Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-24T23:37:19.179Z Has data issue: false hasContentIssue false
  • English
  • Français

Avian haemosporidian infections in rufous-collared sparrows in an Andean dry forest: diversity and factors related to prevalence and parasitaemia

Published online by Cambridge University Press:  26 December 2018

Héctor Cadena-Ortiz ,
Juan S. Mantilla ,
Juan Rivero de Aguilar ,
Diana Flores ,
Daniela Bahamonde ,
Nubia E. Matta  and
Elisa Bonaccorso Open the ORCID record for Elisa Bonaccorso [Opens in a new window]
Héctor Cadena-Ortiz
Affiliation:
Centro de Investigación de la Biodiversidad y Cambio Climático (BioCamb), Universidad Tecnológica Indoamérica, Machala y Sabanilla, Quito, Ecuador Pontificia Universidad Católica del Ecuador, 12 de Octubre y Roca, Quito, Ecuador
Juan S. Mantilla
Affiliation:
Departamento de Biología, Grupo de Investigación Caracterización Genética e Inmunología, Sede Bogotá-Facultad de Ciencias, Universidad Nacional de Colombia, Bogotá, Colombia
Juan Rivero de Aguilar
Affiliation:
Centro de Investigación de la Biodiversidad y Cambio Climático (BioCamb), Universidad Tecnológica Indoamérica, Machala y Sabanilla, Quito, Ecuador
Diana Flores
Affiliation:
Centro de Investigación de la Biodiversidad y Cambio Climático (BioCamb), Universidad Tecnológica Indoamérica, Machala y Sabanilla, Quito, Ecuador
Daniela Bahamonde
Affiliation:
Pontificia Universidad Católica del Ecuador, 12 de Octubre y Roca, Quito, Ecuador
Nubia E. Matta
Affiliation:
Departamento de Biología, Grupo de Investigación Caracterización Genética e Inmunología, Sede Bogotá-Facultad de Ciencias, Universidad Nacional de Colombia, Bogotá, Colombia
Elisa Bonaccorso*
Affiliation:
Centro de Investigación de la Biodiversidad y Cambio Climático (BioCamb), Universidad Tecnológica Indoamérica, Machala y Sabanilla, Quito, Ecuador Laboratorio de Biología Evolutiva, Instituto BIOSFERA y Colegio de Ciencias Biológicas y Ambientales, Universidad San Francisco de Quito, Diego de Robles y Vía Interoceánica, 17-1200-841 Quito, Ecuador
*
Author for correspondence: Elisa Bonaccorso, E-mail: ebonaccorso@usfq.edu.ec
Get access Rights & Permissions [Opens in a new window]

Abstract

Despite intensive research during the last few decades, understanding of ecological and physiological factors related to haemosporidian infections in birds is still fragmentary. Since more model organisms are needed in order to understand these infections in the wild, we analysed avian haemosporidian infections in the rufous-collared sparrow (Zonotrichia capensis, Emberizidae) in a dry forest of the Ecuadorian Andes. Parasite diversity was screened using molecular and morphological approaches. By molecular diagnosis, we identified three linages that were phylogenetically placed in the context of molecular haemosporidian diversity and associated with a morphospecies. By microscopy, we identified five described morphospecies and one additional undescribed morphospecies. We found that avian haemosporidian prevalence on the study site was 76.3%. Additionally, we used a series of generalized linear models to explore the potential relationship of parasite prevalence and parasitaemia with a set of variables related to physiological and environmental conditions. Although our results revealed associations of haemosporidian infections with precipitation, age and sampling site, the models only explained a small fraction of the variation.

Keywords

Avian malariacoinfectionsEcuadorHaemoproteusHaemosporidaNeotropicsPlasmodium
Type
Research Article
Information
Parasitology , Volume 146 , Issue 6 , May 2019 , pp. 765 - 773
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Present address: Instituto de Salud y Ambiente, Universidad El Bosque, Bogotá−110121, Colombia.

References

Asghar, M, Hasselquist, D, Hansson, B, Zehtindjiev, P, Westerdahl, H and Bensch, S (2015) Hidden cost of infection: chronic malaria accelerates telomere degradation and senescence in wild birds. Science 347, 436–438.Google Scholar
Bennett, GF, Bishop, MA and Peirce, MA (1993) Checklist of the avian species of Plasmodium marchiafava & Celli, 1885 (Apicomplexa) and their distribution by avian family and Wallacean life zones. Systematic Parasitology 26, 171–179.Google Scholar
Bensch, S, Hellgren, O and Pérez-Tris, J (2009) Malavi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources 9, 1353–1358.Google Scholar
Bernotienė, R, Palinauskas, V, Iezhova, I, Murauskaitė, D and Valkiūnas, G (2016) Avian haemosporidian parasites (Haemosporida): a comparative analysis of different polymerase chain reaction assays in detection of mixed infections. Experimental parasitology 163, 31–37.Google Scholar
Cadena-Ortiz, H, Varela, S, Bahamonde-Vinueza, D, Freile, JF and Bonaccorso, E (2015) Birds of Bosque Protector Jerusalem, Guayllabamba Valley, Ecuador. Check List (Luis Felipe Toledo) 11, 1770.Google Scholar
Carlson, JS, Nelms, B, Barker, CM, Reisen, WK, Sehgal, RNM and Cornel, AJ (2018) Avian malaria coinfections confound infectivity and vector competence assays of Plasmodium homopolare. Parasitology Research 117, 2385–2394.Google Scholar
Chomczynski, P (1993) A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques 15, 532–537.Google Scholar
Coon, CCA, García-Longoria, L, Martin, LB, Magallanes, S, de Lope, F and Marzal, A (2016) Malaria infection negatively affects feather growth rate in the housesparrow (Passer domesticus). Journal of Avian Biology 47, 779–787.Google Scholar
Cornet, S, Nicot, A, Rivero, A and Gandon, S (2014) Evolution of plastic transmission strategies. PLoS Pathogens 10, e1004308.Google Scholar
Cosgrove, CL, Wood, MJ, Day, KP and Sheldon, BC (2008) Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. Journal of Animal Ecology 77, 540–548.Google Scholar
Davidar, P and Morton, ES (1993) Living with parasites: prevalence of a blood parasite and its effect on survivorship in the purple martin. The Auk 110, 109–116.Google Scholar
Eldridge, BF (2005) Mosquitoes, the Culicidae. In Marquardt, WC (ed.), Biology of Disease Vectors 2ª Ed. New York, USA: Academic Press, pp. 95–111.Google Scholar
Ellis, VA, Medeiros, MCI, Collins, MD, Sari, EHR, Coffey, ED, Dickerson, RC, Lugarini, C, Stratford, JA, Henry, DR, Merrill, L, Matthews, AE, Hanson, AA, Roberts, JR, Joyce, M, Kunkel, MR and Ricklefts, RE (2017) Prevalence of avian haemosporidian parasites is positively related to the abundance of host species at multiple sites within a region. Parasitology Research 116, 73–80.Google Scholar
Escallón, C, Weinstein, NM, Tallant, JA, Wojtenek, W, Rodríguez-Saltos, CA, Bonaccorso, E and Moore, IT (2016) Testosterone and Haemosporidian parasites along a Tropical elevational gradient in Rufous-collared sparrows, (Zonotrichia capensis). Journal of Experimental Zoology 00A, 1–10.Google Scholar
Fecchio, A, Svensson-Coelho, M, Bell, J, Ellis, VA, Medeiros, MC, Trisos, CH, Blake, JG, Loiselle, BA, Tobias, JA, Fanti, R, Coffey, ED, de Faria, IP, Pinho, JB, Felix, G, Braga, EM, Anciaes, M, Tkach, V, Bates, J, Witt, C, Weckstein, JD, Ricklefts, RE and Farias, IP (2017) Host associations and turnover of haemosporidian parasites in manakins (Aves: Pipridae). Parasitology 144, 984–993.Google Scholar
Ferraguti, M, Martínez-de la Puente, J, Bensch, S, Roiz, D, Ruiz, S, Viana, DS, Soriguer, RC and Figuerola, J (2017) Ecological determinants of avian malaria infections: an integrative analysis at landscape, mosquito and vertebrate community levels. Journal of Animal Ecology 87, 1–14.Google Scholar
Gabaldón, A, Ulloa, G and Zerpa, N (1988) Plasmodium cathemerium, cepa de Icteridae inoculable a palomas, patos y pavos; sus vectores y utilidad en enseñanza e investigación. Boletín de la Dirección de Malariología y Saneamiento Ambiental 28, 53–68.Google Scholar
Galen, SC and Witt, CC (2014) Diverse avian malaria and other haemosporidian parasites in Andean house wrens: evidence for regional co-diversification by host-switching. Journal of Avian Biology 45, 374–386.Google Scholar
Garvin, MC, Homer, BL and Greiner, EC (2003) Pathogenicity of Haemoproteus danilewskyi, Kruse, 1890, in blue jays (Cyanocitta cristata). Journal of Wildlife Diseases 39, 161–169.Google Scholar
González, AD, Lotta, IA, García, LF, Moncada, LI and Matta, NE (2015) Avian haemosporidians from Neotropical highlands: evidence from morphological and molecular data. Parasitology International 64, 48–59.Google Scholar
Green, AJ (2001) Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82, 1473–1483.Google Scholar
Ham-Dueñas, JG, Chapa-Vargas, L, Stracey, CM and 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.Google Scholar
Jones, MR, Cheviron, ZA and Carling, MD (2013) Spatial patterns of avian malaria prevalence in Zonotrichia capensis on the western slope of the Peruvian Andes. Journal of Parasitology 99, 903–905.Google Scholar
Jones, MR, Cheviron, ZA and Carling, MD (2014) Variation in positively selected major histocompatibility complex class I loci in rufous-collared sparrows (Zonotrichia capensis). Immunogenetics 66, 693–704.Google Scholar
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Mentjies, P and Drummond, A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics (Oxford, England) 28, 1647–1649.Google Scholar
Knowles, SCL, Wood, MJ, Alves, R, Wilkin, TA, Bensch, S and Sheldon, BC (2011) Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population. Molecular Ecology 20, 1062–1076.Google Scholar
Lanfear, R, Frandsen, PB, Wright, AM, Senfeld, T and Calcott, B (2016) Partitionfinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.Google Scholar
Larkin, MA, Blackshields, G, Brown, NP, Chenna, R, McGettigan, PA, McWilliam, H, Valentin, F, Wallace, IM, Wilm, A, Lopez, R, Thompson, JD, Gibson, TJ and Higgins, DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics (Oxford, England) 23, 2947–2948.Google Scholar
Levin, II, Zwiers, P, Deem, SL, Geest, EA, Higashiguchi, JM, Iezhova, TA, Jimenez-Uzcategui, GD, Kim, H, Morton, JP, Perlut, NG, Renfrew, RB, Sari, EHR, Valkiūnas, G and Parker, PG (2013) Multiple lineages of avian malaria parasites (Plasmodium) in the Galapagos Islands and evidence for arrival via migratory birds. Conservation Biology 27, 1366–1377.Google Scholar
Librado, P and Rozas, J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics (Oxford, England) 25, 1451–1452.Google Scholar
MAE (Ministerio del Ambiente del Ecuador) (2013) Sistema de Clasificación de los Ecosistemas del Ecuador Continental. Quito, Ecuador: Subsecretaría de Patrimonio Natural.Google Scholar
Mantilla, S, González, AD, Lotta, IA, Moens, M, Pacheco, A, Escalante, AA, Valkiūnas, G, Moncada, LI, Pérez-Tris, J and Matta, NE (2016) Haemoproteus erythrogravidus n. sp. (Haemosporida, Haemoproteidae): description and molecular characterization of a widespread blood parasite of birds in South America. Acta Tropica 159, 86–94.Google Scholar
Martinsen, ES, Sidor, IF, Flint, S, Cooley, J and Pokras, MA (2007) Morphologically defined subgenera of Plasmodium from avian hosts: test of monophyly by phylogenetic analysis of two mitochondrial genes. Parasitology 134, 483–490.Google Scholar
Marzal, A, Bensch, S, Reviriego, M, Balbontin, J and de Lope, F (2008) Effects of malaria double infection in birds: one plus one is not two. Journal of Evolutionary Biology 21, 979–987.Google Scholar
Marzal, A, García-Longoria, L, Cárdenas Callirgos, JM and Sehgal, RNM (2015) Invasive avian malaria as an emerging parasitic disease in native birds of Peru. Biological Invasions 17, 39–45.Google Scholar
Moore, IT, Bonier, and Wingfield, FJC (2005) Reproductive asynchrony and population divergence between two tropical bird populations. Behavioral Ecology 16, 755–762.Google Scholar
Mullen, GR (2002) Biting midges (Ceratopogonidae). In Mullen, G and Durden, L (eds), Medical and Veterinary Entomology. San Diego, USA: Academic Press, pp. 163–183.Google Scholar
Oakgrove, KS, Harrigan, RJ, Loiseau, C, Giers, S, Seppi, B and Sehgal, RNM (2014) Distribution, diversity and drivers of blood-borne parasite coinfections in Alaskan bird populations. International Journal for Parasitology 44, 717–727.Google Scholar
Pacheco, MA, Matta, NE, Valkiunas, G, Parker, PG, Mello, B, Stanley, CE Jr, Lentino, M, Garcia-Amado, MA, Cranfield, M, Pond, SL and Escalante, AA (2018) Mode and rate of evolution of haemosporidian mitochondrial genomes: timing the radiation of avian parasites. Molecular Biology Evolution 35, 383–403.Google Scholar
Pérez-Tris, J, Hasselquist, D, Hellgren, O, Krizanauskiene, A, Waldenström, J and Bensch, S (2005) What are malaria parasites? Trends in Parasitology 21, 209–211.Google Scholar
R Development Core Team (2008) A language and environment for statistical computing. R Foundation for Statistical Computing 1, 2673.Google Scholar
Reiczigel, J (2003) Confidence intervals for the binomial parameter: some new considerations. Statistics in Medicine 22, 611–621.Google Scholar
Reiczigel, J and Rózsa, L (2005) Quantitative Parasitology 3.0. Budapest.Google Scholar
Reinoso-Pérez, MT, Canales-Delgadillo, JC, Chapa-Vargas, L and 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 and Vectors 9, 307.Google Scholar
Ridgely, RS and Greenfield, PJ (2001) The Birds of Ecuador. Ithaca, USA: Cornell University Press.Google Scholar
Rising, J and Jaramillo, A (2017). Rufous-collared sparrow (Zonotrichia capensis). In: del Hoyo, J, Elliott, A, Sargatal, J, Christie, DA and de Juana, E. (eds), Handbook of the Birds of the World Alive. Barcelona: Lynx Edicions. Available at http://www.hbw.com/node/61910 (accessed 23 August 2017).Google Scholar
Ronquist, F and Huelsenbeck, JP (2003) Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England) 19, 1572–1574.Google Scholar
Rózsa, L, Reiczigel, J and Majoros, G (2000) Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228–232.Google Scholar
Santiago-Alarcón, D, Palinauskas, V and Schaefer, HM (2012) Diptera vectors of avian Haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biological Reviews 87, 928–964.Google Scholar
Stephens, M and Donnelly, P (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. American Journal of Human Genetics 73, 1162–1169.Google Scholar
Valkiūnas, G (2005) Avian Malaria Parasites and Other Haemosporidia. Boca Raton, USA: CRC Press.Google Scholar
Valkiūnas, G and Iezhova, T (2018) Keys to the avian malaria parasites. Malaria Journal 17, 212.Google Scholar
Vanstreels, RET, da Silva-Filho, RP, Kolesnikovas, CKM, Bhering, RCC, Ruoppolo, V, Epiphanio, S, Amaku, M, Junior, FCF and Martins Braga, EM (2015) Epidemiology and pathology of avian malaria in penguins undergoing rehabilitation in Brazil. Veterinary Research 46, 30.Google Scholar
Venables, WN and Ripley, BD (2002) MASS: modern applied statistics with S. Issues of Accuracy and Scale 868.Google Scholar
Waldenström, J, Bensch, S, Hasselquist, D and Ostman, O (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology 90, 191–194.Google Scholar
Walther, EL, Valkiūnas, G, González, AD, Matta, NE, Ricklefs, RE, Cornel, A and Sehgal, RNM (2014) Description, molecular characterization, and patterns of distribution of a widespread New World avian malaria parasite (Haemosporida: Plasmodiidae), Plasmodium (novyella) homopolare sp. nov. Parasitology Research 113, 3319–3332.Google Scholar
Wood, MJ, Cosgrove, CL, Wilkin, TA, Knowles, SCL, Day, KP and Sheldon, BC (2007) Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology 16, 3263–3273.Google Scholar