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Beta diversity, prevalence, and specificity of avian haemosporidian parasites throughout the annual cycle of Chilean Elaenia (Elaenia chilensis), a Neotropical austral migrant

Published online by Cambridge University Press:  27 September 2022

Alan Fecchio*
Affiliation:
Programa de Pós-graduação em Ecologia e Conservação da Biodiversidade, Universidade Federal de Mato Grosso, Cuiabá, MT, Brazil Laboratorio de Ecología de Aves, Centro de Investigación Esquel de Montaña y Estepa Patagónica (CIEMEP), CONICET – Universidad Nacional de la Patagonia San Juan Bosco, Esquel, Chubut, Argentina
Raphael I. Dias
Affiliation:
Faculdade de Ciências da Educação e Saúde, Centro Universitário de Brasília, Brasília, DF, Brazil
Gabriel M. De La Torre
Affiliation:
Programa de Pós-graduação em Ecologia e Conservação, Universidade Federal do Paraná, Curitiba, PR, Brazil
Jeffrey A. Bell
Affiliation:
Department of Biology, University of North Dakota, Grand Forks, ND, USA
M. Cecilia Sagario
Affiliation:
Grupo de Ecología Terrestre de Neuquén, Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA–CONICET and UNComahue), and Centro de Ecología Aplicada del Neuquén (CEAN), Junín de los Andes, Neuquén, Argentina
Cristian A. Gorosito
Affiliation:
Laboratorio de Ecología de Aves, Centro de Investigación Esquel de Montaña y Estepa Patagónica (CIEMEP), CONICET – Universidad Nacional de la Patagonia San Juan Bosco, Esquel, Chubut, Argentina
Carolina C. dos Anjos
Affiliation:
Programa de Pós-graduação em Medicina Tropical, Faculdade de Medicina, Universidade de São Paulo, São Paulo, SP, Brazil
Camile Lugarini
Affiliation:
Centro Nacional de Pesquisa e Conservação de Aves Silvestres, Instituto Chico Mendes de Conservação da Biodiversidade, Florianópolis, SC, Brazil
Vítor Q. Piacentini
Affiliation:
Departamento de Biologia e Zoologia & Programa de Pós-graduação em Zoologia, Instituto de Biociências, Universidade Federal de Mato Grosso, Cuiabá, MT, Brazil
João B. Pinho
Affiliation:
Programa de Pós-graduação em Ecologia e Conservação da Biodiversidade, Universidade Federal de Mato Grosso, Cuiabá, MT, Brazil
Karin Kirchgatter
Affiliation:
Programa de Pós-graduação em Medicina Tropical, Faculdade de Medicina, Universidade de São Paulo, São Paulo, SP, Brazil Laboratório de Bioquímica e Biologia Molecular, Superintendência de Controle de Endemias, São Paulo, SP, Brazil
Robert E. Ricklefs
Affiliation:
Department of Biology, University of Missouri-St. Louis, St. Louis, MO, USA
Fabio Schunck
Affiliation:
Brazilian Committee for Ornithological Records – CBRO, Brazil
Victor R. Cueto
Affiliation:
Laboratorio de Ecología de Aves, Centro de Investigación Esquel de Montaña y Estepa Patagónica (CIEMEP), CONICET – Universidad Nacional de la Patagonia San Juan Bosco, Esquel, Chubut, Argentina
*
Author for correspondence: Alan Fecchio, E-mail: alanfecchio@gmail.com

Abstract

Migratory birds are implicated in dispersing haemosporidian parasites over great geographic distances. However, their role in sharing these vector-transmitted blood parasites with resident avian host species along their migration flyway is not well understood. We studied avian haemosporidian parasites in 10 localities where Chilean Elaenia, a long-distance Neotropical austral migrant species, spends part of its annual cycle to determine local parasite transmission among resident sympatric host species in the elaenia's distributional range across South America. We sampled 371 Chilean Elaenias and 1,818 birds representing 243 additional sympatric species from Brazilian wintering grounds to Argentinian breeding grounds. The 23 haemosporidian lineages found in Chilean Elaenias exhibited considerable variation in distribution, specialization, and turnover across the 10 avian communities in South America. Parasite lineage dissimilarity increased with geographic distance, and infection probability by Parahaemoproteus decreased in localities harbouring a more diverse haemosporidian fauna. Furthermore, blood smears from migrating Chilean Elaenias and local resident avian host species did not contain infective stages of Leucocytozoon, suggesting that transmission did not take place in the Brazilian stopover site. Our analyses confirm that this Neotropical austral migrant connects avian host communities and transports haemosporidian parasites along its distributional range in South America. However, the lack of transmissive stages at stopover site and the infrequent parasite lineage sharing between migratory host populations and residents at breeding and wintering grounds suggest that Chilean Elaenias do not play a significant role in dispersing haemosporidian parasites, nor do they influence local transmission across South America.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Alcala, N, Jenkins, T, Christe, P and Vuilleumier, S (2017) Host shift and cospeciation rate estimation from co-phylogenies. Ecology Letters 20, 10141024.CrossRefGoogle ScholarPubMed
Altizer, S, Bartel, R and Han, BA (2011) Animal migration and infectious disease risk. Science 331, 296302.CrossRefGoogle ScholarPubMed
Anjos, CC, Chagas, CRF, Fecchio, A, Schunck, F, Costa-Nascimento, MJ, Monteiro, EF, Mathias, BS, Bell, JA, Guimarães, LO, Comiche, KJM, Valkiūnas, G and Kirchgatter, K (2021) Avian malaria and related parasites from resident and migratory birds in the Brazilian Atlantic Forest, with description of a new Haemoproteus species. Pathogens 10, 103.CrossRefGoogle ScholarPubMed
Barrow, LN, McNew, SM, Mitchell, N, Galen, SC, Lutz, HL, Skeen, H, Valqui, T, Weckstein, JD and Witt, CC (2019) Deeply conserved susceptibility in a multi-host, multi-parasite system. Ecology Letters 22, 987998.CrossRefGoogle Scholar
Baselga, A (2010) Partitioning the turnover and nestedness components of beta diversity. Global Ecology and Biogeography 19, 134143.CrossRefGoogle Scholar
Baselga, A and Orme, CDL (2012) betapart: an R package for the study of beta diversity. Methods in Ecology and Evolution 3, 808812.CrossRefGoogle Scholar
Bates, D, Mächler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 148.CrossRefGoogle Scholar
Bauer, S and Hoye, BJ (2014) Migratory animals couple biodiversity and ecosystem functioning worldwide. Science 344, 1242552.CrossRefGoogle ScholarPubMed
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, 13531358.CrossRefGoogle ScholarPubMed
Bobeva, A, Zehtindjiev, P, Ilieva, M, Dimitrov, D, Mathis, A and Bensch, S (2015) Host preferences of ornithophilic biting midges of the genus Culicoides in the Eastern Balkans. Medical and Veterinary Entomology 29, 290296.CrossRefGoogle ScholarPubMed
Bravo, SP, Cueto, VR and Gorosito, CA (2017) Migratory timing, rate, routes and wintering areas of white-crested Elaenia (Elaenia albiceps chilensis), a key seed disperser for Patagonian Forest regeneration. PLoS ONE 12, e0170188.CrossRefGoogle Scholar
Canard, EF, Mouquet, N, Mouillot, D, Stanko, M, Miklisova, D and Gravel, D (2014) Empirical evaluation of neutral interactions in host-parasite networks. The American Naturalist 183, 468479.CrossRefGoogle ScholarPubMed
Chakarov, N, Kampen, H, Wiegmann, A, Werner, D and Bensch, S (2020) Blood parasites in vectors reveal a united blackfly community in the upper canopy. Parasites and Vectors 13, 309.CrossRefGoogle ScholarPubMed
Cueto, VR and Gorosito, CA (2018) Seasonal changes in bird assemblages of a forest-steppe ecotone in North Patagonia. Ornitología Neotropical 29, 349358.Google Scholar
Cueto, VR, Sagario, MC and Lopez de Casenave, J (2016) Do migrating white-crested Elaenia (Elaenia albiceps chilensis) use stopover sites en route to their breeding areas? Evidence from the central Monte desert, Argentina. Emu 116, 301304.CrossRefGoogle Scholar
de Angeli Dutra, D, Fecchio, A, Braga, ÉM and Poulin, R (2021 a) Haemosporidian taxonomic composition, network centrality and partner fidelity between resident and migratory avian hosts. Oecologia 197, 501509.CrossRefGoogle ScholarPubMed
de Angeli Dutra, D, Filion, A, Fecchio, A, Braga, ÉM and Poulin, R (2021 b) Migrant birds disperse haemosporidian parasites and affect their transmission in avian communities. Oikos 130, 979988.CrossRefGoogle Scholar
De La Torre, GM, Fecchio, A, Bell, JA and Campião, KM (2022) Host evolutionary history rather than avian functional traits drives the Plasmodium regional assembly in the Atlantic Forest. Functional Ecology 38, 18731886.CrossRefGoogle Scholar
Dray, S and Dufour, A (2007) The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software 22, 120.CrossRefGoogle Scholar
Dufour, P, Descamps, S, Chantepie, S, Renaud, J, Guéguen, M, Shiffers, K, Thuiller, W and Lavergne, S (2019) Reconstructing the geographic and climatic origins of long-distances bird migrations. Journal of Biogeography 47, 155166.CrossRefGoogle Scholar
Emmenegger, T, Bauer, S, Dimitrov, D, Marin, JO, Zehtindjiev, P and Hahn, S (2018) Host migration strategy and blood parasite infections of three sparrow species sympatrically breeding in Southeast Europe. Parasitology Research 117, 37333741.CrossRefGoogle ScholarPubMed
Fallon, SM, Ricklefs, RE, Swanson, BL and Bermingham, E (2003) Detecting avian malaria: an improved polymerase chain reaction diagnostic. The Journal of Parasitology 89, 10441047.CrossRefGoogle ScholarPubMed
Fecchio, A, Wells, K, Bell, JA, Tkach, VV, Lutz, HL, Weckstein, JD, Clegg, SM and Clark, NJ (2019 a) Climate variation influences host specificity in avian malaria parasites. Ecology Letters 22, 547557.CrossRefGoogle ScholarPubMed
Fecchio, A, Bell, JA, Pinheiro, RBP, Cueto, VR, Gorosito, CA, Lutz, HL, Gaiotti, MG, Paiva, LV, França, LF, Toledo-Lima, G, Tolentino, M, Pinho, JB, Tkach, VV, Fontana, CS, Grande, JM, Santíllan, MA, Caparroz, R, Roos, AL, Bessa, R, Nogueira, W, Moura, T, Nolasco, EC, Comiche, KJM, Kirchgatter, K, Guimarães, LO, Dispoto, JH, Marini, , Weckstein, JD, Batalha-Filho, H and Collins, MD (2019 b) Avian host composition, local speciation and dispersal drive the regional assembly of avian malaria parasites in South American birds. Molecular Ecology 28, 26812693.CrossRefGoogle ScholarPubMed
Fecchio, A, Lima, MR, Bell, JA, Schunck, F, Corrêa, AH, Beco, R, Jahn, AE, Fontana, CS, Silva, TH, Repenning, M, Braga, ÉM, Garcia, JE, Lugarini, C, Silva, JCR, Andrade, LHM, Dispoto, JH, Anjos, CC, Weckstein, JD, Kirchgatter, K, Ellis, VA, Ricklefs, RE and De La Torre, GM (2021 a) Loss of forest cover and host functional diversity increases prevalence of avian malaria in the Atlantic Forest. International Journal for Parasitology 51, 719728.CrossRefGoogle ScholarPubMed
Fecchio, A, Clark, NJ, Bell, JA, Skeen, H, Lutz, HL, De La Torre, GM, Vaughan, JA, Tkach, VV, Schunck, F, Ferreira, FC, Braga, ÉM, Lugarini, C, Wamiti, W, Dispoto, JH, Galen, SC, Kirchgatter, K, Sagario, MC, Cueto, VR, González-Acuña, D, Inumaru, M, Sato, Y, Schumm, YR, Quillfeldt, P, Pellegrino, I, Dharmarajan, G, Gupta, P, Robin, VV, Ciloglu, A, Yildirim, A, Huang, X, Chapa-Vargas, L, Álvarez-Medizábal, P, Santiago-Alarcon, D, Drovetski, SV, Hellgren, O, Voelker, G, Ricklefs, RE, Hackett, SJ, Collins, MD, Weckstein, JD and Wells, K (2021 b) Global drivers of avian haemosporidian infections vary across zoogeographical regions. Global Ecology and Biogeography 30, 23932406.CrossRefGoogle Scholar
Felsenstein, J (2004) Inferring Phylogenies, 1st Edn. Sunderland, USA: Sinauer Associates, Inc.Google Scholar
Figuerola, J and Green, AJ (2000) Haematozoan parasites and migratory behaviour in waterfowl. Evolutionary Ecology 14, 143153.CrossRefGoogle Scholar
Galen, SC, Borner, J, Martinsen, ES, Schaer, J, Austin, CC, West, CJ and Perkins, SL (2018) The polyphyly of Plasmodium: comprehensive phylogenetic analyses of the malaria parasites (order Haemosporida) reveal widespread taxonomic conflict. Royal Society Open Science 5, 171780.CrossRefGoogle ScholarPubMed
Gotelli, NJ (2000) Null model analysis of species co-occurrence patterns. Ecology 81, 26062621.CrossRefGoogle Scholar
Grafen, A (1989) The phylogenetic regression. Philosophical Transactions of the Royal Society B Biological Sciences 326, 119157.Google ScholarPubMed
Gutiérrez, JS, Piersma, T and Thieltges, DW (2019) Micro- and macroparasite species richness in birds: the role of host life history and ecology. Journal of Animal Ecology 88, 12261239.CrossRefGoogle ScholarPubMed
Hall, TA (1999) BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Hasle, G (2013) Transport of ixodid ticks and tick-borne pathogens by migratory birds. Frontiers in Cellular and Infection Microbiology 3, 48.CrossRefGoogle ScholarPubMed
Hellgren, O, Waldenström, J and Bensch, S (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. The Journal of Parasitology 90, 797802.CrossRefGoogle ScholarPubMed
Hijmans, RJ (2019) geosphere: Spherical Trigonometry. R package version 1.5–10. Available at https://CRAN.R-project.org/package=geosphere (accessed 13 March 2022).Google Scholar
Ippi, S, Anderson, CB, Rozzi, R and Elphick, CS (2009) Annual variation of abundance and composition in forest bird assemblages on Navarino Island, Cape Horn Biosphere Reserve. Chile. Ornitología Neotropical 20, 231245.Google Scholar
Jenkins, T, Thomas, GH, Hellgren, O and Owens, IPF (2012) Migratory behavior of birds affects their coevolutionary relationship with blood parasites. Evolution 66, 740751.CrossRefGoogle ScholarPubMed
Jetz, W, Thomas, GH, Joy, JB, Hartmann, K and Mooers, AO (2012) The global diversity of birds in space and time. Nature 491, 444448.CrossRefGoogle ScholarPubMed
Koprivnikar, J and Leung, TLF (2015) Flying with diverse passengers: greater richness of parasitic nematodes in migratory birds. Oikos 124, 399405.CrossRefGoogle Scholar
Leung, TLF and Koprivnikar, J (2016) Nematode parasite diversity in birds: the role of host ecology, life history and migration. Journal of Animal Ecology 85, 14711480.CrossRefGoogle ScholarPubMed
Medeiros, MCI, Hamer, GL and Ricklefs, RE (2013) Host compatibility rather than vector-host encounter rate determines the host range of avian Plasmodium parasites. Proceedings of the Royal Society of London B: Biological Sciences 280, 20122947.Google ScholarPubMed
Merino, S, Moreno, J, Vasquez, RA, Martinez, J, Sánchez-Monsálvez, I, Estades, CF, Ippi, S, Sabat, P, Rozzi, R and Mcgehee, E (2008) Haematozoa in forest birds from southern Chile: latitudinal gradients in prevalence and parasite lineage richness. Austral Ecology 33, 329340.CrossRefGoogle Scholar
Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R, Legendre, P, McGlinn, D, Minchin, PR, O'Hara, RB, Simpson, GL, Solymos, P, Stevens, MHH, Szoecs, E and Wagner, H (2019) vegan: Community Ecology Package. R package version 2.5–6. Available at https://CRAN.R-project.org/package=vegan (accessed 13 March 2022).Google Scholar
Paradis, E, Claude, J and Strimmer, K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289290.CrossRefGoogle ScholarPubMed
Pérez-Rodríguez, A, Khimoun, A, Ollivier, A, Eraud, C, Faivre, B and Garnier, S (2018) Habitat fragmentation, not habitat loss, drives the prevalence of blood parasites in a Caribbean passerine. Ecography 41, 18351849.CrossRefGoogle Scholar
Poulin, R and Mouillot, D (2003) Parasite specialization from a phylogenetic perspective: a new index of host specificity. Parasitology 126, 473480.CrossRefGoogle ScholarPubMed
Pulgarín-R, PC, Gómez, C, Bayly, NJ, Bensch, S, FitzGerald, A, Starkloff, N, Kirchman, J, González-Prieto, AM, Hobson, KA, Ungvari-Martin, J, Skeen, H, Castaño, MI and Cadena, CD (2019) Migratory birds as vehicles for parasite dispersal? Infection by avian haemosporidians over the year and throughout the range of a long-distance migrant. Journal of Biogeography 46, 8396.CrossRefGoogle Scholar
Ramey, AM, Schmutz, JA, Reed, JA, Fujita, G, Scotton, BD, Casler, B, Fleskes, JP, Konishi, K, Uchida, K and Yabsley, MJ (2015) Evidence for intercontinental parasite exchange through molecular detection and characterization of haematozoa in northern pintails (Anas acuta) sampled throughout the North Pacific Basin. International Journal for Parasitology: Parasites and Wildlife 4, 1121.Google ScholarPubMed
R Core Team (2020) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/.Google Scholar
Reiczigel, J, Foldi, J and Ozsvari, L (2010) Exact confidence limits for prevalence of disease with an imperfect diagnostic test. Epidemiology and Infection 138, 16741678.CrossRefGoogle ScholarPubMed
Ricklefs, RE, Gray, JD, Latta, SC and Svensson-Coelho, M (2011) Distribution anomalies in avian haemosporidian parasites in the southern Lesser Antilles. Journal of Avian Biology 42, 570584.CrossRefGoogle Scholar
Ricklefs, RE, Medeiros, M, Ellis, VA, Svensson-Coelho, M, Blake, JG, Loiselle, BA, Soares, L, Fecchio, A, Outlaw, D, Marra, PP, Latta, SC, Valkiūnas, G, Hellgren, O and Bensch, S (2017) Avian migration and the distribution of malaria parasites in New World passerine birds. Journal of Biogeography 44, 11131123.CrossRefGoogle Scholar
Rodriguez, MD, Doherty, PF, Piaggio, AJ and Huyvaert, KP (2021) Sex and nest type influence avian blood parasite prevalence in a high-elevation bird community. Parasites and Vectors 14, 145.CrossRefGoogle Scholar
Sambrook, J and Russell, DW (2001) Molecular Cloning: A Laboratory Manual, 3rd Edn. New York, USA: Cold Spring Harbor Laboratory Press.Google Scholar
Santiago-Alarcon, D, Palinauskas, V and Schaefer, HM (2012 a) Diptera vectors of avian haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biological Reviews 87, 928964.CrossRefGoogle ScholarPubMed
Santiago-Alarcon, D, Havelka, P, Schaefer, HM and Segelbacher, G (2012 b) Bloodmeal analysis reveals avian Plasmodium infections and broad host preferences of Culicoides (Diptera: Ceratopogonidae) vectors. PLoS ONE 7, e31098.CrossRefGoogle ScholarPubMed
Smith, MM and Ramey, AM (2015) Prevalence and genetic diversity of haematozoa in South American waterfowl and evidence for intercontinental redistribution of parasites by migratory birds. International Journal for Parasitology: Parasites and Wildlife 4, 2228.Google ScholarPubMed
Stevenson, TN, Nunes, T, Heuer, C, Marshall, J, Sanchez, J, Thornton, R, Reiczigel, J, Robison-Cox, J, Sebastiani, P, Solymos, P, Yoshida, K, Jones, G, Pirikahu, S and Firestone, S (2020) epiR: An R Package for the Analysis of Epidemiological Data. R package version 1.0–15. Available at http://CRAN.R-project.org/package=epiR (accessed 14 September 2021).Google Scholar
Valkiūnas, G (2005) Avian Malaria Parasites and Other Haemosporidia, 2nd Edn. Boca Raton, USA: CRC Press.Google Scholar
Waldenström, J, Bensch, S, Kiboi, S, Hasselquist, D and Ottosson, U (2002) Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Ecology 11, 15451554.CrossRefGoogle ScholarPubMed
Weckstein, JD (2004) Biogeography explains cophylogenetic patterns in toucan chewing lice. Systematic Biology 53, 154164.CrossRefGoogle ScholarPubMed
Wilman, H, Belmaker, J, Simpson, J, de la Rosa, C, Rivadeneira, MM and Jetz, W (2014) EltonTraits 1.0: species-level foraging attributes of the world's birds and mammals. Ecology 95, 20272027.CrossRefGoogle Scholar
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