Estuarine, Coastal and Shelf Science 115 (2012) 1E13

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Estuarine, Coastal and Shelf Science 115 (2012) 1e13

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Estuarine, Coastal and Shelf Science

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Recent changes in the marine ecosystems of the northern Adriatic Sea

Michele Giani a,*, Tamara Djakovac b, Danilo Degobbis b, Stefano Cozzi c, Cosimo Solidoro a, Serena Fonda Umani d a Istituto Nazionale di Oceanograﬁa e di Geoﬁsica Sperimentale, via A. Piccard 54, 34014 Trieste, Italy b Center for Marine Research, Rudjer Boskovic Institute (CMR), Rovinj, Croatia c Istituto di Scienze Marine, CNR, Trieste, Italy d Dipartimento di Scienze della Vita, Università di Trieste, Trieste, Italy article info abstract

Article history: This review of studies on long term series on river discharges, oceanographic features, plankton, fish and Received 14 August 2012 benthic compartments, collected since the 1970s revealed significant changes of mechanisms and trophic Accepted 27 August 2012 structures in the northern Adriatic ecosystems. A gradual increase of eutrophication pressure occurred Available online 7 September 2012 during the 1970s until the mid 1980s, followed by a reversal of the trend, particularly marked in the 2000s. This trend was ascribed to the combination of a reduction of the anthropogenic impact, mainly Keywords: due to a substantial decrease of the phosphorus loads, and of climatic modifications, resulting in long-term changes a decline of atmospheric precipitations and, consequently, of the runoff in the northern Adriatic Sea. nutrients fi hypoxia Signi cant decreases of the phytoplankton abundances were observed after the mid 1980s, concurrently trophic levels with changes in the species composition of the communities, with an evident shift toward smaller cells marine ecosystems or organism sizes. Moreover, changes in the zooplankton community were also observed. A decrease of Adriatic Sea demersal fishes, top predators and small pelagic fishes was ascribed to both overfishing and a demise of eutrophication. Macrozoobenthic communities slowly recovered in the last two decades after the anoxia events of the 1970s and 1980s. An increasing number of non-autochthonous species has been recorded in the last decades moreover the increasing seawater temperature facilitated the spreading of thermophilic species. Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction autumn, whereas in winter cooling and cold north-easterly wind cause intense mixing and the formation of dense waters. The The northern Adriatic Sea (NAd) is the shallowest (<60 m), land impact of nutrient loads from Italian rivers is more marked along locked, northernmost region of the Mediterranean (Fig. 1). the western and northern coastal areas, extending in period of The general circulation of NAd is driven by the combination of water column stratification over larger areas (e.g. Degobbis et al., wind stress, river runoff and surface buoyancy fluxes, exchange at 2000; Cozzi and Giani, 2011). These processes together with the southern boundary, and physiographic constraints. The Po and remineralization sustain a high primary production. In contrast, in other river discharges originate a southward, intense, coastal the eastern more oligotrophic NAd, less influenced by river current along the western coast (Western Adriatic Current, WAC), discharges, remineralization processes are more relevant than which fuels and sustains a cyclonic circulation, while on the eastern external nutrient inputs. side of the basin, the weak, warm and salty Eastern Adriatic Current Combined effects of the anthropogenic impact and regional (EAC) flows along the eastern coast. At depth, a colder and denser climate changes are causing modifications of the physical and water mass moves southwards. A bathymetric controlled trans- chemical oceanographic characteristics of the NAd, influencing its verse current along the 50 m isobath, re-circulate the EAC into the biota. These modifications are documented by a growing amount of WAC (Poulain et al., 2001). data, so that their re-analysis is important to better clarify the In this region, water column stratification, caused by freshwater current state of this marine ecosystem and to address future buoyancy and heating of the sea surface, occurs from spring to mid research. In this paper the main changes observed during the last four * Corresponding author. decades in the NAd ecosystem are summarized, based on results of E-mail address: [email protected] (M. Giani). this Special Issue on “Fluctuations and trends in the northern

Fig. 1. The northern Adriatic Sea. Main sampling stations where long time series were collected. The Eastern Adriatic Current (EAC), the Istrian Coastal Countercurrent (ICCC), and the Western Adriatic Current (WAC) are also shown.

Adriatic marine systems: from annual to decadal variability” and 2. Influence of climate changes on circulation, hydrologic and on other recent scientific papers. Conclusions on some key oceanographic properties parameters are further corroborated by analyses of unpublished data updating the existing long term series. Modifications in The NAd is under the influence of pronounced seasonal and environmental conditions, caused by natural and anthropogenic inter-annual up to multi-decadal climate fluctuations over Europe pressures, and their effects from lower trophic levels up to fishes (Camuffo et al., 2000). These fluctuations, which can be identified are considered. by indices, like the Northern Atlantic Oscillation (NAO), modify the M. Giani et al. / Estuarine, Coastal and Shelf Science 115 (2012) 1e13 3 sea circulation and influence the composition of biological An unusually marked increase in salinity since the 2000 was communities, from micro-organisms, both in plankton and evidenced from the analyses of trends over the years 1976e benthos, to fishes and other organisms (Conversi et al., 2010; Gordo 2006 in the entire NAd (Solidoro et al., 2009) and 1972e2009 et al., 2011). in the eastern NAd (Djakovac et al., 2012)andintheGulfof An increase in air temperature of 0.9 C was detected in Europe Trieste (Malacicetal.,2006). This increase was attributed both from 1901 to 2005, with a significative trend since the 1980s to reduced river outflows and to a more sustained inflow from (þ0.4 C/decade; Alcamo et al., 2007). This warming has decreased the central Adriatic. In fact, frequently, and particularly in precipitations (35e40%), especially in southern Europe, including spring and summer, freshwater from the Po River spreads over snow over the Alps and, consequently, the runoff in the northern large areas of the NAd and even up to the opposite coast, Adriatic watersheds (Cozzi and Giani, 2011). The highest spring markedly enhancing stratification and modifying the circulation increase of air temperature in the Po River valley during the period pattern (Degobbis et al., 2000). In these seasons, semi- 1865e2002 was measured in the years 1997e2002 (Deserti et al., permanent cyclonic and anticyclonic subregional gyres 2005). Analyses of sea surface temperature data collected in the develop, enclosing a larger part of freshened water, and thus NAd have evidenced markedly higher temperatures (up to 5 C) in reducing the water exchange with the central Adriatic (Krajcar, all seasons of the period 1988e1999 with respect to the period 2003). These gyres are larger in summer, with development of 1911e1987 (Russo et al., 2002). The differences were more the south-easterly Istrian Coastal Countercurrent (ICCC; e.g. pronounced in the western NAd, especially in winter and spring. Supicetal.,2000). In fact, the ICCC replaces the Eastern Adriatic Moreover, comparisons between these two periods indicated that Current (EAC) that contributes in more saline and oligotrophic a significant increase of surface salinity, mainly due to a reduction waters from the central Adriatic, and is more frequent in the of freshwater discharge, occurred after 1988, particularly in the colder seasons. ICCC appeared frequently in the period 1966e western NAd, except in autumn. Similar changes were also 1997, and its intensity was significantly correlated with some observed in the eastern NAd, during the period 1921e2000, in the lags to airesea heat fluxes in combination with Po River flow entire water column (Supic et al., 2004). Interannual changes of rates, particularly in August (Supicetal.,2000). High intensity surface temperature correlated with heat flux and NAO index, of the ICCC coincided with events of near anoxia, anoxia and/or while salinity and density variability depended mainly on the Po mucilage events. In contrast, in the period 2000e2009 the ICCC River discharge. This increasing trend was also measured in the were much less frequent than in the period 1972e1999 surface layer of the open NAd waters (Degobbis et al., 2000), (Djakovac et al., 2012). particularly in spring, continuing up to date (Fig. 2). In the period The enhanced entrapment of air CO2 was estimated to have 1976e2006, a considerable increase of surface temperature was already caused a seawater acidification of 0.05e0.14 pH units in the observed during spring and summer also in the western coastal western Mediterranean Sea (The MerMex Group et al., 2011) and waters (Solidoro et al., 2009). also in the NAd dense waters, (0.06 pH units from 1983 to 2008, A major consequence of warming is the sea-level rise (SLR), Luchetta et al., 2010). In the Gulf of Trieste, the annual cycle of pCO2 mostly due to thermal expansion of the seawater and melting of in the surface waters is controlled by warming, reversing the heat low-latitude glaciers. A linear increasing trend of SLR of 0.7 mm yr 1, flux from the atmosphere to the sea. In the upper layer, biological smaller than in the world oceans, was computed for data collected CO2 uptake was partially compensated by inputs from karstic during the period 1930e1999 in the eastern NAd (Bakar Bay, Orlic, waters (Cantoni et al., 2012). Conversely, the respiration of organic 2001). This difference was due to regional and local effects as also carbon leads to significant increase of dissolved inorganic carbon shown in the Venice Lagoon (Carbognin et al., 2004). and decrease of pH in the deeper waters.

Fig. 2. Multidecadal variations of temperature anomalies in the western and eastern northern Adriatic. Anomalies are calculated using the methods reportedinDjakovac et al. (2012). Thin solid lines represent the anomalies, bold solid lines represent linear regression ﬁt and p the signiﬁcance. 4 M. Giani et al. / Estuarine, Coastal and Shelf Science 115 (2012) 1e13

Changes in formation of dense waters, as well as their volumes TN levels remained much higher. Po River discharges of total and physical properties, are also expected, with potential conse- organic matter account for 255,000 t yr 1 of carbon, of which z50% quences on Mediterranean thermohaline circulation and on the in particulate forms (Pettine et al., 1998). capability of the NAd to sequestrate carbon through air CO2 Diffuse sources are the most important for the N load, due to dissolution and the continental shelf pump mechanism intense agriculture within the Po Valley, although wastewater (Krasakopoulou et al., 2011; Solidoro personal communication). disposal in the watersheds and along the coast is also significant, contributing for 35% of the total N and P loads in the NAd as 3. Inputs of continental freshwaters and nutrients a whole, and even 60% for the Po River (Palmeri et al., 2005). Similarly, wastewater disposal represents an important input of TP, The anthropogenic impact in the NAd is larger than in the rest of in coastal waters as the Gulf of Trieste (Cozzi et al., 2008). The mean the Adriatic, due to high river discharges, mainly from the Po River contribution of atmospheric depositions (wet and dry) in the NAd w (mean flow 47 km3 yr 1 in the period 1917e2008; Cozzi and Giani, was estimated to account for 14% of the total inputs of both TN 2011). Freshets occur most frequently in spring (due to rain and and TP (Degobbis and Gilmartin, 1990). However, in some high melting snow in the Alps and Apennines) and/or during autumn industrialized coastal areas, like the Gulf of Trieste this source may heavy raining events. Thus, in the NAd the runoff significantly be much more important (Malej et al., 1997). depends on interannual oscillations of precipitations, which might be easily affected in the future by climate modifications (Zanchettin 4. Trends of eutrophication pressure and its consequences on et al., 2008; Cozzi et al., 2012). This dependence resulted in stronger the oxygen budget (weaker) precipitation and higher (lower) discharges during negative (positive) anomalies of the NAO index. 4.1. Long-term changes of nutrient, organic matter and chlorophyll A marked decrease of the Po River flow as well as of minor rivers a concentrations was observed in the last decade with a significant shift in 2003 (Fig. 3; Cozzi and Giani, 2011; Djakovac et al., 2012; Mozetic et al., The annual external input of nutrients, mostly anthropogenic, is 2012). In this period the most prolonged droughts have occurred, of the same order of magnitude as the regenerated amounts during even more severe than during the 1940s (Zanchettin et al., 2008). In their seasonal cycle (Degobbis and Gilmartin, 1990). Therefore, fact, since 1980 the flow rate of the minor rivers, was also small changes of these inputs, combined with changes in the water fl substantially reduced (33%). Consequently, in the years 2003e exchange rate with the central Adriatic, which is strongly in u- fl fi 2007, the nutrient discharges in the NAd, estimated for the period enced by climatic uctuations, signi cantly affected the eutrophi- 1998e2002 to amount up to 262,000 t yr 1 for total nitrogen (TN), cation pressure in the NAd. Changes of mean surface salinity and e 11,10 0 t y 1 for total phosphorus (TP) and 196,000 t yr 1 for temperature in the open NAd during the period 1972 2000 were generally well correlated with Po River flow rates, except during the orthosilicate (SiO4), decreased by 50e70% (Cozzi and Giani, 2011). A similar decrease (60e70%) was calculated for the rivers of the Gulf late 1980s, when salinity was lower and temperatures higher than of Trieste (Cozzi et al., 2012). expected from such correlations (Degobbis et al., 2000; Djakovac, Nutrient discharges were characterized by marked overloads of 2003). This departure was explained by unusually long periods of meteorological stability, during which freshwater mixing was TN and SiO4 compared to TP (molar ratios TN/TP ¼ 48e208, DIN limited to a thinner surface layer, in which heat accumulation was (dissolved inorganic nitrogen)/PO4 (orthophosphates) ¼ 37e418, SiO (silicates)/DIN ¼ 0.5e1.0), which increasingly enhanced the favored. Higher nutrient concentrations in seawater were 4 e e P-limitation of the primary production in the NAd (Cozzi and Giani, measured during 1972 1978 as compared to 1980 1985, despite 2011). In fact, in the period 2003e2007 (Cozzi and Giani, 2011)it the increased DIN and PO4 levels in the Po River waters. This was fl was evident a doubling of TN and a halving of P compounds in the due to higher ow rates in the earlier period. After 1986, the fl Po River water, compared to the period 1979e1984 (Marchetti et al., average ow rate of the Po River was similar to the preceding 1985), These changes, which were already observed in 1989e1994, period, but the seawater concentrations of PO4 were lower (Fig. 4a), were mainly a consequence of polyphosphate reduction in deter- whereas DIN (Fig. 4b) and SiO4 concentrations were higher, mainly gents (Degobbis et al., 2000, 2005). Thus, while the TP concentra- due to changes in the Po River nutrient composition (Degobbis tion has recently returned at levels of the late 1960s and 1970s, the et al., 2000). In relation to this, when compared at the same salinity (i.e. same dilution degree, independently from the freshwater discharge rate), the Chl a concentrations and the primary 3000 production rates were higher in periods of higher river PO4 concentrations, but not of DIN concentrations. The mean Po River 2500 flow rate in recent years (2003e2009) was significantly lower than in the previous period (1972e1999; Fig. 3). Consequently, a marked 2000 -1 increase in surface salinity and decrease in PO4 and Chl a concen- s

3 trations occurred in the eastern NAd during the more recent period 1500 (Djakovac et al., 2012), as well as at the western waters (Fig. 4a, d). fi Q / m Q / 1000 Concurrently, a signi cant increasing trend of the DIN/PO4 ratio occurred (Fig. 4c). The decreasing Chl a trend was statistically 500 significant at 10 m (Fig. 4d), being the surface data more variable. In contrast, during late winter and in spring DIN concentrations were 0 higher in 2000e2009, despite the lower freshwater discharge and fl 1970 1975 1980 1985 1990 1995 2000 2005 2010 increased in ows of oligotrophic waters by EAC. This DIN increase (Fig. 4b) was very probably due to an enhanced reduction of the PO4 Time / year concentration after 2000, already observed since the late 1980s, limiting further the phytoplankton growth and resulting in a more Fig. 3. Multidecadal variations of the mean annual flow of Po River. Solid line repre- fi sents regime shift determined according to Rodionov (2004), probability: 0.05, cut-off marked accumulation of unused DIN. Overall, a signi cant length: 7 yr. decreasing trend of the PO4 and Chl a concentrations (Fig. 4a, d) and M. Giani et al. / Estuarine, Coastal and Shelf Science 115 (2012) 1e13 5

Fig. 4. Multidecadal anomalies of a) phosphates concentrations (c(PO4)), b) dissolved inorganic nitrogen concentrations (c(DIN)), c) DIN/PO4 ratio and d) chlorophyll a concentrations (c(Chla)) in the western and eastern North Adriatic. Anomalies are calculated using the methods reported in Djakovac et al. (2012). Thin solid lines represent the anomalies, bold solid lines represent linear regression ﬁt and p the signiﬁcance.

an increasing trend of DIN (Fig. 4b) and of DIN/PO4 ratio (Fig. 4c) although they still exceeded the Redfield values, due to an excess of were detected during the last four decades. C and N in relation to P. Remarkably, anomaly events were absent or Other analyses over the period 1970e2007 confirmed the less intense in 2003 and 2005e2007, when the freshwater flow aforementioned observations, showing significant decreasing rates were lower than usual and the EAC ingression more marked. trends for PO4, ammonium and Chl a concentrations in the NAd, but Dissolved organic carbon (DOC) accounted for 80e90% of the not for nitrate and SiO4 (Solidoro et al., 2009; Mozetic et al., 2010). total OC (dissolved and particulate) in the water column. Analyses These changes were marked in the 2000s, particularly in the area of multiyear DOC concentration highlighted pronounced seasonal directly affected by Po River discharges. In the more oligotrophic cycle in the NAd, as with winter minima and summer maxima (59e eastern coastal waters the decrement was the lowest, while inter- 166 mM). Stratification of the water column, circulation and inten- mediate values were obtained for the Gulf of Trieste, the Gulf of sity and timing of primary production and bacterial C demand are Venice and the central open waters. Related to this, the concen- the main factors causing accumulation of organic matter during tration of surface active organic substances, primarily phyto- summer, which was highly variable from year to year (26e75 mM; plankton exudates and their degradation products, also Pettine et al., 2001; Giani et al., 2005; De Vittor et al., 2008). considerably decreased in the upper water column during the Dissolved organic nitrogen (DON) and phosphorus (DOP) are an period 2003e2010 compared to 1998e2003 (Gasparovic, 2012). important reservoir of these elements in the NAd, accounting for Seasonal and multi-year variations of nutrient concentrations 49e99% and 60e100% of the TDN and TDP (Cozzi et al., 2004), and their stoichiometric ratios were studied in the Gulf of Trieste in Lipizer et al. (2012) on a 12-yr times series in the Gulf of Trieste the period 1999e2010 (Lipizer et al., 2011, 2012; Cossarini et al., found the lowest concentration of DIN and the highest concentra- 2012). The mechanism of seasonal variations, similarly as in the tions of DON (74% of total N) and DOP (76% of total P) together to NAd open waters, depended on freshwater discharge, mainly from the lowest contribution of PO4 (5% of TP) during a period charac- the Isonzo River, triggering phytoplankton blooms, heat exchange terized by high ingressions of salty waters. Freshwater loads and with the atmosphere, ingression of nutrient-depleted waters (EAC), high chlorophyll events were also characterized by increases of C water column stratification, and wind mixing. The ratios between and N in all pools, whereas an excess of DOC over DON occurred organic carbon, nitrogen and phosphorus, both in the dissolved and during the freshets. particulate pools (C:N:P), as well as between DIN and PO4 markedly The degradation of organic matter along the water column is increased during events of extremely high freshwater discharges, mediated by enzymes released into the environment by plank- much richer in N than in P, as well as a consequence of intense tonic organisms. Significant negative correlations between phytoplankton blooms. In contrast, increased ingressions of high leucine aminopeptidase (AMA) activity and salinity suggested the salinity EAC and heterotrophic processes reduced the ratios, importance of river inputs in providing allochthonous organic 6 M. Giani et al. / Estuarine, Coastal and Shelf Science 115 (2012) 1e13 matter for microbial metabolism (La Ferla et al., 2002). Marked magnitude lower than the loss for TN and TP, whereas a much decreasing vertical gradients of AMA and alkaline phosphatase higher release was estimated for SiO4. In the western NAd about (APA) were established in stratified water column. During late 85% of C, 60% of TP, 40% of TN and 85% of SiO4 settled yearly on the spring and summer, prokaryotic and phytoplankton can utilize sediment are recycled to the water column (Giordani et al., 1992). DOP producing APA, and, thus, satisfying their seasonal P Different studies evidenced a marked spatial and seasonal vari- requirements (Ivancic et al., 2009). Autumn and winter mixing in ability of benthic fluxes, although only a few examined interannual the water column processes drastically decreased APA in upper variabilities and were mostly limited to the Gulf of Trieste (Kemp waters, because of dilution and supply of regenerated nutrients et al., 1999 and reference therein). In this region the nutrients from deeper waters. The maximum rates of hydrolysis of AMA, a- regeneration in the sediment is sufficient to support benthic and b-glucosidase (a-andb-GLU), b-galactosidase (b-GAL), APA microalgal growth but not the phytoplankton growth (Bertuzzi and lipase (LIP) in the Gulf of Trieste in the period 2000e2005 et al., 1996). TP, TN and organic C started to excessively accumu- varied markedly during the year with winter minima and late in the sediment of the Gulf of Trieste since 1950, as a conse- maxima from April to October (Celussi and Del Negro, 2012). quence of increasing use in inorganic fertilizers and detergents During summer, APA, LIP and AMA reached their highest activi- (Ogrinc and Faganeli, 2006). ties, while polysaccharide degradation prevailed in spring and autumn during phytoplankton blooms. APA/AMA ratio was 4.2. Water oxygenation and hypoxia/anoxia events generally low, indicating that microbial communities were rarely P-limited, probably by using organic P sources. A pronounced The combined effects of high primary production, organic year-to-year variability of degradation patterns was observed, in matter riverine loads, persistent stratification of the water column, particular for AMA and APA. Mixing processes affected, especially and increased bottom water residence time led to a progressive a-andb-GLU activity, possibly as a consequence of resuspension consumption of dissolved oxygen (DO) in the bottom layers of large of organic matter from the seabed. Large-impact phenomena, areas with reduced lateral advection (Degobbis et al., 2000; Tedesco such as the heat wave in 2003 and mucilage, influenced the et al., 2007; Solidoro et al., 2009). degradation of specific substrates. Mucilage enhanced LIP, APA Hypoxia (DO < 2mgL1, i.e. <1.4 ml L 1) has been often and AMA whereas their pronounced inhibition was observed considered a recurrent feature of NAd and one of the most signif- during summer 2003. Celussi and Del Negro (2012) also icant source of environmental risk for its ecosystems. Hypoxic hypothesized that prevailing glycolytic activities after 2002 might episodes have been reported especially in the western NAd and be connected to the ongoing reduction in autotrophic biomass close to the Po River mouth during the 1970s and 1980s (Rinaldi (Mozeticetal.,2010), which might have deprived microbial et al., 1992), but the scientific literature describes only few anoxia communities of monomeric sugars of marine origin during events at the basin scale: 1977 (Degobbis et al., 1979) and 1989 (Ott, winterespring periods. 1992; Giani et al., 1992; Degobbis et al., 2000). However after 2000, Preliminary budget estimations showed that exchange rates of only few cases of dissolved oxygen saturation lower than 20% has nutrients at the seawateresediment interface are lower than those been observed (Socal et al., 2008; Solidoro et al., 2009). In fact, due to water mass exchange with the central Adriatic (Degobbis a time series of DO along the Po-Rovinj transect (bottom layer, and Gilmartin, 1990). Remarkably, yearly burial represents an Fig. 5) showed that the frequency of hypoxia was reduced in the last important loss of TP and SiO4, accounting for 36% and 20% of the two decades, and no occurrence of anoxia in the open waters of total loss, respectively, while denitrification in the sediment (42% of NAd (Fig. 5) was detected. the total) is almost as important for TN loss as in advective Consumption of DO in bottom layers prevails over production exchanges with the central Adriatic. In contrast, regeneration rate from August (in the western area) to November (in the central and and release from the surface sediment appeared to be one order of eastern area; Degobbis et al., 2000), until the water column remains

Fig. 5. Dissolved oxygen concentrations (c(O2)) in the bottom layers at 5 stations along the profile Rovinj e Po River delta in the period summereautumn 1972e2009. Labeled years 1 indicates occurrence of hypoxia (c(O2)<1.4 ml L ). Updated from Djakovac (2006). M. Giani et al. / Estuarine, Coastal and Shelf Science 115 (2012) 1e13 7 stratified. This process was more rapid when the Po River flow rates 1994, when the dinoflagellates abundance was lower. This group were high in spring, as, for example, during the period 1972e1978, was more abundant in the mid 1980s. In the period 1989e1994 peaking in 1977, when anoxia developed in November. In the significant changes in the species composition occurred, with period 1988e1991 hypoxia events were more marked than ex- a shift to smaller size species. Investigations were extended to the pected from the Po River flow rate, primary production, and P loads period 1972e2009 (Maric et al., 2012). Regime shift analysis iden- (Fig. 5). This was probably due to unusually stable meteorological tified upward shifts in the 1980s and a major downwards shifts in conditions and to consequent delayed mixing of the water column 2000 of the total phytoplankton. The abundances of all principal and reduced water exchange with the central Adriatic. fractions (diatoms, dinoflagellates and nanophytoplankton) were Measurements in sediment core based on phytoplankton markedly lower in the period 2000e2009 than in the period 1972e remains and foraminiferal records at a site near the Po River pro- 2009. These changes were related mainly to an increase of salinity delta, deposited in the last 100 years, indicated an increasing and, in a minor measure, to fluctuations of temperature and eutrophication, particularly after the 1930s and first signs of anoxia nutrients, particularly PO4. since the 1960s (Duijnstee et al., 2004). The variability of the phytoplankton abundance and composi- A reconstruction over 150 years, carried out in a sediment core tion in the Gulf of Venice during the period 1990e1999 was due to at the same site, based on Dinoflagellate cysts, evidenced a decrease the influence of several rivers, water exchange with the Lagoon of of the heterotrophic/autotrophic ratio after 1978, concomitant with Venice, and complex circulation patterns (Bernardi Aubry et al., an increase of near-anoxic or anoxic events (Sangiorgi and Donders, 2004). The main limiting factors for phytoplankton were light, 2004). From 1960 to 1978 the dinocysts diversity decreased indi- temperature and strong meteorological events. Nutrients, mainly cating stressful conditions in the NAd. PO4 were limiting only in cases of prolonged drought periods. Over the 10-year study, a decrease in PO4 concentrations was observed, 5. Plankton dynamics mainly due to substitution of polyphosphate in detergents with other fillers in the late 1980s. The studied area was subdivided into 5.1. Viruses, prokaryotes and flagellates three zones, characterized by different eutrophication levels. In each zone, phytoplankton was similar in terms of community A significant relationship between viruses and prokaryotes structure, although different in abundance. As expected in was obtained from data collected in 2001 over the entire Adriatic a nutrient-enriched system, the community was dominated by Sea (Corinaldesi et al., 2003), very similar to that found in 1991e diatoms over most of the year. The importance of dinoflagellates 1993 by Weinbauer and Suttle (1996), which was interpreted as was generally low, with significant abundances only in JuneeJuly. the lack of any change in prokaryotic and viruses abundance over Bernardi Aubry et al. (2012) did not evidence any significant the previous decade. The Authors also observed that viral change in both phytoplankton abundance and species composition distribution was even more significantly related to prokaryotic at two offshore stations between the periods 1999e2001 and turnover. Karuza et al. (2012) analyzed a 10-year time series of 2003e2006. They found that the phytoplankton community was both viruses and prokaryotes (heterotrophic-HP, autotrophiceAP) composed of 372 taxa and was dominated by diatoms, although it collected monthly in the Gulf of Trieste. Viral abundances were only partially matched the ecological succession previously comparable to those found by Corinaldesi et al. (2003). Abun- described in a more coastal area. dance of HP ranged from 0.4 to 38$108 L 1, while AP fluctuated Conversely, in the Gulf of Trieste, on a larger and continuous from 0.01 to 594$106 L 1. No clear temporal patterns of viral data set (1986e2010) Cabrini et al. (2012) found significant changes abundance were noticed, while both HP and AP presented a late in both abundance and composition of phytoplankton (Fig. 6). The summer peak. The only positive significant relationship was major shift in abundance was detected in 1993e1994 (as already found between temperature and viruses. pointed out by Fonda Umani et al., 2004 and Kamburska and Fonda- Over the period 1990e2002 Ivancic et al. (2010) observed along the transect RovinjePo River delta (Fig. 1) prokaryotic abundances in the same order of magnitude reported by Corinaldesi et al. 10000000 (2003), afterwards (2003e2008) they registered a drastic 60 decrease and a shift toward biomass production rather than toward fi reproduction. Signi cant relationships were found between HP and -3 temperature and chlorophyll a concentration, respectively. After 50 m

2003, as a consequence of lower HP biomass, heterotrophic ﬂag- -1 1000000 ellates abundance (HF) decreased by about three times. Weakened 40 coupling between HP and HF conﬁrmed a minor role of grazing pressure in controlling HP after 2003. 30 5.2. Microphytoplankton abundance and diversity 100000

Phytoplankton / cell L / cell Phytoplankton 20 Measurements of phytoplankton abundance along the proﬁle RovinjePo River delta (Fig. 1) from 1990 to 2004 evidenced that

mg / (dw) biomass Zooplankton intense blooms (over 106 cells L 1) often appeared when the 10 southward ICCC was pronounced. Blooms ﬂoated up to 30 days, typically in March, or appeared simultaneously in separate gyres 10000 0 with different species compositions (Kraus and Supic, 2011). 1985 1990 1995 2000 2005 2010 Long-term studies on the microphytoplankton community Time / year composition identiﬁed 344 species in the period 1972e1994 Fig. 6. Variations during the last decades of mean annual phytoplankton abundances (Miokovic, 1999). The lowest number of species was observed in (triangles) and zooplankton biomass - expressed as dry weight (dw, circles) e in the e the period 1984 1988, when the eutrophication pressure was Gulf of Trieste. Redrawn from Cabrini et al. (2012) and Mozetic et al. (2012), respec- enhanced. The diatom abundance was higher in the period 1989e tively. Dotted lines represent the regime shift periods. 8 M. Giani et al. / Estuarine, Coastal and Shelf Science 115 (2012) 1e13

Umani, 2009) mainly due to a dramatic decrease of phytoflagel- system. Based on different trophic pyramid structures the Authors lates. As regard species composition, only few species maintained hypothesized that metazoan biomass can be supported by the same seasonality, although in both periods the ecological bacterial biomass. successions resembled the one found in the Gulf of Venice in term The analysis of 10 yr observation of plankton community and of functional guilds. On the contrary, in the eastern part of the Gulf biogeochemical data in the Gulf of Trieste (Cossarini et al., 2012) of Trieste, Mozetic et al. (2012) found a reduction of phytoplankton corroborated the conceptual scheme of ecosystem functioning in due to the decrease of diatom blooms intensity and to a shift toward coastal area of freshwater influence proposed in Solidoro et al. smaller size cells. Over the period 1989e2009 a regime shift in (2007) and Fonda Umani et al. (2007), in agreement with major 2002e2003 was identified, which encompassed physical, chemical energy paths within the planktonic food web are fueled along the and biological parameters, and one of the most evident features traditional food chain during a first phase, in which river nutrient was the increase of nanoplankton fraction. The Authors speculated input sustain large diatom blooms, but through the microbial food that in the first period (1989e2003) the bottom up control pre- web and the microbial loop in a second and third phase, when more vailed as well as the “classic” food web, while in the second period oligotrophic conditions are present, and heterotrophic processes with reduced resources the switch from bottom-up to top-down prevail on autotrophic ones. These conclusion were definitely control can occur seasonally. The striking differences between the confirmed by the experimental estimates of carbon fluxes along the two coastal sites of the Gulf of Trieste pointed out a more local pelagic trophic web and the possible export to the bottom for the control of riverine inputs and anthropogenic forcing. same area (Fonda Umani et al., 2012). On the base of 21 grazing experiments the Authors were able to depict the seasonal evolution 5.3. Micro- and mesozooplankton of the system, which was autotrophic in the first part of the year and became heterotrophic in the second one shifting the H/A ratio Data on microzooplankton in the NAd are scarce as evidenced by from 0.12 in winter to 1.17 in summer when all the system was Fonda Umani et al. (2010) who already noted that there were almost totally supported by the prokaryotic biomass and produc- relevant changes in tintinnid’s community composition between tion. In the first part of the year primary production exceeded the old surveys (1983e1994) and the more recent ones (1995e respiration, whereas in the second one the latter largely exceeded. 2002). In the Gulf of Trieste Monti et al. (2012) over the period Respiration was particularly high in all the autumn experiments 1986e2010, observed dramatic changes not of total abundance, but probably because of the refractory nature of DOC, which accumu- of microzooplankton community composition. Aloricate ciliates late over seasons. dominated in both periods, but tintinnids drastically decreased, The experimental evidence of the regular alternation of the two mainly because of the lack of spring peaks, characteristic for the trophic modes, obtained at one sampling coastal site, corroborates previous period. Substantial changes in tintinnid composition were the findings of Cossarini et al. (2012) on a larger area of the Gulf of also observed with the almost complete disappearance of some Trieste over an 8-yr period. The Authors evidenced also the species and the arrival of some “new entries”. differences in timing and intensity of the biogeochemical processes Comparing three periods (1991e1995, 1999e2001, 2003e among the three considered areas, suggesting that spatial differ- 2006) Bernardi Aubry et al. (2012) evidenced a clear decrease of ences are inherent for a coastal system under the direct influence of cladoceran abundance in autumn in the Gulf of Venice. In a river, and recommending to use different references term for contrast, small copepods (i.e. Oncaea spp. and Diaxis pygmaea) different sub-areas. increased. Nevertheless, the Authors depicted an ecological succession with a pronounced maximum in summer. Similar 6. Changes in benthic communities changes of the copepod community, as well as a general increase, were observed over a period of almost 30 years by Kamburska 6.1. Microphytobenthos and Fonda-Umani (2006) and Conversi et al. (2009) in the Gulf of Trieste. The latter Authors observed also significant phenolog- Very few estimates of microphytobenthos productivity have ical changes in most of the dominant copepod species. The been published. In the Gulf of Trieste, the annual benthic primary Authors hypothesized that the observed changes were mostly production is 36 g C m 2 yr 1 (Bertuzzi et al., 1996). The micro- related to the general increase in the sea surface temperature, phytobenthic community did not seem to be photosynthetically which induced a northerly displacement of the “warm” species active throughout the whole year. From August to December, low/ and the large, possibly critical, reduction in the abundance of negative microphytobenthic productivity values are originated by a “cold” species (Pseudocalanus elongatus). On the same long term a shift from the autotrophic to heterotrophic metabolism of benthic data set Kamburska and Fonda-Umani (2009) found a relevant diatoms that occurs in correspondence with low photosynthetically shift of mesozooplankton biomass since 2001e2002 in compar- active radiation and/or high temperatures at the bottom. The ison with the 1980s. Observed changes of mesozooplankton warming of seawater, changes of salinity, and covering of the biomass significantly match with shift in copepod abundance, seafloor by episodic high sedimentations due to extreme river phytoplankton, temperature and NAO index. In the eastern part of floods and by the presence of mucilage were also identified as the Gulf of Trieste Mozetic et al. (2012) found as well shift in factors able to modify the benthic diatom associations (Cibic et al., mesozooplankton biomass (Fig. 6), which only partially over- 2012). lapped those found by Kamburska and Fonda-Umani (2009). Data of benthic photosynthesis measured in the area south of Po 2 1 Recently, Fuks et al. (2012) described the changes that can Delta (2e23 mmol O2 m d ) indicated that dissolved oxygen occur in the pelagic food web structure in the NAd by using a 5 yr produced in this compartment is basically consumed within the data set on nutrients, phytoplankton, bacteria, protozoan and sediment, as it never exceeds the consumption rates (3e 2 1 metazoan. They described the switches in the trophic pyramid 34 mmol O2 m d ; Epping and Helder, 1997; Moodley et al., along the water column in the eastern and western part of the 1998). These values correspond to an estimated benthic respira- NAd in oligotrophic and eutrophic conditions. In the former the tion of 54e89 g C m 2 yr 1 equal to 67e90% of the carbon reaching microbial food web prevailed with a heterotrophic/autotrophic the seafloor. An estimate of the benthic microalgal gross production ratio in the range 1.2e1.7. “Classic” food web on the contrary (H/ (i.e. based on O2 fluxes across sedimentewater interface) has been A ¼ 0.3e0.7) were detected when nutrient inputs enriched the performed by Kemp et al. (1999) for the entire NAd obtaining M. Giani et al. / Estuarine, Coastal and Shelf Science 115 (2012) 1e13 9

a value of 30 g C m 2 y 1. Microphytobenthic primary production which was related to an increase of oxygen concentration and of has been estimated to contribute to z15% of the total production in sand content in the sediments. This shift was further confirmed by the NAd and to 40% in the Gulf of Trieste (Kemp et al., 1999). observations carried out from 2004 to 2006 (N’Siala Massamba et al., 2008). The long term decline of the Chamelea gallina clam 6.2. Macrobenthos fishery in the western NAd has been instead attributed to the reduction of riverine nutrients and of primary producers, although High macrofaunal biomass (9e16 g C m 2) and production (11e overfishing might have played a role (Romanelli et al., 2009). 19 g C m 2 yr 1) characterize the area South of Po Delta, indicating A 20 yr long study carried out in the eastern NAd showed that the presence of consistent inputs of organic matter from the water soft-bottom polychaete declined after the anoxic event of 1989 column and an intense benthicepelagic coupling (Moodley et al., leading the macrobenthic communities to an instability with the 1998). However, submerged macrophytes that were dominant dominance of bivalves (Mikac et al., 2011). During the recovery the primary producers in shallow-water soft-bottom areas of the NAd contribution of bivalves to the overall diversity and abundance have become much less abundant over the last century. Algal decreased gradually. vegetation on the rocky coast in the eastern NAd has also declined Also on a local scale (e.g. the Bay of Muggia, Gulf of Trieste) since the 1970s (Newell and Ott, 1999). The cause of these reduc- a general recover of the macrobenthic community was observed in tions has been attributed to an increased turbidity of the waters 1994 in respect to 1981, which in turn was in worst conditions than and to the overgrazing by flourishing sea urchin populations (Falace in 1975 (Solis-Weiss et al., 2004). et al., 2010). Mass mortalities of benthic macrofauna have been reported in 7. Changes in fish communities particular during the 1970s and 1980s, as a consequence of repeated events of hypoxia and anoxia. The largest mortalities were The NAd is one of the most productive area of the Mediterra- due to the anoxic crisis of 1974, 1977, 1983 and 1989 (Fedra et al., nean and one of the most relevant fishing ground. Historical 1976; Stachowitsch, 1984; Ott, 1992; Orel et al., 1993). In the last ecology studies, suggest that in the NAd fish community structure decades no mass mortalities due to hypoxia at regional scale were has been changing for centuries, even before industrial fishing reported. The deposition of mucilage aggregates causes stress and occurrence, possibly as a result of artisanal fishing and other damages on benthic organisms (e.g. Stachowitsch et al., 1990; anthropogenic impacts, climatic factors, eutrophication trends Castelli and Prevedelli, 1992; Devescovi and Ivesa, 2007), though (Fortibuoni et al., 2010; Lotze et al., 2011). the concurrence of hypoxic conditions can obscure the role of Anyway, significant changes in fish community composition and mucilage in causing mortalities of benthic organisms. in abundances of many species have been certainly occurring e and In the last three decades, a spreading of more than 40 non- accelerating e during last decades, after the 1950s, as evidenced indigenous species was also observed in the NAd (Occhipinti- both by analysis of fishery independent information and from Ambrogi, 2002). It included 14 macrophytes (Orlando-Bonaca, landings statistic (Fortibuoni et al., 2010). In particular, it has been 2010 and references therein), as well as 26 animals: among them, observed a decline of elasmobranches (sharks, rays and skates) only two were non-benthic species. This phenomenon was mainly tuna, swordfish, marine mammals and large demersal, and, more caused by shipping/maritime transport, aquaculture activities or by generally, of large-sized and late-maturing species proportion in a diffusion through the Suez Canal or Gibraltar Strait (Crocetta, fish composition as well as diadromous fish (eel, sturgeon) and 2011). Most of these species are of indo-pacific or Australian small pelagics (Grbec et al., 2002; Santojanni et al., 2006; Ferretti origin. The number of taxonomic units involved in bio-invasions is et al., 2008; Coll et al., 2010; Fortibuoni et al., 2010; Lotze et al., probably underestimated and their effects on the local ecosystems 2011; and references therein). Analysis of fishery independent are still poorly known. data collected after the 1980s (Coll et al., 2010) evidences that fish Macroepifauna communities are widely distributed in the NAd community has not recovered in the last two decades, and actually and largely consist of interspecific high biomass multispecies a decreasing trend is still going on in total biomass, in the average clumps (Fedra et al., 1976). Shelly hard substrates provide the base trophic level of fish community and in the demersal/pelagic ratio for sessile, suspension feeding colonizers (mostly sponges, ascidian, for many species, including both demersal, and pelagic ones. anemones or bivalves), which in turn serve as substrate for addi- Analyses based on catches confirmed that e since mid 1980s e tional vagile or hemisessile organisms (Riedel et al., 2008). The small pelagic catches were not recovering too (Grbec et al., 2002; clumps of epibenthic organisms which characterized the area of the Coll et al., 2010). Gulf of Trieste before the mid 1970s, reaching mean biomasses of Changes in fish abundance and community composition might 370 g m 2 (Fedra et al., 1976), declined after the mass mortality of result from the superposition of fishing effects, driven by techno- 1983, without a subsequent recover because of a following anoxic logical evolution and market dynamic, and by environmental crisis in 1988 and of trawling fishing activity (Kollmann and effects, influenced by anthropogenic and natural stressors. Beside Stachowitsch, 2001). In particular, the trawling fishing has been direct effects, such as fishing mortality or changes in habitat suit- shown to cause severe impact on benthic biocenoses also in other ability, pressures can induce indirect effects, such as the modifi- areas of the NAd (Giovanardi et al., 1998). cation of nursery areas, changes in juvenile survival, potentially Changes of benthic macrofauna along the Emilia Romagna coast induced by changes in phenology and consequent lack of in 1985 were observed with respect to previous analyses in 1934e synchronization (matchemismatch) between predators require- 36 (Crema et al., 1991). The new biocenoses showed a large abun- ments and presence of prey, successful invasion of alien species, dance of Corbula gibba, a species typical of the transition zone evolutionary changes. As an example of direct effect, an increasing between detrital and muddy bottoms. This dominance and the trend of thermophilic taxa, which appear to expand northward, has good richness in biodiversity was interpreted as an immature, been reported in the Adriatic Sea (Dulcic et al., 2004; Azzurro et al., transitory successional stage due to intermittent recovery after 2011 and references therein), concurrently with changes in periodic disturbances. Analyzing the seasonal variations of mac- oceanographic properties. As an example of indirect effect, changes robenthic community from 1996 to 2000 in the same area, in environmental conditions, and in particular in river discharges, Occhipinti-Ambrogi et al. (2002) observed a shift in the community clearly influence the recruitment of anchovy in the northern and structure, mainly due to the substitution of C. gibba by Ampelisca, central Adriatic (Santojanni et al., 2006). 10 M. Giani et al. / Estuarine, Coastal and Shelf Science 115 (2012) 1e13

Table 1 Major environmental changes observed in the Northern Adriatic sea.

Environmental changes Data series Area Direction Period of main changes References Air temperature 1865e2002 Po River watershed [ Since 1997 Deserti et al., 2005

Precipitation 1831e2003 Po River watershed Y Since 1920s, enhanced Zanchettin et al., 2008 Evapotranspiration [ in 2000s

Sea level 1971e2002 Venice Lagoon [ Since 1970s Carbognin et al., 2004 1930e1999 East. NAd (Bakar Bay) Since 1980s Orlic, 2001

River water discharge 1917e2008 Po River 1975e2008, enhanced Cozzi and Giani, 2011 since 2003 1980e2008 minor NAd rivers Y Since the 1980s Cozzi et al., 2012 1989e2009 Rivers in the Gulf of Trieste 2003e2007 Mozetic et al, 2012

River loads of N 1973e2007 Po River [ 1970s to 1990s Cozzi and Giani, 2011 2000e2007 Po and minor rivers Y In 2000s Cozzi et al., 2012

River load of P 1968e2007 Po River Y Since the late 1980s Cozzi and Giani, 2011 2000e2007 Rivers in the Gulf of Trieste 2003e2007 Cozzi et al., 2012

River load of Si 1995e2007 Po River Y 2003e2007 Cozzi and Giani, 2011 2000e2007 Rivers in the Gulf of Trieste 2003e2007 Cozzi et al., 2012

Seawater temperature 1911e1999 Open waters of NAd [ Since 1980s (peak in 2003) Russo et al., 2002 1921e2000 Eastern NAd Supic et al., 2004 1991e2003 Eastern Gulf of Trieste Malacic et al., 2006 1985e2005 Western NAd Tedesco et al., 2007 1972e2009 Open waters of NAd This study

Seawater salinity 1911e1999 Open NAd [ Since 2000 Russo et al., 2002 1991e2003 Eastern Gulf of Trieste Malacic et al., 2006 1976e2006 Open and coastal NAd Solidoro et al., 2009 1972e2009 Eastern NAd Djakovac et al., 2012 1989e2009 Eastern Gulf of Trieste Mozetic et al., 2012

PO4 in seawater 1972e1995 Open NAd Since 1986 Degobbis et al., 2000 1976e2006 Open and coastal NAd Y Enhanced since 2000 Solidoro et al., 2009 1972e2009 Eastern NAd Djakovac et al., 2012

DIN in seawater 1972e1995 Open NAd [ Since 1986 Degobbis et al., 2000 1972e2009 Eastern NAd Enhanced since 2000 Djakovac et al., 2012

SiO4 in seawater 1972e1995 Open NAd [ Since 1986 Degobbis et al., 2000

Surface active organic 1998e2010 Open NAd Y Since 2000 Gasparovic, 2012 matter (SAS)

Frequency of marked 1972e2009 Open NAd [ Since the 1970s This study hypoxia Y Since mid 1990s

Chlorophyll a 1970e2007 Open and coastal NAd Since 2000 Mozetic et al., 2010 1972e2009 Open NAd Y This study 1989e2009 Eastern Gulf of Trieste Since 2005 Mozetic et al., 2012

Phytoplankton abundance 1972e2009 Eastern NAd Since 2000 Maric et al., 2012 1989e2009 Eastern Gulf of Trieste Y Mozetic et al., 2012 1986e2010 Western Gulf of Trieste Since 1994 Cabrini et al., 2012

Phytoplankton size 1989e2009 Eastern Gulf of Trieste Y Since 2004 Mozetic et al., 2012

Microzooplankton abundance 1986e2010 Western Gulf of Trieste / Monti et al., 2012

Tintinnids abundance 1986e2010 Western Gulf of Trieste Y Since 1998 Monti et al., 2012

Mesozooplankton abundance 1970e2005 Western Gulf of Trieste [ Since 1988 Conversi et al., 2009

Mesozooplankton biomass 1972e2005 Western Gulf of Trieste [ Since 2001 Kamburska & Fonda Umani, 2009 1989e2009 Eastern Gulf of Trieste Since 2004 Mozetic et al., 2012 1975e2000 North-Central Adriatic Y Since 1980s Coll et al., 2010

Fish communty average 1975e2000 North-Central Adriatic Y Since 1980s Coll et al., 2010 trophic level

Demersal/pelagic 1975e2000 North-Central Adriatic Y Since 1985 Coll et al., 2010

Demersal ﬁsh biomass 1975e2000 North-Central Adriatic Y Since 1980s Coll et al., 2010

Small pelagic (catches) 1975e2000 North-Central Adriatic Since 1980s Coll et al., 2010 1975e2000 North-Central Adriatic Y Since 1980s Santojanni, 2006 1950e2000 Central-South Adriatic Since 1970s Grbec et al., 2002

Y Decrease, [ Increase, / Not trend. M. Giani et al. / Estuarine, Coastal and Shelf Science 115 (2012) 1e13 11

8. Summary and conclusions efficiency and resilience. The reversal in the eutrophication trend, and the consequent reduction in plankton productivity, altered this Long-term ecological studies reported significant modifications balance, possibly increasing the risk of collapse of fisheries and of the environmental conditions in the NAd (Table 1), due to climatic increasing the probability of occurrence of major changes in fluctuations and changes of the anthropogenic pressure, as: ecosystem structure and functioning. The increasingly frequent outbreaks of jellyfishes (Kogovsek et al., 2010), the endangerment - a warming of surface waters at regional scale; of key-stone species, the replacement of top predator species, the - a marked decrease of the freshwater outflow during the 2000s, decrease in small pelagic catches are examples of such changes. due to reduction of precipitations, that, together with Also the fact that the demersal/pelagic ratio has not been increasing frequency of the EAC ingression, caused a rise of increasing, despite the reductions in the eutrophication processes surface salinity, being more markedly in the western area; and in the frequency of hypoxia events might be seen as a symptom - a decrease of the appearance frequency of ICCC after the 2000, of the lack of resilience of the system. which reduced the water residence time; Nonetheless, the evident effort of the scientific community - an increased river loads of N coupled to decreased P loads, due over the last decades to include in the long term ecological to enforcements of environmental law; studies also the microbial compartment, many parameters - an increased DIN/PO4 ratio in the waters due to reduction of fundamental to describe the functioning of the ecosystems in the riverine TP and to a limitation of N uptake by phytoplankton; NAd, as primary production, respiration, temporal variation of the - an acidification of dense waters due to the increase of atmo- sedimentewater fluxes are still undersampled both spatially and spheric CO2; temporally.

These environmental changes had relevant consequences for Acknowledgments the ecosystem, which responses were: The compilation of this paper was supported by the Perseus - a reduction of the phytoplankton biomass and its surface active FP7-OCEAN-2011-287600 Project, the MEDSEA FP7-ENV-2010- excretions due to a decrease of TP concentrations, particularly 265103 Project, and the Croatian Ministry of Science project in the western NAd; 0982705-2731. The data to update the long time series were kindly fl - a reduction in the intensity and frequency of late winter diatom provided by CMR Rovinj and ARAP Emilia Romagna (Po River ow). blooms since 1994; - a general trend toward small size species, which can explain References the decrease of chlorophyll a concentration; - a dramatic decrease of tintinnids’ abundance and a significant Alcamo, J., Moreno, J.M., Nováky, B., Bindi, M., Corobov, R., Devoy, R.J.N., Giannakopoulos, C., Martin, E., Olesen, J.E., Shvidenko, A., 2007. Europe. 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