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Home , Dinoflagellate, Noctiluca scintillans

Journal of the Marine 1 Bloom of the heterotrophic 2 Biological Association of the 3 United (Macartney) Kofoid & 4 Swezy, 1921 and tunicates Salpa fusiformis 5 6 cambridge.org/mbi Cuvier, 1804 and Salpa maxima Forskål, 1775 in 7 8 the open southern Adriatic in 2009 9 10 11 Original Article 1 1 1 2 2 Mirna Batistić , Rade Garić , Nenad Jasprica , Stijepo Ljubimir and Josip Mikuš 12 Cite this article: Batistić M, Garić R, Jasprica 13 š 1 N, Ljubimir S, Miku J (2018). Bloom of the Institute for Marine and Coastal Research, University of Dubrovnik, Kneza Damjana Jude 12, 20000 Dubrovnik, 14 heterotrophic dinoflagellate Noctiluca 2 Ć ć Croatia and Department of Aquaculture, University of Dubrovnik, ira Cari a 4, 20000 Dubrovnik, Croatia 15 scintillans (Macartney) Kofoid & Swezy, 1921 and tunicates Salpa fusiformis Cuvier, 1804 16 and Salpa maxima Forskål, 1775 in the open Abstract 17 southern Adriatic in 2009. Journal of the This study was conducted in February, April and June 2009 at three stations in the southern 18 Marine Biological Association of the United Adriatic. Occurrence of the dinoflagellate Noctiluca scintillans and tunicates Salpa fusiformis 19 Kingdom 1–10. https://doi.org/10.1017/ S0025315418001029 and Salpa maxima in high abundances for the oligotrophic open sea, indicates the importance 20 of physical forcing (vertical mixing) and inflow of -enriched Atlantic water, due to the 21 Received: 30 May 2018 Bimodal Oscillating System (BiOS) mechanism, into the Adriatic Sea thus creating an envir- 22 Revised: 15 October 2018 onment favourable for their rapid increase. This is the first time a bloom of N. scintillans has 23 Accepted: 26 October 2018 been recorded in the open southern Adriatic (OSA). High abundance of Noctiluca and salp 24 Key words: populations in the OSA was characterized by low abundance of and other zoo- 25 Adriatic Sea; BiOS mechanism; Mediterranean , with obvious trophic implications (reduction of food availability to crustacean pri- 26 Sea; Noctiluca bloom; salp bloom; trophic mary consumers). Moreover, during the S. maxima bloom in June 2009, calanoid 27 interaction; vertical mixing − and appendicularians were almost completely absent (<1 ind. m 3). 28 Author for correspondence: 29 Rade Garić, E-mail: [email protected] 30 Introduction 31 32 The species investigated in this study belong to two different and very distant taxonomic 33 groups ( and tunicates) but they have some characteristics in common: (i) 34 high feeding efficiency, (ii) low prey selectivity (with preference for phytoplankton) and (iii) 35 population outbursts under favourable conditions. The opportunistic omnivorous dinoflagel- 36 late species Noctiluca scintillans (Macartney) Kofoid and Swezy 1921 (syn. milaris Suriray 37 1836) is one of the most prominent ‘’ organisms. This large-sized dinoflagellate can 38 be categorized in the same size range with micro- to mesozooplankton communities 39 (Elbrächter & Qi, 1998). Measurements of Noctiluca scintillans in the northern Adriatic indi- 40 cated a maximal cell diameter of up to 1000 µm (Mikaelyan et al., 2014). Noctiluca scintillans 41 is broadly distributed and mainly found in temperate and sub-tropical coastal waters. Red-tide 42 forming Noctiluca is a neritic species and oceanic occurrences are rare (Steidinger & Tangen, 43 1996; Harrison et al., 2011 and references therein). The ability of the species to reproduce rap- 44 idly, together with its polyphagous feeding behaviour, enables population outbursts under 45 favourable conditions, frequently dominating the >200 µm fraction of the plankton (Uhlig 46 & Sahling, 1990; Shanks & Walters, 1996; Elbrächter & Qi, 1998). The diet of the species con- 47 sists of a broad spectrum of prey, including phytoplankton, nauplii and eggs of , 48 organic and (Schaumann et al., 1988; Kirchner et al., 1996; Elbrächter & Qi, 49 1998; Quevedo et al., 1999), thus the species may prey on organisms theoretically higher up in 50 the trophic web. This feeding can lead to competition with other grazers, such as copepods 51 that are reliant on the same food source (Elbrächter & Qi, 1998). Noctiluca has also been 52 implicated in the decline of fisheries in a variety of locations (Huang & Qi, 1997; Smayda, 53 1997; Thangaraja et al., 2007). 54 Salps are filter-feeders, distributed widely in the world , and often recognized as con- 55 spicuous members of zooplankton assemblages. They are characterized by high feeding effi- 56 ciency (Madin & Kremer, 1995; Madin & Deibel, 1998), rapid growth (Heron, 1972; Heron 57 © Marine Biological Association of the United 58 Kingdom 2018 & Benham, 1985; Andersen & Nival, 1986; Madin & Deibel, 1998) and unusual history with alternation of asexual and sexual reproduction (Alldredge & Madin, 1982). These features 59 enable them to form extensive swarms (Kremer, 2002) with hundreds of specimens per cubic 60 metre (Deevey, 1971). These can affect the trophodynamics in surface waters hampering the 61 development of other zooplankton (Berner, 1967; Alldredge & Madin, 1982) by the reduction 62 of phytoplankton (Dubischar & Bathman, 1997; Madin & Deibel, 1998) and by their capability 63 of exploiting small particles over a wide size range, from bacteria to large and micro- 64 zooplankton (Kremer & Madin, 1992). Salps are significant contributors to oceanic carbon 65 flux with very fast growth rates and through their fast-sinking, resistant faecal pellets 66 (Henschke et al., 2013; Smith et al., 2014). 67 In this study we investigated the occurrence of blooms of Noctiluca scintillans and salps in 68 2009 in the open southern Adriatic (OSA) waters which are usually considered as oligotrophic 69 2 Mirna Batistić et al.

(Cerino et al., 2012 and references therein). The southern Adriatic with an inverted microscope (Olympus IX 71) equipped with 70 is the deepest part of the Adriatic (reaching a maximum depth of phase contrast. Microphytoplankton taxa (cells >20 µm) were 71 1242 m), characterized by winter convection events and dense counted at a magnification of 200× in 2–8 transects of the central 72 water formation for the eastern Mediterranean deep circulation part of the chamber and at 100× in transects along the rest of the 73 cell. Winter convection injects into the euphotic zone, base-plate. (cells 2–20 µm) were counted in 74 thereby stimulating phytoplankton development in the otherwise 50 randomly selected fields along the settling chamber base-plate 75 oligotrophic OSA (Gačić et al., 2002; Batistić et al., 2012; Ljubimir at 600×. Results are expressed as number of cells per litre (abun- 76 et al., 2017). In addition, the southern Adriatic is the entry point dance). Cells were counted as nanophytoplankton or microphyto- 77 for advection of water masses of different thermohaline properties plankton size classes according to their maximum cellular linear 78 and nutrient load originating from the Ionian Sea (IS). The dimension. In the case of the chain-forming taxa (e.g. 79 exchange of the southern Adriatic and Ionian Sea are intimately ), chain length was considered, instead of single cell 80 linked by means of the mechanism of the Bimodal Oscillating size, which was smaller than 20 µm and species were attributed 81 System (BiOS) that changes the circulation of the North Ionian to the larger size class. The microphytoplankton fraction was 82 Gyre (NIG) from cyclonic to anticyclonic, and vice versa, on a divided into several groups: diatoms (Heterokontophyta, 83 decadal time scale, during which advection of Atlantic Water Bacillariophyceae); dinoflagellates (Dinophyta, ); 84 (AW) or Levantine Intermediate Water (LIW), respectively, to coccolithophorids (Prymnesiophyta, Prymnesiophyceae); silico- 85 the Adriatic prevails (Gačić et al., 2010). (Heterokontophyta, Dictyochophyceae); and other 86 Blooms of Noctiluca scintillans have not previously been groups with taxa found only sporadically – chlorophytes (Chloro- 87 recorded in the OSA. In contrast, in the northern Adriatic, N. phyta, ); euglenophytes (Euglenophyceae) and 88 scintillans blooms are regular events which usually occur in the cryptophytes (Cryptophyta). Nanophytoplankton cells, in general, 89 spring-summer period (Fonda-Umani et al., 2004; Mikaelyan were not determined to species rank, except in cases when recog- 90 et al., 2014). Salp blooms have been rarely documented in the nition of some taxa (e.g. ) were possible. Small 91 area and they have been attributed to either Salpa maxima (2–10 µm), more or less spherical mono- or biflagellate speci- 92 (Babnik, 1948; Boero et al., 2013)orS. fusiformis (Kršinić, mens, which could not be identified, were included in a group 93 1998). However, OSA waters have not regularly been sampled named Unidentified phytoflagellates. 94 for plankton in the past so these blooms which are usually of For each station and date, the mean for the 0–100 m water col- 95 short duration and patchy distribution might have been over- umn was calculated using the phytoplankton abundance data for 96 looked by standard monitoring. the seven sampling depths (0, 5, 10, 20, 50, 75 and 100 m). The 97 The aim of this paper was to investigate the occurrence of standard deviation (±SD) for the average abundance was also 98 blooms of three species from two distinct taxonomic groups in calculated. 99 OSA waters, usually considered as oligotrophic. Our intention Satellite surface maps were taken from the site of 100 was to understand the physical and biological context in which the Copernicus (Marine environment monitoring service; 101 these blooms occur. This would give us improved understanding http://marine.copernicus.eu/). 102 for prediction of the occurrence of such events in the future. In Zooplankton were sampled with vertical hauls of a Nansen 103 addition, we reviewed the potential of these species to serve as opening–closing net (manufactured by the Institute for Marine 104 possible indicators of changes of trophic status of the area in and Coastal Research, University of Dubrovnik) with a 250-μm 105 some parts of the . mesh (114-cm diameter, 380 cm length) in two layers, surface 106 (0–50 m) and subsurface (50–100 m). This mesh also provided 107 a representative sample for the dinoflagellate Noctiluca scintillans 108 Materials and methods because of its size (200–2000 µm in diameter). Average hauling 109 −1 This study was conducted at three stations in the South Adriatic: speed was 1 m s . Samples were preserved in a 2.5% formalin– 110 nearshore station P-100 (100 m depth) and open sea stations solution buffered with CaCO3. 111 P-300 (300 m depth) and P-1200 (1200 m depth) on 23 Mesozooplankton and N. scintillans were counted and identi- 112 February, 23 April and 15 June 2009 along the central transect fied with an Olympus stereomicroscope SZX9 at 25× and 40×. For 113 of the South Adriatic (Figure 1) with RV ‘Naše More’. calanoid copepods and appendicularians, sub-samples up to 1/32 114 Meteorological parameters such as air temperature and wind of the original sample volume were counted depending on zoo- 115 speed, were extracted from monthly climatological reports issued plankton abundance. Aliquots were determined in such a way 116 by the Croatian Meteorological and Hydrological Service that at least 200 individuals were counted in total. The entire 117 (DHMZ) for the Dubrovnik station. Meteorological data for catch was examined for salps. The abundance of all groups is pre- 118 −3 Dubrovnik were representative for the area given the fact that sented as the number of specimens per cubic metre (ind. m ). 119 bura wind develops when dense, cold and dry continental air Additionally, during zooplankton sampling, the sea surface was 120 surges towards the sea down the mountain slopes. The wind observed (visual census) for blooms. 121 blows from the eastern Adriatic coast across the Adriatic, towards Large salps such as Salpa maxima are hard to quantify using 122 Italy, and causes basin-scale effects. The data were analysed for plankton nets due to their patchy distribution and large chains 123 February 2009 in order to determine if meteorological conditions of aggregate zooids. For such large gelatinous , a visual 124 were favourable for inducing vertical mixing in the open sea. census is the most appropriate method (Boero et al., 2013). We 125 Temperature and salinity profiles (0–1200 m, averaged over estimated their abundance as number of zooids per square 126 2 1-m intervals) were taken with a CTD multiparametric sonde metre (m ). 127 (SEA Bird Electronics Inc., USA). 128 Water samples for phytoplankton were taken with 5-litre 129 Niskin bottles at 0, 5, 10, 20, 50, 75 and 100 m. Phytoplankton Results 130 samples were fixed with neutralized formaldehyde (2% final con- 131 Meteorological conditions centration). Only the phytoplankton fraction larger than 2 µm, 132 recognizable under the light microscope were taken into account. Meteorological conditions were analysed for February 2009. 133 A subsample of 100 ml was settled in an Utermöhl chamber Temperature, wind direction and speed are important in creating 134 (Utermöhl, 1958). Phytoplankton abundance was determined preconditions for winter vertical mixing which is important for 135 Journal of the Marine Biological Association of the United Kingdom 3

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Fig. 1 - B/W online, B/W in print 165 Fig. 1. Sampling stations. 166 167 168 the enrichment of upper layers by nutrients and development of rather uniform (Figure 3). In June thermal stratification formed, 169 phytoplankton in winter and spring in the open sea of the south- with the thermocline positioned between 20 and 30 m depth. A 170 ern Adriatic. Meteorological conditions in February 2009 were maximum temperature of 24.81°C was recorded at the surface 171 characterized by several episodes of the bura, the region’s cold, at P-1200 while for the other two stations maximum temperature 172 dry north-easterly wind (Figure 2). Between 13 and 20 did not exceed 22°C. Below 30 m quite uniform thermal condi- 173 −1 February, wind speed was between 7 and 10 m s . This was tions were present, 13.7–14.6°C. Salinity increased in an offshore 174 accompanied by a marked drop in air temperature from 16 to direction and ranged between 31.97–38.61 at P-100, 37.18–38.65 175 20 February, which fell briefly below 0°C. These conditions natur- at P-300 and 38.15–38.68 at P-1200. A halocline was formed at 176 ally favour cooling of surface water and can be expected to have all three stations. It was shallowest at station P-100 and deeper 177 triggered vertical convection in the South Adriatic Pit. at stations P-300 and P-1200. 178 Satellite surface chlorophyll maps for the southern Adriatic, 179 provided by the Copernicus marine environment monitoring service 180 Hydrographic parameters and −3 (Figure 4), indicated medium-high (around 0.3 to 0.5 mg m ) 181 Physical properties of the east South Adriatic (SA) along the chlorophyll concentration (chl-a) prior to our sampling (from 182 57-km cross-shore section (stations P-100, P-300 and P-1200) the beginning of February until mid-February), which then 183 had noteworthy features. In February, due to cold air conditions, started to decrease towards the end of month. In March surface 184 −3 an inverse stratification, with slightly cooler water on the surface chl-a started to increase and reached from 0.5 to 0.7 mg m 185 and warmer water below the surface, was observed in investigated until the beginning of April 2009. Chl-a values declined slightly 186 stations. The vertical distribution of thermal properties in towards the end of April. From the beginning of June, until 187 February in the upper 100 m (Figure 3) showed slightly warmer mid-June, the surface chl-a signature was low. 188 water at P-300 (13.59°C–13.72°C). At P-1200 and at P-100 the 189 temperature maximum in the upper layer did not exceed 13.59° 190 C. Salinity gradually increased in the offshore direction, P-100 191 Abundance of phytoplankton (37.79–38.42), P-300 (38.18–38.22), P-1200 (38.54–38.67). In 192 April, due to heating, stratification started to form in a surface In February 2009, microphytoplankton abundance was low. There 193 layer with the thermocline positioned between 25 and 30 m was a slight offshore increase with highest abundance (1.2–3.0 × 194 3 −1 depth. The temperature maximum was in the upper 5 m, 16.07° 10 cells l ) in the 20–75 m layer at P-1200. Microphytoplankton 195 C at P-300, 15.65°C at P-100 and 15.45°C at P-1200. Below was composed mostly of coccolithophorids (with percentage con- 196 30 m, relatively uniform thermal conditions (>13.3°C and tribution of 44–60%) and dinoflagellates (32–39%) at stations 197 <14.5°C) were present. Salinity increased in the offshore direction: P-100 and P-300, while diatoms dominated (46%) at station 198 P-100 (36.15–38.29), P-300 (37.89–38.51), P-1200 (38.35–38.65). P-1200. In general, there was no difference in nanophytoplankton 199 The vertical salinity distribution indicated that major fluctuations abundance among stations (averages for the 0–100 layer were 200 4 −1 occurred in the upper 30 m while down to 100 m, salinity was from 3.5, 3.3 and 3.2 × 10 cells l at P-100, P-300 and P-1200 201 4 Mirna Batistić et al.

202 203 204 205 206 207 208 209 210 211 212 213 214 215 216 217 218 219 220 221 222 223 224 225 226 227 228 229 230 231 232 233 234 235 236 237 238 239 240 241 242 243 244 245 246 247 248 249 250 251 Fig. 2 - Colour online, B/W in print 252 Fig. 2. Air temperature, wind speed and direction (clockwise, from north) at Dubrovnik meteorological station. Squares on the wind speed chart denote wind gusts. 253 Shaded portion indicates the cruise dates. 254 255 256 3 −1 with a standard deviation (SD) of 5.6, 9.6 and 3.8 × 10 cells l , (49%) at P-300. Average nanophytoplankton abundances of the 257 5 −1 respectively). 0–100 layer were 6.3, 2.3 and 1.3 × 10 cells l at P-100, P-300 258 In April 2009, phytoplankton abundance decreased in the dir- and P-1200, respectively. Average nanophytoplankton abun- 259 ection from near-shore to the open sea stations (Figure 5). dances of the 0–100 layer were 6.3 ± 2.7, 2.3 ± 0.3 and 1.3 ± 260 5 −1 Average microphytoplankton abundances of the 0–100 layer 0.8 × 10 cells l at P-100, P-300 and P-1200, respectively. 261 3 −1 2 were 3.9 ± 3.6, 3.1 ± 2.0 and 1.47 ± 0.8 × 10 cells l at P-100, In June 2009, microphytoplankton varied from 7.5 × 10 to 262 4 −1 3 P-300 and P-1200, respectively. Microphytoplankton abundances 1.3 × 10 cells l (average of the 0–100 layer 3.8 ± 4.1 × 10 cells 263 −1 2 3 −1 in the surface layer (0–10 m) were two (at P-300 and P-1200) or l ) at P-100; from 6.2 × 10 to 9.2 × 10 cells L (average of 264 3 −1 three times (at P-100) greater than in the layer from 20 to 100 m. the 0–100 layer 4.6 ± 2.9 × 10 cells l ) at P-300; and from 265 2 3 −1 Dinoflagellates dominated (46–58%) in the microphytoplankton 8.0 × 10 to 6.1 × 10 cells l (average of the 0–100 layer 2.9 ± 266 3 −1 in April at P-100 and P-1200, while coccolithophorids prevailed 1.9 × 10 cells l ) at P-1200 (Figure 5). The bulk of 267 Journal of the Marine Biological Association of the United Kingdom 5

268 269 270 271 272 273 274 275 276 277 278 279 280 281 282 283 284 285 286 287 288 289 290 291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308 309 Fig. 3 - Colour online, B/W in print 310 Fig. 3. Vertical profiles of temperature (°C) and salinity along the investigated transect in the southern Adriatic (February, April and June 2009). 311 312 313 microphytoplankton were made up of dinoflagellates (52–70%) at In April 2009, the abundance of N. scintillans markedly 314 −3 all stations. Nanophytoplankton abundances decreased in the off- increased in the offshore direction. A maximum of 80 cells m 315 shore direction, and their average values in the 0–100 layer were was registered in the upper 50 m at the deep open sea station, 316 5 −1 2.1 ± 1.1, 1.9 ± 1.0 and 1.8 ± 1.1 × 10 cells l at stations P-100, P-1200, while very low values were registered at stations P-300 317 −3 P-300 and P-1200, respectively. and P-100 in the upper 50 m (0.04–0.06 cells m ). Noctiluca 318 scintillans was absent from the 50–100 m layer of P-300 and 319 −3 P-100 (Figure 6), while at P-1200 0.7 cells m were recorded. 320 Abundance of three bloom-forming species (Noctiluca Similarly, Salpa fusiformis reached a high abundance of 321 scintillans, Salpa fusiformis, S. maxima), calanoid copepods −3 21 ind. m at the open sea station P-1200 in the 0–50 m layer. 322 and appendicularians Very low abundances of Salpa fusiformis were registered on sta- 323 −3 In February 2009, Noctiluca scintillans occurred in high abun- tions P-300 and P-100 (0.08–1.8 ind. m and it was absent at 324 −3 −3 dance of 21.4 cells m and 343 cells m in the 0–50 m layer P-100 in the 50–100 m layer) (Figure 6). Calanoid copepods 325 of open sea stations P-1200 and P-300, respectively. Maximal were the most abundant mesozooplankton group with maximum 326 −3 −3 abundance of 403 cells m in the 0–50 m layer was registered of 622 ind. m at P-100 in the 0–50 m layer. In general, the low- 327 at shallower station P-100. Abundance of calanoid copepods est abundance of calanoid copepods was at P-300. Abundance of 328 −3 increased from the open sea towards the coast (max. appendicularians was low, less than 14 ind. m at the coastal sta- 329 −3 −3 486 ind. m at station P-100, 50–100 m), while appendicularian tion and 6 ind. m at the open sea stations (Figure 6). 330 abundance increased in the offshore direction (maximum abun- In June 2009, large zooids of S. maxima (avg. 10 cm in length) 331 −3 dance of 236 ind. m at station P-1200, 50–100 m layer) accumulated in high numbers at the surface (Figure 7) of the deep 332 (Figure 6). open sea station P-1200. According to the visual census, we 333 6 Mirna Batistić et al.

334 335 336 337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 Fig. 4 - Colour online, B/W in print 361 Fig. 4. Chlorophyll a satellite images during the investigated period. 362 363 364 −2 estimated their abundance to be 1.5 ind. m . Presumably due to at the open sea till mid-February. Moreover, recent investigation 365 the high feeding presure of S. maxima and competition for the in the OSA indicates increase of phytoplankton abundance and 366 −3 same food, only 1 ind. m of calanoid copepods was found biomass during winter (Ljubimir et al., 2017). However, very 367 −3 2 −1 and appendicularians were almost absent (max. 0.1 ind. m ) low abundance of microphytoplankton (10 cells l in the first 368 (Figure 6). Salpa maxima was not recorded at the station P-300 10 m) registered at the time of sampling in the OSA, from 23– 369 and P-100 where calanoid copepods dominated with 111 and 24 February, is likely due to a combination of grazing pressure 370 −3 579 ind. m in the 0–50 m layer, respectively. Appendicularian by Noctiluca and other herbivorous zooplankton (calanoid cope- 371 abundance was moderate at both stations, with maximum of pods and appendicularians), and vertical mixing of moderate 372 −3 40 ind. m at station P-300 in the 0–50 m layer. intensity which did not exceed 400 m (Ljubimir et al., 2017). 373 According to a study in Sagami Bay, reduction in phytoplankton 374 abundance was mainly controlled by Noctiluca grazing (Baek 375 Discussion et al., 2009). Diatoms, which are the preferred food source for 376 The open southern Adriatic (OSA) is oligotrophic and phyto- Noctiluca scintillans (Harrison et al., 2011), dominated in the 377 plankton abundance and biomass are typically low (Viličić microphytoplankton population at the open sea station P-1200 378 et al., 1989, 1994; Viličić, 1991, 1998; Turchetto et al., 2000; in February. In April 2009, N. scintillans was still present at 379 Cerino et al., 2012). High abundance of Noctiluca scintillans, the OSA deepest station (P-1200) in relatively high abundance 380 Salpa fusiformis and S. maxima in February, April and June in the 0–50 m depth layer alongside with S. fusiformis. 381 2009 in the two open sea stations (P-300 and P-1200) indirectly Accordingly, low abundance of microphytoplankton, particularly 382 indicates the possibility that the OSA is not exclusively oligo- diatoms, was registered at station P-1200 likely due to the grazing 383 trophic, at least at certain times of the year, from winter to pressure of N. scintillans and S. fusiformis. It is interesting that, 384 early summer. In February and April 2009, a N. scintillans unlike February 2009, in April 2009 these two species were not 385 −3 bloom (with maximal abundance up to 343 cells m ) was regis- registered at the open sea station P-300 and nearshore station 386 tered for the first time in the OSA. In contrast, based on long- P-100. This indicates that they had enough food at the surface 387 term studies, the shallow highly eutrophic northern Adriatic is layer of the deepest open sea station (P-1200), which is confirmed 388 the site of a prominent spring-summer bloom (order of magni- by satellite chl-a prior to the sampling date (Figure 4). A bloom of 389 3 6 tude 10 –10 ) of this species, with some blooms (order of magni- another salp species, S. maxima, occurred in June 2009 at the 390 3 tude 10 ) also in winter (Fonda-Umani et al., 2004; Mikaelyan same station. Records of salp blooms in the OSA are rather 391 et al., 2014). Unusual high abundance for the open sea of N. scin- scant in the literature. The possible reason is that gelatinous zoo- 392 tillans in February 2009 in the OSA indicates some changes of the plankton blooms are usually of short duration and might be over- 393 trophic status of the area may have occurred. According to looked by standard net monitoring and therefore have not been 394 Harrison et al.(2011) Noctiluca blooms, in coastal or offshore reported in the past. The only reports of S. maxima blooms in 395 areas, may be a manifestation of , since increase the OSA are from July 1940 (Babnik, 1948), June 1998 and 396 in nutrients leads to increase in phytoplankton abundance, March–May 2013 (Boero et al., 2013). For S. fusiformis the only 397 which is the preferred food of N. scintillans. This presumption report is from March 1990 (Kršinić, 1998). During the S. maxima 398 is supported by satellite chl-a which showed medium-high chl-a bloom in June 2009, calanoid copepods and appendicularians, 399 Journal of the Marine Biological Association of the United Kingdom 7

400 401 402 403 404 405 406 407 408 409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 Fig. 5 - B/W online, B/W in print 430 Fig. 5. Distribution of micro- and nanophytoplankton abundances along the investigated transect in the southern Adriatic in February, April and June 2009. 431 432 433 which are strong competitors for the same food resources, were periphery of the NIG. Conversely, a cyclonic phase in the NIG 434 almost completely absent from the surface up to 100 m depth depresses the nitricline along the borders of the Northern 435 −3 (<1 ind. m ). Abundance of microphytoplankton was low with Ionian Gyre, favouring inflow of nutrient-poorer but saltier 436 very low diatom contribution (Figure 5). Satellite chl-a was also Levantine Intermediate Water (LIW) (Civitarese et al., 2010). In 437 low (Figure 4). Salps have extremely high clearing rates and can 2009, the OSA was enriched by nutrients in two ways: due to 438 feed on all sizes of phytoplankton, from viruses to , com- inflow of AW (salinity did not exceed 38.68) and by winter verti- 439 peting with crustacean filter feeders (Bone, 1998). Because of the cal mixing which injects nutrients into the euphotic zone from 440 swarming potential of these large microphages they are able to deeper layers, thereby stimulating phytoplankton increase in the 441 control phytoplankton blooms (Fortier et al., 1994) and to otherwise oligotrophic OSA. This is in accordance with uniform 442 increase the transfer of biogenic carbon to the bottom through salinity and temperature (Figure 3), and high nutrient values, par- 443 their fast-sinking, resistant, faecal pellets. ticularly nitrate, evident at the deepest station P-1200 in February 444 Blooms of Noctiluca and salps at the OSA might be indirect (max. 6 µM) and April 2009 (max. 4.5 µM) (Ljubimir et al., 2017). 445 indicators of eutrophication of the area, since an increase in nutri- During February 2009, prior to our sampling date, several epi- 446 ents leads to an increase in phytoplankton, their main food source sodes of strong wind (the region’s cold, dry northwind bura) 447 as a grazer. Recently, in situ and satellite chl-a data have indicated were responsible for substantial heat loss at the air–sea interface. 448 that phytoplankton blooms in the OSA are more frequent than we This produced dense surface water and consequent convective 449 previously assumed and with some interannual variability mixing (Gačić et al., 2002) that, at offshore station P-1200, 450 (Santoleri et al., 2003;D’Ortenzio & d’Alcala, 2009). This variabil- extended to 400 m (Ljubimir et al., 2017). The evolution of this 451 ity is dependent on the meteorological conditions that affect the convective event was also captured by a series of surface chloro- 452 open-ocean convection which drives the mixing and uplifting of phyll images taken by satellites. The images show moderately 453 nutrients from the rich intermediate layers into the euphotic high chl-a concentration at the beginning of February and subse- 454 zone. It is further modulated by incursions of different water quent chl-a minimum (due to convection-driven sinking of 455 masses into the OSA, especially during winter, that modify not phytoplankton to the deep) extending over a wide area of the 456 only thermohaline properties, but also chemical properties (dif- Southern Adriatic at the end of February. The chl-a minimum 457 ferent nutrient load) of the area (Gačić et al., 2002; Civitarese corresponds with the cooling event a few days before (16–20 458 et al., 2010). Water exchange between the Southern Adriatic February), after which a significant increase of chl-a was observed 459 and Ionian Sea is intimately linked by means of the Bimodal over the following 2–3 weeks (beginning of March). 460 Oscillating System (BiOS) mechanism that changes the circulation During the period from 2009 to 2013, only in 2011 did winter 461 of the North Ionian Gyre (NIG) from cyclonic to anticyclonic and vertical mixing not occur in the OSA (Ljubimir et al., 2017). It is 462 vice versa, on a decadal time scale (Gačić et al., 2010). When the likely that blooms of salps, and possible Noctiluca (only registered 463 NIG is anticyclonic, Atlantic Water (AW) enters the SA, decreas- in this investigation), occurred also in other following open 464 ing salinity and increasing nutrients from upwelling at the sea vertical mixing but were not observed because of the dynamics 465 Fig. 6 - Colour online, B/W in print 50 i.6. Fig. 8 – 0 )i eray pi n ue2009. June and April February, in m) 100 itiuino bnacsof abundances of Distribution otlc scintillans Noctiluca , ap fusiformis Salpa aaodcppd n pedclrasa h he ttosi w aes(0 layers two in stations three the at appendicularians and copepods calanoid , in Batisti Mirna – 0mand m 50 ć tal. et 531 530 529 528 527 526 525 524 523 522 521 520 519 518 517 516 515 514 513 512 511 510 509 508 507 506 505 504 503 502 501 500 499 498 497 496 495 494 493 492 491 490 489 488 487 486 485 484 483 482 481 480 479 478 477 476 475 474 473 472 471 470 469 468 467 466 Journal of the Marine Biological Association of the United Kingdom 9

such as vertical mixing and inflow of water masses of different 532 properties, driven by the BiOS mechanism, on the biology of 533 the OSA in winter and spring. Such exceptional bloom events 534 as we registered in February (N. scintillans), April (N. scintillans 535 and S. fusiformis) and June (S. maxima) 2009 probably had a sig- 536 nificant impact on the functioning of the marine ecosystem of the 537 southern Adriatic, in particular on the carbon transfer across the 538 pelagic food web and the proportion of sinking carbon. These 539 hypotheses need to be confirmed in future investigations. 540 541 Acknowledgements. We would like to thank Jakica Njire for her help with 542 illustrations and the Captains and crews of research vessels ‘Naše more’ and 543 ‘Baldo Kosić’ for their assistance during sampling cruises. This paper was pre- sented at the 52nd European Symposium held in Piran, 544 Slovenia. 545 546 Funding. This research was funded by Croatian Ministry of Science and 547 Education (grant number 275-0000000-3186) and Croatian Science 548 Foundation (IP-2014-09-2945, project AdMedPlan). 549 550 551 References 552 Alldredge AL and Madin LP (1982) Pelagic tunicates: unique herbivores in 553 the marine plankton. Bioscience 32, 655–663. 554 Andersen V and Nival P (1986) A model of the population dynamics of salps 555 in coastal waters of the Ligurian Sea. Journal of Plankton Research 8, 1091– 556 1110. 557 Babnik P (1948) Hidromeduze iz srednjega in južnega Jadrana v letih 1939. in 558 1940. (Hydromedusae from the Middle and South Adriatic 1939 and 1940). 559 – Acta Adriatica 3, 275 344 (in Slovenian, English summary). 560 Baek SH, Shimode S, Kim HC, Han MS and Kikuchi T (2009) Strong 561 bottom-up effects on phytoplankton community caused by a rainfall during 562

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