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Multilayer Networks Assisting to Untangle Direct and Indirect Pathogen Transmission in Bats

  • Host Microbe Interactions
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Abstract

The importance of species that connect the different types of interactions is becoming increasingly recognized, and this role may be related to specific attributes of these species. Multilayer networks have two or more layers, which represent different types of interactions, for example, between different parasites and hosts that are nonetheless connected. The understanding of the ecological relationship between bats, ectoparasites, and vector-borne bacteria could shed some light on the complex transmission cycles of these pathogens. In this study, we investigated a multilayer network in Brazil formed by interactions between bat-bacteria, bat-ectoparasite, and ectoparasite-bacteria, and asked how these interactions overlap considering different groups and transmission modes. The multilayer network was composed of 31 nodes (12 bat species, 14 ectoparasite species, and five bacteria genera) and 334 links, distributed over three layers. The multilayer network has low modularity and shows a core-periphery organization, that is, composed of a few generalist species with many interactions and many specialist species participating in few interactions in the multilayer network. The three layers were needed to accurately describe the multilayer structure, while aggregation leads to loss of information. Our findings also demonstrated that the multilayer network is influenced by a specific set of species that can easily be connected to the behavior, life cycle, and type of existing interactions of these species. Four bat species (Artibeus lituratus, A. planirostris, Phyllostomus discolor, and Platyrrhinus lineatus), one ectoparasite species (Steatonyssus) and three bacteria genera (Ehrlichia, hemotropic Mycoplasma and Neorickettsia) are the most important species for the multilayer network structure. Finally, our study brings an ecological perspective under a multilayer network approach on the interactions between bats, ectoparasites, and pathogens. By using a multilayer approach (different types of interactions), it was possible to better understand these different ecological interactions and how they affect each other, advancing our knowledge on the role of bats and ectoparasites as potential pathogen vectors and reservoirs, as well as the modes of transmission of these pathogens.

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Funding

This research was funded by FAPESP (The São Paulo Research Foundation—Process #2018/02753–0 and #2017/14124–4); FUNDECT (Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul, Case 59/300.187/2016); CNPq (National Council for Scientific and Technological Development) for the Productivity Grant to MRA (CNPq Process #302420/2017–7), DMB-B (CNPq Process # 303802/2021–9), and HMH (CNPq Process #308768/2017–5); FAPERJ/CAPES—E-26/202.158/2015—Rio de Janeiro Postdoctoral Research Support Program for the stipends conceded to ECL; FAPEMIG (Foundation for Research Support of the State of Minas Gerais) for the Postdoctoral scholarship to CSS (RED-00253–16). The funders had no role in the design of the study, in the sampling, analyses, interpretation of data, in the writing of the manuscript, or in the decision to publish the results.

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Authors and Affiliations

  1. Fundação Oswaldo Cruz de Mato Grosso do Sul, Campo Grande, MS, Brazil

    Daniel Maximo Correa Alcantara

  2. Laboratório de Imunoparasitologia, Departamento de Patologia, Reprodução e Saúde Única, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual “Júlio de Mesquita Filho” (UNESP), Jaboticabal, SP, Brazil

    Priscila Ikeda, Victória Valente Califre de Mello, Rosangela Zacarias Machado & Marcos Rogério André

  3. Departamento de Biologia Geral, Programa de Pós-Graduação em Botânica Aplicada, Universidade Estadual de Montes Claros, Montes Claros, MG, Brazil

    Camila Silveira Souza

  4. Laboratório de Biologia Parasitária, Programa de Pós-Graduação em Biotecnologia, Universidade Católica Dom Bosco, Campo Grande, MS, Brazil

    Jaire Marinho Torres & Heitor Miraglia Herrera

  5. Laboratório de Ecologia de Mamíferos, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

    Elizabete Captivo Lourenço

  6. Laboratório de Coleções Zoológicas, Instituto Butantan, São Paulo, SP, Brazil

    Ricardo Bassini-Silva

  7. Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, SP, Brazil

    Darci Moraes Barros-Battesti

  8. Setor de Zoologia, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, Campo Grande, MS, Brazil

    Gustavo Graciolli

  9. Laboratório de Imunoparasitologia, Departamento de Patologia, Reprodução e Saúde Única, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual “Júlio de Mesquita Filho” (UNESP), Campus de Jaboticabal, Via de Acesso Prof. Paulo Donato Castellane, s/n, CEP: 14884-900, Jaboticabal, SP, Brazil

    Marcos Rogério André

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  1. Daniel Maximo Correa Alcantara
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  2. Priscila Ikeda
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Correspondence to Marcos Rogério André.

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Alcantara, D.M.C., Ikeda, P., Souza, C.S. et al. Multilayer Networks Assisting to Untangle Direct and Indirect Pathogen Transmission in Bats. Microb Ecol 86, 1292–1306 (2023). https://doi.org/10.1007/s00248-022-02108-3

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