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Paramonostomum deseado n. sp. (Digenea: Notocotylidae) parasitizing the South American Black Oystercatcher and their atypical life cycle from the Patagonian coast

Published online by Cambridge University Press:  17 August 2022

Estefanía Bagnato
Affiliation:
Laboratorio de Investigaciones en Evolución y Biodiversidad (LIEB), Facultad de Ciencias Naturales y Ciencias de la Salud, Universidad Nacional de la Patagonia San Juan Bosco (UNPSJB), Ruta Nacional N° 259, 16.4 km, (9200) Esquel, Chubut, Argentina
Carmen Gilardoni*
Affiliation:
Laboratorio de Parasitología (LAPA), Instituto de Biología de Organismos Marinos (IBIOMAR, CCT CONICET-CENPAT), Boulevard Brown 2915, (9120) Puerto Madryn, Chubut, Argentina
Juan José Lauthier
Affiliation:
Facultad de Medicina, Instituto de Investigaciones en Microbiología y Parasitología Médica (IMPaM), Universidad de Buenos Aires (UBA-CONICET), Paraguay 2155, Piso 12, (1121) Ciudad Autónoma de Buenos Aires, Argentina
Florencia Cremonte
Affiliation:
Laboratorio de Parasitología (LAPA), Instituto de Biología de Organismos Marinos (IBIOMAR, CCT CONICET-CENPAT), Boulevard Brown 2915, (9120) Puerto Madryn, Chubut, Argentina
*
Author for correspondence: Carmen Gilardoni, E-mail: gilardonicarmen@gmail.com

Abstract

By way of morphological and molecular analysis we describe a new species of notocotylid, Paramonostomum deseado n. sp., parasitizing Haematopus ater from Argentina and we contribute to elucidate its life cycle. Within this genus, 4 groups can be morphologically distinguished according to body shape: ‘Oval’, ‘Pyriform’, ‘Elongate’, ‘Overlong’. The new species belongs to the ‘Elongate group’, which presents a wide variation in body length (597–4500 μm). The new species, Paramonostomum caeci from Australia, Paramonostomum actitidis from the Caribbean and Paramonostomum alveoelongatum from Russia share the smallest range of body size in this group (<1130 μm). The new species more closely resembles P. actitidis but differs from it by cirrus-sac length, which is shorter in the new species (97–146 vs 280–430 μm in P. actitidis), and egg size which is larger in the new species (25–33 vs 18–20 μm in P. actitidis). Paramonostomum deseado n. sp. uses the limpet Nacella magellanica as both first and second intermediate hosts in which metacercariae encyst inside the redia. This is the first abbreviated cycle described for notocotylid species. Ribosomal RNA sequences provided for adults (ITS1, ITS2 and 28S) and metacercariae inside the rediae (ITS1) support the species identification and the correspondence among stages. Phylogenetic analysis based on 28S placed P. deseado n. sp. close to other Notocotylus spp. and Paramonostomum anatis. Molecular results demonstrate that the hosts involved in the life cycles and the habitat more than morphological differences are determining the phylogenetic relationships in members of Notocotylidae.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Aranzamendi, MC, Bastida, R and Gardenal, CN (2011) Different evolutionary histories in two sympatric limpets of the genus Nacella (Patellogastropoda) in the South-western Atlantic coast. Marine Biology 158, 24052418. doi: 10.1007/s00227-011-1742-3CrossRefGoogle Scholar
Assis, JCA, Lopez-Hernández, D, Pulido-Murillo, EA, Melo, AL and Pinto, HA (2019) A morphological, molecular and life cycle study of the capybara parasite Hippocrepis hippocrepis (Trematoda: Notocotylidae). PLoS ONE 14, e0221662. doi: 10.1371/journal.pone.0221662CrossRefGoogle ScholarPubMed
Bagnato, E, Gilardoni, C, Di Giorgio, G and Cremonte, F (2015) A checklist of marine larval trematodes (Digenea) in molluscs from Argentina, Southwestern Atlantic coast. Check List 11, 110. doi: 10.15560/11.4.1706CrossRefGoogle Scholar
Barton, DP and Blair, D (2005) Family Notocotylidae Lühe, 1909. In Jones, A, Bray, RA and Gibson, DI (eds), Keys to the Trematoda, vol 2. London, UK: CABI Publishing and The Natural History Museum, pp. 383396.Google Scholar
Birmani, NA, Dharejo, AM, Naz, S, Khan, MM and Shaikh, AM (2013) Paramonostomum bubaki n. sp. (Digenea: Notocotylidae) from the Black Coot, Fulica atra (Gruiformes: Rallidae), in South Central Pakistan. International Scholarly Research Notices 2013, 15. doi: 10.1155/2013/656050Google Scholar
Birmani, NA, Dharejo, AM and Khan, MM (2020) Paramonostomum dadui n.sp. (Trematoda, Notocotylidae) in Fulica atra (Aves, Rallidae) of Manchhar Lake, Sindh, Pakistan. Pakistan Journal of Parasitology 69, 2125.Google Scholar
Blasco-Costa, I, Cutmore, SC, Miller, TL and Nolan, MJ (2016) Molecular approaches to trematode systematics: ‘best practice’ and implications for future study. Systematic Parasitology 93, 295306. doi: 10.1007/s11230-016-9631-2CrossRefGoogle ScholarPubMed
Boyce, K, Hide, G, Craig, PS, Harris, PD, Reynolds, C, Pickles, A and Rogan, MT (2012) Identification of a new species of digenean Notocotylus malhamensis n. sp. (Digenea: Notocotylidae) from the bank vole (Myodes glareolus) and the field vole (Microtus agrestis). Parasitology 139, 16301639. doi: 10.1017/S0031182012000911CrossRefGoogle Scholar
Bush, AO, Lafferty, KD, Lotz, JM, Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. Revisited. Journal of Parasitology 83, 575583. doi: 10.2307/3284227CrossRefGoogle Scholar
Cable, RM, Connor, RS and Balling, JW (1960) Digenetic trematodes of Puerto Rican shore birds. Scientific Survey of Porto Rico and the Virgen Islands 17, 187225.Google Scholar
Capasso, S, Servián, A, Tkach, VV and Diaz, JI (2020) Notocotylus chionis (Trematoda: Notocotylidae) and Notocotylus sp. from shorebirds in southern Patagonian wetlands of Argentina: morphological and molecular studies. Polar Biology 43, 19571966. doi: 10.1007/s00300-020-02753-9CrossRefGoogle Scholar
Creplin, FCH (1846) Nachtrage zu Gurlt's Verzeichniss der Thiere, bei welchen Entozoen gefunden worden sind. Archiv für Naturgeschichte (Berlin) 1, 129160.Google Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772. doi: 10.1038/nmeth.2109CrossRefGoogle ScholarPubMed
Dereeper, A, Guignon, V, Blanc, G, Audic, S, Buffet, S, Chevenet, F, Dufayard, JF, Guindon, S, Lefort, V, Lescot, M, Claverie, JM and Gascuel, O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research 36, 465469. doi: 10.1093/nar/gkn180CrossRefGoogle ScholarPubMed
Dereeper, A, Audic, S, Claverie, JM and Blanc, G (2010) BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evolutionary Biology 10, 1-6. doi: 10.1186/1471-2148-10-8CrossRefGoogle ScholarPubMed
Diaz, JI, Gilardoni, C, Lorenti, E and Cremonte, F (2020) Notocotylus primulus n. sp. (Trematoda: Notocotylidae) from the crested duck Lophonetta specularioides (Aves, Anatidae) from Patagonian coast, southwestern Atlantic Ocean. Parasitology International 74, 101976. doi: 10.1016/j.parint.2019.101976CrossRefGoogle Scholar
Dollfus, R (1966) Sur Monostoma petasatum Deslongchamps 1824 et son cycle évolutif à deux hôtes. Annales de Parasitologie (Paris) 41, 289299.Google Scholar
Drago, FB, Lunaschi, LI, Hinojosa-Sáez, AC and González-Acuña, D (2007) First record of Australapatemon burti and Paramonostomum pseudalveatum (Digenea) from Anas georgica (Aves, Anseriformes) in Chile. Acta Parasitologica 52, 201205. doi: 10.2478/s11686-007-0040-1CrossRefGoogle Scholar
Evans, DW, Irwin, SWB and Fitzpatrick, SM (1997) Metacercarial encystment and in vivo cultivation of Cercaria lebouri Stunkard 1932 (Digenea: Notocotylidae) to adults identified as Paramostomum chabaudi Van Strydonck 1965. International Journal for Parasitology 27, 12991304. doi: 10.1016/S0020-7519(97)00102-1CrossRefGoogle ScholarPubMed
Fernandes, BMM, Justo, MCN, Cárdenas, MQ and Cohen, SC (2015) South American trematodes parasites of birds and mammals. Rio de Janeiro, Brazil: Oficina de Livros.Google Scholar
Filimonova, LV (1985) Trematode fauna of the USSR. Notocotylidae. Moscow: Nauka.Google Scholar
Fraija-Fernández, N, Olson, PD, Crespo, EA, Raga, JA, Aznar, FJ and Fernández, M (2015) Independent host switching events by digenean parasites of cetaceans inferred from ribosomal RNA. International Journal for Parasitology 45, 167173. doi: 10.1016/j.ijpara.2014.10.004CrossRefGoogle Scholar
Garkavi, BL (1965) Paramonostomum anatis n. sp. (Trematoda: Notocotylinae Kosack, 1911) from clomlie duck. Proceedings of the Krasnodar Scientific Research. vet. Stations 3, 325327.Google Scholar
Garkavi, BL (1968) Developmental cycles of Paramonostomum pseudalveatum Price, 1931 and Paramonostomum anatis Garkawi, 1965 (Trematoda, Notocotylidae). Helminths of man, animals and plants and measures of their control. Moscow, Russia: Izdatel'stvo Akademii Nauk SSSR, pp. 140145.Google Scholar
Gilardoni, C, Di Giorgio, G, Bagnato, E and Cremonte, F (2019) Survey of trematodes in intertidal snails from Patagonia, Argentina: new larval forms and diversity assessment. Journal of Helminthology 93, 342351. doi: 10.1017/S0022149X18000329CrossRefGoogle ScholarPubMed
Gilardoni, C, Di Giorgio, G, Bagnato, E, Pina, S, Rodrigues, P and Cremonte, F (2020) A potential zoonotic parasite, the digenean Gymnophalloides nacellae, on the Magellanic coast in the southwestern Atlantic Ocean: its life cycle and geographical distribution. Polar Biology 43, 725734. doi: 10.1007/s00300-020-02674-7CrossRefGoogle Scholar
Gonchar, A and Galaktionov, KV (2020) New data support phylogeographic patterns in a marine parasite Tristriata anatis (Digenea: Notocotylidae). Journal of Helminthology 94, e79. doi: 10.1017/S0022149X19000786CrossRefGoogle Scholar
Gonchar, A and Galaktionov, KV (2021) It is marine: distinguishing a new species of Catatropis (Digenea: Notocotylidae) from its freshwater twin. Parasitology 148, 7483. doi: 10.1017/S0031182020001808CrossRefGoogle ScholarPubMed
Gonchar, A and Galaktionov, KV (2022) The Pacific Notocotylus atlanticus (Digenea: Notocotylidae). Parasitology International 88, 102559. doi: 10.1016/j.parint.2022.102559CrossRefGoogle ScholarPubMed
Gonchar, A, Jouet, D, Skírnisson, K, Krupenko, D and Galaktionov, KV (2019) Transatlantic discovery of Notocotylus atlanticus (Digenea: Notocotylidae) based on life cycle data. Parasitology Research 118, 14451456. doi: 10.1007/s00436-019-06297-8CrossRefGoogle ScholarPubMed
Graefe, G (1968) Paramonostomum antarcticum n. sp. (Trematoda: Notocotylidae) und Beobachtungen zur Larvenentwicklung in der Antarktis. Zeitschrift für Parasitenkde 30, 207232.Google Scholar
Harwood, PD (1939) Notes on Tennessee helminths. IV. North American trematodes of the subfamily Notocotylinae. Journal of the Tennessee Academy of Science 14, 332340.Google Scholar
Hechinger, RF (2012) Faunal survey and identification key for the trematodes (Platyhelminthes: Digenea) infecting Potamopyrgus antipodarum (Gastropoda: Hydrobiidae) as first intermediate host. Zootaxa 3418, 127. doi: 10.11646/zootaxa.3418.1.1CrossRefGoogle Scholar
Holton, AL (1984) A redescription of Coitocaecum parvum Crowcroft, 1945 (Digenea: Allocreadiidae) from crustacean and fish hosts in Canterbury. New Zealand Journal of Zoology 11, 18.CrossRefGoogle Scholar
Huelsenbeck, JP and Ronquist, F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755. doi: 10.1093/bioinformatics/17.8.754CrossRefGoogle ScholarPubMed
Izrailskaia, AV, Besprozvannykh, VV, Tatonova, YV, Nguyen, HM and Ngo, HD (2019) Developmental stages of Notocotylus magniovatus Yamaguti, 1934, Catatropis vietnamensis n. sp., Pseudocatatropis dvoryadkini n. sp., and phylogenetic relationships of Notocotylidae Lühe, 1909. Parasitology Research 118, 469481. doi: 10.1007/s00436-018-6182-2CrossRefGoogle Scholar
Jones, NV and Williams, IC (1969) Paramonostomum signiensis n. sp. (Trematoda: Notocotylidae) from the Sheathbill, Chionis alba (Gmelin), at Signy Island, South Orkney Islands. Journal of Helminthology 43, 5357.CrossRefGoogle Scholar
Joyeux, C (1922) Recherches sur les notocotyles. Bulletin de la Société de Pathologie Exotique et de sa Filiale de l'Ouest-African 15, 331343.Google Scholar
Kulachkova, VG (1954) The life cycle and pathogenic significance of the trematode, Paramonostomum alveatum (Mehlis, 1846). Trudi Problemnikhi Tematicheskikh Soveshchani. Akademiya Nauk SSSR 4, 118122.Google Scholar
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 15471549. doi: 10.1093/molbev/msy096CrossRefGoogle ScholarPubMed
Lühe, BVM (1909) Parasitische Plattwürmer, I: trematodes. In Brauer, HVA (ed.), Die Süsswasserfauna Deutschlands. Jena, Germany: Verlag von Gustav Fischer, p. 230.Google Scholar
McDonald, ME (1981) Keys to trematodes reported in waterfowl, Resource Publication 142.Washington, DC, USA: Department of the Interior, Fish and Wildlife Services.Google Scholar
Nasir, P, Díaz, MT and Guevara, DLDE (1970) Some avian digenetic trematodes of eastern Venezuela. Rivista di Parassitologia 31, 107112.Google ScholarPubMed
Odening, K (1966) Physidae and Planorbidae als Wirte in den Lebenszyklen einheimischer Notocotylidae (Trematoda: Paramphistomida). Zeitschrift fur Parasitenkunde 27, 210239.CrossRefGoogle ScholarPubMed
Odening, K (1982) Paramonostomum antarcticum (Trematoda, Notocotylidae) in Larus dominicanus from South Shetlands (Antarctica). Angewandte Parasitologie 23, 137143.Google ScholarPubMed
Povedano, HE (2016) Aves de la provincia de Río Negro-Identificación-Distribución-Estatus. La Plata, Buenos Aires, Argentina: Hernán Emilio Povedano.Google Scholar
Price, EW (1931) Four new species of trematode worms from the muskrat, Ondrata zibethica with a key to the trematode parasites of the muskrat. Proceedings of the United States National Museum 79, 113.Google Scholar
Sasaki, M, Kobayashi, M, Yoshino, T, Asakawa, M and Nakao, M (2021) Notocotylus ikutai n. sp. (Digenea: Notocotylidae) from lymnaeid snails and anatid birds in Hokkaido, Japan. Parasitology International 83, 102318. doi: 10.1016/j.parint.2021.102318CrossRefGoogle Scholar
Skirnisson, K and Galaktionov, KV (2002) Life cycles and transmission patterns of seabird digeneans in SW Iceland. Sarsia 87, 144151.CrossRefGoogle Scholar
Smith, SJ and Hickman, JL (1983) Two notocotylid trematodes from birds in Tasmania and their life histories. Royal Society of Tasmania 117, 85103.CrossRefGoogle Scholar
Stunkard, HW (1967) Studies on the trematode genus Paramonostomum Lühe, 1909 (Digenea: Notocotylidae). Biological Bulletin 132, 133145.CrossRefGoogle ScholarPubMed
Stunkard, HW and Dunihue, FW (1931) Notes on trematodes from a Long Island duck with description of a new species. Biological Bulletin 60, 179186.CrossRefGoogle Scholar
Thebo, KA, Naz, S, Dharejo, AM, Siyal, S and Birmani, NA (2019) A new record and new species of a digenic trematode from common pochard Aythya ferina (Anseriformes: Anatidae) in Sindh, Pakistan. Journal of Entomology and Zoology Studies 7, 151154.Google Scholar
Travassos, L (1921) Trematódeos novos II. Brazil Médico 35, 179180.Google Scholar
Travassos, L, Freitas, JFT and Kohn, A (1969) Trematódeos do Brasil. In Memórias do Instituto Oswaldo Cruz, Vol. 67, pp. 705707Google Scholar
Van Strydonck, D (1965) Espèces du genre Paramonostomum Lühe, 1909 (fam. Notocotylidae Lühe, 1909). Annales de Parasitologie Humaine et Comparee 40, 141148.CrossRefGoogle Scholar
Velasquez, CC (1969) Life history of Paramonostomum philippinensis sp. n. (Trematoda: Digenea: Notocotylidae). Journal of Parasitology 55, 289292.CrossRefGoogle Scholar
Winterbourn, MJ (1973) Larval Trematoda parasitising the New Zealand species of Potamopyrgus (Gastropoda: Hydrobiidae). Mauri Ora 2, 1730.Google Scholar
Woods, RW (2014) Conservation assessment of the Blackish Oystercatcher Haematopus ater. International Wader Studies 20, 109115.Google Scholar
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