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“Invasion” in the Russian Arctic: Is Global Climate Change a Real Driver? a Remarkable Case of Two Nudibranch Species

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“Invasion” in the Russian Arctic: Is Global Climate Change a Real Driver? a Remarkable Case of Two Nudibranch Species Ruthenica, 2019, vol. 29, No. 2: 103-113. © Ruthenica, 2019 Published online March 5, 2019 http: www.ruthenica.com “Invasion” in the Russian Arctic: is global Climate Change a real driver? A remarkable case of two nudibranch species Irina A. EKIMOVA1,5, Tatiana I. ANTOKHINA2, Dimitry М. SCHEPETOV1,3,4 1Lomonosov Moscow State University, Leninskie Gory 1-12, 119234 Moscow, RUSSIA; 2A.N. Severtsov Institute of Ecology and Evolution of Russian Academy of Sciences, Leninsky prospect 33, Moscow 119071, RUSSIA; 3N.K. Koltzov Institute of Developmental Biology of Russian Academy of Sciences, Vavilov str. 26, 119334 Moscow, RUSSIA; 4National Research University Higher School of Economics, Myasnitskaya str. 20, 101000 Moscow, RUSSIA 5Corresponding author; E-mail: [email protected] ABSTRACT. In present paper, we report the first find- global warming affects this region drastically, which ings of two large and conspicuous nudibranch species possibly causes massive introduction of boreal spe- for Russian waters – Goniodoris nodosa and Flabelli- cies into the Arctic [Chan et al., 2018]. Recently na pellucida. Both species show wide distribution in new species of various invertebrate taxa were re- the northeastern Atlantic waters or even in the north- corded for the first time for the Barents Sea and western Atlantic in the case of F. pellucida. The mor- consequently attributed as novel invasions: nudi- phology of both species was studied using anatomical dissections and scanning electron microscopy. Molec- branch molluscs [Martynov et al., 2006; Zakharov, ular diversity was assessed by sequencing of COI marker Jorgensen, 2017], caenogastropods [Kantor et al., and reconstruction of haplotype networks. In the Bar- 2008], bivalves [Deart et al., 2013], cephalopods ents Sea, both species show minor genetic differences [Golikov et al., 2013; 2014], annelids [Rzhavsky et from their European relatives and similar morphological al., 2011], and echinoderms [Zakharov et al., 2016]. characters. Putative explanations of new findings for In further text, we use term “invasion” in a sense Russian Arctic are discussed. used in works concerning the Russian Arctic fauna, i.e. any introduction of new populations not caused by a gradual area expansion. Introduction In the present work, we follow recent trend in updating of the Barents Sea faunistics with discov- Discussion of global Climate Change as a driver ering of two conspicuous nudibranch species (Mol- of biocenotic changes is a growing prominent trend lusca, Gastropoda) new to Russian waters and this in biodiversity studies during the last decades [Post area in particular. Dorid nudibranch Gonidodoris et al., 2009; Wassmann et al., 2011]. At the same nodosa (Montagu, 1808) is reported from North- time, with growth of anthropogenic pressure many East Atlantic (north Spain, along French Atlantic introduction events have been reported. Such events coast to British Isles) to the North Sea and western are numerous for aquatic ecosystems due to long- Barents Sea with Varangerfjord as the northernmost term disruption in marine communities, caused by location [Thompson, Brown, 1984; Eversten, agricultural and industrial projects and ballast wa- Bakken, 2002; 2005] (Fig. 1A). A cladobranch, ters acting as a vector of invasion [Ruiz et al., Flabellina pellucida (Alder et Hancock, 1843) is a 2000; Occhipinti-Ambrogi, Savini, 2003]. These widespread species, being reported from North- two phenomena often tend to be discussed as coin- West Atlantic (from Massachusetts to North Cana- ciding. Contemporary methods of molecular phylo- da), Mediterranean coast, North-East Atlantic (Brit- genetics give us a powerful tool to distinguish real ish Isles, Norway and Faeroes) with central Nor- invasions from cases of understudied fauna, and way as the easternmost and northernmost location recent events from ones that occurred in relatively [Lemche, 1929; Kuzirian, 1979; Thompson, Brown, distant past [Leydet, Helberg, 2015]. A prominent 1984; Eversten, Bakken, 2005] (Fig. 1B). At least case of such putative Climate Change role is the for F. pellucida the previously known easternmost Barents Sea fauna expansion. This area is a key- record is in about 1300 kilometers to the south- stone for Arctic biodiversity and hydrology, linking west and therefore its findings in the Barents Sea Atlantic and Arctic water masses. It is believed that can be attributed as an invasion event. However, 104 I.A. Ekimova, T.I. Antokhina, D.M. Schepetov FIG. 1. Known distribution of studied species in northern Europe (circles indicate previous records, triangles and squares - original data). A. Goniodoris nodosa. B. Flabellina pellucida. Teriberka area includes Teriberka Bay and Zelenaya Inlet; Ura- Guba area incudes Ura Inlet. РИС. 1. Известное распространение исследованных видов в водах северной Европы (круги обозначают предыдущие находки, треугольники и квадраты - оригинальные данные). A. Goniodoris nodosa. B. Flabellina pellucida. Район с.Териберки включает губы Териберская и Зелёная; район с.Ура-губы включает губу Ура. other explanations are plausible, e.g. survey incom- taxonomy of the family Flabellinidae s.l. is contro- pleteness, gradual area expansion or restoration of versial and different generic divisions have been depressed native population, etc. Therefore, our proposed [Korshunova et al., 2017a; Gosliner et main goal is to investigate molecular and morpho- al., 2018]. According to recent revision by Kor- logical diversity of F. pellucida and G. nodosa from shunova et al. [2017a], the species Flabellina pel- the Barents Sea as thoroughly as possible with lucida has been transferred into a new genus Car- available specimens. ronella Korshunova, Martynov, Bakken, Evertsen, Fletcher, Mudianta, Saito, Lundin, Schrödl et Pic- Material and methods ton, 2017. However, Gosliner et al. [2018] suggest- ed retaining most of Flabellinidae s.l. diversity in the Material genus Flabellina McMurtrie, 1831 until a dedicated Material was collected in three localities of the revision is undertaken. For ease of comparison and Murmansk coast of the Barents Sea during summer comprehension we use a stable version of Flabellin- and autumn seasons of 2015 and 2018: (1) Zelenaya idae s.l. taxonomy in the present study as published Inlet, 25-27 Aug. 2015, 2 specimens of F. pelluci- in Furfaro et al. [2018]. da; (2) Teriberka Bay, 25 Aug. – 1 Sep. 2018, 4 Morphological analysis specimens of F. pellucida, 2 specimens of G. no- dosa; (3) Ura Inlet, 18 Nov. 2018, 2 specimens of The external morphology of the specimens was F. pellucida (Table 1). Specimens were collected studied under a stereomicroscope. The buccal mass during scuba diving at depths of 2-20 m on hard of each specimen was extracted and soaked in bottoms. Water temperature in the collection sites proteinase K solution for 2 hours at 55oC to dissolve ranged from +7 to +10ºC in August-September and connective and muscle tissues, leaving only the was +5ºC in November. Each mollusc was relaxed radula and the jaws. The coated radulae were exam- and photographed using Sony NEX-5N camera and ined and photographed using scanning electron mi- then fixed in 96° ethanol. Several specimens were croscope EVO-40 Zeiss. The reproductive system photographed in their natural environment under of both species was examined using the stereomi- water using the same camera. Voucher specimens croscope. The features of the jaws of F. pellucida and DNA samples are stored in the personal collec- were analyzed under the stereomicroscope and scan- tion of the first author and are available by a re- ning electron microscope JEOL JSM. quest. Molecular analysis Taxonomic remarks DNA was extracted from small pieces of foot As discussed in several recent works the alpha- tissue using PALL™ AcroPrep 96-well plates by Two new nudibranch species for Russian waters 105 Table 1. Specimens used in the present study with information on vouchers and GenBank accession numbers. Таблица 1. Изученные особи с указанием регистрационных номеров ГенБанка. COI GB Species Voucher Location accession Reference number Barents Sea, Russia, Flabellina pellucida IEF57 MK533612 This study Zelenaya Inlet Barents Sea, Russia, Flabellina pellucida IEFp10 MK533605 This study Zelenaya Inlet Barents Sea, Russia, Flabellina pellucida IEFp9 MK533606 This study Teriberka Bay Barents Sea, Russia, Flabellina pellucida IEFp8 MK533607 This study Teriberka Bay Barents Sea, Russia, Flabellina pellucida IEFp3 MK533608 This study Teriberka Bay Barents Sea, Russia, Flabellina pellucida IEFp2 MK533609 This study Teriberka Bay Barents Sea, Russia, Ura Flabellina pellucida IEIn3 MK533610 This study Inlet Barents Sea, Russia, Ura Flabellina pellucida IEIn1 MK533611 This study Inlet ZMMU:Op- Korshunova et Flabellina pellucida North Sea, Norway, Gulen MF523349 514 al., 2017 ZMMU:Op- Korshunova et Flabellina pellucida North Sea, Norway, Gulen MF523350 513 al., 2017 NTNU- Korshunova et Flabellina pellucida North Sea, Norway, Gulen MG452617 VM:68824 al., 2017 NTNU- Korshunova et Flabellina pellucida North Sea, Norway, Gulen MG452618 VM:68823 al., 2017 Barents Sea, Russia, Goniodoris nodosa IEGn1 MK533614 This study Teriberka Bay Barents Sea, Russia, Goniodoris nodosa IEGn4 MK533613 This study Teriberka Bay Wollscheid- Goniodoris nodosa unknown NE Atlantic, Spain AF249788 Lengeling et al., 2001 Barco et al., Goniodoris nodosa MT09684 North Sea KR084683 2016 PA LL C o r p . [Ivanova et al., 2006]. Extracted DNA µM stock), 1 µL of genomic DNA and 17.7 µL of was used as a template
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