Ranavirus and helminth parasite co-infection in invasive American bullfrogs in the Atlantic forest, Brazil

Emerging infectious diseases threaten amphibian species across the globe. In Brazil, the American bullfrog (Aquarana catesbeiana) is a highly invasive species that can potentially transmit parasites and pathogens to native amphibians. This is the first assessment of co-infection of Ranavirus and hel...

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Main Authors: Lauren V. Ash, Karla Magalhães Campião, Cauê Pinheiro Teixeira, Nicholas J. Gotelli
Format: Article
Language:English
Published: Elsevier 2024-04-01
Series:International Journal for Parasitology: Parasites and Wildlife
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213224424000208
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author Lauren V. Ash
Karla Magalhães Campião
Cauê Pinheiro Teixeira
Nicholas J. Gotelli
author_facet Lauren V. Ash
Karla Magalhães Campião
Cauê Pinheiro Teixeira
Nicholas J. Gotelli
author_sort Lauren V. Ash
collection DOAJ
description Emerging infectious diseases threaten amphibian species across the globe. In Brazil, the American bullfrog (Aquarana catesbeiana) is a highly invasive species that can potentially transmit parasites and pathogens to native amphibians. This is the first assessment of co-infection of Ranavirus and helminth macroparasites in invasive populations of bullfrogs in South America. We collected, measured, and euthanized 65 specimens of A. catesbeiana sampled from 9 sites across three states of Brazil in the Atlantic Forest biome. We collected and identified helminth macroparasites and sampled host liver tissue to test for the presence and load of Ranavirus with quantitative PCR. We documented patterns of prevalence, parasite load, and co-infection with generalized linear mixed models, generalized logistic regressions, and randomization tests. Most individual bullfrogs did not exhibit clinical signs of infection, but the overall Ranavirus prevalence was 27% (95% confidence interval, [CI 17–38]). Bullfrogs were infected with helminth macroparasites from 5 taxa. Co-infection of helminth macroparasites and Ranavirus was also common (21% CI [12–31]). Bullfrog size was positively correlated with total macroparasite abundance and richness, and the best-fitting model included a significant interaction between bullfrog size and Ranavirus infection status. We observed a negative correlation between Ranavirus viral load and nematode abundance (slope = −0.22, P = 0.03). Invasive bullfrogs (A. catesbeiana) in Brazil were frequently infected with both Ranavirus and helminth macroparasites, so adult bullfrogs could serve as reservoir hosts for both pathogens and parasites. However, many macroparasites collected were encysted and not developing. Coinfection patterns suggest a potential interaction between Ranavirus and macroparasites because helminth abundance increased with bullfrog size but was lower in Ranavirus infected individuals. Future studies of bullfrogs in the Atlantic Forest should investigate their potential role in pathogen and parasite transmission to native anurans.
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spelling doaj.art-23e8429e2e9649ffb228d91bb9245ae82024-04-05T04:40:42ZengElsevierInternational Journal for Parasitology: Parasites and Wildlife2213-22442024-04-0123100924Ranavirus and helminth parasite co-infection in invasive American bullfrogs in the Atlantic forest, BrazilLauren V. Ash0Karla Magalhães Campião1Cauê Pinheiro Teixeira2Nicholas J. Gotelli3University of Vermont, Department of Biology, 109 Carrigan Drive, Burlington, VT, 05403, USA; Corresponding author.Laboratório de Interações Biológicas, Departamento de Zoologia, Universidade Federal do Paraná, UFPR, Curitiba, Paraná, BrazilLaboratório de Interações Biológicas, Departamento de Zoologia, Universidade Federal do Paraná, UFPR, Curitiba, Paraná, BrazilUniversity of Vermont, Department of Biology, 109 Carrigan Drive, Burlington, VT, 05403, USAEmerging infectious diseases threaten amphibian species across the globe. In Brazil, the American bullfrog (Aquarana catesbeiana) is a highly invasive species that can potentially transmit parasites and pathogens to native amphibians. This is the first assessment of co-infection of Ranavirus and helminth macroparasites in invasive populations of bullfrogs in South America. We collected, measured, and euthanized 65 specimens of A. catesbeiana sampled from 9 sites across three states of Brazil in the Atlantic Forest biome. We collected and identified helminth macroparasites and sampled host liver tissue to test for the presence and load of Ranavirus with quantitative PCR. We documented patterns of prevalence, parasite load, and co-infection with generalized linear mixed models, generalized logistic regressions, and randomization tests. Most individual bullfrogs did not exhibit clinical signs of infection, but the overall Ranavirus prevalence was 27% (95% confidence interval, [CI 17–38]). Bullfrogs were infected with helminth macroparasites from 5 taxa. Co-infection of helminth macroparasites and Ranavirus was also common (21% CI [12–31]). Bullfrog size was positively correlated with total macroparasite abundance and richness, and the best-fitting model included a significant interaction between bullfrog size and Ranavirus infection status. We observed a negative correlation between Ranavirus viral load and nematode abundance (slope = −0.22, P = 0.03). Invasive bullfrogs (A. catesbeiana) in Brazil were frequently infected with both Ranavirus and helminth macroparasites, so adult bullfrogs could serve as reservoir hosts for both pathogens and parasites. However, many macroparasites collected were encysted and not developing. Coinfection patterns suggest a potential interaction between Ranavirus and macroparasites because helminth abundance increased with bullfrog size but was lower in Ranavirus infected individuals. Future studies of bullfrogs in the Atlantic Forest should investigate their potential role in pathogen and parasite transmission to native anurans.http://www.sciencedirect.com/science/article/pii/S2213224424000208RanavirusHelminthCo-infectionLithobates catesbeianusAquarana catesbeianaInvasive species
spellingShingle Lauren V. Ash
Karla Magalhães Campião
Cauê Pinheiro Teixeira
Nicholas J. Gotelli
Ranavirus and helminth parasite co-infection in invasive American bullfrogs in the Atlantic forest, Brazil
International Journal for Parasitology: Parasites and Wildlife
Ranavirus
Helminth
Co-infection
Lithobates catesbeianus
Aquarana catesbeiana
Invasive species
title Ranavirus and helminth parasite co-infection in invasive American bullfrogs in the Atlantic forest, Brazil
title_full Ranavirus and helminth parasite co-infection in invasive American bullfrogs in the Atlantic forest, Brazil
title_fullStr Ranavirus and helminth parasite co-infection in invasive American bullfrogs in the Atlantic forest, Brazil
title_full_unstemmed Ranavirus and helminth parasite co-infection in invasive American bullfrogs in the Atlantic forest, Brazil
title_short Ranavirus and helminth parasite co-infection in invasive American bullfrogs in the Atlantic forest, Brazil
title_sort ranavirus and helminth parasite co infection in invasive american bullfrogs in the atlantic forest brazil
topic Ranavirus
Helminth
Co-infection
Lithobates catesbeianus
Aquarana catesbeiana
Invasive species
url http://www.sciencedirect.com/science/article/pii/S2213224424000208
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