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Evidence that host ecology drives first intermediate host use in the Didymozoidae (Trematoda: Hemiuroidea): an asexual infection in a vermetid (Gastropoda)

Published online by Cambridge University Press:  09 December 2022

C. Louvard Open the ORCID record for C. Louvard [Opens in a new window] ,
R. D. Corner ,
S. C. Cutmore  and
T. H. Cribb
C. Louvard*
Affiliation:
Marine Parasitology Laboratory, The University of Queensland, School of Biological Sciences, St Lucia, QLD 4072, Australia
R. D. Corner
Affiliation:
Marine Parasitology Laboratory, The University of Queensland, School of Biological Sciences, St Lucia, QLD 4072, Australia
S. C. Cutmore
Affiliation:
Queensland Museum, Biodiversity and Geosciences Program, South Brisbane, Queensland 4101, Australia
T. H. Cribb
Affiliation:
Marine Parasitology Laboratory, The University of Queensland, School of Biological Sciences, St Lucia, QLD 4072, Australia
*
Author for correspondence: C. Louvard, E-mail: clarisse.louvard@uqconnect.edu.au
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Abstract

The Didymozoidae (Trematoda: Hemiuroidea) is among the most speciose trematode families, known from a wide range of marine teleost fishes. Despite their richness, however, didymozoid life cycles are unusually poorly known; only two first intermediate hosts are known, a marine bivalve (Anadara trapezia) and a pelagic gastropod (Firoloida desmarestia). This study uses multi-locus molecular sequence data to identify a novel first intermediate host for the family, a sessile gastropod of the genus Thylacodes Guettard (Vermetidae). The didymozoid infection is not identified to species but, based on molecular phylogenetic analyses, it is close to Saccularina magnacetabula Louvard et al., 2022, which uses a bivalve as a first intermediate host. The distribution of known first intermediate hosts of didymozoids (a bivalve, a holoplanktonic gastropod and a sessile gastropod that feeds with the use of mucus nets) suggests that first intermediate host use within the Didymozoidae has been opportunistically driven by the trophic ecology of potential mollusc hosts and has involved significant host-switching events.

Keywords

DidymozoidaeHemiuroidealife cycleVermetidaephylogeny
Type
Research Paper
Information
Journal of Helminthology , Volume 96 , 2022 , e88
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Agosta, SJ and Klemens, JA (2008) Ecological fitting by phenotypically flexible genotypes: implications for species associations, community assembly and evolution. Ecology Letters 11(11), 1123–1134.10.1111/j.1461-0248.2008.01237.xCrossRefGoogle ScholarPubMed
Akaike, HA (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19(6), 716–723.10.1109/TAC.1974.1100705CrossRefGoogle Scholar
Anderson, GR (1998) Inference of phylogeny and taxonomy within the Didymozoidae (Digenea) from the second internal transcribed spacer (ITS2) of ribosomal DNA. Systematic Parasitology 41(1), 87–94.10.1023/A:1006024128098CrossRefGoogle Scholar
Araujo, SB, Pires Braga, M, Brooks, DR, Agosta, SJ, Hoberg, EP, von Hartenthal, FW and Boeger, WA (2015) Understanding host-switching by ecological fitting. PLoS One 10(10), e0139225.10.1371/journal.pone.0139225CrossRefGoogle ScholarPubMed
Blair, D (1984) Elytrophallus carettae sp. n. (Digenea: Hemiuridae) from the stomach of loggerhead turtles (Caretta caretta L.) from Australia. Proceedings of the Helminthological Society of Washington 51(1), 135–139.Google Scholar
Bonnevie, K (1916) Mitteilungen über Pteropoden. 1. Beobachtungen über den Geschlechtsapparat von Cuverina columnella Rang [Notices of Pteropods. 1. Observations on the reproductive system of Cuverina columnella Rang]. Jenaische Zeitschrift für Naturwissenschaft 54(1), 245–276. [In German.]Google Scholar
Bowles, J, Hope, M, Tiu, WU, Liu, XS and McManus, DP (1993) Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum. Acta Tropica 55(4), 217–229.10.1016/0001-706X(93)90079-QCrossRefGoogle ScholarPubMed
Brooks, DR, O'Grady, RT and Glen, DR (1985) Phylogenetic analysis of the Digenea (Platyhelminthes: Cercomeria) with comments on their adaptive radiation. Canadian Journal of Zoology 63(2), 411–443.10.1139/z85-062CrossRefGoogle Scholar
Buchmann, W (1924) Über den Pharynx der Heteropoden [About the pharynx of the heteropods]. Zeitschrift für Anatomie und Entwicklungsgeschichte 73(1), 501–540.10.1007/BF02117185CrossRefGoogle Scholar
Calhoun, DM, Curran, SS, Pulis, EE, Provaznik, JM and Franks, JS (2013) Hirudinella ventricosa (Pallas, 1774) Baird, 1853 represents a species complex based on ribosomal DNA. Systematic Parasitology 86(1), 197–208.10.1007/s11230-013-9439-2CrossRefGoogle ScholarPubMed
Castresana, J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology & Evolution 17(4), 540–552.10.1093/oxfordjournals.molbev.a026334CrossRefGoogle ScholarPubMed
Castro, T (2019) Parasitological study of the Peruvian scallop Argopecten purpuratus (Lamarck, 1819), in Sechura and Samanco Bays, Peru. Boletín Instituto del Mar del Perú 34(1), 135–150.Google Scholar
Claxton, AT, Fuehring, AD, Andres, MJ, Moncrief, TD and Curran, SS (2017) Parasites of the vermilion snapper, Rhomboplites aurorubens (Cuvier), from the western Atlantic Ocean. Comparative Parasitology 84(1), 1–14.10.1654/1525-2647-84.1.1CrossRefGoogle Scholar
Corner, RD, Cribb, TH and Cutmore, SC (2022) Vermetid gastropods as key intermediate hosts for a lineage of marine turtle blood flukes (Digenea: Spirorchiidae), with evidence of transmission at a turtle rookery. International Journal for Parasitology 52(4), 225–241.10.1016/j.ijpara.2021.08.008CrossRefGoogle Scholar
Cribb, TH, Anderson, GR, Adlard, RD and Bray, RA (1998) A DNA-based demonstration of a three-host life-cycle for the Bivesiculidae (Platyhelminthes: Digenea). International Journal for Parasitology 28(11), 1791–1795.10.1016/S0020-7519(98)00127-1CrossRefGoogle ScholarPubMed
Cribb, TH, Bray, RA and Littlewood, DTJ (2001) The nature and evolution of the association between digeneans, molluscs and fishes. International Journal for Parasitology 31(9), 997–1011.10.1016/S0020-7519(01)00204-1CrossRefGoogle ScholarPubMed
Cribb, TH, Bray, RA, Olson, PD and Littlewood, DTJ (2003) Life cycle evolution in the Digenea: A new perspective from phylogeny. Advances in Parasitology 54(1), 197–254.10.1016/S0065-308X(03)54004-0CrossRefGoogle ScholarPubMed
Cribb, TH, Chick, RC, O'Connor, W, O'Connor, S, Johnson, D, Sewell, KB and Cutmore, SC (2017a) Evidence that blood flukes (Trematoda: Aporocotylidae) of chondrichthyans infect bivalves as intermediate hosts: indications of an ancient diversification of the Schistosomatoidea. International Journal for Parasitology 47(3), 885–891.10.1016/j.ijpara.2017.05.008CrossRefGoogle ScholarPubMed
Cribb, TH, Crespo-Picazo, JL, Cutmore, SC, Stacy, BA, Chapman, PA and García-Párraga, D (2017b) Elucidation of the first definitively identified life cycle for a marine turtle blood fluke (Trematoda: Spirorchiidae) enables informed control. International Journal for Parasitology 47(1), 61–67.10.1016/j.ijpara.2016.11.002CrossRefGoogle ScholarPubMed
Cribb, TH, Chapman, PA, Cutmore, SC and Huston, DC (2020) Pronocephaloid cercariae (Platyhelminthes: Trematoda) from gastropods of the Queensland coast, Australia. Journal of Helminthology 94(1), e105.CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9(8), 772.10.1038/nmeth.2109CrossRefGoogle ScholarPubMed
de Buron, I, Colon, BL, Siegel, SV, Oberstaller, J, Rivero, A and Kyle, DE (2018) First evidence of polychaete intermediate hosts for Neospirorchis spp. marine turtle blood flukes (Trematoda: Spirorchiidae). International Journal for Parasitology 48(14), 1097–1106.10.1016/j.ijpara.2018.08.002CrossRefGoogle ScholarPubMed
Dereeper, A, Guignon, V, Blanc, G, et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research 36(Web Server issue), W465–W469.10.1093/nar/gkn180CrossRefGoogle ScholarPubMed
Dollfus, R-P (1950) Hôtes et distribution géographique des cercaires cystophores [Hosts and geographical distribution of cystophore cercariae]. Annales de Parasitologie Humaine et Comparée 25(4), 276–296. [In French.]10.1051/parasite/1950254276CrossRefGoogle Scholar
Evans, WA and Heckmann, RA (1973) The life history of Sanguinicola klamathensis. Life Sciences 13(9), 1285–1291.10.1016/0024-3205(73)90013-1CrossRefGoogle Scholar
Gabe, M (1966) Contribution à l'histologie de Firoloida desmaresti Lesueur [Contribution to the histology of Firoloida desmaresti Lesueur]. Vie et Milieu 17(2), 845–960. [In French.]Google Scholar
Hafeezullah, M (1990) Digenetic trematodes of marine fishes of India (superfamily Hemiuroidea: families Lecithasteridae and Bunocotylidae). Records of the Zoological Survey of India 86(3–4), 493–504.CrossRefGoogle Scholar
Hassanine, RME-S (2006) The life cycle of Diploproctodaeum arothroni Bray and Nahhas, 1998 (Digenea: Lepocreadiidae), with a comment on the parasitic castration of its molluscan intermediate host. Journal of Natural History 40(19–20), 1211–1222.10.1080/02678290600883767CrossRefGoogle Scholar
Hirsch, GC (1915) Die Ernahrungsbiologie fleischfressender Gastropoden. I [The nutritional biology of carnivorous gastropods. I]. Zoologische Jahrbücher (Abteilung für allegemeine Zoologie und Physiologie der Tiere) 35(1), 357–504. [In German.]Google Scholar
Hochberg, FG and Seapy, RR (1985) Parasites of holopelagic molluscs (Abstract). International Symposium on Marine Plankton (July 1984), Tokai University, Shimizu, Japan. Bulletin of marine science 37(2), 767.Google Scholar
Hughes, RN (1978) The biology of Dendropoma corallinaceum and Serpulorbis natalensis, two South African vermetid gastropods. Zoological Journal of the Linnean Society 64(2), 111–127.10.1111/j.1096-3642.1978.tb01063.xCrossRefGoogle Scholar
Hurvich, CM and Tsai, CL (1993) A corrected Akaike information criterion for vector autoregressive model selection. Journal of Time Series Analysis 14(3), 271–279.CrossRefGoogle Scholar
Jousson, O, Bartoli, P and Pawlowski, J (2000) Cryptic speciation among intestinal parasites (Trematoda: Digenea) infecting sympatric host fishes (Sparidae). Journal of Evolutionary Biology 13(5), 778–785.10.1046/j.1420-9101.2000.00221.xCrossRefGoogle Scholar
Kappner, I, Al-Moghrabi, SM and Richter, C (2000) Mucus-net feeding by the vermetid gastropod Dendropoma maxima in coral reefs. Marine Ecology Progress Series 204(3), 309–313.CrossRefGoogle Scholar
Kechemir, N (1978) Démonstration expérimentale d'un cycle biologique à quatre hôtes obligatoires chez les Trématodes Hémiurides [Experimental demonstration of an obligate four-host life cycle in hemiurid trematodes]. Annales de Parasitologie Humaine et Comparée 53(1), 75–92. [In French.]10.1051/parasite/1978531075CrossRefGoogle Scholar
Køie, M (1982) The redia, cercaria and early stages of Aporocotyle simplex Odhner, 1900 (Sanguinicolidae) – a digenetic trematode which has a polychaete annelid as the only intermediate host. Ophelia 21(2), 115–145.CrossRefGoogle Scholar
Køie, M (1989) On the morphology and life history of Lecithaster gibbosus (Rudolphi, 1802) Lühe, 1901 (Digenea, Hemiuroidea). Parasitology Research 75, 361–367.10.1007/BF00931131CrossRefGoogle Scholar
Køie, M (1995) The life-cycle and biology of Hemiurus communis Odhner, 1905 (Digenea, Hemiuridae). Parasite 2(Suppl 2), 195–202.CrossRefGoogle Scholar
Køie, M and Lester, RJG (1985) Larval didymozoids (Trematoda) in fishes from Moreton Bay, Australia. Proceedings of the Helminthological Society of Washington 52(2), 196–203.Google Scholar
Køie, M, Karlsbakk, E and Nylund, A (2002) A cystophorous cercaria and metacercaria in Antalis entalis (L.) (Mollusca, Scaphopoda) in Norwegian waters, the larval stage of Lecithophyllum botryophoron (Olsson, 1868) (Digenea, Lecithasteridae). Sarsia: North Atlantic Marine Science 87(4), 302–311.10.1080/00364820260400807CrossRefGoogle Scholar
Kück, P, Meusemann, K, Dambach, J, Thormann, B, von Reumont, BM, Wägele, JW and Misof, B (2010) Parametric and non-parametric masking of randomness in sequence alignments can be improved and leads to better resolved trees. Frontiers in Zoology 7(1), 10.CrossRefGoogle ScholarPubMed
Kusama, Y, Nakano, T and Asakura, A (2021) Mucus-net feeding behavior by the sessile gastropod Thylacodes adamsii (Gastropoda: Vermetidae). Publications of the Seto Marine Biological Laboratory 46(1), 55–69.10.5134/265454CrossRefGoogle Scholar
Lester, RJG and Newman, LJ (1986) First rediae and cercariae to be described from heteropods. Journal of Parasitology 72(1), 195–197.10.2307/3281823CrossRefGoogle Scholar
Littlewood, DTJ (1994) Molecular phylogenetics of cupped oysters based on partial 28S ribosomal RNA gene sequences. Molecular Phylogenetics & Evolution 3(3), 221–229.CrossRefGoogle Scholar
Littlewood, DTJ, Rohde, K and Clough, KA (1997) Parasite speciation within or between host species? – phylogenetic evidence from site-specific polystome monogeneans. International Journal for Parasitology 27(11), 1289–1297.CrossRefGoogle ScholarPubMed
Littlewood, DTJ, Curini-Galletti, M and Herniou, EA (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics & Evolution 16(3), 449–466.10.1006/mpev.2000.0802CrossRefGoogle ScholarPubMed
Lockyer, AE, Olson, PD and Littlewood, DTJ (2003) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biological Journal of the Linnean Society 78(2), 155–171.10.1046/j.1095-8312.2003.00141.xCrossRefGoogle Scholar
Louvard, C, Cutmore, SC, Yong, RQ-Y, Dang, C and Cribb, TH (2022) First elucidation of a didymozoid life cycle: Saccularina magnacetabula n. gen. n. sp. infecting an arcid bivalve. International Journal for Parasitology 52, 407–425.CrossRefGoogle Scholar
Lozano-Cobo, H, Oceguera-Figueroa, A, Silva-Segundo, CA, Robinson, CJ and Gómez-Gutiérrez, J (2022) Finding a needle in a haystack: larval stages of Didymozoidae (Trematoda: Digenea) parasitizing marine zooplankton. Parasitology Research 121(9), 2661–2672.10.1007/s00436-022-07593-6CrossRefGoogle Scholar
Madhavi, R (1980) Life history of Allocreadium handiai Pande, 1937 (Trematoda: Allocreadiidae) from the freshwater fish Channa punctata Bloch. Zeitschrift für Parasitenkunde 63(1), 89–97.10.1007/BF00927729CrossRefGoogle Scholar
Martin, SB, Cutmore, SC and Cribb, TH (2018a) Revision of Podocotyloides Yamaguti, 1934 (Digenea: Opecoelidae), resurrection of Pedunculacetabulum Yamaguti, 1934 and the naming of a cryptic opecoelid species. Systematic Parasitology 95(1), 1–31.10.1007/s11230-017-9761-1CrossRefGoogle ScholarPubMed
Martin, SB, Sasal, P, Cutmore, SC, Ward, S, Aeby, GS and Cribb, TH (2018b) Intermediate host switches drive diversification among the largest trematode family: evidence from the Polypipapiliotrematinae n. subf. (Opecoelidae), parasites transmitted to butterflyfishes via predation of coral polyps. International Journal for Parasitology 48(14), 1107–1126.CrossRefGoogle ScholarPubMed
Martin, SB, Downie, AJ and Cribb, TH (2020) A new subfamily for a clade of opecoelids (Trematoda: Digenea) exploiting marine fishes as second-intermediate hosts, with the first report of opecoelid metacercariae from an elasmobranch. Zoological Journal of the Linnean Society 188(2), 455–472.Google Scholar
Martorelli, SR (1989) Estudios parasitológicos en biotopos lénticos de la República Argentina y desarrollo del ciclo biológico monoxeno de la metacercaria progenética de Genarchella Travassos, 1928 (Digenea, Hemiuridae) parásita Littoridina parchappei (Mollusca, Hidrobiidae) [Parasitological studies in lentic biotopes of the Argentine Republic and development of the monoxene biological cycle of the progenetic metacercaria of Genarchella Travassos, 1928 (Digenea, Hemiuridae) parasite Littoridina parchappei (Mollusca, Hidrobiidae)]. Revista del Museo de la Plata 14(157), 109–117. [In Spanish.]Google Scholar
Mateo, E, Peña, C, Guzmán, E and López, R (1985) Parásito causante de castración de la concha de abanico (Argopecten purpuratus) [Parasite that causes castration of the scallop shell (Argopecten purpuratus)]. Boletín de Lima (Peru) 40(1), 81–86. [In Spanish.]Google Scholar
Mele, S, Pennino, MG, Piras, MC, Macías, D, Gómez-Vives, MG, Alemany, F, Montero, FE, Garippa, G and Merella, P (2016) The ecology of the Atlantic black skipjack Euthynnus alletteratus (Osteichthyes: Scombridae) in the western Mediterranean Sea inferred by parasitological analysis. Parasitology 143(10), 1330–1339.10.1017/S0031182016000792CrossRefGoogle ScholarPubMed
Morales-Ávila, JR, Saldierna-Martínez, RJ, Moreno-Alcántara, M and Violante-González, J (2018) New insights on the role of the holoplanktonic mollusk Firoloida desmarestia (Gastropoda: Pterotracheidae) as host for digenetic trematodes. Parasitology Research 117(7), 2149–2158.10.1007/s00436-018-5902-yCrossRefGoogle ScholarPubMed
Nikolaeva, VM (1965) [On the developmental cycle of trematodes belonging to the family Didymozoidae (Monticelli, 1888) Poche, 1907]. Zoologicheskii Zhurnal 44(1), 1317–1327. [In Russian.]Google Scholar
Okutani, T (1961) Notes on the genus Carinaria (Heteropoda) from Japanese and adjacent waters. Publications of the Seto Marine Biological Laboratory 9(2), 333–352.CrossRefGoogle Scholar
Olson, PD, Cribb, TH, Tkach, VV, Bray, RA and Littlewood, DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33(7), 733–755.10.1016/S0020-7519(03)00049-3CrossRefGoogle ScholarPubMed
Palombi, A (1941) Cercaria dentali Pelseneer, forma larvale di Ptychogonimus megastoma (Rud.) [Cercaria dentali Pelseneer, larval form of Ptychogonimus megastoma (Rud.)]. Rivista di Parassitologia 5(1), 127–128. [In Italian.]Google Scholar
Palombi, A (1942) Il ciclo biologico di Ptychogonimus megastoma (Rud.). Osservazioni sulla morfologia e fisiologia delle forme larvali e considerazioni filogenetiche [The life cycle of Ptychogonimus megastoma (Rud.). Observations on the morphology and physiology of larval forms and phylogenetic considerations]. Rivista di Parassitologia 6(1), 117–172. [In Italian.]Google Scholar
Palumbi, SR (1996) Nucleic acids II: the polymerase chain reaction. Molecular Systematics 1(1), 205–247.Google Scholar
Pankov, P, Webster, BL, Blasco-Costa, I, Gibson, DI, Littlewood, DTJ, Balbuena, JA and Kostadinova, A (2006) Robinia aurata n. g., n. sp. (Digenea: Hemiuridae) from the mugilid Liza aurata with a molecular confirmation of its position within the Hemiuroidea. Parasitology 133(2), 217–227.10.1017/S0031182006000126CrossRefGoogle Scholar
Pinto, HA, de Melo, AL and Brant, SV (2015) Where are the South American freshwater turtle blood flukes (Trematoda: Spirorchiidae)? The first morphological and molecular analysis of spirorchiid cercariae from freshwater snails in Brazil. Parasitology International 64(6), 553–558.10.1016/j.parint.2015.08.001CrossRefGoogle ScholarPubMed
Pleijel, F, Jondelius, U, Norlinder, E, Nygren, A, Oxelman, B, Schander, C, Sundberg, P and Thollesson, M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics & Evolution 48(1), 369–371.10.1016/j.ympev.2008.03.024CrossRefGoogle Scholar
Pozdnyakov, SE and Gibson, DI (2008) Family Didymozoidae Monticelli, 1888. pp. 631–734. In Bray, RA, Gibson, DI and Jones, A (Eds) Keys to the trematoda, Vol. 3. London, CAB International and Natural History Museum.Google Scholar
Prévôt, G (1969) Les trématodes larvaires parasites de Vermetus triqueter Bivone (gastéropode prosobranche marin) de Golfe de Marseille [Parasite larval trematodes of Vermetus triqueter Bivone (marine prosobranch gastropod) from the Gulf of Marseilles]. Bulletin de la Société Zoologique de France 94(1), 463–470. [In French.]Google Scholar
Richter, G (1968) Heteropoden und Heteropodenlarven im Oberflächenplankton des Golfs von Neapel [Heteropods and heteropod larvae in the surface plankton of the Gulf of Naples]. Pubblicazioni della Stazione zoologica di Napoli 36(1), 346–400. [In German.]Google Scholar
Ronquist, F, Teslenko, M, van der Mark, P, et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3), 539–542.10.1093/sysbio/sys029CrossRefGoogle ScholarPubMed
Sambrook, J and Russell, DW (2001) Molecular cloning: A laboratory manual, 3rd edn. 2344 pp. Cold Spring Harbor, New York, Cold Spring Harbor Laboratory Press.Google Scholar
Schrandt, MN, Andres, MJ, Powers, SP and Overstreet, RM (2016) Novel infection site and ecology of cryptic Didymocystis sp. (Trematoda) in the fish Scomberomorus maculatus. Journal of Parasitology 102(3), 297–305.10.1645/15-772CrossRefGoogle ScholarPubMed
Seapy, R (1980) Predation by the epipelagic heteropod mollusk Carinaria cristata forma japonica. Marine Biology 60(1), 137–146.CrossRefGoogle Scholar
Shimazu, T, Cribb, TH, Miller, TL, Urabe, M, Van Ha, N, Binh, TT and Shed'ko, MB (2014) Revision of Isoparorchis Southwell, 1913 (Digenea, Hemiuroidea, Isoparorchiidae), parasites of the air bladder of freshwater catfishes: a molecular and morphological study. Bulletin of the National Museum of Nature and Science, Series A 40(1), 15–51.Google Scholar
Shoop, WL (1989) Systematic analysis of the Diplostomidae and Strigeidae (Trematoda). Journal of Parasitology 75(1), 21–32.10.2307/3282929CrossRefGoogle ScholarPubMed
Sokolov, SG, Atopkin, DM, Gordeev, II and Shedko, MB (2018) Phylogenetic position of the genus Gonocerca Manter, 1925 (Trematoda, Hemiuroidea), based on partial sequences of 28S rRNA gene and a reconsideration of taxonomic status of Gonocercinae Skrjabin et Guschanskaja, 1955. Parasitology International 67(1), 74–78.CrossRefGoogle Scholar
Sokolov, SG, Atopkin, DM, Urabe, M and Gordeev, II (2019) Phylogenetic analysis of the superfamily Hemiuroidea (Platyhelminthes, Neodermata: Trematoda) based on partial 28S rDNA sequences. Parasitology 146(5), 596–603.CrossRefGoogle ScholarPubMed
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9), 1312–1313.10.1093/bioinformatics/btu033CrossRefGoogle ScholarPubMed
Stunkard, HW (1973) Observations on Tubulovesicula pinguis (Linton, 1910) Manter, 1947 and on systematics of the hemiuroid trematodes. Biological Bulletin 145(3), 607–626.10.2307/1540641CrossRefGoogle ScholarPubMed
Szidat, L (1956) Über den Entwicklungszyklus mit progenetischen Larvenstadium von Genarchella genarchella und die Moglichkeit einer hormonalen Beeinflussung der Parasiten durch ihre Wirtstiere [About the development cycle with progenetic larval stage of Genarchella genarchella and the possibility of a hormonal influence of the parasites by their host animals]. Zeitschrift für Tropenmedizin und Parasitologie 7(2), 239–283. [In German.]Google Scholar
Thiriot-Quiévreux, C (1969) Organogenèse larvaire du genre Atlanta (mollusque hétéropode) [Larval organogenesis of the genus Atlanta (heteropod mollusc)]. Vie et Milieu 20(2), 347–396. [In French.]Google Scholar
Thiriot-Quiévreux, C (1973) Observations de la radula des hétéropodes (Mollusca: Prosobranchia) au microscope électronique à balayage et interprétation fonctionelle [Observations of the radula of heteropods (Mollusca: Prosobranchia) under the scanning electron microscope and functional interpretation]. Comptes Rendus de l'Académie des Sciences, Serie D 276, 761–764. [In French.]Google Scholar
Thomas, LJ (1939) Life cycle of a fluke, Halipegus eccentricus n. sp., found in the ears of frogs. Parasitology 25(3), 207–221.CrossRefGoogle Scholar
Vande Vusse, FJ (1980) A pelagic gastropod first intermediate host for a hemiuroid trematode. Journal of Parasitology 66(1), 167–168.CrossRefGoogle Scholar
Vercammen-Grandjean, PH and Heyneman, D (1964) Pulmovermis and Hydrophitrema, hemiurid lung flukes of sea snakes: new host records with a corrigendum and reevaluation. Journal of Helminthology 38(3–4), 360–382.10.1017/S0022149X00033915CrossRefGoogle ScholarPubMed
Wardle, WJ (1975) Cercaria anadarae sp. n. parasitizing a bivalve mollusc, Anadara brasiliana (Lamarck), from the northwest Gulf of Mexico. Journal of Parasitology 61(6), 1048–1049.CrossRefGoogle Scholar
Wee, NQ-X, Cribb, TH, Corner, RD, Ward, S and Cutmore, SC (2021) Gastropod first intermediate hosts for two species of Monorchiidae Odhner, 1911 (Trematoda): I can't believe it's not bivalves! International Journal for Parasitology 51(6), 1035–1046.CrossRefGoogle Scholar
World Register of Marine Species (2022a) Didymozoidae Monticelli, 1888. In World register of marine Species. WoRMS Editorial Board. Available at http://www.marinespecies.org/aphia.php?p=taxdetails&id=108466 (accessed 5 April 2022).Google Scholar
World Register of Marine Species (2022b) Hemiuroidea Looss, 1899. in World register of marine Species. WoRMS Editorial Board. Available at http://www.marinespecies.org/aphia.php?p=taxdetails&id=108418. (accessed 11 June 2022)Google Scholar
Yagi, K, Terashima, H, Takano, K and Uraguchi, K (2007) Molecular identification of animal foreign substances in foods and food products - Identification of a parasite in the muscle of crescent sweetlips Plectorhinchus cinctus. Vol. 57. Hokkaido, Japan, Hokkaido Institute of Public Health.Google Scholar
Yamaguti, S (1970) Digenetic Trematodes of Hawaiian fishes. 436 pp. Tokyo, Keigaku Publishing Co.Google Scholar