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Larval Digenean Parasitizing Amphibian Hosts from the Argentinian Chaco Region

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Abstract

Purpose

The diversity of larval digenetic trematodes can provide information on one or more intermediate hosts prior to maturation into the definitive host; on host activity and distribution; and in some cases, on environmental perturbations. In this context, the goal of the present study was to analyse the trematode larvae found in adult amphibians collected from the Argentinian Chaco Region. Few studies have been reported on the systematics of larval digeneans in amphibians.

Methods

A total of 167 specimens of frogs (Leptodactylus macrosternum, Leptodactylus latinasus, Lepidobatrachus laevis, Lepidobatrachus llanensis and Lysapsus limellum) and toads (Rhinella bergi) were examined for larval digeneans. Frogs and toads were collected in two Argentinian ecoregions (Dry Chaco and Humid Chaco); between June 2002 and December 2019. Morphology of each taxon was studied in detail using light microscopy and scanning electron microscopy (SEM).

Results

Fourteen different taxa of the families Diplostomidae (Alariinae gen sp., Didelphodiplostomum sp., Pharingostomoides sp. and Tylodelphys sp.), Proterodiplostomidae (Heterodiplostomum lanceolatum), and Strigeidae (Strigea spp.) were found infecting the body cavity, mesentery, muscle, fluid in the spinal cord canal, and cranial cavity of amphibians. All species are described and illustrated, and their life cycles are briefly discussed.

Conclusion

These infections provide new information on the morphology, morphometry, and composition of the diversity of mesocercariae and metacercariae in amphibians, thus contributing to the knowledge of potential intermediate hosts. In addition, our results serve as an indicator of parasite and host biodiversity in different ecoregions of the Gran Chaco.

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Data Availability

The data used in this study are included in the manuscript.

References

  1. Koprivnikar J, Marcogliese DJ, Rohr JR, Orlofske SA, Raffel TR, Johnson PT (2012) Macroparasite infections of amphibians: what can they tell us? EcoHealth 9:342–360. https://doi.org/10.1007/s10393-012-0785-3

    Article  PubMed  Google Scholar 

  2. Ostrowski de Núñez M, Hamann MI, Rumi A (1997) Estudio de trematodes larvales en Biomphalaria spp. (Mollusca, Planorbidae) de la localidad de San Roque, provincia de Corrientes. Argentina Physis 54:7–15

    Google Scholar 

  3. Hamann MI, Kehr AI, González CE (2013) Biodiversity of trematodes associated with amphibians from different habitats in Corrientes Province, Argentina. J Helminthol 87:286–300. https://doi.org/10.1017/S0022149X12000302

    Article  CAS  PubMed  Google Scholar 

  4. Hamann MI, Kehr AI, González CE (2013) Helminth communities in the burrowing toad, Rhinella fernandezae, from northeastern Argentina. Biologia 68:1155–1162. https://doi.org/10.2478/s11756-013-0272-5

    Article  Google Scholar 

  5. Hamann MI, Kehr AI, González CE (2014) Helminth community structure in the Argentinian bufonid Melanophryniscus klappenbachi: Importance of habitat use and season. Parasitol Res 113:3639–3649. https://doi.org/10.1007/s00436-014-4029-z

    Article  PubMed  Google Scholar 

  6. Hamann MI, Fernández MV, González CE (2019) Metacercariae of Strigeidae parasitizing amphibians of the Chaco region in Argentina. Anais Acad Brasil Ci 91:1–6. https://doi.org/10.1590/0001-3765201920180044

    Article  Google Scholar 

  7. Hamann MI, González CE, Fernández MV (2020) Trematodes parasites associated with amphibians from a rice field in the northeastern Argentina. Food Web. https://doi.org/10.1016/j.fooweb.2019.e00139

    Article  Google Scholar 

  8. Odening K (1967) Die Lebenzyklen von Strigea falconispalumbi (Virbog), S. striges (Schrank) und S. sphaerula (Rudolphi) im Raum Berlin Zool. Sb. Abt System Geogr U Ökol 94:1–67

    Google Scholar 

  9. Combes C, Bartoli P, Theron A (2002) Trematode transmission strategies. In: Lewis EE, Campbell JF, Sukhdeo MWK (eds) The behavioural ecology of parasites CABI, Wallingford, UK, pp 1–12

  10. Bush AO, Fernández JC, Esch GW, Seed JR (2001) Parasitism. The diversity and ecology of animal parasites. University Press, London, Cambridge

    Google Scholar 

  11. Marcogliese DJ, King KC, Salo HM, Fournier M, Brousseau P, Spear P, Champoux L, McLaughlin JD, Boily M (2009) Combined effects of agricultural activity and parasites on biomarkers in the bullfrog, Rana catesbeiana. Aquat Toxicol 9:126–134. https://doi.org/10.1016/j.aquatox.2008.10.001

    Article  CAS  Google Scholar 

  12. Hamann MI, González CE (2009) Larval digenetic trematodes in tadpoles of six amphibian species from Northeastern Argentina. J Parasitol 5:623–628. https://www.jstor.org/stable/27735626

  13. Morello J, Matteuci SD, Rodriguez AF, Silva ME (2012) Ecorregiones y complejos ecosistémicos argentinos. Orientación Gráfica Editora, Buenos Aires, Argentina

  14. Frost D (2021) Amphibian species of the world: an online reference. Version 6.1. American Museum of Natural History, New York. https://amphibiansoftheworld.amnh.org/index.php. doi.org/https://doi.org/10.5531/db.vz.0001. Accessed 12 August 2022

  15. Goater T, Goater CP (2001) Ecological monitoring and assessment network (EMAN) protocols for measuring biodiversity: Parasites of amphibians and reptiles. http:// www.eman-rese.ca/eman/ecotools/protocols/terrestrial/herp parasites/intro.html. Accessed 13 August 2021

  16. Yamaguti S (1971) Synopsis of the digenetic trematodes of vertebrates. Keigaku Publishing Company, Tokyo

    Google Scholar 

  17. Yamaguti S (1975) A synoptical review of life histories of digenetic trematodes of vertebrates. Keigaku Publishing Co., Tokyo

    Google Scholar 

  18. Gibson DI, Jones A, Bray RA (2002) Keys to the Trematoda. CABI Publishing and The Natural History Museum, London

    Book  Google Scholar 

  19. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: margolis et al. Revisited. J Parasitol 83:575–583

    Article  CAS  PubMed  Google Scholar 

  20. Szidat L (1969) Development, and behaviour of new strigeatoid metacercariae from subtropical fishes of South America. J Fisheries Res Board Can 26:753–786

    Article  Google Scholar 

  21. Queiroz MS, López-Hernández D, Locke SA, Pinto HA, Anjos LA (2019) Metacercariae of Heterodiplostomum lanceolatum (Trematoda: Proterodiplostomidae) found in Leptodactylus podicipinus (Anura: Leptodactylidae) from Brazil: a morphological, molecular and ecological study. J Helminthol. https://doi.org/10.1017/S0022149X19000646

    Article  PubMed  Google Scholar 

  22. Niewiadomska K (2002) Superfamily Diplostomoidea Poirier. In: Gibson DI, Jones A, Bray RA (eds). Keys to the Trematoda, CABI, Publishing and The Natural History Museum. London, UK, pp 231–241

  23. Ozolina Z, Deksne G, Pupins M, Gravele E, Gavarane I, Kirjusina M (2021) Alaria alata mesocercariae prevalence and predilection sites in amphibians in Latvia. Parasitol Res 120:145–152. https://doi.org/10.1007/s00436-020-06951-6

    Article  PubMed  Google Scholar 

  24. Kästner C, Bier NS, Mayer-Scholl A, Nöckler K, Richter MH, Johne (2021) Prevalence of Alaria alata mesocercariae in wild boars from Brandenburg, German. Parasitol Res 120:2103–2108. https://doi.org/10.1007/s00436-021-07178-9

    Article  PubMed  PubMed Central  Google Scholar 

  25. Fried B, Graczyk TK (1997) Advance in trematode biology. CRC Press, Boca Raton

    Google Scholar 

  26. Odening K (1961) Der dunckersche Muskelegel kann experimentell auf Affen übertragen werden. Monatsh Vet 16:395–399

    Google Scholar 

  27. Odening K (1963) Zur diagnostik der Mesocercarie von Alaria alata, eines möglichen Parasiten des Menschen in Europa, an Hand experimenteller befunde beim Affen. Mber Dtsch Akad Wiss Berlin 5:385–390

    Google Scholar 

  28. Fugassa MH (2020) Updated checklist of helminths found in terrestrial mammals of Argentine Patagonia. J Helminthol 94:1–56. https://doi.org/10.1017/s0022149x20000462

    Article  Google Scholar 

  29. Dubois G (1976) Description de l’adulte présumé de Bursotrema tetracotyloides Szidat, 1960, et d’une nouvelle spéce du genre Didelphodiplostomum Dubois, 1944, parasites de Didelphys azarae Temminck, 1825 (Trematoda: Alarinae). Ann Parasitol 51:341–347

    Article  CAS  Google Scholar 

  30. Blasco-Costa I, Poulin R, Presswell B (2017) Morphological description and molecular analyses of Tylodelphys sp. (Trematoda: Diplostomidae) newly recorded from the freshwater fish Gobiomorphus cotidianus (common bully) in New Zealand. J Helminthol 91:332–345. https://doi.org/10.1017/S0022149X16000298

    Article  CAS  PubMed  Google Scholar 

  31. Chikhlyaev IV, Ruchin AB (2022) Ecological analysis and biodiversity of the helminth community of the Pool frog Pelophylax lessonae (Amphibia: Anura) from floodplain and forest water bodies. Diversity 14:247. https://doi.org/10.3390/d14040247

    Article  Google Scholar 

  32. Drago FB, Lunaschi LI (2015) Update of checklist of digenean parasites of wild birds from Argentina, with comments about the extent of their inventory. Neotropical Helminthol 9:325–350

    Google Scholar 

  33. Szidat L, Nani A (1951) Diplostomiasis cerebralis del Pejerrey. Una grave Epizootia que afecta a la economía nacional producida por larvas de trematodes que destruyen el cerebro de los pejerreyes. Rev Inst Nac Inv Cs Nat (Argentina) 1:323–394

    Google Scholar 

  34. Flores V, Baccala N (1998) Multivariate analyses in the taxonomy of two species of Tylodelphys Diesing, 1850 (Trematoda: Diplostomidae) from Galaxias maculatus (Teleostei: Galaxiidae). Syst Parasitol 40:221–227

    Article  Google Scholar 

  35. Quaggiotto EA, Valverde F (1992) Nuevas metacercarias del género Tylodelphys (Trematoda, Diplostomatidae) en poblaciones lacustres de Galaxias maculatus (Teleostei, Galaxiidae). Bol Chil Parasitol 47:19–24

    CAS  PubMed  Google Scholar 

  36. Lunaschi LI, Sutton CA (1985) Trematodes de reptiles incorporados a la colección helmintológica del museo de La Plata. Neotropica 31:69–81

    Google Scholar 

  37. Lunaschi L, Drago FB (2010) Platyhelminthes, trematoda, digenea carus, 1863: distribution extension in argentina and new anura and ophidia hosts. Check List 6:447–450

    Article  Google Scholar 

  38. Hamann MI, Kehr AI, González CE (2006) Species affinity and infracommunity ordination of helminths of Leptodactylus chaquensis (Anura: Leptodactylidae) in two contrasting environments from northeastern Argentina. J Parasitol 92:1171–1179. https://doi.org/10.1645/ge-862r1.1

    Article  CAS  PubMed  Google Scholar 

  39. Martín J, López P (1990) Amphibians and reptiles as prey of birds in Southwestern Europe. Smithsonian Herpetological Information. Washington

  40. Panasci T, Whitacre DF (2000) Diet and foraging behavior of nesting roadside hawks in Petén, Guatemala. Wilson Bulletin 112:555–558

    Article  Google Scholar 

  41. Cortéz-Gómez AM, Ruiz-Agudelo CA, Valencia-Aguilar A, Ladle RJ (2015) Ecological functions of neotropical amphibians and reptiles: a review. Univ Sci 20:229–245

    Google Scholar 

  42. Lunaschi L, Drago FB (2006) Strigeids parasites of the roadside hawk, Buteo magnirostris (Aves: Falconiformes), from Argentina. Zootaxa 1106:25–33

    Article  Google Scholar 

  43. Lunaschi LI, Drago FB (2009) Species of Strigea (Digenea: Strigeidae), parasites of the savanna hawk Buteogallus meridionalis (Aves: Accipitridae) from Argentina, with the description of a new species. Folia Parasitol 56:268–274

    Article  Google Scholar 

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Acknowledgements

We thank Dr Margarita Ostrowski de Núñez for reviewing a draft version of the manuscript and making useful suggestions. We also thank the office of the Secretary of Natural Resources of Corrientes Province and Formosa Province, Argentina in authorizing the capture of amphibians for this research.

Funding

Financial support were provided by Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) through grant PIP 11220150100119, PUE 22920180100001CO, and Secretaría General de Ciencia y Técnica (SGCyT) PI 18Q001, 21Q001.

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All authors collected the data and provided critical feedback and helped shape the research, analysis and manuscript.

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Correspondence to M. I. Hamann.

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We certify that anuran species reported in the study is not threatened, and all procedures were approved by the ethics committee of the institution where the study was conducted.

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Hamann, M.I., Fernández, M.V. & González, C.E. Larval Digenean Parasitizing Amphibian Hosts from the Argentinian Chaco Region. Acta Parasit. 68, 194–207 (2023). https://doi.org/10.1007/s11686-022-00650-1

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