Seasonal Variability in Dinophysis Spp. Abundances and Diarrhetic Shellfish Poisoning Outbreaks Along the Eastern Adriatic Coast
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Article in press - uncorrected proof Botanica Marina 51 (2008): 449–463 ᮊ 2008 by Walter de Gruyter • Berlin • New York. DOI 10.1515/BOT.2008.067 Seasonal variability in Dinophysis spp. abundances and diarrhetic shellfish poisoning outbreaks along the eastern Adriatic coast Zˇ ivana Nincˇevic´-Gladan*, Sanda Skejic´, Mia difficulties in culturing. Research on Dinophysis species Buzˇancˇic´ , Ivona Marasovic´, Jasna Arapov, increased greatly after they were linked to algal biotoxins Ivana Ujevic´, Natalia Bojanic´, Branka Grbec, and diarrhetic shellfish poisoning (DSP) (Yasumoto et al. Grozdan Kusˇpilic´ and Olja Vidjak 1980). The main dinoflagellates causing DSP belong to genera Prorocentrum and Dinophysis. In contrast to Institute of Oceanography and Fisheries, Sˇ etalisˇteI. Prorocentrum, Dinophysis blooms are rare, but they can Mesˇtrovic´a 63, 21000 Split, Croatia, induce poisoning even at low cell densities (Bruno et al. e-mail: [email protected] 1998). * Corresponding author Sedmak and Fanuko (1991) reported the presence of several Dinophysis species in the Adriatic Sea. Previous research conducted in the northern Adriatic Sea and along the western coast showed that Dinophysis distri- Abstract bution follows a strong seasonal pattern (Sidari et al. Annual dynamics and ecological characteristics of the 1995a, Bernardi Aubry et al. 2000, Vila et al. 2001). In genus Dinophysis spp. and associated shellfish toxicity eastern Mediterranean waters, increased abundances of events were studied from 2001 to 2005 during monitoring Dinophysis spp. can be detected at different times of the fieldwork in the coastal waters of the eastern Adriatic year (Koukaras and Nikolaidis 2004). Seawater temper- Sea. Analysis of the seasonal occurrence of Dinophysis ature and water column stability seem to be the most species identified D. acuminata and D. sacculus as typ- important factors controlling their abundances (Delmas ical spring species, D. caudata, D. fortii and D. rotundata et al. 1992, Bernardi Aubry et al. 2000, Koukaras and as summer and late summer species and D. tripos as a Nikolaidis 2004). winter species. The highest abundances occurred when The occurrence of shellfish poisoning in the Adriatic there were large differences between surface and bottom Sea was first noted in 1989 in the northern part (Boni et temperatures and salinities. D. caudata, D. sacculus and al. 1992, Della Loggia et al. 1993, Marasovic´et al. 1998). D. rotundata abundances had significant relationships Toxic compounds other than the more frequently detect- with Dt, while the highest abundances of D. acuta, D. ed okadaic acid (OA) and dinophysistoxin-1 (DTX-1) were fortii and D. tripos were associated with high Ds values. found to be involved in DSP phenomena (Pavela-Vrancˇic´ Much higher abundances of D. caudata and D. fortii in et al. 2002). offshore compared to inshore waters of the northern This study analyses data obtained during the harmful Adriatic Sea and the significant inverse relationship of algal bloom (HAB) monitoring program on shellfish these species’ abundances with salinity suggested the resources in Croatian coastal waters of the eastern Adri- possibility of their transport by Italian river-influenced atic Sea from 2001 to 2005. The purpose of this program coastal waters towards the eastern Croatian coast during was (1) to find out which Dinophysis species appear in the summer season and under stratified conditions. Tox- Croatian coastal waters and to determine their icity events occurred more frequently in the more eutro- seasonal and spatial occurrence patterns based on the phicated northern Adriatic Sea than in the southern 5-year study period, and (2) to determine DSP toxin pro- Adriatic Sea and mostly succeeded the rainfall periods. files occurring at Croatian shellfish farms. On the basis Diarrhetic shellfish poisoning (DSP) toxin profile analyses of the results, we describe the dynamics of Dinophysis identified okadaic acid and yessotoxin as the main DSP species and DSP toxicity occurrence along the eastern toxins occurring in Croatian waters. coast of the Adriatic Sea, both of which have been poorly reported so far. Keywords: Adriatic Sea; algal toxins; Dinophysis spp.; shellfish toxicity. Materials and methods Investigated area Introduction The area investigated comprised five different shellfish Dinoflagellates of the cosmopolitan genus Dinophysis farming zones along the eastern Adriatic coast and sta- (Sournia 1986) occur in various coastal waters (Halle- tion VB located in the eastern part of Kasˇtela Bay in the graeff 2003), including those of the Adriatic Sea (France middle Adriatic Sea (Figure 1). and Mozeticˇ 2006). The ecology and ecophysiology In the northern Adriatic Sea, the first area investigated of Dinophysis species are poorly understood, mostly is located along the western coast of the Istrian penin- because they occur in low abundance, but also due to sula, comprising stations IP1 (11 m) and IP2 (8 m) located 2008/38 Article in press - uncorrected proof 450 Zˇ . Nincˇevic´-Gladan et al.: Seasonal variability of Dinophysis spp. and DSP outbreaks Figure 1 The study area, showing six investigated areas and 13 sampling stations along the eastern Adriatic coast. in a shellfish farming area, and IP3 (18 m) located in wild Armanda 1980). Phytoplankton blooms are known to shellfish stocks (Figure 1A). The shellfish farm is located occur sporadically (Marasovic´ and Vukadin 1982, Mara- 4–5 km south of the Mirna River estuary, without signif- sovic´ et al. 1991, 1995). Data obtained from this station icant freshwater or sewage water inflow, and is therefore were analyzed separately due to different sampling meth- convenient for shellfish farming. The second area inves- odology and absence of the shellfish farms in the adja- tigated is a shellfish farm placed in the very narrow, land cent waters. incised, 600 m long Lim Bay (Figure 1B). The maximum In the South Adriatic Sea, sampling stations are locat- depth of 33 m is at the entrance of the Bay. Station LB1 ed in Mali Ston Bay, which is one of the most important (14 m) is located in the shallow inner part, which is the shellfish farming areas in Croatia (Figure 1F). The bay is most productive area due to the strong influence of located at the end of the Neretva Channel. The outer part ground waters enriched with organic matter. The third is under the occasional influence of the River Neretva, area investigated, containing station NB1 (10 m) is locat- whose influence in the inner part of the bay is weak ed in the land incised and enclosed Novigrad Bay, and (Vukadin 1981). Four sampling stations MSB1, MSB2, is influenced by the River Zrmanja estuary (Figure 1C). A MSB3, and MSB4 are located in this Bay, with depths stratified water column with a sharp and shallow halo- from 7 m to 8 m at all stations. cline characterizes this area. Nutrient concentrations and distributions indicate oligotrophic conditions in the bay Field surveys (Buric´ et al. 2004). In the mid Adriatic Sea, stations Sˇ B1 (8 m), Sˇ B2 (11 m), Field surveys were conducted from January 2001 to and Sˇ B3 (17 m) are located in the Sˇ ibenik Bay (Figure December 2005. In the colder part of the year (from 1D). This area, influenced by the Krka River estuary, is November to March), sampling was performed on a one of the most productive bays along the east Adriatic monthly basis. In the warmer period from April to Octo- coast, with freshwater present in the surface ber, sampling was carried out every 2 weeks, but only layer throughout the entire area. Station VB (18 m) is the higher abundances were used in the analysis. At located in a shallow, semi-enclosed, eastern part of the shellfish farms, phytoplankton samples were collected larger Kasˇtela Bay in the mid Adriatic Sea (Figure 1E). with a plankton net (mouth diameter 29 cm, mesh size This locality is characterized by reduced water exchange 20 mm) towed vertically from near bottom to the surface. with the larger Bay area, and increased nutrient concen- The results were expressed as the number of cells m-2. trations originating from anthropogenic pollution (Zore- According to an earlier study by Sidari et al. (1995b) and Article in press - uncorrected proof Zˇ . Nincˇevic´-Gladan et al.: Seasonal variability of Dinophysis spp. and DSP outbreaks 451 our previous field experiences, net sampling is more suit- spiracids, AZAs) in Centro Ricerche Marine di Cesenatico able for the detection of low abundance species, such (Italy). as Dinophysis spp. Since cells tend to aggregate at dif- In 2001, DSP positive samples were investigated only ferent depths in the water column, we believe that it is for concentrations of OA using the PP2A (Protein-Phos- more accurate to express their abundance per m2 rather phatase Assay) (Holmes 1991, Tubaro et al. 1996). In than dividing their abundances by volume of filtered 2004 and 2005, positive samples were investigated fur- water, which could lead to the underestimation of their ther for lipophilic toxins using liquid chromatography density. Abundances per m2 were calculated as N=P=F, tandem mass spectrometry (LC-MS/MS; Quilliam et al. where N is the number of organisms in the counting 2001). LC-MS/MS analyses were performed using a chamber, P is a proportion of total volume to subsample 1200 dm-3 triple quadrupole mass spectrometer (Varian volume and F is net factor calculated as 1 m2 divided by Inc., Walnut Creek, CA, USA). net area (r2p). Apart from the vertical net hauls, additional phyto- Meteorological data plankton samples were taken with a 1.7 l Niskin bottle in the surface layer in 2001. Regional precipitation data along the west coast of the In 2001 at station VB in Kasˇtela Bay, phytoplankton Istrian peninsula (Rovinj) used in the analyses were samples were taken with a 1.7 l Niskin bottle at 0, 5, 10, obtained from the State Hydrographic Institute.