The Invasion Success of the Cyanobacterium
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Aquatic Invasions (2017) Volume 12, Issue 3: 333–341 DOI: https://doi.org/10.3391/ai.2017.12.3.07 Open Access © 2017 The Author(s). Journal compilation © 2017 REABIC Special Issue: Invasive Species in Inland Waters Research Article The invasion success of the cyanobacterium Cylindrospermopsis raciborskii in experimental mesocosms: genetic identity, grazing loss, competition and biotic resistance Guntram Weithoff*, Anne Taube and Sarah Bolius University of Potsdam, Institute for Biochemistry and Biology, Dept. Ecology and Ecosystem Modelling, Am Neuen Palais 10, D-14469 Potsdam, Germany *Corresponding author E-mail: [email protected] Received: 8 November 2016 / Accepted: 5 August 2017 / Published online: 4 September 2017 Handling editor: Angela Boggero Editor’s note: This study was first presented at the special session on aquatic invasive species at the 33rd Congress of the International Society of Limnology (SIL) (31 July – 5 August 2016, Torino, Italy) (http://limnology.org/meetings/past-sil-congress/). This special session has provided a venue for the exchange of information on ecological impacts of non-native species in inland waters. Abstract The potentially toxic, invasive cyanobacterium Cylindrospermopsis raciborskii, originating from sub-tropical regions, has spread into temperate climate zones in almost all continents. Potential factors in its success are temperature, light and nutrient levels. Grazing losses through zooplankton have been measured in the laboratory but are typically not regarded as a factor in (failed) invasion success. In some potentially suitable lakes, C. raciborskii has never been found, although it is present in water bodies close by. Therefore, we tested the invasive potential of three different isolates introduced into natural plankton communities using laboratory mesocosm experiments under three grazing levels: ambient zooplankton densities, removal of large species using 100 µm mesh and a ca. doubling of large species. Three C. raciborskii isolates originating from the same geographic region (North-East Germany) were added separately to the four replicates of each treatment and kept in semi-continuous cultures for 21 days. Two isolates disappeared from the mesocosms and were also not viable in filtered lake water indicating that the lake water itself or the switch from culture medium to lake water led to the decay of the inoculated C. raciborskii. Only one out of the three isolates persisted in the plankton communities at a rather low level and only in the treatment without larger zooplankton. This result demonstrates that under potentially suitable environmental conditions, top-down control from zooplankton might hamper the establishment of C. raciborskii. Non-metric multidimensional scaling showed distinct variation in resident phytoplankton communities between the different grazing levels, thus differential grazing impact shaped the resident community in different ways allowing C. raciborskii only to invade under competitive (= low grazing pressure) conditions. Furthermore, even after invasion failure, the temporary presence of C. raciborskii influenced the phytoplankton community. Key words: alien species, Cyanobacteria, competitive resistance, consumptive resistance, herbivory, harmful algae, microbial invasion Introduction are much less studied, with only a few exceptions. One microbial invader that has received a lot of Besides many prominent and obvious examples of attention is the cyanobacterium Cylindrospermopsis biological invasions in freshwater systems, a number raciborskii (Woloszynska) Seenayy et Subba Raju, of less visible invasions occur and may cause serious that has spread from tropical to temperate regions problems (Litchman 2010). These microbial invasions worldwide (for reviews see Padisák 1997; Sukenik 333 G. Weithoff et al. et al. 2012; Antunes et al. 2015; Wilk-Wózniak et al. another one of the same species, at least under certain 2016) with a number of negative effects on water environmental conditions (Marinho et al. 2013; quality such as bloom formation, decreased water Burford et al. 2016). To test this, we performed a transparency and toxin production (Sukenik et al. laboratory experiment using natural water from a lake 2015). where C. raciborskii has not previously been found Typical habitats in temperate regions are shallow (data from local water authorities). In particular, we eutrophic lakes that have a well-mixed water column tested the hypothesis that a) the invasion success of throughout the season or are at least periodically C. raciborskii is strain-dependent and b) whether mixed (Mehnert et al. 2010). A number of ecological invasion success might be hampered by competitive and physiological traits have been assigned to explain or consumptive resistance. Therefore, we tested the its invasion success including a high intraspecific invasion success of three different genotypes of C. phenotypic plasticity (Padisák 1997; Bonilla et al. raciborskii in natural plankton communities in which 2012; Soares et al. 2013; Bolius et al. in press), high we manipulated zooplankton biomass at three levels. phosphorus uptake rates (Istvánovics et al. 2000; Burford et al. 2006), adaptation to warmer temperatures Methods (e.g. Briand et al. 2004; Mehnert et al. 2010; Bonilla et al. 2016), N-fixation (Saker and Neilan 2001; The three cultures of C. raciborskii genotypes used Spröber et al. 2003; Moisander et al. 2012) and the in this study were kept in a modified Woods Hole -1 presence of akinetes (Wiedner et al. 2007; Mehnert et medium WC with a concentration of 80 µg PO4-P L al. 2014). However, none of these traits is unique for and a pH of 8, buffered with 2 mM HEPES. All C. raciborskii but common for some other cyano- genotypes originated from lakes in North-East bacteria and/or eukaryotic phytoplankton. Besides Germany: 26D9 was isolated from Rangsdorfer See, these bottom-up factors, C. raciborskii may also suffer 52º17′19″N; 13º24′14″E, (Mehnert et al. 2010; Ramm from herbivory despite its filamentous form which et al. 2012), ZIE 11 from Zierker See, 53º21′41″N; typically reduces edibility for zooplankton (Lampert 13º02′09″ E, (Haande 2008; Sperfeld et al. 2010; 1987). However, cladorerans (Soares et al. 2009a; Mehnert et al. 2010) and MEL 07 from Melangsee, Panosso and Lürling 2010) and copepods (Rangel et 52º09′40″N; 13º59′18″E. DNA-fingerprinting revealed al. 2016) but also rotifers (Soares et al. 2010; that these are indeed different genotypes and their Sperfeld et al. 2010; Kâ et al. 2012) have been growth rates measured under laboratory semi- shown to ingest and/or even suppress C. raciborskii continuous turbidostat conditions differed: 0.26 d-1 in small-scale laboratory experiments. This suggests (26D9), 0.21 d-1 (ZIE 11) and 0.36 d-1 (MEL 07) that a combination of traits in relation to (Bolius et al. in press). All genotypes were negatively environmental conditions drives the invasion success tested for the cyanobacteria toxin cylindrospermopsin of C. raciborskii. In the past, potential reasons or (using Liquid Chromatography-Mass Spectrometry, factors responsible for the invasion success of C. Haande et al. 2008 and C. Wiedner, pers. comm.) raciborskii have been derived from studies on phy- They differed significantly in length and diameter: siology, life history or genetics. Experimental studies ZIE11 had the shortest filaments with a length of 62 under near-natural conditions in a community context µm ± 37µm (SD) and a width of 1.56 µm; strain are lacking, although needed to elaborate which traits 26D9: length 99 µm ± 36 µm (SD), width 1.89 µm; under what kind of environmental conditions are MEL07: length 266 µm ± 136 µm, width 1.84 µm responsible for invasion success. (n = 50 each). Biotic resistance, i.e. when biotic interactions prevent A mixed epilimnetic water sample from 1 to 2 m an invasion event, can be due to strong competition depth was taken from eutrophic Lake Glindower See (competitive resistance) or predation (consumptive using a 3.5 L Ruttner-type sampler on August 14th resistance). For freshwater systems, consumptive 2014. From this sample, relevant limnological para- resistance is often more important than competitive meters were determined and the same water was used resistance (Alofs and Jackson 2014). Such invader- to set-up the experiment. On the site, a vertical depth environment relations can also be influenced by the profile was taken using a multi-parameter probe genotype of the invader. It is a general notion, also (Idronaut, Italy) measuring temperature, pH, O2-satu- known as the paradox of invasion (Roman and Darling ration, O2-concentration and conductivity. Vertical 1997) that the inoculum of an invasive species consists light penetration of photosynthetically active radiation only of one or very few genotypes. Despite the (400–700 nm) was measured using an underwater resulting impoverished gene pool, some species are spherical light sensor (Li-Cor 193) corrected for extremely successful invaders. Thus, a specific changes in surface irradiance using a second sensor genotype might be much more successful than measuring in air. 334 The invasion success of the cyanobacterium Cylindrospermopsis raciborskii in experimental mesocosms For chlorophyll-a analysis, subsamples were determined for days 3, 12 and 21 using an inverted filtered on GF/C glass fibre filters (Whatman) and microscope (Thalheim Optik, Jena) and standard chlorophyll-a was extracted over night with hot algal counting procedures (Utermöhl 1958). To ethanol.