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Ecological and molecular associations between neotropical wild felids and Taenia (Cestoda: Taeniidae) in the Atlantic Forest: a new report for Taenia omissa

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Abstract

Ecological associations between wild felids and parasites from the Taeniidae family are related to predator–prey interactions, where felids act as definitive hosts while their prey, herbivores and/or omnivores, act as intermediate hosts. In the Atlantic Forest, six neotropical felid species coexist in sympatry, but the ecological parasite-host interactions remain poorly studied. Taenia omissa is a tapeworm that parasitizes cougars (Puma concolor) as its only definitive host and their ungulate prey as intermediate hosts. The aim of this study was to identify tapeworms present in road-killed fauna using both molecular and morphological characteristics and their predator–prey relationship. Adult tapeworms found in a cougar, a jaguarundi (Herpailurus yagouaroundi), and two ocelots (Leopardus pardalis); and metacestodes found in a red brocket deer (Mazama americana) and a wild guinea pig (Cavia aperea) were analyzed. Through morphological analysis of rostellar hooks and molecular analysis of the mitochondrial genetic marker cox1, Taenia omissa adult individuals were identified in the cougar, and metacestodes in the red brocket deer, proving the existence of a full host-parasite life cycle in the Atlantic Forest region. This new report reveals the southernmost record of T. omissa and broadens its geographic distribution. In addition, isolates of the Taenia genus divergent from those described so far in molecular databases were reported and suggested a wild cycle that involves the jaguarundi and agouti (Dasyprocta asarae) as definitive and intermediate hosts, respectively. These results highlight the complexity of the tapeworm population in the region and the need to study it with both morphological and molecular approaches.

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Availability of data and materials

The sequences identified in this study were deposited in the GenBank database under accession numbers OQ921985 (CAMi1), OQ921986 (MAMi1), OQ921987 (PCMi1_1), OQ921988 (PCMi1_2), OQ921989 (HYMi1), OQ921990 (LPMi1), and OQ92191 (LPMi2).

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Acknowledgements

We acknowledge the ongoing collaboration of the Regional Technical Delegation NEA National Parks and Subtropical Ecological Research Center (CIES) for technical assistance and to “Proyecto Yaguareté” for their constant collaboration. Also, we acknowledge the park rangers from National Park Iguazu for collaborating with monitoring and collecting road-killed animals with warm and special thanks to our friend Ricardo Melzew, to the veterinarian Dante Dinucci for his continuous predisposition to collaborate by collecting samples, and to Claudia Vergara Páez and Matias Alvarez for assistance with the high-quality images. Thanks to Andrea Ferrari Kristeller for the linguistic revision.

Funding

This work was carried out with funding from PNUD PGTF/INT/21/K09 (L.K.); CONICET (L.K., J.P.A, and N. M.); UBACYT 20020190100261BA (L.K.); ANPCyT PICT 2021 00018, PICT 2020 02513, PICT2017 3176 (L. K, L. A., and N. M.); and PICT 2021 00795 (N. M. and L. K.)

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Contributions

J. A., N. M., and L. A. carried out the experiments. J.A., N. M., and L.K. wrote the main manuscript text. J.A. prepared Figs. 1, 2, 3, 4, and 5; L. A. and N. M. performed de phylogenetic analysis and prepared Fig. 6. L. K. supervised the project. All authors discussed the results and contributed to the final manuscript.

Corresponding author

Correspondence to Laura Kamenetzky.

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The authors declare no competing interests.

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Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary Data S1.

 Sequence alignment used for phylogenetic analysis. (FAS 12 KB)

Supplementary Fig. S1.

Unrooted bayesian phylogeny including samples from this study, Taenia omissa and Taenia spp. GenBank records and all homologous sections of cox1 gene are from the RefSeq GenBank database.  Posterior probability values> 0.60 are indicated at the nodes. (PDF 2925 KB)

Supplementary Table S1.

Sequence identity matrix created from the same alignment used for phylogenetic analysis using BioEdit. (XLSX 25 KB)

Supplementary Table S2.

Supplementary Table S2. BLASTn results using LPMi1 as a query against the Nucleotide collection (nr/nt) database. (XLSX 29 KB)

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Arrabal, J.P., Arce, L.F., Macchiaroli, N. et al. Ecological and molecular associations between neotropical wild felids and Taenia (Cestoda: Taeniidae) in the Atlantic Forest: a new report for Taenia omissa. Parasitol Res 122, 2999–3012 (2023). https://doi.org/10.1007/s00436-023-07989-y

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