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Using the Critical Salinity (Scrit) Concept to Predict Invasion Potential of the Anemone Diadumene Lineata in the Baltic Sea

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Using the Critical Salinity (Scrit) Concept to Predict Invasion Potential of the Anemone Diadumene Lineata in the Baltic Sea Mar Biol (2016) 163:227 DOI 10.1007/s00227-016-2989-5 INVASIVE SPECIES - ORIGINAL PAPER Using the critical salinity (Scrit) concept to predict invasion potential of the anemone Diadumene lineata in the Baltic Sea Imke Podbielski1,2 · Christian Bock3 · Mark Lenz1 · Frank Melzner1 Received: 3 March 2016 / Accepted: 10 September 2016 © Springer-Verlag Berlin Heidelberg 2016 Abstract It is widely assumed that the ability of an intro- a fivefold population growth through asexual reproduction duced species to acclimate to local environmental condi- at high salinities (34 and 24). Biomass increase under these tions determines its invasion success. The sea anemone conditions was significantly higher (69 %) than at a salin- Diadumene lineata is a cosmopolitan invader and shows ity of 14. At a salinity of 7, anemones ceased to reproduce extreme physiological tolerances. It was recently discov- asexually, their biomass decreased and metabolic depres- ered in Kiel Fjord (Western Baltic Sea), although the brack- sion was observed. Five main intracellular osmolytes were ish conditions in this area are physiologically challenging identified to be regulated in response to salinity change, for most marine organisms. This study investigated salin- with osmolyte depletion at a salinity of 7. We postulate that ity tolerance in D. lineata specimens from Kiel Fjord in depletion of intracellular osmolytes defines a critical salin- order to assess potential geographical range expansion of ity (Scrit) that determines loss of fitness. Our results indicate the species in the Baltic Sea. In laboratory growth assays, that D. lineata has the potential to invade the Kattegat and we quantified biomass change and asexual reproduction Skagerrak regions with salinity >10. However, salinities of rates under various salinity regimes (34: North Sea, 24: the Baltic Proper (salinity <8) currently seem to constitute Kattegat, 14: Kiel Fjord, 7: Baltic Proper). Furthermore, we a physiological limit for the species. used 1H-NMR-based metabolomics to analyse intracellular osmolyte dynamics. Within four weeks D. lineata exhibited Introduction Responsible Editor: E. Briski. In marine ecosystems, the distribution of organisms is reg- ulated by their physiological characteristics, environmen- Reviewed by S. Wijnhover and an undisclosed expert. tal factors, their dispersal potential and ecological inter- This article is part of the Topical Collection on Invasive Species. actions. Invasive species (sensu Goodwin et al. 1999) are often characterized by a high tolerance to abiotic stress that Electronic supplementary material The online version of this may also have predetermined their invasion success (Lenz article (doi:10.1007/s00227-016-2989-5) contains supplementary et al. 2011). Geographical range expansions of marine ani- material, which is available to authorized users. mals into brackish waters are thought to be limited by the * Imke Podbielski organism’s ability to tolerate hypoosmotic conditions (Dahl [email protected] 1956). The capability of tolerating a wide salinity range is especially important for sessile osmoconformers, since they 1 GEOMAR Helmholtz Centre for Ocean Research Kiel, Hohenbergstr 2, 24105 Kiel, Germany cannot avoid unfavourable conditions and are incapable of actively adjusting their extracellular osmolarity. 2 Leibniz Center for Tropical Marine Ecology (ZMT), Fahrenheitstraße 6, 28359 Bremen, Germany The Baltic Sea is the largest brackish sea worldwide with a surface area of 0.4 million km2 and is characterized 3 Alfred-Wegener-Institute Helmholtz Centre for Polar and Marine Research, Am Handelshafen 12, by a steep salinity gradient from west to east (Janssen et al. 27570 Bremerhaven, Germany 1999). It hosts over 100 non-indigenous species, of which 1 3 227 Page 2 of 15 Mar Biol (2016) 163:227 11°0’E 20°0’E 28°0’E N 62°0’N Bothnian 55°0’N Flensburg Sea Geltinger Maasholm Bight Fehmarn Eckernförde Helsinki St. Petersburg d Kiel Grömitz Bay of Finlan Tallinn 58°0’N 58°0’N North Sea Salinity Göteborg 34 0 Riga 5 Kattegat 10 Arhus 24 Baltic Proper 15 Copenhagen 20 7 Vilnius 25 Western 30 54°0’N Baltic Minsk 54°0’N 14 35 Kiel Gdansk Rostock 0 100 200 300 400 km Hamburg 12°0’E 20°0’E 28°0’E Fig. 1 Salinity regime of the Baltic Sea. The modelled mean bottom verified sightings (for coordinates see Table 1). Black stars mark the salinity of the Baltic Sea is depicted in blue tones (from: http://www. locations where the absence of the anemone was recorded, and red emodnet-seabedhabitats.eu). Coloured lines represent isolines of the stars mark the presence of the species. A higher resolution of the Kiel respective experimental treatment. The small map shows the distri- Fjord area can be seen in the supplementary material (Fig. 3). Back- bution of Diadumene lineata along the German Western Baltic Sea ground map from: http://www.eea.europa.eu coast recorded in the rapid assessment survey including additional approximately 70 % have established stable populations understanding of how abiotic factors affect the distribu- (Ojaveer et al. 2010). Salinity (next to temperature) has tion of marine species (Munday et al. 2013). Deviations of been described as the key limiting factor for the spread of environmental variables from the respective optimum are marine organisms into the Baltic Sea (Bonsdorff 2006) and known to affect a species’ metabolism, growth, and even- several taxa are restricted to the more saline waters of the tually fitness (Guppy and Withers 1999). Thus, determin- Kattegat and Western Baltic Sea (WBS), including native ing the threshold at which hypoosmotic conditions impact anthozoans (sea anemones) (Leppäkoski et al. 2002). In fitness in a given marine species can help to estimate its addition, projected increases in precipitation and resulting expansion potential into brackish waters. desalination of the Baltic Sea will likely shift distribution Osmoconformers allow fluctuations in their extracel- boundaries of native and invasive organisms within the next lular osmolarity that correspond to changes in the envi- decades (Gräwe et al. 2013) (Fig. 1). ronment and achieve acclimation via cellular volume The assessment of the (transgenerational) acclima- regulation (Pierce 1982). To prevent cellular swelling or tion potential to environmental stress can provide an shrinking, concentrations of compatible organic osmolytes 1 3 Mar Biol (2016) 163:227 Page 3 of 15 227 or inorganic ions are modulated (Yancey 2001). Usually, in actinians (Yancey et al. 2010). Shick (1976) reports that both substance classes are utilized by marine organisms, taurine and glycine comprise over 70 % of the FAA pool albeit at different time scales. Inorganic ions are typi- in D. lineata. Methylamines have only rarely been investi- cally used in response to short-term and rapid changes in gated in anthozoans (corals: Yancey et al. 2010), albeit they external osmolarity, while organic osmolytes are utilized are known as important intracellular osmolytes in other during long-term acclimation (Silva and Wright 1994). marine invertebrates (Silva and Wright 1994). Compatible organic osmolytes have the advantage of not The extreme tolerance of D. lineata to environmental interacting with intracellular metabolism, whereas inor- stress combined with its rapid clonal reproduction may ganic ions and certain amino acids can have strong perturb- determine its invasion success. The aim of this study was to ing effects on vital functions, such as cellular enzymatic investigate the salinity tolerance of D. lineata experimen- reactions (Bowlus and Somero 1979). Thus, osmoconform- tally in order to assess whether novel D. lineata popula- ers employ a variety of cellular regulatory mechanisms to tions, which were recently found in the WBS (Kiel Fjord, maintain relatively constant concentrations of intracellular salinity 12–20), have the potential for further geographical inorganic ions when external salinity fluctuates. range expansion in the Baltic Sea. For this, we used two Cellular osmoregulation is an energy-dependent process. approaches: First, we studied metabolism, growth and The physiological response to moderate abiotic stress often asexual reproduction capacity (a proxy for evolutionary fit- involves an increase in metabolic activity or a repartitioning ness) of D. lineata acclimated to different osmotic condi- of cellular energy allocation to compensate for the elevated tions representing different parts of the Baltic Sea as well energy demand induced by the stressor (Pan et al. 2015). as the North Sea. We hypothesized that fitness decreases Severe stress may, however, exceed the organism’s capac- with decreasing salinity. Second, we analysed intracellu- ity to supply ATP from food or internal storages to sustain lar osmolytes of the anemone from non-targeted metabolic routine metabolism. Many species subsequently reduce profiles using 1H-NMR spectroscopy to identify cellular metabolism to conserve energy and extend survival time, mechanisms of osmoregulation. We aimed to identify the although a down-regulation of metabolic processes cannot main organic osmolytes responsible for D. lineata’s ability be maintained permanently (Guppy and Withers 1999). to acclimate to a wide range of salinities. We hypothesize Here, we report for the first time the presence of the that a depletion of the intracellular osmolyte pool causes anemone Diadumene lineata (Verrill 1871, scientific syn- a physiological stress response and defines the capacity onyms are Haliplanella luciae Verrill
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