon BC. 2007. Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology. 16(15):3263–3273. ISSN: 0962-1083. https://doi.org/10.1111/j.1365-294x.2007.03362.x
YANGA S, Martinez-Gomez JE, Sehgal RNM, Escalante P, Camacho FC, Bell DA. 2011. A preliminary survey for avian pathogens in Columbiformes birds on Socorro Island, Mexico. Pacific Conservation Biology. 17(1):11–20. ISSN: 1038-2097. https://doi.org/10.1071/PC110011
YOSHIMOTO M, Ozawa K, Kondo H, Echigoya Y, Shibuya H, Sato Y, Sehgal RN. 2021. A fatal case of a captive snowy owl (Bubo scandiacus) with Haemoproteus infection in Japan. Parasitology Research. 120(1):277–288. ISSN: 1432-1955. https://doi.org/10.1007/s00436-020-06972-1
