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The taxonomic and phylogenetic status of digeneans from the genus Timoniella (Digenea: Cryptogonimidae) in the Black and Baltic seas

  • Y. Kvach (a1) (a2) (a3), A. Bryjová (a1), P. Sasal (a4) (a5) and H.M. Winkler (a6)
Abstract

Timoniella spp. are cryptogonimid flukes (Digenea: Cryptogonimidae) that parasitize the guts of fish in brackish waters. Timoniella imbutiforme, a species from the Mediterranean Sea, is recorded in the Black Sea, while T. balthica has been described from the Baltic Sea. In this paper, we clarify the taxonomic status of Timoniella populations in the Baltic and Black seas. Adults and metacercariae of Timoniella spp. were sampled from localities in the Mediterranean Sea (France), Black Sea (Ukraine) and Baltic Sea (Germany) and subjected to molecular and morphological analysis, including Bayesian phylogenetic reconstruction based on concatenated sequences of ITS1–ITS2–28S. This allowed us to construct a new key to species of the genus Timoniella. Our results suggest that T. balthica forms part of the Boreal–Atlantic relict fauna of the Black Sea and should now be considered a junior synonym of T. imbutiforme.

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Corresponding author
Author for correspondence: Y. Kvach, E-mail: yuriy.kvach@gmail.com
References
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Barnes, RSK (1989) What, if anything, is a brackish-water fauna? Transactions of the Royal Society of Edinburgh, Earth Sciences 80, 235240.
Bartoli, P and Bray, RA (1987) Redescriptions of two cryptogonimid digeneans from the fish Dentex dentex (L., 1758) (Sparidae) in the Mediterranean Sea. Systematic Parasitology 10, 117127.
Bartoli, P and Gibson, DI (1995) Three rare and little known cryptogonimid digeneans from the sciaenid fish Sciaena umbra (L.) in the western Mediterranean. Systematic Parasitology 30, 121139.
Bartoli, P and Gibson, DI (2000) Three little known acanthostomine digeneans from Uranoscopus scaber L. in the western Mediterranean. Systematic Parasitology 46, 123141.
Bartoli, P and Gibson, DI (2007) Synopsis of the life cycles of Digenea (Platyhelminthes) from lagoons of the northern coast of the western Mediterranean. Journal of Natural History 41, 15531570.
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, 217229.
Brooks, DR (1980) Revision of the Acanthostominae Poche, 1926 (Digenea: Cryptogonimidae). Zoological Journal of the Linnean Society 70, 313332.
Chernyshenko, А (1949) Novye gelminty ryb Chernogo morya. Pratsi Odeskogo Universytetu 4, 7991.
Cribb, TH and Bray, RA (2010) Gut wash, body soak, blender and heat-fixation: approaches to the effective collection, fixation and preservation of trematodes of fishes. Systematic Parasitology 76, 17.
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, 17911795.
Culurgioni, J, Sabatini, A, De Murtas, R, Mattiucci, S and Figus, V (2014) Helminth parasites of fish and shellfish from the Santa Gilla Lagoon in southern Sardinia, Italy. Journal of Helminthology 88, 489498.
Dawson, CE (1986) Syngnathidae. pp. 628639 in Whitehead, PJP, Bauchot, M-L, Hureau, J-C, Nielsen, J and Tortonese, E (Eds) Fishes of the North-eastern Atlantic and the Mediterranean, Vol. 2. Paris, Unesco.
Dethier, MN (1992) Classifying marine and estuarine natural communities: an alternative to the Cowardin system. Natural Areas Journal 12, 90100.
Dollfus, RP, Chabaud, AG and Golvan, YJ (1957) Helminthes de la région de Banyuls. V. Nouveau Distome Aphalloïdes coelomicola n. gen. n. sp. de la cavité générale d'un Gobius d'eau saumâtre. Annales de Parasitologie 32, 2940.
Domnich, IF and Sarabeev, VL (2000) Suchasna fauna parazytiv ryb u pivnichniy chastyni Azovskogo morya. Visnyk Zaporizkogo Universytetu 1, 224231.
El-Darsh, HEM and Whitfield, PJ (1999) The parasite community infecting flounders, Platichthys flesus, in the tidal Thames. Journal of Helminthology 73, 203214.
El-Darsh, HEM and Whitfield, PJ (2000) Ultrastructure of the tegument of the metacercariae of Timoniella imbutiforme. Journal of Helminthology 74, 5766.
Fischthal, JH (1980) Some digenetic trematodes of marine fishes from Israel's Mediterranean coast and their zoogeography, especially those from Red Sea immigrant fishes. Zoologica Scripta 9, 1123.
Georgiev, B, Biserkov, V and Genov, T (1986) In toto staining method for cestodes with iron acetocarmine. Helminthologia 23, 279281.
Jayawardena, UA, Tkach, VV, Navaratne, AN, Amerasinghe, PH and Rajakaruna, RS (2013) Malformations and mortality in the Asian common toad induced by exposure to pleurolophocercous cercariae (Trematoda: Cryptogonimidae). Parasitology International 62, 246252.
Johnstone, J (1906) Internal parasites and diseased conditions of fishes. Proceedings and Transactions of the Liverpool Biological Society 20, 151185.
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Mentjies, P and Drummond, A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 16471649.
Køie, M (1983) Digenetic trematodes from Limanda limanda (L.) (Osteichthyes, Pleuronectidae) from Danish and adjacent waters, with special reference to their life-histories. Ophelia 22, 201228.
Korniychuk, YM and Gaevskaya, AV (2004) The first record of Aphallus tubiarum (Trematoda, Cryptogonimidae) in the Black Sea. Vestnik Zoologii 38, 7980.
Krasnovyd, V, Kvach, Y and Drobiniak, O (2012) The parasite fauna of the gobiid fish (Actinopterygii, Gobiidae) in the Sykhyi Lyman, Black Sea. Vestnik Zoologii 46, 483490.
Kvach, Y (2005) A comparative analysis of helminth faunas and infection of ten species of gobiid fishes (Actinopterygii: Gobiidae) from the North-Western Black Sea. Acta Ichthyologica et Piscatoria 35, 103110.
Kvach, Y (2010) Helminths of the marbled goby (Pomatoschistus marmoratus), a Mediterranean immigrant in the Black Sea fauna. Vestnik Zoologii 44, 509518.
Kvach, Y and Oğuz, MC (2009) Communities of metazoan parasites of two fishes of the Proterorhinus genus (Actinopterygii: Gobiidae). Helminthologia 46, 168176.
Kvach, Y and Winkler, HM (2011) The colonization of the invasive round goby Neogobius melanostomus by parasites in new localities in the South-Western Baltic Sea. Parasitology Research 109, 769780.
Kvach, Y, Bryjová, A, Sasal, P and Winkler, HM (2017) A revision of the genus Aphalloides (Digenea: Cryptogonimidae), parasites of European brackish water fishes. Parasitology Research 116, 19731980.
Lanfear, R, Calcott, B, Ho, SYW and Guindon, S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 16951701.
Littlewood, DTJ (1994) Molecular phylogenetics of cupped oysters based on partial 28S rRNA gene sequences. Molecular Phylogenetics and Evolution 3, 221229.
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, 12891297.
Looss, A (1901) Ueber die Fascioliden genera Stephanochasmus, Acanthochasmus, und einige andere. Zentralblatt für Bakteriologie und Parazitenkunde 29, 595661.
Luton, K, Walker, D and Blair, D (1992) Comparison of ribosomal internal transcribed spacers from two congeneric species of flukes (Platyhelminthes: Trematoda: Digenea). Molecular and Biochemical Parasitology 56, 323328.
Maillard, C (1973) Etude du cycle évolutif du Trématode: Acanthostomum imbutiforme (Molin, 1859) Gohar, 1934, parasite de Morone labrax (Linné, 1758). Annales Parasitologie humaine et comparée 48, 3346.
Maillard, C (1974) Cycle évolutif de Timoniella praeteritum (Looss, 1901) (Trematoda, Acanthostomidae) parasite de Morone labrax (Teleostei, Serranidae). Bulletin de la Société Zoologique de France 99, 245257.
Maillard, C, Lambert, A and Raibaut, A (1980) Nouvelle forme de distomatose larvaire. Étude d'un Trématode pathogène pour les alevins de Daurades (Sparus aurata L., 1758) en closerie. Comptes Rendus de l'Académie des Sciences 290, 535538.
Malek, M (2004) Parasites as discrimination keys in two sympatric species of gobies. Bulletin of the European Association of Fish Pathologists 24, 173179.
Marengo, M, Durieux, EDH, Marchand, B and Francour, P (2014) A review of biology, fisheries and population structure of Dentex dentex (Sparidae). Reviews in Fish Biology and Fisheries 24, 10651088.
McDowall, AA and James, BL (1988) The functional morphology of the circumoral spines of Timoniella imbutiforme (Molin, 1859) Brooks, 1980 (Digenea: Acanthostomidae). International Journal for Parasitology 18, 523530.
Miller, TL and Cribb, TH (2008a) Eight new species of Siphoderina Manter, 1934 (Digenea, Cryptogonimidae) infecting Lutjanidae and Haemulidae (Perciformes) off Australia. Acta Parasitologica 53, 344364.
Miller, TL and Cribb, TH (2008b) Family Cryptogonimidae Ward, 1917. pp. 51112 in Bray, RA, Gibson, DI and Jones, A (Eds) Keys to the Trematoda, Vol. 3. Wallingford, CAB International.
Molin, R (1859) Nuovi Myzelmintha raccolti ed esaminati. Sitzungsberichte der Kaiserlichen Akademie Wissenschaften Wien, Mathematisch Naturwissenschaftliche 37, 818854.
Naydenova, NN (1974) Parazitofauna ryb semeystva Gobiidae Chernogo i Azovskogo morey. Kiev, Naukova Dumka.
Nicoll, W (1915) A list of the trematode parasites of British marine fishes. Parasitology 7, 339378.
Oliveira, F, Erzini, K and Gonçalves, JMS (2007) Feeding habits of the deep-snouted pipefish Syngnathus typhle in a temperate coastal lagoon. Estuarine, Coastal and Shelf Science 72, 337347.
Pampoulie, C, Lambert, A, Rosecchi, E, Crivelli, AJ, Bouchereaut, J-L and Morand, S (2000) Host death: A necessary condition for the transmission of Aphalloides coelomicola Dollfus, Chabaud, and Golvan, 1957 (Digenea, Cryptogonimidae)? Journal of Parasitology 86, 416417.
Radujković, BM and Šundić, D (2014) Parasitic flatworms (Platyhelminthes: Monogenea, Digenea, Cestoda) of fishes from the Adriatic Sea. Natura Montenegrina 13, 7280.
Rebecq, JM (1960) Timoniella atherinae nov. gen. nov. sp. (Trematoda: Acanthostomotidae) metacercaire parasite d'Atherina mochon C.V. pp. 257–262 in Libro Homenaje al Dr. Eduardo Caballero y Caballero, Jubileo 1930–1960. México, Editorial Politeécnica.
Reimer, L (1970) Digene Trematoden und Cestoden der Ostseefische als natürliche Fischmarken. Parasitologische SchriftenReiche 20, 1144.
Reimer, LW, Hildebrand, A, Scharberth, D and Walter, U (1996) Trematodes of the brackish waters of the Baltic Sea and their distribution together with that of related species in other European areas. Applied Parasitology 37, 177185.
Ronquist, F and Huelsenbeck, JP (2003) Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.
Sey, O (1970) Parasitic helminths occurring in Adriatic fishes. Part II (Flukes and Tapeworms). Acta Adriatica 13, 315.
Smith, CL (1990) Moronidae. pp. 692694 in Quero, JC, Hureau, JC, Karrer, C, Post, A and Saldanha, L (Eds) Check-list of the fishes of the eastern tropical Atlantic (CLOFETA), Vol. 2. Lisbon, JNICT.
Sterud, E (2002) Parasites of wild sea bass Dicentrarchus labrax from Norway. Diseases of Aquatic Organisms 48, 209212.
Zaitsev, YP (1998) Samoe sinee v mire. New York, UN Publication.
Zaitsev, Y and Mamaev, V (1997) Biological diversity in the Black Sea: a study of change and decline. New York, UN Publication.
Zander, CD (2001) The guild as a concept and a means in ecological parasitology. Parasitology Research 87, 484488.
Zander, CD (2003) Four-year monitoring of parasite communities in gobiid fishes of the south-western Baltic. I. Guild and component community. Parasitology Research 90, 502511.
Zander, CD and Reimer, LW (2002) Parasitism at the ecosystem level in the Baltic Sea. Parasitology 124, S119S135.
Zander, CD, Reimer, LW and Barz, K (1999) Parasite communities of the Salzhaff (Northwest Mecklenburg, Baltic Sea). I. Structure and dynamics of communities of littoral fish, especially small-sized fish. Parasitology Research 85, 356372.
Zander, CD, Koçoglu, O, Skroblies, M and Strohbach, U (2002) Parasite populations and communities from the shallow littoral of the Orther Bight (Fehmarn, SW Baltic Sea). Parasitology Research 88, 734744.
Zenkevich, LA (1963) Biologiya morey SSSR. Moskva, Izdatelsto AN SSSR.
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