Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2021-03-22
Page range: 404–418
Abstract views: 225
PDF downloaded: 13

A new schistosome (Digenea: Schistosomatidae) from the nasal tissue of South America black-necked swans, Cygnus melancoryphus (Anatidae) and the endemic pulmonate snail Chilina gibbosa

Laboratorio de Parasitología, INIBIOMA (CONICET-Universidad Nacional del Comahue).
Laboratorio de Parasitología, INIBIOMA (CONICET-Universidad Nacional del Comahue).
Laboratorio de Parasitología, INIBIOMA (CONICET-Universidad Nacional del Comahue).
Museum of Southwestern Biology, Center for Evolutionary and Theoretical Immunology, Department of Biology, University of New Mexico.
Museum of Southwestern Biology, Center for Evolutionary and Theoretical Immunology, Department of Biology, University of New Mexico
Platyhelminthes cercariae Argentina Chilina gibbosa Nasusbilharzia n. gen. Nasusbilharzia melancorhypha n. sp. nasal tissue snail Schistosomatidae waterfowl

Abstract

To date, 9 species of Schistosomatidae have been found parasitizing the nasal tissues of mammal and bird hosts in the Eastern Hemisphere, 5 species in Rwanda (Africa), 2 in Australia (Oceania) and 2 in Eurasia. During a parasitological survey of black necked swans, Cygnus melancoryphus, an anatid endemic to South America, schistosome worms in the nasal tissue were found; the first in the Americas. Morphological results based on male worms and in isolated eggs. The worms have a spiny tegument, filiform body with rounded posterior end, two muscular suckers, a robust gynaecophoric channel with thickened cross bands, and around 130 testes. The eggs are elongate with an asymmetrical bulge, with a slender process at one end and a longer curved process at the other. Diagnostic morphological characteristics do not match with any schistosome genus. Part of the mitochondrial cox1 and nuclear DNA 28S partial genes were sequenced and compared to Schistosomatidae in GenBank. The genetic results confirm the distinctiveness of the specimens since they do not group with any described genus or undescribed lineage other than cercariae of “Chilina lineage 1” that emerge from the Patagonian Chilina gibbosa, a freshwater snail endemic to South America. Based on morphological and genetic characterization of these schistosomes, these specimens represent a new genus and species that parasitizes black necked swans as adults in the nasal tissue, and C. gibbosa is the first intermediate host, both hosts being endemic to South America.

 

References

  1. Akramova, F., Azimov, D. & Shakarboev, E. (2010) The morphology and biology of the trematode Gigantobilharzia acotylea (Digenea, Schistosomatidae). Vestnik Zoologii, 44, 403–412.

    https://doi.org/10.2478/v10058-010-0026-6

    Ashrafi, K., Nouroosta, A., Sharifdini, M., Mahmoudi, M.R., Rahmati, B. & Brant, S.V. (2018) Genetic diversity of an avian nasal schistosome causing cercarial dermatitis in the Black Sea-Mediterranean migratory route. Parasitology Research, 117, 3821–3833.

    https://doi.org/10.1007/s00436-018-6087-0

    Agrawal, M.C. (2012) Schistosomes and schistosomiasis in South Asia. Springer, New Delhi, 350 pp.

    https://doi.org/10.1007/978-81-322-0539-5

    BirdLife International (2016) Cygnus melancoryphus. The IUCN Red List of Threatened Species, 2016, e.T22679846A92832118.

    https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T22679846A92832118.en

    Blair, D. & Islam, K.S. (1983) The life-cycle and morphology of Trichobilharzia australis n. sp. (Digenea: Schistosomatidae) from the nasal blood vessels of the black duck (Anas superciliosa) in Australia, with a review of the genus Trichobilharzia. Systematic Parasitology, 5, 89–117.

    https://doi.org/10.1007/BF00049237

    Brant, S., Morgan, J.T., Mkoji, G.M., Snyder, S.D., Rajapakse, R.P.V. & Loker, E.S. (2006) An approach to revealing blood fluke life cycles, taxonomy, and diversity: provision of key reference data including DNA sequence from single life cycle stages. Parasitology, 92, 77–88.

    https://doi.org/10.1645/GE-3515.1

    Brant, S.V., Jouet, D., Ferte, H. & Loker, E.S. (2013) Anserobilharzia gen. n. (Digenea, Schistosomatidae) and redescription of A. brantae (Farr & Blankemeyer, 1956) comb. n. (syn. Trichobilharzia brantae), a parasite of geese (Anseriformes). Zootaxa, 3670 (2), 193–206.

    https://doi.org/10.11646/zootaxa.3670.2.5

    Brant, S.V., Loker, E.S., Casalins, L. & Flores, V. (2017) Phylogenetic placement of a schistosome from an unusual marine snail host, the false limpet (Siphonaria lessoni) and gulls (Larus dominicanus) from Argentina with a brief review of marine schistosomes. Journal of Parasitology, 103, 75–82.

    https://doi.org/10.1645/16-43

    Del Hoyo, J., Elliott, A. & Sargatal, J. (1992) Handbook of the Birds of the World. Vol. 1. Lynx Editions, Barcelona, 696 pp.

    Ebbs, E., Loker, E.S., Davis, N.E., Flores, V., Veleizán, A. & Brant, S.V. (2016) Schistosomes with wings: how host phylogeny and ecology shape the global distribution of Trichobilharzia querquedulae (Schistosomatidae). International Journal for Parasitology, 46, 669–677.

    https://doi.org/10.1016/j.ijpara.2016.04.009

    Fain, A. (1955a) Recherches sur les Schistosomes d’Oiseaux au Ruanda-Urundi (Congo belge) Découverte d’une nouvelle bilharziose aviaire. La trichobilharziose nasale, le description de Schistosomes nouveaux. Revue de Zoologie et de Botanique Africaines, 51, 373–387.

    Fain, A. (1955b) Étude sur les schistosomes d’oiseaux au Ruanda-Urundi (Congo Belge) un nouveau schistosome du tantale ibis (Ibis ibis Lin). Gigantobilharzia tantali n. sp. Annales de Parasitologie Humaine et Comparée, 30, 321–329.

    https://doi.org/10.1051/parasite/1955304321

    Fain, A. (1956) Les Schistosomes d’Oiseaux du Genre Trichobilharzia Skrjabin et Zakharow, 1920 au Ruanda-Urundi. Revue de Zoologie et de Botanique Africaines, 54, 147–178.

    Fain, A. (1959) Un nouveau schistosome du genre Trichobilharzia dans les fosses nasales du canard nain. Revue de Zoologie et de Botanique Africaines, 60, 227–232.

    Fakhar, M., Ghobaditara, M., Brant, S.V., Karamian, M., Gohardehi, S. & Bastania, R. (2016) Phylogenetic analysis of nasal avian schistosomes (Trichobilharzia) from aquatic birds in Mazandaran Province, northern Iran. Parasitology International, 65, 151–158.

    https://doi.org/10.1016/j.parint.2015.11.009

    Flores V. R., Brant S. V. & Loker E. S. (2015). Avian schistosomes from the South American endemic gastropod genus Chilina (Pulmonata, Chilinidae), with a brief review of South American schistosome species. Journal of Parasitology, 101, 565–576.

    https://doi.org/10.1645/14-639

    Fuentealba, C., Figueroa , R. & Morrone, J.J. (2010) Análisis de endemismo de moluscos dulceacuícolas de Chile. Revista Chilena de Historia Natural, 83, 289–298.

    https://doi.org/10.4067/S0716-078X2010000200009

    González-Acuña, D., Moreno, L., Cichino, A., Mironov, S. & Kinsella M. (2010) Checklist of the parasites of the black-necked swan, Cygnus melanocoryphus (Aves: Anatidae), with new records from Chile. Zootaxa, 2637 (1), 55–68.

    https://doi.org/10.11646/zootaxa.2637.1.3

    Horák, P., Kolářová, L. & Dvořák, J. (1998) Trichobilharzia regenti n. sp. (Schistosomatidae, Bilharziellinae), a new nasal schistosome from Europe. Parasite, 5, 349–357.

    https://doi.org/10.1051/parasite/1998054349

    Horák, P., Mikeš, L., Lichtenbergová, L., Skála, V., Soldánová, M. & Brant, S.V. (2015) Avian schistosomes and outbreaks of cercarial dermatitis. Clinical Microbiology Review, 28, 165–190.

    https://doi.org/10.1128/CMR.00043-14

    Huelsenbeck, J.P. & Ronquist, F. (2001). MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755.

    https://doi.org/10.1093/bioinformatics/17.8.754

    Islam, K.S. (1986) The morphology and life-cycle of Trichobilharzia arcuata n. sp. (Schistosomatidae: Bilharziellinae) a nasal schistosome of water whistle ducks (Dendrocygna arcuata) in Australia. Systematic Parasitology, 8, 117–128.

    https://doi.org/10.1007/BF00009868

    Khalil, L.F. (2002) Family Schistosomatidae Stiles and Hassall, 1898. In: Gibson, D., Jones, A. & Bray, R. (Eds.), Keys to Trematode. Vol. 1. CABI Org., The Natural History Museum, London, pp. 419–432.

    https://doi.org/10.1079/9780851995472.0419

    Kolářová, L., Rudolfová, J., Hampl, V. & Skírnisson, K. (2006) Allobilharzia visceralis gen. nov., sp. nov. (Schistosomatidae-Trematoda) from Cygnus cygnus (L.) (Anatidae). Parasitology International, 55, 179–186.

    https://doi.org/10.1016/j.parint.2005.10.009

    Lunaschi, L., Cremonte, F. & Drago, F. (2007) Checklist of digenean parasites of birds from Argentina. Zootaxa, 1403 (1), 1–36.

    https://doi.org/10.11646/zootaxa.1403.1.1

    Martorelli, S.R. (1981) Dendritobilharzia rionegrensis sp. nov. (Digenea: Schistosomatidae). Parásita de las venas mesentéricas de Fulica rufrifrons (Aves: Rallidae). Neotrópica, 27, 171–177.

    Martorelli, S.R. (1984) Sobre una cercaria de la familia Schistosomatidae (Digenea) parásita de Chilina gibbosa Sowerby, 1841 en el lago Pellegrini, Provincia de Río Negro, República Argentina. Neotrópica, 30, 97–106.

    Martorelli, S.R. (1989) Estudios parasitológicos en la albufera de Mar Chiquita, provincia de Buenos Aires, República Argentina. II: Cercarias (Digenea) parásitas de Heleobia conexa (Mollusca: Hydrobiidae), pertenecientes a las familias Schistosomatidae, Haploporidae y Homalometridae. Neotrópica, 35, 81–90.

    Morgan, J.A.T., Dejong, R.J., Adeoye, G.O., Ansa, E.D.O., Barbosa, C.S., Brémind, P., Cesari, I.M., Charbonnel, N., Correa, L.R., Coulibaly, G., D’Andrea, P.S., De Souza, C.P., Doenhoff, M.J., File, S., Idris, M.A., Incani, R.N., Jarne, P., Karanja, D.M.S., Kazibwe, F., Kpikpi, J., LWambo, N.J.S., Mabaye, A., Magalhaes, L.A., Makundi, A., Moné, H., Mouahid, G., Muchemi, G.M., Mungai, B.N., Séne, M., Southgate, V., Tchuenté, L.A.T., Théron, A., Yousif, F., Zanotti‐Magalhaes, E.M., Mkoji, G.M. & Loker, E.S. (2005) Origin and diversification of the human parasite Schistosoma mansoni. Molecular Ecology, 14, 3889–3902.

    https://doi.org/10.1111/j.1365-294X.2005.02709.x

    Posada, D. & Crandall, K.A. (1998) Modeltest: Testing the model of DNA substitution. Bioinformatics, 14, 817–818.

    https://doi.org/10.1093/bioinformatics/14.9.817

    Odhner, T. (1910) Gigantobilharzia acotylea n. g. n. sp., ein mit den Bilharzien verwandter Blutparasit von enormer Lange. Zoologischer Anzeiger, 35, 380–385.

    Ostrowski de Núñez, M. (1978) Fauna de agua dulce de la República Argentina. VII. Cercarias de la familia Schistosomatidae (Trematoda, Digenea). Revista del Museo Argentino de Ciencias Naturales Bernardino Rivadavia, 3, 65–76.

    Oyarzún-Ruiz, P., Muñoz, P., Paredes, E., Valenzuela, G. & Ruiz, J. (2019) Gastrointestinal helminths and related histopathological lesions in black-necked swans Cygnus melancoryphus from the Carlos Anwandter Nature Sanctuary, Southern Chile. Revista Brasileira de Parasitologia Veterinária, 28, 613–624.

    https://doi.org/10.1590/s1984-29612019063

    Rao, M.A.N. (1933). Bovine nasal schistosomiasis in the Madras Presidency with a description of the parasite. Indian Journal of Veterinary Science and Animal Husbandry, 3, 29–38.

    Rumi, A., Gutiérrez Gregoric, D.E., Núñez, V. & Darrigran, G.A. (2008) Malacología Latinoamericana. Moluscos de agua dulce de Argentina. Revista de Biología Tropical, 56, 77–111.

    https://doi.org/10.15517/rbt.v56i1.5510

    Sambon, L.W. (1907) New or little known African Entozoa. Journal of Tropical Medicine and Hygiene, 10, 117

    Skrjabin, K.I. & Zakharov, N.P. (1920) Zwei neue Trematodengattungen aus den Blutgefässen der Vögel. (Beitrag zur Kenntnis der Helminthenfauna der Vögel Russlands) [in Russian] Izvestiya Donskogo Veterinarnogo Instituta, 2, 1–6.

    Szidat, L. (1951) Cercarias schistosómicas y dermatitis schistosómica humana en la República Argentina. Comunicación del Instituto Nacional de Investigación de las Ciencias Naturales, Ciencias Zoológicas, Tomo II, 129–150.

    Szidat, L. (1958) Investigaciones sobre Cercaria chascomusi n. sp. agente causal de la una nueva enfermedad humana en la Argentina. Boletín del Museo de Ciencias Naturales ‘‘Bernardino Rivadavia’’ e Instituto Nacional de Investigación de las Ciencias Naturales, Ciencias Zoológicas, 18, 1–16.

    Valenzuela, G., Araya, A., Oyarzún-Ruiz, P. & Muñoz, P. (2018) Helmintofauna del cisne de cuello negro Cygnus melancoryphus (Aves: Anatidae) del Santuario de la Naturaleza Carlos Anwandter, Valdivia, Chile. Revista Mexicana de Biodiversidad, 89, 568–571.

    https://doi.org/10.22201/ib.20078706e.2018.2.2323

    Valdovinos-Zarges, C.V. (2006) Estado de conocimiento de los gasterópodos dulceacuícolas de Chile. Gayana, 70, 88–95.

    https://doi.org/10.4067/S0717-65382006000100014

    Vande Vusse, F.J. (1980) A review of the genus Dendritobilharzia Skrjabin and Zakharow 1920 (Trematoda: Schistosomatidae). Journal of Parasitology, 66, 814–822.

    https://doi.org/10.2307/3280675