Hostname: page-component-848d4c4894-x24gv Total loading time: 0 Render date: 2024-05-14T14:39:17.633Z Has data issue: false hasContentIssue false
  • English
  • Français

Identification of the avian tracheal trematode Typhlocoelum cucumerinum (Trematoda: Cyclocoelidae) in a host–parasite–environment system: diagnosis, life cycle and molecular phylogeny

Published online by Cambridge University Press:  09 June 2021

Jordana C. A. Assis Open the ORCID record for Jordana C. A. Assis [Opens in a new window] ,
Danimar López-Hernández ,
Samantha Favoretto ,
Lilian B. Medeiros ,
Alan L. Melo ,
Nelson R. S. Martins  and
Hudson A. Pinto
Jordana C. A. Assis*
Affiliation:
Laboratório de Biologia de Trematoda, Department of Parasitology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
Danimar López-Hernández
Affiliation:
Laboratório de Biologia de Trematoda, Department of Parasitology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
Samantha Favoretto
Affiliation:
Department of Veterinary Medicine, Universidade Federal de Lavras, Lavras, Brazil
Lilian B. Medeiros
Affiliation:
Laboratório de Doenças das Aves, Department of Preventive Veterinary Medicine, Veterinary School, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
Alan L. Melo
Affiliation:
Laboratório de Biologia de Trematoda, Department of Parasitology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
Nelson R. S. Martins
Affiliation:
Laboratório de Doenças das Aves, Department of Preventive Veterinary Medicine, Veterinary School, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
Hudson A. Pinto
Affiliation:
Laboratório de Biologia de Trematoda, Department of Parasitology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
*
Author for correspondence: Jordana C. A. Assis, E-mail: jordanaalvesc@hotmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Typhlocoelum cucumerinum is a tracheal parasite of birds widely distributed across the globe. Nevertheless, aspects of the biology of this cyclocoelid are still poorly understood. Herein, we report the finding of T. cucumerinum in definitive and intermediate hosts from an urban waterbody of Brazil. The parasite was initially detected during the necropsy of domestic Muscovy ducks (Cairina moschata) found dead in the locality. Coproparasitological tests in live animals revealed that 12/47 (25.53%) Muscovy ducks and 2/8 (25%) mallards (Anas platyrhynchos platyrhynchos) were infected with T. cucumerinum. Moreover, rediae and metacercariae morphologically similar to T. cucumerinum were found in 3/248 (1.33%) Biomphalaria straminea collected in the same waterbody frequented by the birds. The conspecificity between the adult and the larval stages was confirmed molecularly (100% similarity in Cox-1). Moreover, the phylogenetic position of T. cucumerinum was determined for the first time based on partial fragments of the 28S, Cox-1 and Nad-1 genes. The species grouped with other members of the subfamily Typhlocoelinae with sequences available, but the data obtained do not support the distinctiveness of the genera Typhlocoelum and Tracheophilus. Further studies involving a broader range of species can result in taxonomic rearrangements in Typhlocoelinae.

Keywords

Typhlocoelinaelife cycledomestic waterfowlphylogeny
Type
Research Article
Information
Parasitology , Volume 148 , Issue 11 , September 2021 , pp. 1383 - 1391
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barry, MR (1959) Flukes in the respiratory tract of ducks. Australian Veterinary Journal 35, 432.CrossRefGoogle Scholar
Branton, SL, Deaton, JW, Gerlach, H and Ruff, MD (1985) Cyclocoelum mutabile infection and aortic rupture in an American coot (Fulica americana). Avian Diseases 29, 246–249.CrossRefGoogle Scholar
Clements, JF, Schulenberg, TS, Iliff, MJ, Billerman, SM, Fredericks, TA, Sullivan, BL and Wood, CL (2019) The eBird/Clements Checklist of Birds of the World:v2019. Available at https://www.birds.cornell.edu/clementschecklist/download/.Google Scholar
Dawes, B (1968) The Trematoda. London, UK: Cambridge University Press.Google Scholar
Diesing, KM (1850) Systema Helminthum, vol. 1. Braumüller: Voindobonae.Google Scholar
Dubois, G (1959) Revision des Cyclocoelidae Kossack 1911. Revue Suisse de Zoologie 66, 67–147.CrossRefGoogle Scholar
Dubois, G (1965) Notes sur les Cyclocoelidae Kossack, 1911 (Trematoda). Revue Suissse de Zoologie 72, 413–427.CrossRefGoogle Scholar
Frandsen, F and Christensen, NO (1984) An introductory guide to the identification of cercariae from African freshwater snails with special reference to cercariae of trematode species of medical and veterinary importance. Acta Tropica 41, 181–202.Google ScholarPubMed
Galaktionov, KV and Dobrovolskij, AA (2003) The Biology and Evolution of Trematodes. Dordrecht, Boston, London: Kluwer Academic Publishers.CrossRefGoogle Scholar
Galosi, L, Heneberg, P, Rossi, G, Sitko, J, Magi, GE and Perrucci, S (2019) Air sac trematodes: Morishitium polonicum as a newly identified cause of death in the common blackbird (Turdus merula). International Journal for Parasitology: Parasites and Wildlife 9, 74–79.Google Scholar
Ginetsinskaia, TA (1949) The life-cycle of the trematode Cyclocoelum microstomum (Creplin, 1829). Comptes Rendus de l´Acadadémie des Sciences de l´URSS 58, 509–512.Google Scholar
Gomez-Puerta, LA, Salas, MY, Lopez-Urbina, MT and Gonzalez, AE (2018) Diagnóstico morfológico y molecular de Cyclocoelum mutabile (Trematoda: Cyclocoelidae) en el Perú. Revista Peruana de Biologia 25, 315–320.CrossRefGoogle Scholar
Gower, WC (1939) Catalogue of the helminths of ducks. American Midland Naturalist 22, 580–628.CrossRefGoogle Scholar
Hoffman, W, Pons, JA and Janer, JL (1934) The sedimentation–concentration method in schistosomiasis mansoni. Puerto Rico Journal of Public Health and Tropical Medicine 9, 283–291.Google Scholar
Hoyos, CFE, Benavides, YMH and Garay, ODV (2017) Primer registro de Typhlocoelum cucumerinum (Trematoda: Typhlocoelidae) en Cairina moschata domestica (Aves: Anatidae) en Colombia. Revista de Medicina Veterinaria 33, 35–41.Google Scholar
Kanev, I, Radev, V and Fried, B (2002) Family Typhlocoelidae Harrah, 1922. In Gibson, DI, Jones, A and Bray, RA (eds), Keys to the Trematoda, volume I. London, UK: CAB International and The Natural History Museum, pp. 155–158.Google Scholar
Kinsella, JM and Forrester, DJ (1972) Helminths of the Florida duck, Anas platyrhynchus fulvigula. Proceedings of the Helminthological Society of Washington 39, 173–176.Google Scholar
Kossack, WE (1911) Über Monostomiden. Zoologische Jahrbücher Systematik 31, 491–590.Google Scholar
Krull, WH (1940) Notes on Typhlocoelum cymbium (Diesing, 1850); Cyclocoelidae. Transactions of the American Microscopical Society 59, 290–293.CrossRefGoogle Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA 7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Evolutionary Genetics Analysis 33, 1870–1874.Google ScholarPubMed
Lal, MB (1936) A new genus of trematodes of the Sub-family Typhlocoelinae from the shoveller duck, Spatula clypeata. Proceedings of the Indian Academy of Sciences – Section B 4, 45–51.Google Scholar
Lavery, HJ (1970) The comparative ecology of waterfowl in North Queensland. Wildfowl 21, 69–77.Google Scholar
Li, Y, Ma, XX, Lv, QB, Hu, Y, Qiu, HY, Chang, QC and Wang, CR (2020) Characterization of the complete mitochondrial genome sequence of Tracheophilus cymbius (Digenea), the first representative from the family Cyclocoelidae. Journal of Helminthology 94, e101.CrossRefGoogle Scholar
López-Jiménez, A, Pérez-Ponce, L and García-Varela, M (2018) Molecular data reveal high diversity of Uvulifer (Trematoda: Diplostomidae) in Middle America, with the description of a new species. Journal of Helminthology 92, 725–739.CrossRefGoogle ScholarPubMed
Manter, HW and Williams, OL (1928) Some monostomes from North American birds. Transactions of the American Microscopical Society 47, 90–93.CrossRefGoogle Scholar
McDonald, ME (1981) Key to Trematodes Reported in Waterfowl. Washington, USA: United States Department of the Interior – Fish and Wildlife Service.Google Scholar
McLaughlin, JD (1976) Experimental studies on the life cycle of Cyclocoelum mutabile (Zeder) (Trematoda: Cyclocoelidae). Canadian Journal of Zoology 54, 48–54.CrossRefGoogle Scholar
McLaughlin, JD (1986) The biology of Cyclocoelum mutabile (Trematoda) infections in American coots. Proceedings of the Helminthological Society of Washington 53, 177–181.Google Scholar
Middleton, BA and van der Valk, AG (1987) The food habits of greylag and bartheaded geese in the Keoladeo National Park, India. Botany Publication and Papers 88, 94–102.Google Scholar
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES science gateway for inference of phylogenetic trees. Conference: Gateway Computing Environments Workshop (GCE), 2010. DOI: 10.1109/GCE.2010.5676129.CrossRefGoogle Scholar
Miura, O, Kuris, AM, Torchin, ME, Hechinger, RF, Dunham, EJ and Chiba, S (2005) Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). International Journal for Parasitology 35, 793–780.CrossRefGoogle Scholar
Morgan, JAT and Blair, D (1998) Relative merits of nuclear ribosomal internal transcribed spacers and mitochondrial CO1 and ND1 genes for distinguishing among Echinostoma species (Trematoda). Parasitology 116, 289–297.CrossRefGoogle Scholar
Ohlweiler, FP, Eduardo, JM, Takahashi, FY, Crein, GA, Luca, LR and Oliveira, RC (2013) Larvas de trematódeos associadas a moluscos de água doce em municípios da Região Metropolitana de São Paulo, Estado de São Paulo, Brasil. Revista Pan-Amazônica de Saúde 4, 37–48.CrossRefGoogle Scholar
Oliveira, MB, Oliveira, ASS, Azevedo, APP, Silva, JR, Medeiros, TRN, Silva, GVSF, Cruz, MS and Bogéa, T (2020) Occurrence of Biomphalaria glabrata and Physa acuta (Gastropoda: Mollusca) snails in Quinta da Boa Vista Municipal Park, Rio de Janeiro, RJ, Brazil. Journal of Tropical Pathology 49, 274–282.Google Scholar
Paraense, WL (1970) Planorbídeos hospedeiros intermediários do Schistosoma mansoni. In Cunha, AS (ed). Esquistossomose mansoni. São Paulo, Brasil: Ed USP, pp. 13–30.Google Scholar
Paraense, WL (1994) Lymnaea peregrina Clessin, 1882, synonym of Lymnaea columella Say, 1817 (Gastropoda: Lymnaeidae). Memórias do Instituto Oswaldo Cruz 89, 561–566.CrossRefGoogle Scholar
Paraense, WL and Pointier, JP (2003) Physa acuta Draparnaud, 1805 (Gastropoda: Physidae): a study of topotypic specimens. Memórias do Instituto Oswaldo Cruz 98, 513–517.CrossRefGoogle ScholarPubMed
Pérez-Ponce de León, G and Hernández-Mena, DI (2019) Testing the higher-level phylogenetic classification of Digenea (Platyhelminthes, Trematoda) based on nuclear rDNA sequences before entering the age of the ‘next-generation’ Tree of Life. Journal of Helminthology 93, 260–276.CrossRefGoogle ScholarPubMed
Rambaut, A (2012) FigTree v.1.4.2: Tree Figure Drawing Tool. Available at http://tree.bio.ed.ac.uk/software/figtree.Google Scholar
Ronquist, F, Teslenko, M, Mark, PVD, Ayres, DL, Darling, A, Hohna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Ruiz, JM (1952) Contribuição ao estudo de formas larvárias de trematódeos brasileiros. 3 – Fauna de Belo Horizonte e Jaboticatubas, Estado de Minas Gerais. Memórias do Instituto Butantan 24, 45–62.Google Scholar
Schafranski, NL, Freitas, MG and Costa, JO (1975) Ciclo biológico de Typhlocoelum cucumerinum (Rudolphi, 1809) (Trematoda: Cyclocoelidae). Revista Brasileira de Biologia 35, 519–526.Google Scholar
Scott, ME, Rau, ME and McLaughlin, D (1980) Prevalence and intensity of Typhlocoelum cucumerinum (Digenea) in wild anatids of Quebec, Canada. Journal of Wildlife Diseases 16, 71–75.CrossRefGoogle ScholarPubMed
Scott, ME, Rau, ME and McLaughlin, JD (1982) A comparison of aspects of the biology of two subspecies of Typhlocoelum cucumerinum (Digenea: Cyclocoelidae) in three families of snails (Physidae, Lymnaeidae and Planorbidae). International Journal for Parasitology 12, 123–133.CrossRefGoogle Scholar
Silva, ROS, Gómez, SYM, Medeiros, LB, Marques, MVR, Silva, ASG, Mureb, EN, Junior, CAO, Favoretto, SM, Lobato, FCF and Martins, NRS (2017) Antitoxin therapy of natural avian botulism outbreaks occurred in Brazil. Anaerobe 48, 115–117.CrossRefGoogle ScholarPubMed
Sitko, J, Bizos, J and Heneberg, P (2017) Central European parasitic flatworms of the Cyclocoelidae Stossich, 1902 (Trematoda: Plagiorchiida): molecular and comparative morphological analysis suggests the reclassification of Cyclocoelum obscurum (Leidy, 1887) into the Harrahium Witenberg, 1926. Parasitology 144, 368–383.CrossRefGoogle ScholarPubMed
Soulsby, EJL (1982) Helminths, Artrhopods and Protozoa of Domesticated Animals, 7th Edn, London, UK: Baillière Tindall.Google Scholar
Stunkard, HW (1934) The life cycle of Typhlocoelum cymbium (Diesing, 1850). Kossack 1911 (Trematoda, Cydocoelidae). A contribution to the phytogeny of the Monostomes. Bulletin de la Société Zoologique de France 59, 447–466.Google Scholar
Szidat, LR (1932) Zur Entwicklungsgeschichte der Cyclocoeliden. Der Lebenszyklus von Tracheophilus sisowi Skrj. 1923. Zoologischer Anzeiger 100, 205–213.Google Scholar
Taft, SJ (1973) Some aspects of the larval development of Cyclocoelum obscurum (Trematoda: Cyclocoelidae). Journal of Parasitology 59, 90–93.CrossRefGoogle Scholar
Taft, SJ (1975) Aspects of the life history of Cyclocoelum brasilianum Stossich 1902 (Trematoda: Cyclocoelidae). Journal of Parasitology 61, 1041–1043.CrossRefGoogle Scholar
Taft, SJ (1986) Aspects of larval development and histochemistry of Ophthalmophagus singularis (Trematoda: Cyclocoelidae). Journal of Parasitology 72, 136–141.CrossRefGoogle Scholar
Taft, SJ and Heard, RW (1978) Aspects of the larval development of Ophthalmophagus sp. (Trematoda: Cyclocoelidae). Journal of Parasitology 64, 597–600.CrossRefGoogle Scholar
Tang, CT and Tang, C (1978) Studies on trematodes of the family Cyclocoelidae of Fujian with further remarks on the life history and epidemiology of Tracheophilus cymbius (Dies., 1850) Skrjabin, 1913. Acta Zoologica Sinica 24, 91–101 (in Chinese).Google Scholar
Taylor, MA, Coop, RL and Wall, RL (2017) Parasitologia Veterinária, 4th Edn, Rio de Janeiro, Brasil: Guanabara Koogan.Google Scholar
Tkach, VV, Littlewood, TJ, Olson, PD, Kinsella, M and Swiderski, Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56, 1–15.CrossRefGoogle Scholar
Tkach, VV, Kudlai, O and Kostadinova, A (2016) Molecular phylogeny and systematics of the Echinostomatoidea Looss, 1899 (Plathelminthes: Digenea). International Journal for Parasitology 46, 171–185.CrossRefGoogle Scholar
Travassos, L, Freitas, JFT and Kohn, A (1969) Trematódeos do Brasil. Memórias do Instituto Oswaldo Cruz 67, 583–586.Google Scholar
Urabe, M, Nor Hashim, EN, Uni, S, Iwaki, T, Halim, MRA, Marziki, ME, Udin, AS, Zainuri, NA, Omar, H, Agatsuma, T, Uga, S, Takaoka, H, Azirun, MS and Ramli, R (2020) Description and molecular characteristics of Morishitium polonicum malayense Urabe, Nor Hashin & Uni, n. subsp. (Trematoda: Cyclocoelidae) from the Asian glossy starling, Aplonis panayensis strigata (Passeriformes: Sturnidae) in Penisular Malaysia. Parasitology International 76, 102074.CrossRefGoogle Scholar
Yamaguti, S (1971) Synopsis of Digenetic Trematodes of Vertebrates, volume I and II. Tokyo, Japan: Keigaku Publishing.Google Scholar
Yamaguti, S (1975) A Synoptical Review of Life Histories of Digenetic Trematodes of Vertebrates. Tokyo, Japan: Keigaku Publishing.Google Scholar
Supplementary material: File

Assis et al. supplementary material

Assis et al. supplementary material

Download Assis et al. supplementary material(File)
File 21.5 KB