Can Increases in Temperature Stimulate Blooms of the Toxic Benthic Dinoflagellate Ostreopsis Ovata?

Harmful Algae 10 (2011) 165–172 Contents lists available at ScienceDirect Harmful Algae journal homepage: www.elsevier.com/locate/hal Can increases in temperature stimulate blooms of the toxic benthic dinoflagellate Ostreopsis ovata? Edna Grane´li a,*, Nayani K. Vidyarathna a, Enzo Funari b, P.R.T. Cumaranatunga c, Raffaeli Scenati b a Marine Ecology Department, Linnaeus University, 39182 Kalmar, Sweden b Environment & Health Dept., National Institute of Health, v.le Regina Elena 299, 00161 Rome, Italy c Dept. of Fisheries & Aquaculture, Faculty of Fisheries & Marine Sciences and Technology, University of Ruhuna, Matara, Sri Lanka ARTICLE INFO ABSTRACT Article history: Ostreopsis ovata Fukuyo is an epiphytic, toxic dinoflagellate, inhabiting tropical and sub-tropical waters Received 12 February 2010 worldwide and also in certain temperate waters such as the Mediterranean Sea. Toxic blooms of O. ovata Received in revised form 22 April 2010 have been reported in SE Brazil in 1998/99 and 2001/02 and the French–Italian Riviera in 2005 and 2006. Accepted 6 September 2010 These blooms had negative effects on human health and aquatic life. Chemical analyses have indicated that O. ovata cells produce palytoxin, a very strong toxin, only second in toxicity to botulism. Increase in Keywords: water temperature by several degrees has been suggested as the reason for triggering these blooms. Four Ostreopsis ovata laboratory experiments were performed with O. ovata isolated from Tyrrhenian Sea, Italy to determine Benthic dinoflagellate the effects of water temperature and co-occurring algae on the cell growth and/or the toxicity of O. ovata. Toxicity Palytoxin The cells were grown under different temperatures ranging from 16 8Cto308C, and cell densities, Temperature growth rates and the cell toxicities were studied. Results indicated high water temperatures (26–30 8C) Climate change increased the growth rate and biomass accumulation of O. ovata. In mixed cultures of O. ovata with other co-occurring algae, biomass decreased due to grazing by ciliates. Cell toxicity on the other hand was highest at lower temperatures, i.e., between 20 and 22 8C. The present study suggests that sea surface temperature increases resulted by global warming could play a crucial role inducing the geographical expansion and biomass accumulation by blooms of O. ovata. ß 2010 Elsevier B.V. All rights reserved. 1. Introduction Climate Change, continued emissions will lead to increase of world average temperature by 1.8–4 8C over the 21st century (IPCC, 2007). Climate-induced changes and other anthropogenic activities Since the oceans are core components of the climate system, these have been attributed to be the major driving forces behind the changes have a particular significance on the structure and function stimulation, distribution and the intensification of harmful algal of the marine ecosystems. The direct and indirect impacts of the blooms on the last decades (Van Dolah, 2000; Anderson et al., increases in greenhouse gas concentrations on the ocean will include 2002; Hallegraeff, 2003; Grane´li, 2004; Glibert et al., 2005; Cloern increasing sea surface temperatures, acidification, changes to the et al., 2005). The ecological and biogeochemical significance of density structure of the upper ocean which will alter vertical mixing blooms depend strongly on the species composition of the growing of waters, intensification/weakening of upwelling winds and community, which is shaped by changing physical dynamics over changes in the timing and volume of freshwater runoff into coastal multiple time scale (Cloern et al., 2005). These physical dynamics marine waters (Moore et al., 2008). may vary from the local winds and heat flux that result in a The processes that select a particular algal species to increase in stratification inside a small bay, to the ocean – basin scale cell numbers ultimately forming a bloom are still unresolved atmospheric processes that produce variability in wind-driven questions (Cloern et al., 2005). It is however, well understood that circulation patterns (Cloern et al., 2005). the growth and toxicity of many toxic dinoflagellates are There is near unanimous scientific consensus that the world may influenced by physical factors such as temperature, salinity, light be entering a period of global warming in response to atmospheric and by the amount of inorganic nutrients available, which play a greenhouse gas accumulation generated due to human activities significant role on the bloom formation (Morton et al., 1992; (Van Dolah, 2000). According to the Intergovernmental Panel on Grane´li and Flynn, 2006). Warmer temperatures may result in expanded ranges of warm water Harmful algal species such as Gambierdiscus toxicus, which * Corresponding author. Tel.: +46 0 480 447307; fax: +46 0 480 447305. was evident by the high abundance and extended distribution of G. E-mail address: [email protected] (E. Grane´li). toxicus in higher latitudes in response to elevated sea surface 1568-9883/$ – see front matter ß 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.hal.2010.09.002 166 E. Grane´li et al. / Harmful Algae 10 (2011) 165–172 temperature during the warm phases of ENSO cycle (Hales et al., Tyrrhenian Sea; (2) to determine whether the optimum tempera- 1999; Chateau-Degat et al., 2005). Low temperature has been ture to growth would be the same for the highest production of reported to decrease the growth rate and to increase the toxin toxin and (3) to find whether O. ovata cells produce allelochemicals concentration of PSP (Paralytic Shellfish Poisoning) producing at high temperatures, which allow the species to out-compete the dinoflagellates such as, Alexandrium catenella, A. cohorticula and other co-existing algae. To answer these questions we performed Gymnodinium catenatum (Ogata et al., 1989; Grane´li and Flynn, four laboratory experiments with O. ovata and its co-occurring 2006). Indirect impacts of increased temperature may also favor species under different temperatures. algal blooms, e.g., coral bleaching events free up space for macroalgae to colonize making available more habitats for benthic 2. Materials and methods epiphytic toxic dinoflagellates to explore (Moore et al., 2008). Interactions of toxin producing algal species with non-toxic Four experiments were performed at the Linnaeus University, algal species can be a factor of ultimate importance, on the Sweden. Seawater from the Genova Bay and cultures of O. ovata, structuring of the plankton communities. Specially if the toxins are Kalmar Algae Collection (KAC 85) which was used for the the same as allelopathic substances, which are released into the experiments were shipped to Sweden. O. ovata cells were isolated water, enabling the harmful species to out-compete co-occurring from seaweeds collected from the Tyrrhenian Sea, Italy in 2007 phytoplankton species (Grane´li and Johansson, 2003b; Legrand during a bloom of O. ovata. Prior to commencement of the et al., 2003; Glibert et al., 2005), it will ultimately determine which experiments, O. ovata cells were grown in f/10 media (Guillard and phytoplankton species will be able to co-exist and what their Ryther, 1962), prepared using water brought from Italy (filtered population size will be. Allelochemicals seems to be grazer through Whatman GF/C glass-fibre filters and autoclaved). These deterrents in most of the cases (Grane´li and Johansson, 2003a; cultures were maintained at a salinity of 38 psu, temperature of 2 À1 Fistarol et al., 2004). Reductions in grazer abundance due to 25 8C and illuminated under 140 mEcm S by cool-white Osram deterrent substances can also play a key role in the development of tubes and exposed to 16:8 hr light: dark cycle. Algal species found toxic algal blooms (Smetacek, 2001; Guisande et al., 2002; in natural community assemblages were collected from Monte Frango´ pulos et al., 2004). Argentario, Tyrrhenian Sea, Italy and brought to Sweden. Much less information is available in the international scientific literature regarding interactions concerning benthic harmful 2.1. Experiment 1 dinoflagellates. The existing knowledge on species distribution and factors involved in the production of toxins are on the benthic The aims of the experiment 1 were to determine the optimum dinoflagellates producing ciguatera (Morton et al., 1992; Van temperature for growth of O. ovata and effect of temperature on Dolah, 2000; Lewis, 2001; Chateau-Degat et al., 2005; Yasumoto exudation of allelochemicals. et al., 1977). Three treatments were used in this experiment, viz. Oovata Ostreopsis ovata Fukuyo is a toxic benthic dinoflagellate, monocultures, a natural community assemblage and a mixture of inhabiting tropical and sub-tropical waters worldwide. Ostreopsis the two. Polystyrene 8 ml Petri dishes (3.5 cm in diameter) were species are often found in epiphytic association with red and used for the experiment. Stock cultures for controls were brown macroalgae (Faust et al., 1996; Grane´ li et al., 2002). Recent prepared by diluting 100 ml of O. ovata monoculture and occurrence of O. ovata blooms has been also recorded from many 100 ml of natural community assemblage with 150 ml of f/10 temperate regions (Shears and Ross, 2009). O. ovata has attracted medium and the mixed treatment was prepared by mixing attention during the past years due to its unusual blooms and 100 ml of O. ovata monoculture and 100 ml of natural community production of palytoxin, which is one of the most potent known assemblage diluted with 50 ml of f/10 medium to obtain the existing toxin. O. ovata and O. lenticularis have been shown to same initial cell concentrations for each treatment. Five produce palytoxin and its analogues (e.g. ostreosin-D), that can millilitres from each of the three stock solutions were poured cause human fatalities by accumulating higher up in marine food into the petri dishes and tightly closed using paraffin. Each webs (Grane´ li et al., 2002; Rhodes et al., 2002; Ashton et al., treatment was exposed to 6 temperatures (16 8C, 20 8C, 24 8C, 2003; Taniyama et al., 2003; Ciminiello et al., 2006; Monti et al., 26 8C, 28 8C, 30 8C) in triplicates.

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