Abstract
Migration can modify interaction dynamics between parasites and their hosts with migrant hosts able to disperse parasites and impact local community transmission. Thus, studying the relationships among migratory hosts and their parasites is fundamental to elucidate how migration shapes host–parasite interactions. Avian haemosporidians are some of the most prevalent and diverse group of wildlife parasites and are also widely studied as models in ecological and evolutionary research. Here, we contrast partner fidelity, network centrality and parasite taxonomic composition among resident and non-resident avian hosts using presence/absence data on haemosporidians parasitic in South American birds as study model. We ran multilevel Bayesian models to assess the role of migration in determining partner fidelity (i.e., normalized degree) and centrality (i.e., weighted closeness) in host–parasite networks of avian hosts and their respective haemosporidian parasites. In addition, to evaluate parasite taxonomic composition, we performed permutational multivariate analyses of variance to quantify dissimilarity in haemosporidian lineages infecting different host migratory categories. We observed similar partner fidelity and parasite taxonomic composition among resident and migratory hosts. Conversely, we demonstrate that migratory hosts play a more central role in host–parasite networks than residents. However, when evaluating partially and fully migratory hosts separately, we observed that only partially migratory species presented higher network centrality when compared to resident birds. Therefore, migration does not lead to differences in both partner fidelity and parasite taxonomic composition. However, migratory behavior is positively associated with network centrality, indicating migratory hosts play more important roles in shaping host–parasite interactions and influence local transmission.
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Availability of data and materials
A part of the data that support the findings of this study is openly available at https://onlinelibrary.wiley.com/doi/10.1111/mec.15094 and http://130.235.244.92/Malavi/ (Bensch et al. 2009). The other portion of the data that support our findings can be shared by Prof. Érika Martins Braga under reasonable request.
References
Altizer S, Bartel R, Han BA (2011) Animal migration and infectious disease risk. Science (80-) 331:296–302. https://doi.org/10.1126/science.1194694
Anjos CC, Chagas CRF, Fecchio A et al (2021) Avian malaria and related parasites from resident and migratory birds in the brazilian atlantic forest, with description of a new Haemoproteus species. Pathogens 10:1–21. https://doi.org/10.3390/pathogens10020103
Bascompte J (2010) Structure and dynamics of ecological networks. Science (80-) 329:765–766. https://doi.org/10.1126/science.1194255
Bauer S, Hoye BJ (2014) Migratory animals couple biodiversity and ecosystem functioning worldwide. Science (80-) 344:1242552. https://doi.org/10.1126/science.1242552
Bell JA, Weckstein JD, Fecchio A, Tkach VV (2015) A new real-time PCR protocol for detection of avian haemosporidians. Parasit Vectors 8:1–9. https://doi.org/10.1186/s13071-015-0993-0
Bensch S, Hellgren O, Érez-Tris PJ (2009) MalAvi: A public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour 9:1353–1358. https://doi.org/10.1111/j.1755-0998.2009.02692.x
Braga ÉM, Silveira P, Belo NO, Valkiunas 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. https://doi.org/10.1590/S0074-02762011000900002
Bürkner PC (2017) brms: an R package for Bayesian multilevel models using Stan. J Stat Softw 80:27239. https://doi.org/10.18637/jss.v080.i01
Campião KM, Dáttilo W (2020) Biological drivers of individual-based anuran–parasite networks under contrasting environmental conditions. J Helminthol 94:e167. https://doi.org/10.1017/S0022149X20000504
de Angeli Dutra D, Fecchio A, Braga ÉM, Poulin R (2021a) Migratory birds have higher prevalence and richness of avian haemosporidian parasites than residents. Int J Parasitol. https://doi.org/10.1016/j.ijpara.2021.03.001
de Angeli Dutra D, Filion A, Fecchio A et al (2021b) Migrant birds disperse haemosporidian parasites and affect their transmission in avian communities. Oikos 130:979–988. https://doi.org/10.1111/oik.08199
De La Torre GM, Campião KM, Bell JA et al (2021) Avian community composition affects ornithophilic mosquito and avian malaria turnover across an interfluvial system in southern Amazonia. J Avian Biol 52:1–12. https://doi.org/10.1111/jav.02701
Dixon P (2003) Computer program review VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930
Dormann C, Gruber B, Fründ J (2008) Introducing the bipartite package: analysing ecological networks. Interaction 1:2413793
Ellis VA, Sari EHR, Rubenstein DR et al (2019) The global biogeography of avian haemosporidian parasites is characterized by local diversification and intercontinental dispersal. Parasitology 146:213–219. https://doi.org/10.1017/S0031182018001130
Fallon SM, Ricklefs RE, Swanson BL, Bermingham E (2003) Detecting avian malaria: an improved polymerase chain reaction diagnostic. J Parasitol 89:1044–1047. https://doi.org/10.1645/ge-3157
Fecchio A, Bell JA, Pinheiro RBP et al (2019a) Avian host composition, local speciation and dispersal drive the regional assembly of avian malaria parasites in South American birds. Mol Ecol 28:2681–2693. https://doi.org/10.1111/mec.15094
Fecchio A, Wells K, Bell JA et al (2019b) Climate variation influences host specificity in avian malaria parasites. Ecol Lett 22:547–557. https://doi.org/10.1111/ele.13215
Fecchio A, Bell JA, Bosholn M et al (2020) An inverse latitudinal gradient in infection probability and phylogenetic diversity for Leucocytozoon blood parasites in New World birds. J Anim Ecol 89:423–435. https://doi.org/10.1111/1365-2656.13117
Fecchio A, Lugarini C, Ferreira A et al (2021) Migration and season explain tick prevalence in Brazilian birds. Med Vet Entomol. https://doi.org/10.1111/mve.12532
Ferreira FC, Rodrigues RA, Ellis VA et al (2017) Habitat modification and seasonality influence avian haemosporidian parasite distributions in southeastern Brazil. PLoS ONE 12:0178791. https://doi.org/10.1371/journal.pone.0178791
Ferreira-Junior FC, de Angeli Dutra D, Silveira P et al (2018) A new pathogen spillover from domestic to wild animals: Plasmodium juxtanucleare infects free-living passerines in Brazil. Parasitology. https://doi.org/10.1017/S003118201800077X
Fortuna MA, Nagavci A, Barbour MA, Bascompte J (2020) Partner fidelity and asymmetric specialization in ecological networks. Am Nat 196:382–389. https://doi.org/10.1086/709961
Hellgren O, Waldenstro J, Bensch S (2004) A new Pcr assay for simultaneous studies of leucocytozoon, plasmodium, and haemoproteus from avian blood. J Parasitol 90:797–802. https://doi.org/10.1645/GE-184R1
Huang X, Ellis V, Jönsson J, Bensch S (2018) Generalist haemosporidian parasites are better adapted to a subset of host species in a multiple host community. Mol Ecol 27:4336–4346. https://doi.org/10.1111/mec.14856
Krasnov BR, Fortuna MA, Mouillot D et al (2012) Phylogenetic signal in module composition and species connectivity in compartmentalized host-parasite networks. Am Nat 179:501–511. https://doi.org/10.1086/664612
Lacorte GA, Flix GMF, Pinheiro RRB et al (2013) Exploring the diversity and distribution of neotropical avian malaria parasites—a molecular survey from Southeast Brazil. PLoS ONE 8:1–9. https://doi.org/10.1371/journal.pone.0057770
Møller AP, Szép T (2011) The role of parasites in ecology and evolution of migration and migratory connectivity. J Ornithol 152:S141–S150. https://doi.org/10.1007/s10336-010-0621-x
Paine RT (1969) A note on trophic complexity and community stability. Am Nat 103:91–93
Pinheiro RBP, Félix GMF, Chaves AV et al (2016) Trade-offs and resource breadth processes as drivers of performance and specificity in a host-parasite system: a new integrative hypothesis. Int J Parasitol 46:115–121. https://doi.org/10.1016/j.ijpara.2015.10.002
Poulin R, de Angeli Dutra D (2021) Animal migrations and parasitism: reciprocal effects within a unified framework. Biol Rev. https://doi.org/10.1111/brv.12704
Poulin R, Krasnov BR, Pilosof S, Thieltges DW (2013) Phylogeny determines the role of helminth parasites in intertidal food webs. J Anim Ecol 82:1265–1275. https://doi.org/10.1111/1365-2656.12101
R Core Team (2020) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. https://www.R-project.org
Remsen Jr JV, Areta JI, Bonaccorso E, Claramunt S, Jaramillo A, Lane DF, Pacheco JF, Robbins MB, Stiles FG, Zimmer KJ (2012) A classification of the bird species of South America. In: American Ornithological Society. http://www.museum.lsu.edu/~Remsen/SACCBaseline.htm. Accessed 24 Aug 2021
Runghen R, Poulin R, Monlleó-Borrull C, Llopis-Belenguer C (2021) Network analysis: ten years shining light on host-parasite interactions. Trends Parasitol 37:445–455. https://doi.org/10.1016/j.pt.2021.01.005
Santiago-Alarcon D, Palinauskas V, Schaefer HM (2012) Diptera vectors of avian Haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biol Rev 87:928–964. https://doi.org/10.1111/j.1469-185X.2012.00234.x
Satterfield DA, Maerz JC, Altizer S (2015) Loss of migratory behaviour increases infection risk for a butterfly host. Proc R Soc B Biol Sci 282:20141734. https://doi.org/10.1098/rspb.2014.1734
Somenzari M, do Amaral PP, Cueto VR, et al (2018) An overview of migratory birds in Brazil. Pap Avulsos Zool 58:3. https://doi.org/10.11606/1807-0205/2018.58.03
Valkiūnas G (2005) Avian malaria parasites and other haemosporidia, 1st edn. CRC Press, Boca Raton, Florida. https://doi.org/10.1201/9780203643792.fmatt
Acknowledgements
We thank Gabriel Moreira Félix for his fundamental advise on our analyses and the MalAvi curators for maintaining the database and for making all data available, as well as all researchers who deposited their data into this public repository. We are also grateful to Lucas Marques for graphical support.
Funding
Daniela Dutra was supported by a doctoral scholarship from the University of Otago. During the project, Alan Fecchio was supported by a postdoctoral fellowship (PNPD scholarship) from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). Érika Braga was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).
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Daniela Dutra and Robert Poulin conceived the idea and designed the study. Daniela Dutra performed the data analyses. Daniela Dutra, Érika Braga and Alan Fecchio collected the data. Daniela Dutra wrote the manuscript with input from all other authors. All authors contributed critically to the drafts and gave final approval for publication.
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Communicated by Eva Kallio.
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de Angeli Dutra, D., Fecchio, A., Braga, É.M. et al. Haemosporidian taxonomic composition, network centrality and partner fidelity between resident and migratory avian hosts. Oecologia 197, 501–509 (2021). https://doi.org/10.1007/s00442-021-05031-5
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DOI: https://doi.org/10.1007/s00442-021-05031-5