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Four new species of Anenterotrema Stunkard, 1938 (Digenea: Dicrocoellidae) infecting phyllostomid bats in the Peruvian Amazon

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Abstract

During a research of digeneans (Platyhelminthes: Trematoda) infecting leaf-nosed bats (Chiroptera: Phyllostomidae) from the Kawsay Biological Station in Madre de Dios, southeastern Peru, four new species were described based on light and scanning electron microscopy (SEM): Anenterotrema paramegacetabulum n. sp. from the seba's short-tailed bat Carollia perspicillata Linnaeus, A. hastati n. sp., A. kawsayense n. sp., and A. peruense n. sp. from the greater spear-nosed bat Phyllostomus hastatus (Pallas). Anenterotrema paramegacetabulum n. sp. differs from all congeners by having a terminal oral sucker, a transversely elongated ventral sucker without clamp-shaped, and by having the testes located immediately posterior to ventral sucker. Anenterotrema hastati n. sp. is easily differentiated from the other congeneric species by having an almost clamp-shaped oral sucker, well-developed cirrus sac, a bilobulated seminal receptacle, and a group of well-developed unicellular glands located anterolateral to cirrus sac. Anenterotrema kawsayense n. sp. is characterized by possessing protuberances on the anterior margin of the oral sucker. Anenterotrema peruense n. sp. is mainly characterized by having the testes located principally anterior to ventral sucker and the cirrus sac located perpendicular to midline of the body. The present finding brings to 12, the number of known species of Anenterotrema. A key to the species of Anenterotrema Stunkard, 1938 is provided.

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Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request

References

  • Achatz, T. J., Cardenas-Callirgos, J. M., & Tkach, V. V. (2018). New Anenterotrema Stunkard, 1938 (Digenea: Anenterotrematidae) from silky short-tailed bat, Carollia brevicauda Schinz, 1821, in Peru. Comparative Parasitology, 85, 78–82.

    Article  Google Scholar 

  • Adhikari, R., Maharjan, M., & Ghimire, T. (2020). Prevalence of Gastrointestinal Parasites in the Frugivorous and the Insectivorous Bats in Southcentral Nepal. Journal of Parasitology Research, 2020, 8880033.

    Article  PubMed  PubMed Central  Google Scholar 

  • Burgin, C. J., Colella, J. P., Kahn, P. L., & Upham, N. S. (2018). How many species of mammals are there? Journal of Mammalogy, 99, 1–14.

    Article  Google Scholar 

  • Calle, C. C., & Arango, J. M. (1999). Nemátodos en la cavidad abdominal y el tracto digestivo de algunos murciélagos colombianos. Caldasia, 21, 10–25.

    Google Scholar 

  • Díaz, M. M., Aguirre, L. F., & Barquez, R. M. (2016). Clave de identificación de los murciélagos del cono sur de sudamérica. Centro de Estudios en Biología Teórica y Aplicada. Cochabamba, Bolivia. 94 pp.

  • Fernandes, T. F., dos Santos, A. N., Furtado, A. P., de Vasconcelos Melo, F. T., & dos Santos, J. N. (2019). A new species of Metadelphis Travassos, 1944 (Digenea: Dicrocoeliidae) from the gall-bladder of Molossus molossus (Pallas) (Chiroptera: Molossidae) in the Brazilian eastern Amazon. Systematic Parasitology, 96(7), 617–624.

    Article  PubMed  Google Scholar 

  • Fernandes, T. F, Dos Santos, J. N., de Vasconcelos Melo, F. T., Achatz, T. J., Greiman, S. E., Bonilla, C. C., & Tkach, V.V. (2021a). Interrelationships of Anenterotrema (Digenea: Dicrocoeliidae) from Neotropical bats (Mammalia: Chiroptera) with description of a new species from Molossus molossus in Brazil. Parasitology Research, 120, 2003–2016.

    Article  PubMed  Google Scholar 

  • Fernandes, T. F., de Vasconcelos Melo, F. T., & Nascimento Dos Santos, J. (2021b). A New species of Allintoshius (Nematoda: Heligmosomoidea) from two species of bats in brazil. Journal of Parasitology, 107(5), 703–709.

    Article  PubMed  Google Scholar 

  • Gibson DI, Santos CP (2008) Family Anenterotrematidae Yamaguti, 1958. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol 3. CAB International and the Natural History Museum, Wallingford, pp 233–260.

  • Guerrero, R., Martin, C., Gardner, S. L., & Bain, O. (2002). New and known species of Litomosoides (Nematoda: Filarioidea): Important adult and larval characters and taxonomic changes. Comparative Parasitology, 69, 177–195.

    Article  Google Scholar 

  • Huancachoque, E., Sáez, G., Cruces, C. L., Mendoza, C., Luque, J. L., & Chero, J. D. (2020). Glossidiella peruensis sp. nov., a new digenean (Plagiorchiida: Plagiorchiidae) from the lung of the brown ground snake Atractus major (Serpentes: Dipsadidae) from Peru. Zoologia, 37, 1–6.

    Article  Google Scholar 

  • Ibañez, N., Jara, C., & Guerra, A. (2005). Helmintos parásitos de mamíferos silvestres de Condorcanqui, Amazonas-Perú. Revista de Biologia, 25, 43–48.

    Google Scholar 

  • ICZN (2012). International Commission on Zoological Nomenclature: Amendment of articles 8, 9, 10, 21 and 78 of the International Code of Zoological Nomenclature to expand and refine methods of publication. Bulletin of Zoological Nomenclature, 69, 161–169.

    Article  Google Scholar 

  • Lunaschi, L. I., & Drago, F. B. (2011). A revision of Anenterotrema Stunkard, 1938 (Digenea: Anenterotrematidae) and a key to its species. Zootaxa, 2775, 50–64.

    Article  Google Scholar 

  • Minaya, D., Saez, G. M., Chero, J., Cruces, C., & Iannacone, J. (2020). Helminth parasites of bats (Chiroptera, Phyllostomidae) in the department of Junin, Peru and check list of records made in Peru. Revista Del Museo Argentino de Ciencias Naturales, Nueva Serie, 22, 57–73.

    Article  Google Scholar 

  • Murillo-García, O. E., & Bedoya-Durán, M. J. (2014). Distribution and abundance of bat assemblages among different forest covers in Gorgona national natural park, Colombia. Revista de Biologia Tropical, 62, 419–434.

    Article  Google Scholar 

  • Pacheco, V., Diaz, S., Graham-Angeles, L., Flores-Quispe, M., Calizaya-Mamani, G., Ruelas, D., & Sánchez-Vendizú, P. (2021). Lista actualizada de la diversidad de los mamíferos del Perú y una propuesta para su actualización. Revista Peruana de Biología, 28(4), e21019.

    Article  Google Scholar 

  • Santos, C. P., & Gibson, D. I. (2015). Checklist of the Helminth Parasites of South American Bats. Zootaxa, 3937, 471–499.

    Article  PubMed  Google Scholar 

  • Sikes, R. S. (2016). 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy, 97(3), 663–688.

    Article  PubMed  PubMed Central  Google Scholar 

  • Simões, R., Fraga-Neto, S., Vilar, E. M., Maldonado, A., & do Val Vilela, R. (2019). A New Species of Bidigiticauda (Nematoda: Strongylida) from the Bat Artibeus Planirostris (Chiroptera: Phyllostomidae) in the Atlantic Forest and a Molecular Phylogeny of the Molineid Bat Parasites. The Journal of Parasitology, 105(5), 783–792.

    Article  Google Scholar 

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Acknowledgements

We thank to Kawsay Biological Station for the support in the present investigation. The authors are grateful to the following people who helped to the collection of bats in Peru: Julie Van den Broeck, Rodrigo Espinoza, and Liz Lopez.

Funding

CLC was supported by a student fellowship from the Coordenação de Aperfeiçoamento de Pessoal do Ensino Superior, Brazil (CAPES) - Finance Code 001.

Author information

Authors and Affiliations

  1. Laboratorio de Zoología de Invertebrados, Departamento Académico de Zoología, Facultad de Ciencias Biológicas (FCB), Universidad Nacional Mayor de San Marcos (UNMSM), Av. Universitaria cruce con Av. Venezuela cuadra 34, Lima, Peru

    Edson R. Cacique, Ruperto Severino, Celso Cruces & Jhon D. Chero

  2. Kawsay Biological Station, Madre de Dios, Peru

    Raúl Bello & Hugo Zamora

  3. Museo de Historia Natural de la Universidad Nacional de San Agustín de Arequipa, Arequipa, Peru

    Hugo Zamora & Katherin Mares

  4. Laboratorio de Parasitología General y Especializada, Facultad de Ciencias Naturales y Matemática, Universidad Nacional Federico Villarreal (UNFV), Código postal 15007, El Agustino, Lima, Peru

    Gloria Saéz

  5. Programa de Pós-Graduação em Biologia Animal da Universidade Federal Rural do Rio de Janeiro, BR 465, Km 7, Seropédica, Rio de Janeiro, CEP 23890-000, Brazil

    Celso Cruces

  6. Laboratorio de Zoología, Facultad de Ciencias Biológicas, Universidad Ricardo Palma (URP), Av. Alfredo Benavides 5440, Santiago de Surco, Lima, Peru

    Jhon D. Chero

Authors
  1. Edson R. Cacique
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  2. Raúl Bello
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  3. Hugo Zamora
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  4. Katherin Mares
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  5. Gloria Saéz
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  6. Ruperto Severino
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  7. Celso Cruces
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  8. Jhon D. Chero
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Contributions

E.R.C., C.C., R.S., and J.D.C. wrote the main manuscript text. E.R.C., C.C., G.S., and J.D.C. prepared figures. R.B., H.Z., and K.M. collected the bat specimens. All authors reviewed the manuscript.

Corresponding author

Correspondence to Jhon D. Chero.

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All applicable institutional, national and international guidelines for the care and use of animals were followed.

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Cacique, E.R., Bello, R., Zamora, H. et al. Four new species of Anenterotrema Stunkard, 1938 (Digenea: Dicrocoellidae) infecting phyllostomid bats in the Peruvian Amazon. Syst Parasitol 100, 531–542 (2023). https://doi.org/10.1007/s11230-023-10103-6

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  • DOI: https://doi.org/10.1007/s11230-023-10103-6

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