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A New Species of Deropristid Trematode from the Sterlet

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A New Species of Deropristid Trematode from the Sterlet applyparastyle “fig//caption/p[1]” parastyle “FigCapt” Zoological Journal of the Linnean Society, 2020, 190, 448–459. With 4 figures. A new species of deropristid trematode from the sterlet Acipenser ruthenus (Actinopterygii: Acipenseridae) and revision of superfamily affiliation of the family Deropristidae Downloaded from https://academic.oup.com/zoolinnean/article/190/2/448/5810955 by guest on 02 October 2020 SERGEY SOKOLOV1, EKATERINA VOROPAEVA1 and DMITRY ATOPKIN2,3* 1A. N. Severtsov Institute of Ecology and Evolution, Leninskij prosp. 33, 119071 Moscow, Russia 2Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of the RAS, 100-letija prosp. 159, 690022 Vladivostok, Russia 3Department of Cell Biology and Genetics, Far Eastern Federal University, Sukhanova Street 8, 690051 Vladivostok, Russia Received 22 November 2019; revised 15 January 2020; accepted for publication 8 February 2020 A new species, Skrjabinopsolus nudidorsalis sp. nov. is described from the sterlet Acipenser ruthenus, caught in the River Volga basin (Russia). This species differs from previously described congeners by the absence of vitelline follicles on the dorsal side of the body. The complete 18S rRNA and partial 28S rRNA gene sequences obtained for S. nudidorsalis are the first molecular data for the family Deropristidae. The results of phylogenetic analysis indicate that Deropristidae is sister to the Monorchiidae + Lissorchiidae group. The results of the phylogenetic study contradict the current taxonomic hypothesis that Deropristidae belongs to the superfamily Lepocreadioidea and allow inclusion of this family in Monorchioidea. The morphological similarity of deropristids to other monorchioids is recognizable from the presence of a bipartite internal seminal vesicle, spinous cirrus and a voluminous, armed metraterm. ADDITIONAL KEYWORDS: 18S – 28S –Monorchioidea – new species – River Volga – Skrjabinopsolus – sturgeons. INTRODUCTION Ivanov, 1936, which was collected from the intestines of the Russian sturgeon Acipenser gueldenstaedtii Acipenseriformes – sturgeons and paddlefishes – are von Brandt & Ratzeburg, 1833, the starry sturgeon one of most ancient groups of ray-finned fish and are Acipenser stellatus Pallas, 1771, the sterlet Acipenser of great scientific and economic importance (Birstein ruthenus Linnaeus, 1758 and the beluga Acipenser et al., 1997; Betancur et al., 2017). Currently, these fish huso Linnaeus, 1758, caught in the River Volga delta species are present in Europe and large parts of Asia (Ivanov & Murygin, 1936). The year of description and North America. The parasite fauna of sturgeons of this trematode genus and species is not indicated and paddlefishes is unique and conditioned by the correctly in previous publications, except that of presence of host-specific high-level taxa (Skrjabina, Shulman (1954). The first time A. S. Ivanov presented 1974; Choudchury & Dick, 2001; Evans et al., 2008). data on Skrjabinopsolus was at the 230th session of In the present study, we focus on trematodes of the the Standing Committee for the Study of Helminth genus Skrjabinopsolus Ivanov, 1936. This genus was Fauna of the USSR Academy of Sciences on 19 May described based on the type species, S. acipenseris 1934. However, these materials were not published. The original description of this taxon was published in the paper of Ivanov & Murygin (1936). *Corresponding author. E-mail: [email protected] [Version of record, published online 21 March 2020; http:// At various times, nine species of trematodes zoobank.org/ urn:lsid:zoobank.org:pub: 093E8C8F-A240-49AC- have been assigned to the genus Skrjabinopsolus, 9384-4BF0B3C27AEB] namely S. acipenseris, S. semiarmatus (Molin, 1858), © 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2020, 190, 448–459 448 A NEW SPECIES OF DEROPRISTID TREMATODE 449 S. skrjabini Osmanov, 1940, S. manteri (Cable, 1952), MATERIAL AND METHODS S. minor Bykhovskaya-Pavlovskaya & Mikailov, SAMPLE COLLECTION 1969, S. elongatus (Madhavi, 1974) (with synonyms of S. indicus Gupta & Ahmad, 1976 and S. kurotchkini Worm specimens were collected in the course of a Parukhin, 1976 as proposed by Hafeezullah, 1984) parasitological investigation of 12 specimens [total and S. sanyaensis Shen, 1990 (e.g. Bykhovskaya- length (TL) = 38–54 cm] from the sterlet, caught in Pavlovskaya & Mikailov, 1969; Hafeezullah, 1984; Shen, the River Oka (River Volga basin) near the village 1990). Skrjabinopsolus elongatus is now considered a of Kletino, Ryazan Oblast, Russia, in June 2019. All member of the monorchiid genus Opisthodiplomonorchis applicable international guidelines for the care and Madhavi, 1974 (Choudhury & Dick, 1998; Madhavi & use of animals were followed by the authors (Directive Bray, 2018). Skrjabinopsolus sanyaensis does not show 2010/63/EU of the European Parliament and of Downloaded from https://academic.oup.com/zoolinnean/article/190/2/448/5810955 by guest on 02 October 2020 the diagnostic characters of either Skrjabinopsolus or the Council of 22 September 2010 on the protection the Deropristidae. Therefore, its systematic position is of animals used for scientific purposes). Catching still unclear (Choudhury & Dick, 1998). of sterlet was carried out by the employees of the The basic features of S. acipenseris, S. skrjabini, Russian Federal Research Institute of Fisheries and S. minor and S. manteri (body and organ size, Oceanography (FSBSI ‘VNIRO’, Moscow) in accordance gonad arrangement, extension of the vitelline fields, with the monitoring programme of the ichthyofauna of distribution of the uterus, egg size, etc.) are highly the middle course of the River Oka. variable (Bykhovsky & Dubinina, 1954; Shulman, The worms collected for morphological study were 1954; Bykhovskaya-Pavlovskaya & Mikailov, fixed in hot 70% ethanol, stained with acetocarmine, 1969, Skrjabina, 1974; Bunyatova & Mikailov, dehydrated in dimethyl phthalate, mounted in Canada 1991; Choudhury & Dick, 1998). In this respect, balsam and studied with the aid of a light microscope Skrjabina (1974) and Choudhury & Dick (1998) Axio Imager A1 (Zeiss AG, Oberkochen, Germany). All considered S. acipenseris, S. skrjabini and S. minor measurements were made in micrometres based on 12 as junior synonyms of S. semiarmatus. Bunyatova adults and four juvenile specimens, unless otherwise & Mikailov (1991) considered that S. manteri and indicated. The measurements of the adults are provided S. semiarmatus are also conspecific. Choudhury as the range of followed by the mean values in round & Dick (1998) recognized S. manteri as a Nearctic brackets and the measurements for the holotype in subspecies of S. semiarmatus – S. semiarmatus square brackets. For the juvenile specimens, only the manteri. At the same time, Choudhury & Dick (2001) range is provided. Specimens were deposited in the considered S. manteri as an independent species Museum of Helminthological Collections at the Centre but without additional argument. Thus, the genus of Parasitology of the A. N. Severtsov Institute of Skrjabinopsolus is most widely considered to consist Ecology and Evolution (IPEE RAS) in Moscow, Russia. of two valid species – S. semiarmatus, identified Specimens destined for molecular analysis were fixed in Europe, Western Asia and the Russian Far East in 96% ethanol and stored at –18 °C. (Skrjabina, 1974; Yukhimenko & Belyaev, 2002; Noie, 2011), and S. manteri, found in North America (Choudhury & Dick, 1998, 2001). EXAMINATION OF FURTHER SPECIMENS FROM MUSEUM According to the present view on systematics of COLLECTIONS the class Trematoda, this genus belongs to the family We studied the morphology of the following museum Deropristidae of the superfamily Lepocreadioidea specimens of Skrjabinopsolus to clarify the differential (Bray, 2005; Bray et al., 2009; Bray & Cribb, 2012). diagnosis of a new species: However, this viewpoint has not been verified with molecular data. • Photos of holotype, paratype and two voucher In 2019, trematode specimens belonging to the specimens of S. manteri from North American genus Skrjabinopsolus were found by E. Voropaeva sturgeons, the National Museum of Natural History in sterlet from the River Volga basin (Russia). (USNM 1337876, USNM 1337877, USNM 1380936, These parasites differ from their congeners by USNM 1384527), Washington DC, United States. a number of morphological characteristics that Photos were kindly provided by Dr Anna Philips. allow us to consider these worms as a new species, • Eighteen voucher specimens of S. semiarmatus Skrjabinopsolus nudidorsalis. In the present paper, (Molin, 1858). Whole-mounted adult specimens we provide a description, drawings and results of the from the beluga, the starry sturgeon and the molecular phylogenetic analysis of this species with bastard sturgeon Acipenser nudiventris Lovetsky, clarifying phylogenetic relationships of the family 1828 caught in the Caspian Sea, April 1964 (IPEE Deropristidae. RAS 1082–1088, 1092). © 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2020, 190, 448–459 450 S. SOKOLOV ET AL. Unfortunately, the procedure of descriptions of 3.1 (Guindon & Gascuel, 2003) and MrBayes v.3.1.2 S. semiarmatus s.s. and two other nominal species, software (Huelsenbeck et al., 2001), respectively. The namely S. acipenseris and S. skrjabini, were performed best nucleotide substitution model, GTR+G+I, was without designation of the place of storage of type estimated with jModeltest v.2.1.5 software (Darriba
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