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Blackfordia Virginica (Mayer, 1910) in the Baltic Sea Cornelia Jaspers1,2* , Bastian Huwer2, Nancy Weiland‑Bräuer3 and Catriona Clemmesen1

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Blackfordia Virginica (Mayer, 1910) in the Baltic Sea Cornelia Jaspers1,2* , Bastian Huwer2, Nancy Weiland‑Bräuer3 and Catriona Clemmesen1 Jaspers et al. Helgol Mar Res (2018) 72:13 https://doi.org/10.1186/s10152-018-0513-7 Helgoland Marine Research ORIGINAL ARTICLE Open Access First record of the non‑indigenous jellyfsh Blackfordia virginica (Mayer, 1910) in the Baltic Sea Cornelia Jaspers1,2* , Bastian Huwer2, Nancy Weiland‑Bräuer3 and Catriona Clemmesen1 Abstract Marine invasions are of increasing concern for biodiversity conservation worldwide. Gelatinous macrozooplank‑ ton contain members, which have become globally invasive, for example the ctenophore Mnemiopsis leidyi or the hydromedusae Blackfordia virginica. B. virginica is characterised by a large salinity tolerance, with a brackish-water habi‑ tat preference, and by a metagenic life history strategy with an alternation between sexually reproducing planktonic medusae and asexually reproducing benthic polyps to complete the life cycle. In this study we analysed 8 years of ichthyoplankton survey data (2010–2017) from the Kiel Canal and 14 ichthyoplankton summer surveys in the central Baltic Sea (2008–2017). We report the frst presence of B. virginica in northern Europe, namely from the southwest‑ ern Baltic Sea and the Kiel Canal. In the Kiel Canal, B. virginica was frst sporadically sighted in 2014 and 2015 and has developed persistent populations since summer 2016. Changes in size-frequency distributions during summer 2016 indicate active recruitment in the Kiel Canal at salinities between 7 and 13 and temperatures > 14 °C. Close vicinity to and direct connection with the southwestern Baltic Sea, where B. virginica was observed during 2017, indicate that the Baltic Sea and other brackish-water habitats of Northern Europe are at risk for colonisation of this non-indigenous species. Our results highlight that monitoring activities should consider gelatinous macrozooplankton for standard assessments to allow for the detection of non-indigenous species at an early stage of their colonisation. Keywords: Hydromedusa, Species translocations, Invasive species, Ballast water, Kiel Canal Background which actually attain large population densities [5], the Global change has wide ranging consequences for the impact of those species which actually do become inva- productivity and functioning of the worlds’ oceans. sive and achieve pest status can be devastating [6, 7]. Among the pressures associated with global change are Te Baltic Sea has a very high proportion of non-indig- overfshing, eutrophication, coastal habitat modifcation enous species compared to the total number of species and species translocations [1]. Te transport of species [8], in that respect ranking among the top 10 afected outside their native dispersal ranges impacts recipient ecosystems worldwide [9]. Further, it is characterised by ecosystems and is leading to a homogenization of the a very steep salinity gradient ranging from 2 in the north worlds’ biota [2, 3]. Lately, it has been documented that east (Bothnian Bay) to 31 at the transition zone to the the rate at which new species are recorded outside their North Sea in the west [10]. Such brackish-water seas, natural habitat boundaries is steadily increasing, with with overall low species richness, have been shown to be no signs of saturation [4]. Even though it is only a small especially vulnerable to invasions [11]. Terefore, large fraction of the originally arriving non-indigenous species areas of the Baltic Sea as well as the Kiel Canal, an artif- cial brackish waterway, can be regarded as high risk areas for the establishment of non-indigenous species. Tis is *Correspondence: [email protected]; [email protected] especially so as the 98 km long Kiel Canal, which con- 1 Evolutionary Ecology of Marine Fishes, GEOMAR – Helmholtz Centre for Ocean Research Kiel, Düsternbrooker Weg 20, 24105 Kiel, Germany nects the North Sea to the SW Baltic Sea, is the busiest Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat​iveco​mmons​.org/licen​ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Jaspers et al. Helgol Mar Res (2018) 72:13 Page 2 of 9 artifcial water way in the world with approx. 80 con- for station reference). Presented size distribution data of tainer ships passing on a daily basis [12, 13]. B. virginica are based on 4% borax bufered formaldehyde An example of a very potent invasive species is the seawater solution without considering shrinkage efects. hydrozoan jellyfsh Blackfordia virginica (Mayer, 1910) [14] Leptothecata (Cnidaria: Hydrozoa) cf. Cornelius Kiel Canal [15, 16]. B. virginica is characterised by a metagenic life Sampling was conducted at the monitoring station NOK history strategy with an alternation between a sexu- (WGS84 coordinates: N54.343, E9.968) which is located ally reproducing medusa and an asexually reproducing at the eastern end of the Kiel Canal at kilometer 85, polyp population to complete the life cycle. Te pelagic approx. 13 km west of the exit to the Baltic Sea, at weekly medusa stage has been found in brackish-water systems or monthly intervals covering the years 2010–2017. To (as reviewed in [17]), while the polyp stage has been con- characterise physical properties of the water column, frmed from brackish-water systems, estuaries as well salinity and temperature profles were taken using the as coastal salt water swamps (e.g. as reviewed in [17]). hand held CTD 48 M (Sea & Sun Technology GmbH, Te origin of this hydromedusa is not clear. It was frst Trappenkamp, Germany). Gelatinous macrozooplank- described by Mayer [14] based on dense accumulations ton was sampled as part of an ongoing ichthyoplank- in Virginia, USA during autumn 1904, but later molecular ton monitoring program using double oblique bongo analyses documented a low genetic diversity, suggesting net tows (60 cm diameter, 500 and 335 µm mesh sizes) that animals went through a bottleneck, as expected dur- through the entire water column. Filtered volumes were ing the translocation process of a non-indigenous species calculated based on fowmeter recordings (Hydrobios, [18]. Tiel found that B. virginica was a common mem- Kiel, Germany) and ranged between 100 and 160 m3, ber of the hydromedusa community of the Black Sea, depending on current strength in the canal. Troughout which suggests that it is actually native to the Black Sea July–October 2017, no bongo net casts could be con- region [19–22]. Apart from these early records, estab- ducted. Terefore, bi-monthly presence during summer lished B. virginica populations were found in other areas was determined by visual confrmations and net tows around the world e.g. India [23, 24], South America (e.g. from land. During October 2017, quantitative samples [17, 25]), North America [20, 22], South Africa [26], and were generated using three independent WP2-net casts southwestern Europe (e.g. [27]). For the Atlantic coast of (60 cm diameter, 200 µm meshed) from 1 m above the southwestern Europe, B. virginica was frst recorded in bottom to the surface. To increase the fltered water vol- 1971 in the Loire estuary, Bay of Biscay, France [28]. In ume for reliable count data, each of the three samples 1984 B. virginica was further observed in the Mira estu- consisted of triplicate WP2-net tows which were pooled ary, Portugal [29], while more recently, animals were leading to 9 individual WP2-net casts. Filtered water recorded in the harbour of Amsterdam, Netherlands [30] volume was estimated from wire length and net open- and in the Gironde estuary, France [27]. In this study we ing of strictly vertical tows. For 2016 and 2017, all bongo describe the frst record of Blackfordia virginica in the samples, preserved in 4% borax bufered formaldehyde Kiel Canal and Kiel Fjord in the southwestern Baltic Sea. seawater solution, were analysed on a light table in the Furthermore, we collate long term ichthyoplankton sur- laboratory for gelatinous macrozooplankton abundance vey data, analysed for gelatinous macrozooplankton, to estimation, while for 2010–2015 non-preserved samples set a baseline confrming presence and absence of Black- were analysed right after catch along with sorting of ich- fordia virginica medusae. Especially the Baltic Sea, one of thyoplankton. Blackfordia virginica were measured to the the largest brackish-water systems of the world, presents nearest mm from preserved samples using a caliper, not a highly suitable habitat for B. virginica, with a potential accounting for shrinkage efects. for severe ecosystem impacts due to grazing on zoo- plankton standing stocks. Baltic Sea During August 2017, a comprehensive survey inves- Methods tigating the gelatinous zooplankton community of the Sampling of hydromedusae Baltic Sea was conducted with R/V Alkor, covering the Te presence and absence of Blackfordia virginica has area from the SW Baltic of Flensburg to the northern been confrmed as part of ongoing gelatinous macrozoo- Gotland Basin (Fig. 1, Additional fle 1: Table S1). Te plankton monitoring initiatives within 4 diferent sam- investigation period is consistent with documented pling programs or survey activities of ichthyoplankton peak abundances of B. virginica in other invaded areas, in the Baltic Sea and Kiel Canal (see detailed descrip- such as the Atlantic coast of France
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