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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, ItalybCenter for Marine Research, Rudjer Boskovic Institute (CMR), Rovinj, Croatiac Istituto di Scienze Marine, CNR, Trieste, ItalydDipartimento di Scienze della Vita, Università di Trieste, Trieste, Italy

a r t i c l e i n f o

Article history:Received 14 August 2012Accepted 27 August 2012Available online 7 September 2012

Keywords:long-term changesnutrientshypoxiatrophic levelsmarine ecosystemsAdriatic Sea

* Corresponding author.E-mail address: [email protected] (M. Giani).

0272-7714/$ e see front matter � 2012 Elsevier Ltd.http://dx.doi.org/10.1016/j.ecss.2012.08.023

a b s t r a c t

This review of studies on long term series on river discharges, oceanographic features, plankton, fish andbenthic compartments, collected since the 1970s revealed significant changes of mechanisms and trophicstructures in the northern Adriatic ecosystems. A gradual increase of eutrophication pressure occurredduring the 1970s until the mid 1980s, followed by a reversal of the trend, particularly marked in the2000s. This trend was ascribed to the combination of a reduction of the anthropogenic impact, mainlydue to a substantial decrease of the phosphorus loads, and of climatic modifications, resulting ina decline of atmospheric precipitations and, consequently, of the runoff in the northern Adriatic Sea.Significant decreases of the phytoplankton abundances were observed after the mid 1980s, concurrentlywith changes in the species composition of the communities, with an evident shift toward smaller cellsor organism sizes. Moreover, changes in the zooplankton community were also observed. A decrease ofdemersal fishes, top predators and small pelagic fishes was ascribed to both overfishing and a demise ofeutrophication.

Macrozoobenthic communities slowly recovered in the last two decades after the anoxia events of the1970s and 1980s.

An increasing number of non-autochthonous species has been recorded in the last decades moreoverthe increasing seawater temperature facilitated the spreading of thermophilic species.

� 2012 Elsevier Ltd. All rights reserved.

1. Introduction

The northern Adriatic Sea (NAd) is the shallowest (<60 m), landlocked, northernmost region of the Mediterranean (Fig. 1).

The general circulation of NAd is driven by the combination ofwind stress, river runoff and surface buoyancy fluxes, exchange atthe southern boundary, and physiographic constraints. The Po andother river discharges originate a southward, intense, coastalcurrent along the western coast (Western Adriatic Current, WAC),which fuels and sustains a cyclonic circulation, while on the easternside of the basin, theweak, warm and salty Eastern Adriatic Current(EAC) flows along the eastern coast. At depth, a colder and denserwater mass moves southwards. A bathymetric controlled trans-verse current along the 50 m isobath, re-circulate the EAC into theWAC (Poulain et al., 2001).

In this region, water column stratification, caused by freshwaterbuoyancy and heating of the sea surface, occurs from spring to mid

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autumn, whereas in winter cooling and cold north-easterly windcause intense mixing and the formation of dense waters. Theimpact of nutrient loads from Italian rivers is more marked alongthe western and northern coastal areas, extending in period ofwater column stratification over larger areas (e.g. Degobbis et al.,2000; Cozzi and Giani, 2011). These processes together withremineralization sustain a high primary production. In contrast, inthe eastern more oligotrophic NAd, less influenced by riverdischarges, remineralization processes are more relevant thanexternal nutrient inputs.

Combined effects of the anthropogenic impact and regionalclimate changes are causing modifications of the physical andchemical oceanographic characteristics of the NAd, influencing itsbiota. These modifications are documented by a growing amount ofdata, so that their re-analysis is important to better clarify thecurrent state of this marine ecosystem and to address futureresearch.

In this paper the main changes observed during the last fourdecades in the NAd ecosystem are summarized, based on results ofthis Special Issue on “Fluctuations and trends in the northern

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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), andthe Western Adriatic Current (WAC) are also shown.

M. Giani et al. / Estuarine, Coastal and Shelf Science 115 (2012) 1e132

Adriatic marine systems: from annual to decadal variability” andon other recent scientific papers. Conclusions on some keyparameters are further corroborated by analyses of unpublisheddata updating the existing long term series. Modifications inenvironmental conditions, caused by natural and anthropogenicpressures, and their effects from lower trophic levels up to fishesare considered.

2. Influence of climate changes on circulation, hydrologic andoceanographic properties

The NAd is under the influence of pronounced seasonal andinter-annual up to multi-decadal climate fluctuations over Europe(Camuffo et al., 2000). These fluctuations, which can be identifiedby 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 biologicalcommunities, from micro-organisms, both in plankton andbenthos, to fishes and other organisms (Conversi et al., 2010; Gordoet al., 2011).

An increase in air temperature of 0.9 �C was detected in Europefrom 1901 to 2005, with a significative trend since the 1980s(þ0.4 �C/decade; Alcamo et al., 2007). This warming has decreasedprecipitations (35e40%), especially in southern Europe, includingsnow over the Alps and, consequently, the runoff in the northernAdriatic watersheds (Cozzi and Giani, 2011). The highest springincrease of air temperature in the Po River valley during the period1865e2002 was measured in the years 1997e2002 (Deserti et al.,2005). Analyses of sea surface temperature data collected in theNAd have evidenced markedly higher temperatures (up to 5 �C) inall seasons of the period 1988e1999 with respect to the period1911e1987 (Russo et al., 2002). The differences were morepronounced in the western NAd, especially in winter and spring.Moreover, comparisons between these two periods indicated thata significant increase of surface salinity, mainly due to a reductionof freshwater discharge, occurred after 1988, particularly in thewestern NAd, except in autumn. Similar changes were alsoobserved in the eastern NAd, during the period 1921e2000, in theentire water column (Supi�c et al., 2004). Interannual changes ofsurface temperature correlated with heat flux and NAO index,while salinity and density variability depended mainly on the PoRiver discharge. This increasing trend was also measured in thesurface layer of the open NAd waters (Degobbis et al., 2000),particularly in spring, continuing up to date (Fig. 2). In the period1976e2006, a considerable increase of surface temperature wasobserved during spring and summer also in the western coastalwaters (Solidoro et al., 2009).

A major consequence of warming is the sea-level rise (SLR),mostly due to thermal expansion of the seawater and melting oflow-latitude glaciers. A linear increasing trendof SLRof 0.7mmyr�1,smaller than in the world oceans, was computed for data collectedduring the period 1930e1999 in the eastern NAd (Bakar Bay, Orli�c,2001). This difference was due to regional and local effects as alsoshown in the Venice Lagoon (Carbognin et al., 2004).

Fig. 2. Multidecadal variations of temperature anomalies in the western and eastern north(2012). Thin solid lines represent the anomalies, bold solid lines represent linear regression

An unusually marked increase in salinity since the 2000 wasevidenced from the analyses of trends over the years 1976e2006 in the entire NAd (Solidoro et al., 2009) and 1972e2009in the eastern NAd (Djakovac et al., 2012) and in the Gulf ofTrieste (Mala�ci�c et al., 2006). This increase was attributed bothto reduced river outflows and to a more sustained inflow fromthe central Adriatic. In fact, frequently, and particularly inspring and summer, freshwater from the Po River spreads overlarge areas of the NAd and even up to the opposite coast,markedly enhancing stratification and modifying the circulationpattern (Degobbis et al., 2000). In these seasons, semi-permanent cyclonic and anticyclonic subregional gyresdevelop, enclosing a larger part of freshened water, and thusreducing the water exchange with the central Adriatic (Krajcar,2003). These gyres are larger in summer, with development ofthe south-easterly Istrian Coastal Countercurrent (ICCC; e.g.Supi�c et al., 2000). In fact, the ICCC replaces the Eastern AdriaticCurrent (EAC) that contributes in more saline and oligotrophicwaters from the central Adriatic, and is more frequent in thecolder seasons. ICCC appeared frequently in the period 1966e1997, and its intensity was significantly correlated with somelags to airesea heat fluxes in combination with Po River flowrates, particularly in August (Supi�c et al., 2000). High intensityof the ICCC coincided with events of near anoxia, anoxia and/ormucilage events. In contrast, in the period 2000e2009 the ICCCwere much less frequent than in the period 1972e1999(Djakovac et al., 2012).

The enhanced entrapment of air CO2 was estimated to havealready caused a seawater acidification of 0.05e0.14 pH units in thewestern Mediterranean Sea (The MerMex Group et al., 2011) andalso in the NAd dense waters, (0.06 pH units from 1983 to 2008,Luchetta et al., 2010). In the Gulf of Trieste, the annual cycle of pCO2in the surface waters is controlled by warming, reversing the heatflux from the atmosphere to the sea. In the upper layer, biologicalCO2 uptake was partially compensated by inputs from karsticwaters (Cantoni et al., 2012). Conversely, the respiration of organiccarbon leads to significant increase of dissolved inorganic carbonand decrease of pH in the deeper waters.

ern Adriatic. Anomalies are calculated using the methods reported in Djakovac et al.fit and p the significance.


Changes in formation of dense waters, as well as their volumesand physical properties, are also expected, with potential conse-quences on Mediterranean thermohaline circulation and on thecapability of the NAd to sequestrate carbon through air CO2dissolution and the continental shelf pump mechanism(Krasakopoulou et al., 2011; Solidoro personal communication).

3. Inputs of continental freshwaters and nutrients

The anthropogenic impact in the NAd is larger than in the rest ofthe Adriatic, due to high river discharges, mainly from the Po River(mean flow 47 km3 yr�1 in the period 1917e2008; Cozzi and Giani,2011). Freshets occur most frequently in spring (due to rain andmelting snow in the Alps and Apennines) and/or during autumnheavy raining events. Thus, in the NAd the runoff significantlydepends on interannual oscillations of precipitations, which mightbe easily affected in the future by climate modifications (Zanchettinet al., 2008; Cozzi et al., 2012). This dependence resulted in stronger(weaker) precipitation and higher (lower) discharges duringnegative (positive) anomalies of the NAO index.

Amarked decrease of the Po River flow as well as of minor riverswas observed in the last decade with a significant shift in 2003(Fig. 3; Cozzi and Giani, 2011; Djakovac et al., 2012; Mozeti�c et al.,2012). In this period the most prolonged droughts have occurred,evenmore severe than during the 1940s (Zanchettin et al., 2008). Infact, since 1980 the flow rate of the minor rivers, was alsosubstantially reduced (�33%). Consequently, in the years 2003e2007, the nutrient discharges in the NAd, estimated for the period1998e2002 to amount up to 262,000 t yr�1 for total nitrogen (TN),11,100 t y�1 for total phosphorus (TP) and 196,000 t yr�1 fororthosilicate (SiO4), decreased by 50e70% (Cozzi and Giani, 2011). Asimilar decrease (60e70%) was calculated for the rivers of the Gulfof Trieste (Cozzi et al., 2012).

Nutrient discharges were characterized by marked overloads ofTN and SiO4 compared to TP (molar ratios TN/TP ¼ 48e208, DIN(dissolved inorganic nitrogen)/PO4 (orthophosphates) ¼ 37e418,SiO4 (silicates)/DIN ¼ 0.5e1.0), which increasingly enhanced theP-limitation of the primary production in the NAd (Cozzi and Giani,2011). In fact, in the period 2003e2007 (Cozzi and Giani, 2011) itwas evident a doubling of TN and a halving of P compounds in thePo Riverwater, compared to the period 1979e1984 (Marchetti et al.,1985), These changes, which were already observed in 1989e1994,were mainly a consequence of polyphosphate reduction in deter-gents (Degobbis et al., 2000, 2005). Thus, while the TP concentra-tion has recently returned at levels of the late 1960s and 1970s, the

1970 1975 1980 1985 1990 1995 2000 2005 2010

Time / year

0

500

1000

1500

2000

2500

3000

Q /

m3

s-1

Fig. 3. Multidecadal variations of the mean annual flow of Po River. Solid line repre-sents regime shift determined according to Rodionov (2004), probability: 0.05, cut-offlength: 7 yr.

TN levels remained much higher. Po River discharges of totalorganicmatter account for 255,000 t yr�1 of carbon, of whichz50%in particulate forms (Pettine et al., 1998).

Diffuse sources are the most important for the N load, due tointense agriculture within the Po Valley, although wastewaterdisposal in the watersheds and along the coast is also significant,contributing for 35% of the total N and P loads in the NAd asa whole, and even 60% for the Po River (Palmeri et al., 2005).Similarly, wastewater disposal represents an important input of TP,in coastal waters as the Gulf of Trieste (Cozzi et al., 2008). Themeancontribution of atmospheric depositions (wet and dry) in the NAdwas estimated to account for w14% of the total inputs of both TNand TP (Degobbis and Gilmartin, 1990). However, in some highindustrialized coastal areas, like the Gulf of Trieste this source maybe much more important (Malej et al., 1997).

4. Trends of eutrophication pressure and its consequences onthe oxygen budget

4.1. Long-term changes of nutrient, organic matter and chlorophylla concentrations

The annual external input of nutrients, mostly anthropogenic, isof the same order of magnitude as the regenerated amounts duringtheir seasonal cycle (Degobbis and Gilmartin, 1990). Therefore,small changes of these inputs, combined with changes in the waterexchange rate with the central Adriatic, which is strongly influ-enced by climatic fluctuations, significantly affected the eutrophi-cation pressure in the NAd. Changes of mean surface salinity andtemperature in the open NAd during the period 1972e2000 weregenerallywell correlatedwith Po River flow rates, except during thelate 1980s, when salinity was lower and temperatures higher thanexpected from such correlations (Degobbis et al., 2000; Djakovac,2003). This departure was explained by unusually long periods ofmeteorological stability, during which freshwater mixing waslimited to a thinner surface layer, in which heat accumulation wasfavored. Higher nutrient concentrations in seawater weremeasured during 1972e1978 as compared to 1980e1985, despitethe increased DIN and PO4 levels in the Po River waters. This wasdue to higher flow rates in the earlier period. After 1986, theaverage flow rate of the Po River was similar to the precedingperiod, but the seawater concentrations of PO4 were lower (Fig. 4a),whereas DIN (Fig. 4b) and SiO4 concentrations were higher, mainlydue to changes in the Po River nutrient composition (Degobbiset al., 2000). In relation to this, when compared at the samesalinity (i.e. same dilution degree, independently from the fresh-water discharge rate), the Chl a concentrations and the primaryproduction rates were higher in periods of higher river PO4concentrations, but not of DIN concentrations. The mean Po Riverflow rate in recent years (2003e2009) was significantly lower thanin the previous period (1972e1999; Fig. 3). Consequently, a markedincrease in surface salinity and decrease in PO4 and Chl a concen-trations occurred in the eastern NAd during the more recent period(Djakovac et al., 2012), as well as at the western waters (Fig. 4a, d).Concurrently, a significant increasing trend of the DIN/PO4 ratiooccurred (Fig. 4c). The decreasing Chl a trend was statisticallysignificant at 10 m (Fig. 4d), being the surface data more variable. Incontrast, during late winter and in spring DIN concentrations werehigher in 2000e2009, despite the lower freshwater discharge andincreased inflows of oligotrophic waters by EAC. This DIN increase(Fig. 4b) was very probably due to an enhanced reduction of the PO4concentration after 2000, already observed since the late 1980s,limiting further the phytoplankton growth and resulting in a moremarked accumulation of unused DIN. Overall, a significantdecreasing trend of the PO4 and Chl a concentrations (Fig. 4a, d) and

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 concen-trations (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)were detected during the last four decades.

Other analyses over the period 1970e2007 confirmed theaforementioned observations, showing significant decreasingtrends for PO4, ammonium and Chl a concentrations in the NAd, butnot for nitrate and SiO4 (Solidoro et al., 2009; Mozeti�c et al., 2010).These changes were marked in the 2000s, particularly in the areadirectly affected by Po River discharges. In the more oligotrophiceastern coastal waters the decrement was the lowest, while inter-mediate values were obtained for the Gulf of Trieste, the Gulf ofVenice and the central open waters. Related to this, the concen-tration of surface active organic substances, primarily phyto-plankton exudates and their degradation products, alsoconsiderably decreased in the upper water column during theperiod 2003e2010 compared to 1998e2003 (Ga�sparovi�c, 2012).

Seasonal and multi-year variations of nutrient concentrationsand their stoichiometric ratios were studied in the Gulf of Trieste inthe period 1999e2010 (Lipizer et al., 2011, 2012; Cossarini et al.,2012). The mechanism of seasonal variations, similarly as in theNAd open waters, depended on freshwater discharge, mainly fromthe Isonzo River, triggering phytoplankton blooms, heat exchangewith the atmosphere, ingression of nutrient-depleted waters (EAC),water column stratification, and wind mixing. The ratios betweenorganic carbon, nitrogen and phosphorus, both in the dissolved andparticulate pools (C:N:P), as well as between DIN and PO4 markedlyincreased during events of extremely high freshwater discharges,much richer in N than in P, as well as a consequence of intensephytoplankton blooms. In contrast, increased ingressions of highsalinity EAC and heterotrophic processes reduced the ratios,

although they still exceeded the Redfield values, due to an excess ofC and N in relation to P. Remarkably, anomaly events were absent orless intense in 2003 and 2005e2007, when the freshwater flowrates were lower than usual and the EAC ingression more marked.

Dissolved organic carbon (DOC) accounted for 80e90% of thetotal OC (dissolved and particulate) in the water column. Analysesof multiyear DOC concentration highlighted pronounced seasonalcycle in the NAd, as with winter minima and summer maxima (59e166 mM). Stratification of the water column, circulation and inten-sity and timing of primary production and bacterial C demand arethe main factors causing accumulation of organic matter duringsummer, which was highly variable from year to year (26e75 mM;Pettine et al., 2001; Giani et al., 2005; De Vittor et al., 2008).

Dissolved organic nitrogen (DON) and phosphorus (DOP) are animportant reservoir of these elements in the NAd, accounting for49e99% and 60e100% of the TDN and TDP (Cozzi et al., 2004),Lipizer et al. (2012) on a 12-yr times series in the Gulf of Triestefound the lowest concentration of DIN and the highest concentra-tions of DON (74% of total N) and DOP (76% of total P) together tothe lowest contribution of PO4 (5% of TP) during a period charac-terized by high ingressions of salty waters. Freshwater loads andhigh chlorophyll events were also characterized by increases of Cand N in all pools, whereas an excess of DOC over DON occurredduring the freshets.

The degradation of organic matter along the water column ismediated by enzymes released into the environment by plank-tonic organisms. Significant negative correlations betweenleucine aminopeptidase (AMA) activity and salinity suggested theimportance of river inputs in providing allochthonous organic


matter for microbial metabolism (La Ferla et al., 2002). Markeddecreasing vertical gradients of AMA and alkaline phosphatase(APA) were established in stratified water column. During latespring and summer, prokaryotic and phytoplankton can utilizeDOP producing APA, and, thus, satisfying their seasonal Prequirements (Ivan�ci�c et al., 2009). Autumn and winter mixing inthe water column processes drastically decreased APA in upperwaters, because of dilution and supply of regenerated nutrientsfrom deeper waters. The maximum rates of hydrolysis of AMA, a-and b-glucosidase (a- and b-GLU), b-galactosidase (b-GAL), APAand lipase (LIP) in the Gulf of Trieste in the period 2000e2005varied markedly during the year with winter minima andmaxima from April to October (Celussi and Del Negro, 2012).During summer, APA, LIP and AMA reached their highest activi-ties, while polysaccharide degradation prevailed in spring andautumn during phytoplankton blooms. APA/AMA ratio wasgenerally low, indicating that microbial communities were rarelyP-limited, probably by using organic P sources. A pronouncedyear-to-year variability of degradation patterns was observed, inparticular for AMA and APA. Mixing processes affected, especiallya- and b-GLU activity, possibly as a consequence of resuspensionof organic matter from the seabed. Large-impact phenomena,such as the heat wave in 2003 and mucilage, influenced thedegradation of specific substrates. Mucilage enhanced LIP, APAand AMA whereas their pronounced inhibition was observedduring summer 2003. Celussi and Del Negro (2012) alsohypothesized that prevailing glycolytic activities after 2002 mightbe connected to the ongoing reduction in autotrophic biomass(Mozeti�c et al., 2010), which might have deprived microbialcommunities of monomeric sugars of marine origin duringwinterespring periods.

Preliminary budget estimations showed that exchange rates ofnutrients at the seawateresediment interface are lower than thosedue to water mass exchange with the central Adriatic (Degobbisand Gilmartin, 1990). Remarkably, yearly burial represents animportant loss of TP and SiO4, accounting for 36% and 20% of thetotal loss, respectively, while denitrification in the sediment (42% ofthe total) is almost as important for TN loss as in advectiveexchanges with the central Adriatic. In contrast, regeneration rateand release from the surface sediment appeared to be one order of

Fig. 5. Dissolved oxygen concentrations (c(O2)) in the bottom layers at 5 stations along the pindicates occurrence of hypoxia (c(O2)<1.4 ml L�1). Updated from Djakovac (2006).

magnitude lower than the loss for TN and TP, whereas a muchhigher release was estimated for SiO4. In the western NAd about85% of C, 60% of TP, 40% of TN and 85% of SiO4 settled yearly on thesediment are recycled to the water column (Giordani et al., 1992).Different studies evidenced a marked spatial and seasonal vari-ability of benthic fluxes, although only a few examined interannualvariabilities and were mostly limited to the Gulf of Trieste (Kempet al., 1999 and reference therein). In this region the nutrientsregeneration in the sediment is sufficient to support benthicmicroalgal growth but not the phytoplankton growth (Bertuzziet al., 1996). TP, TN and organic C started to excessively accumu-late in the sediment of the Gulf of Trieste since 1950, as a conse-quence of increasing use in inorganic fertilizers and detergents(Ogrinc and Faganeli, 2006).

4.2. Water oxygenation and hypoxia/anoxia events

The combined effects of high primary production, organicmatter riverine loads, persistent stratification of the water column,and increased bottom water residence time led to a progressiveconsumption of dissolved oxygen (DO) in the bottom layers of largeareas with reduced lateral advection (Degobbis et al., 2000; Tedescoet al., 2007; Solidoro et al., 2009).

Hypoxia (DO < 2 mg L�1, i.e. <1.4 ml L�1) has been oftenconsidered a recurrent feature of NAd and one of the most signif-icant source of environmental risk for its ecosystems. Hypoxicepisodes have been reported especially in the western NAd andclose to the Po River mouth during the 1970s and 1980s (Rinaldiet al., 1992), but the scientific literature describes only few anoxiaevents at the basin scale: 1977 (Degobbis et al., 1979) and 1989 (Ott,1992; Giani et al., 1992; Degobbis et al., 2000). However after 2000,only few cases of dissolved oxygen saturation lower than 20% hasbeen observed (Socal et al., 2008; Solidoro et al., 2009). In fact,a time series of DO along the Po-Rovinj transect (bottom layer,Fig. 5) showed that the frequency of hypoxiawas reduced in the lasttwo decades, and no occurrence of anoxia in the open waters ofNAd (Fig. 5) was detected.

Consumption of DO in bottom layers prevails over productionfrom August (in the western area) to November (in the central andeastern area; Degobbis et al., 2000), until thewater column remains

rofile Rovinj e Po River delta in the period summereautumn 1972e2009. Labeled years

1985 1990 1995 2000 2005 2010Time / year

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1000000

10000000

Phyt

opla

nkto

n /

cell

L-1

0

10

20

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Zoop

lank

ton

biom

ass

(dw

) / m

g m

-3

Fig. 6. Variations during the last decades of mean annual phytoplankton abundances(triangles) and zooplankton biomass - expressed as dry weight (dw, circles) e in theGulf of Trieste. Redrawn from Cabrini et al. (2012) and Mozeti�c et al. (2012), respec-tively. Dotted lines represent the regime shift periods.


stratified. This process wasmore rapid when the Po River flow rateswere high in spring, as, for example, during the period 1972e1978,peaking in 1977, when anoxia developed in November. In theperiod 1988e1991 hypoxia events were more marked than ex-pected from the Po River flow rate, primary production, and P loads(Fig. 5). This was probably due to unusually stable meteorologicalconditions and to consequent delayed mixing of the water columnand reduced water exchange with the central Adriatic.

Measurements in sediment core based on phytoplanktonremains and foraminiferal records at a site near the Po River pro-delta, deposited in the last 100 years, indicated an increasingeutrophication, particularly after the 1930s and first signs of anoxiasince the 1960s (Duijnstee et al., 2004).

A reconstruction over 150 years, carried out in a sediment coreat the same site, based on Dinoflagellate cysts, evidenced a decreaseof the heterotrophic/autotrophic ratio after 1978, concomitant withan increase of near-anoxic or anoxic events (Sangiorgi and Donders,2004). From 1960 to 1978 the dinocysts diversity decreased indi-cating stressful conditions in the NAd.

5. Plankton dynamics

5.1. Viruses, prokaryotes and flagellates

A significant relationship between viruses and prokaryoteswas obtained from data collected in 2001 over the entire AdriaticSea (Corinaldesi et al., 2003), very similar to that found in 1991e1993 by Weinbauer and Suttle (1996), which was interpreted asthe lack of any change in prokaryotic and viruses abundance overthe previous decade. The Authors also observed that viraldistribution was even more significantly related to prokaryoticturnover. Karuza et al. (2012) analyzed a 10-year time series ofboth viruses and prokaryotes (heterotrophic-HP, autotrophiceAP)collected monthly in the Gulf of Trieste. Viral abundances werecomparable to those found by Corinaldesi et al. (2003). Abun-dance of HP ranged from 0.4 to 38$108 L�1, while AP fluctuatedfrom 0.01 to 594$106 L�1. No clear temporal patterns of viralabundance were noticed, while both HP and AP presented a latesummer peak. The only positive significant relationship wasfound between temperature and viruses.

Over the period 1990e2002 Ivan�ci�c et al. (2010) observed alongthe transect RovinjePo River delta (Fig. 1) prokaryotic abundancesin the same order of magnitude reported by Corinaldesi et al.(2003), afterwards (2003e2008) they registered a drasticdecrease and a shift toward biomass production rather than towardreproduction. Significant relationships were found between HP andtemperature and chlorophyll a concentration, respectively. After2003, as a consequence of lower HP biomass, heterotrophic flag-ellates abundance (HF) decreased by about three times. Weakenedcoupling between HP and HF confirmed a minor role of grazingpressure in controlling HP after 2003.

5.2. Microphytoplankton abundance and diversity

Measurements of phytoplankton abundance along the profileRovinjePo River delta (Fig. 1) from 1990 to 2004 evidenced thatintense blooms (over 106 cells L�1) often appeared when thesouthward ICCC was pronounced. Blooms floated up to 30 days,typically in March, or appeared simultaneously in separate gyreswith different species compositions (Kraus and Supi�c, 2011).

Long-term studies on the microphytoplankton communitycomposition identified 344 species in the period 1972e1994(Miokovi�c, 1999). The lowest number of species was observed inthe period 1984e1988, when the eutrophication pressure wasenhanced. The diatom abundance was higher in the period 1989e

1994, when the dinoflagellates abundance was lower. This groupwas more abundant in the mid 1980s. In the period 1989e1994significant changes in the species composition occurred, witha shift to smaller size species. Investigations were extended to theperiod 1972e2009 (Mari�c et al., 2012). Regime shift analysis iden-tified upward shifts in the 1980s and a major downwards shifts in2000 of the total phytoplankton. The abundances of all principalfractions (diatoms, dinoflagellates and nanophytoplankton) weremarkedly lower in the period 2000e2009 than in the period 1972e2009. These changes were related mainly to an increase of salinityand, in a minor measure, to fluctuations of temperature andnutrients, particularly PO4.

The variability of the phytoplankton abundance and composi-tion in the Gulf of Venice during the period 1990e1999 was due tothe influence of several rivers, water exchange with the Lagoon ofVenice, and complex circulation patterns (Bernardi Aubry et al.,2004). The main limiting factors for phytoplankton were light,temperature and strong meteorological events. Nutrients, mainlyPO4 were limiting only in cases of prolonged drought periods. Overthe 10-year study, a decrease in PO4 concentrations was observed,mainly due to substitution of polyphosphate in detergents withother fillers in the late 1980s. The studied area was subdivided intothree zones, characterized by different eutrophication levels. Ineach zone, phytoplankton was similar in terms of communitystructure, although different in abundance. As expected ina nutrient-enriched system, the community was dominated bydiatoms over most of the year. The importance of dinoflagellateswas generally low, with significant abundances only in JuneeJuly.

Bernardi Aubry et al. (2012) did not evidence any significantchange in both phytoplankton abundance and species compositionat two offshore stations between the periods 1999e2001 and2003e2006. They found that the phytoplankton community wascomposed of 372 taxa and was dominated by diatoms, although itonly partially matched the ecological succession previouslydescribed in a more coastal area.

Conversely, in the Gulf of Trieste, on a larger and continuousdata set (1986e2010) Cabrini et al. (2012) found significant changesin both abundance and composition of phytoplankton (Fig. 6). Themajor shift in abundance was detected in 1993e1994 (as alreadypointed out by Fonda Umani et al., 2004 and Kamburska and Fonda-


Umani, 2009) mainly due to a dramatic decrease of phytoflagel-lates. As regard species composition, only few species maintainedthe same seasonality, although in both periods the ecologicalsuccessions resembled the one found in the Gulf of Venice in termof functional guilds. On the contrary, in the eastern part of the Gulfof Trieste, Mozeti�c et al. (2012) found a reduction of phytoplanktondue to the decrease of diatom blooms intensity and to a shift towardsmaller size cells. Over the period 1989e2009 a regime shift in2002e2003 was identified, which encompassed physical, chemicaland biological parameters, and one of the most evident featureswas the increase of nanoplankton fraction. The Authors speculatedthat in the first period (1989e2003) the bottom up control pre-vailed as well as the “classic” food web, while in the second periodwith reduced resources the switch from bottom-up to top-downcontrol can occur seasonally. The striking differences between thetwo coastal sites of the Gulf of Trieste pointed out a more localcontrol of riverine inputs and anthropogenic forcing.

5.3. Micro- and mesozooplankton

Data onmicrozooplankton in the NAd are scarce as evidenced byFonda Umani et al. (2010) who already noted that there wererelevant changes in tintinnid’s community composition betweenthe old surveys (1983e1994) and the more recent ones (1995e2002). In the Gulf of Trieste Monti et al. (2012) over the period1986e2010, observed dramatic changes not of total abundance, butof microzooplankton community composition. Aloricate ciliatesdominated in both periods, but tintinnids drastically decreased,mainly because of the lack of spring peaks, characteristic for theprevious period. Substantial changes in tintinnid compositionwerealso observed with the almost complete disappearance of somespecies and the arrival of some “new entries”.

Comparing three periods (1991e1995, 1999e2001, 2003e2006) Bernardi Aubry et al. (2012) evidenced a clear decrease ofcladoceran abundance in autumn in the Gulf of Venice. Incontrast, small copepods (i.e. Oncaea spp. and Diaxis pygmaea)increased. Nevertheless, the Authors depicted an ecologicalsuccession with a pronounced maximum in summer. Similarchanges of the copepod community, as well as a general increase,were observed over a period of almost 30 years by Kamburskaand Fonda-Umani (2006) and Conversi et al. (2009) in the Gulfof Trieste. The latter Authors observed also significant phenolog-ical changes in most of the dominant copepod species. TheAuthors hypothesized that the observed changes were mostlyrelated to the general increase in the sea surface temperature,which induced a northerly displacement of the “warm” speciesand the large, possibly critical, reduction in the abundance ofa “cold” species (Pseudocalanus elongatus). On the same long termdata set Kamburska and Fonda-Umani (2009) found a relevantshift of mesozooplankton biomass since 2001e2002 in compar-ison with the 1980s. Observed changes of mesozooplanktonbiomass significantly match with shift in copepod abundance,phytoplankton, temperature and NAO index. In the eastern part ofthe Gulf of Trieste Mozeti�c et al. (2012) found as well shift inmesozooplankton biomass (Fig. 6), which only partially over-lapped those found by Kamburska and Fonda-Umani (2009).

Recently, Fuks et al. (2012) described the changes that canoccur in the pelagic food web structure in the NAd by using a 5 yrdata set on nutrients, phytoplankton, bacteria, protozoan andmetazoan. They described the switches in the trophic pyramidalong the water column in the eastern and western part of theNAd in oligotrophic and eutrophic conditions. In the former themicrobial food web prevailed with a heterotrophic/autotrophicratio in the range 1.2e1.7. “Classic” food web on the contrary (H/A ¼ 0.3e0.7) were detected when nutrient inputs enriched the

system. Based on different trophic pyramid structures the Authorshypothesized that metazoan biomass can be supported bybacterial biomass.

The analysis of 10 yr observation of plankton community andbiogeochemical data in the Gulf of Trieste (Cossarini et al., 2012)corroborated the conceptual scheme of ecosystem functioning incoastal area of freshwater influence proposed in Solidoro et al.(2007) and Fonda Umani et al. (2007), in agreement with majorenergy paths within the planktonic food web are fueled along thetraditional food chain during a first phase, in which river nutrientinput sustain large diatom blooms, but through the microbial foodweb and themicrobial loop in a second and third phase, whenmoreoligotrophic conditions are present, and heterotrophic processesprevail on autotrophic ones. These conclusion were definitelyconfirmed by the experimental estimates of carbon fluxes along thepelagic trophic web and the possible export to the bottom for thesame area (Fonda Umani et al., 2012). On the base of 21 grazingexperiments the Authors were able to depict the seasonal evolutionof the system, which was autotrophic in the first part of the yearand became heterotrophic in the second one shifting the H/A ratiofrom 0.12 in winter to 1.17 in summer when all the system wasalmost totally supported by the prokaryotic biomass and produc-tion. In the first part of the year primary production exceededrespiration, whereas in the second one the latter largely exceeded.Respiration was particularly high in all the autumn experimentsprobably because of the refractory nature of DOC, which accumu-late over seasons.

The experimental evidence of the regular alternation of the twotrophic modes, obtained at one sampling coastal site, corroboratesthe findings of Cossarini et al. (2012) on a larger area of the Gulf ofTrieste over an 8-yr period. The Authors evidenced also thedifferences in timing and intensity of the biogeochemical processesamong the three considered areas, suggesting that spatial differ-ences are inherent for a coastal system under the direct influence ofa river, and recommending to use different references term fordifferent sub-areas.

6. Changes in benthic communities

6.1. Microphytobenthos

Very few estimates of microphytobenthos productivity havebeen published. In the Gulf of Trieste, the annual benthic primaryproduction is 36 g C m�2 yr�1 (Bertuzzi et al., 1996). The micro-phytobenthic community did not seem to be photosyntheticallyactive throughout the whole year. From August to December, low/negative microphytobenthic productivity values are originated bya shift from the autotrophic to heterotrophic metabolism of benthicdiatoms that occurs in correspondencewith low photosyntheticallyactive radiation and/or high temperatures at the bottom. Thewarming of seawater, changes of salinity, and covering of theseafloor by episodic high sedimentations due to extreme riverfloods and by the presence of mucilage were also identified asfactors able to modify the benthic diatom associations (Cibic et al.,2012).

Data of benthic photosynthesis measured in the area south of PoDelta (2e23 mmol O2 m�2 d�1) indicated that dissolved oxygenproduced in this compartment is basically consumed within thesediment, as it never exceeds the consumption rates (3e34 mmol O2 m�2 d�1; Epping and Helder, 1997; Moodley et al.,1998). These values correspond to an estimated benthic respira-tion of 54e89 g C m�2 yr�1 equal to 67e90% of the carbon reachingthe seafloor. An estimate of the benthic microalgal gross production(i.e. based on O2 fluxes across sedimentewater interface) has beenperformed by Kemp et al. (1999) for the entire NAd obtaining


a value of 30 g C m�2 y�1. Microphytobenthic primary productionhas been estimated to contribute toz15% of the total production inthe NAd and to 40% in the Gulf of Trieste (Kemp et al., 1999).

6.2. Macrobenthos

High macrofaunal biomass (9e16 g C m�2) and production (11e19 g C m�2 yr�1) characterize the area South of Po Delta, indicatingthe presence of consistent inputs of organic matter from the watercolumn and an intense benthicepelagic coupling (Moodley et al.,1998). However, submerged macrophytes that were dominantprimary producers in shallow-water soft-bottom areas of the NAdhave become much less abundant over the last century. Algalvegetation on the rocky coast in the eastern NAd has also declinedsince the 1970s (Newell and Ott, 1999). The cause of these reduc-tions has been attributed to an increased turbidity of the watersand to the overgrazing by flourishing sea urchin populations (Falaceet al., 2010).

Mass mortalities of benthic macrofauna have been reported inparticular during the 1970s and 1980s, as a consequence ofrepeated events of hypoxia and anoxia. The largest mortalities weredue to the anoxic crisis of 1974, 1977, 1983 and 1989 (Fedra et al.,1976; Stachowitsch, 1984; Ott, 1992; Orel et al., 1993). In the lastdecades no mass mortalities due to hypoxia at regional scale werereported. The deposition of mucilage aggregates causes stress anddamages on benthic organisms (e.g. Stachowitsch et al., 1990;Castelli and Prevedelli, 1992; Devescovi and Ive�sa, 2007), thoughthe concurrence of hypoxic conditions can obscure the role ofmucilage in causing mortalities of benthic organisms.

In the last three decades, a spreading of more than 40 non-indigenous species was also observed in the NAd (Occhipinti-Ambrogi, 2002). It included 14 macrophytes (Orlando-Bonaca,2010 and references therein), as well as 26 animals: among them,only two were non-benthic species. This phenomenon was mainlycaused by shipping/maritime transport, aquaculture activities or bya diffusion through the Suez Canal or Gibraltar Strait (Crocetta,2011). Most of these species are of indo-pacific or Australianorigin. The number of taxonomic units involved in bio-invasions isprobably underestimated and their effects on the local ecosystemsare still poorly known.

Macroepifauna communities are widely distributed in the NAdand largely consist of interspecific high biomass multispeciesclumps (Fedra et al., 1976). Shelly hard substrates provide the basefor sessile, suspension feeding colonizers (mostly sponges, ascidian,anemones or bivalves), which in turn serve as substrate for addi-tional vagile or hemisessile organisms (Riedel et al., 2008). Theclumps of epibenthic organismswhich characterized the area of theGulf of Trieste before the mid 1970s, reaching mean biomasses of370 g m�2 (Fedra et al., 1976), declined after the mass mortality of1983, without a subsequent recover because of a following anoxiccrisis in 1988 and of trawling fishing activity (Kollmann andStachowitsch, 2001). In particular, the trawling fishing has beenshown to cause severe impact on benthic biocenoses also in otherareas of the NAd (Giovanardi et al., 1998).

Changes of benthic macrofauna along the Emilia Romagna coastin 1985 were observed with respect to previous analyses in 1934e36 (Crema et al., 1991). The new biocenoses showed a large abun-dance of Corbula gibba, a species typical of the transition zonebetween detrital and muddy bottoms. This dominance and thegood richness in biodiversity was interpreted as an immature,transitory successional stage due to intermittent recovery afterperiodic disturbances. Analyzing the seasonal variations of mac-robenthic community from 1996 to 2000 in the same area,Occhipinti-Ambrogi et al. (2002) observed a shift in the communitystructure, mainly due to the substitution of C. gibba by Ampelisca,

which was related to an increase of oxygen concentration and ofsand content in the sediments. This shift was further confirmed byobservations carried out from 2004 to 2006 (N’Siala Massambaet al., 2008). The long term decline of the Chamelea gallina clamfishery in the western NAd has been instead attributed to thereduction of riverine nutrients and of primary producers, althoughoverfishing might have played a role (Romanelli et al., 2009).

A 20 yr long study carried out in the eastern NAd showed thatsoft-bottom polychaete declined after the anoxic event of 1989leading the macrobenthic communities to an instability with thedominance of bivalves (Mikac et al., 2011). During the recovery thecontribution of bivalves to the overall diversity and abundancedecreased gradually.

Also on a local scale (e.g. the Bay of Muggia, Gulf of Trieste)a general recover of the macrobenthic community was observed in1994 in respect to 1981, which in turnwas inworst conditions thanin 1975 (Solis-Weiss et al., 2004).

7. Changes in fish communities

The NAd is one of the most productive area of the Mediterra-nean and one of the most relevant fishing ground. Historicalecology studies, suggest that in the NAd fish community structurehas been changing for centuries, even before industrial fishingoccurrence, possibly as a result of artisanal fishing and otheranthropogenic impacts, climatic factors, eutrophication trends(Fortibuoni et al., 2010; Lotze et al., 2011).

Anyway, significant changes in fish community composition andin abundances of many species have been certainly occurringe andaccelerating e during last decades, after the 1950s, as evidencedboth by analysis of fishery independent information and fromlandings statistic (Fortibuoni et al., 2010). In particular, it has beenobserved a decline of elasmobranches (sharks, rays and skates)tuna, swordfish, marine mammals and large demersal, and, moregenerally, of large-sized and late-maturing species proportion infish composition as well as diadromous fish (eel, sturgeon) andsmall pelagics (Grbec et al., 2002; Santojanni et al., 2006; Ferrettiet al., 2008; Coll et al., 2010; Fortibuoni et al., 2010; Lotze et al.,2011; and references therein). Analysis of fishery independentdata collected after the 1980s (Coll et al., 2010) evidences that fishcommunity has not recovered in the last two decades, and actuallya decreasing trend is still going on in total biomass, in the averagetrophic level of fish community and in the demersal/pelagic ratiofor many species, including both demersal, and pelagic ones.Analyses based on catches confirmed that e since mid 1980s e

small pelagic catches were not recovering too (Grbec et al., 2002;Coll et al., 2010).

Changes in fish abundance and community composition mightresult from the superposition of fishing effects, driven by techno-logical evolution and market dynamic, and by environmentaleffects, influenced by anthropogenic and natural stressors. Besidedirect effects, such as fishing mortality or changes in habitat suit-ability, pressures can induce indirect effects, such as the modifi-cation of nursery areas, changes in juvenile survival, potentiallyinduced by changes in phenology and consequent lack ofsynchronization (matchemismatch) between predators require-ments and presence of prey, successful invasion of alien species,evolutionary changes. As an example of direct effect, an increasingtrend of thermophilic taxa, which appear to expand northward, hasbeen reported in the Adriatic Sea (Dul�ci�c et al., 2004; Azzurro et al.,2011 and references therein), concurrently with changes inoceanographic properties. As an example of indirect effect, changesin environmental conditions, and in particular in river discharges,clearly influence the recruitment of anchovy in the northern andcentral Adriatic (Santojanni et al., 2006).

Table 1Major 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, enhancedin 2000s

Zanchettin et al., 2008Evapotranspiration [

Sea level 1971e2002 Venice Lagoon [ Since 1970s Carbognin et al., 20041930e1999 East. NAd (Bakar Bay) Since 1980s Orli�c, 2001

River water discharge 1917e2008 Po River 1975e2008, enhancedsince 2003

Cozzi and Giani, 2011

1980e2008 minor NAd rivers Y Since the 1980s Cozzi et al., 20121989e2009 Rivers in the Gulf of Trieste 2003e2007 Mozeti�c et al, 2012

River loads of N 1973e2007 Po River [ 1970s to 1990s Cozzi and Giani, 20112000e2007 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, 20112000e2007 Rivers in the Gulf of Trieste 2003e2007 Cozzi et al., 2012

River load of Si 1995e2007 Po River Y 2003e2007 Cozzi and Giani, 20112000e2007 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., 20021921e2000 Eastern NAd Supi�c et al., 20041991e2003 Eastern Gulf of Trieste Mala�ci�c et al., 20061985e2005 Western NAd Tedesco et al., 20071972e2009 Open waters of NAd This study

Seawater salinity 1911e1999 Open NAd [ Since 2000 Russo et al., 20021991e2003 Eastern Gulf of Trieste Mala�ci�c et al., 20061976e2006 Open and coastal NAd Solidoro et al., 20091972e2009 Eastern NAd Djakovac et al., 20121989e2009 Eastern Gulf of Trieste Mozeti�c et al., 2012

PO4 in seawater 1972e1995 Open NAd Since 1986 Degobbis et al., 20001976e2006 Open and coastal NAd Y Enhanced since 2000 Solidoro et al., 20091972e2009 Eastern NAd Djakovac et al., 2012

DIN in seawater 1972e1995 Open NAd [ Since 1986 Degobbis et al., 20001972e2009 Eastern NAd Enhanced since 2000 Djakovac et al., 2012

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

Surface active organicmatter (SAS)

1998e2010 Open NAd Y Since 2000 Ga�sparovi�c, 2012

Frequency of markedhypoxia

1972e2009 Open NAd [ Since the 1970s This study

Y Since mid 1990s

Chlorophyll a 1970e2007 Open and coastal NAd Since 2000 Mozeti�c et al., 20101972e2009 Open NAd Y This study1989e2009 Eastern Gulf of Trieste Since 2005 Mozeti�c et al., 2012

Phytoplankton abundance 1972e2009 Eastern NAd Since 2000 Mari�c et al., 20121989e2009 Eastern Gulf of Trieste Y Mozeti�c et al., 20121986e2010 Western Gulf of Trieste Since 1994 Cabrini et al., 2012

Phytoplankton size 1989e2009 Eastern Gulf of Trieste Y Since 2004 Mozeti�c 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, 20091989e2009 Eastern Gulf of Trieste Since 2004 Mozeti�c et al., 20121975e2000 North-Central Adriatic Y Since 1980s Coll et al., 2010

Fish communty averagetrophic level

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

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 AdriaticY

Since 1980s Coll et al., 20101975e2000 North-Central Adriatic Since 1980s Santojanni, 20061950e2000 Central-South Adriatic Since 1970s Grbec et al., 2002

Y Decrease, [ Increase, / Not trend.



8. Summary and conclusions

Long-term ecological studies reported significant modificationsof the environmental conditions in theNAd (Table 1), due to climaticfluctuations and changes of the anthropogenic pressure, as:

- a warming of surface waters at regional scale;- a marked decrease of the freshwater outflow during the 2000s,due to reduction of precipitations, that, together withincreasing frequency of the EAC ingression, caused a rise ofsurface salinity, being more markedly in the western area;

- a decrease of the appearance frequency of ICCC after the 2000,which reduced the water residence time;

- an increased river loads of N coupled to decreased P loads, dueto enforcements of environmental law;

- an increased DIN/PO4 ratio in the waters due to reduction ofriverine TP and to a limitation of N uptake by phytoplankton;

- an acidification of dense waters due to the increase of atmo-spheric CO2;

These environmental changes had relevant consequences forthe ecosystem, which responses were:

- a reduction of the phytoplankton biomass and its surface activeexcretions due to a decrease of TP concentrations, particularlyin the western NAd;

- a reduction in the intensity and frequency of latewinter diatomblooms since 1994;

- a general trend toward small size species, which can explainthe decrease of chlorophyll a concentration;

- a dramatic decrease of tintinnids’ abundance and a significantincrease in the diversity while total microzooplankton did notshow any significant abundance variation;

- a mesozooplankton increase both in number of individuals andin biomass;

- a macrobenthos recovery in areas previously impacted byeutrophication;

- decreasing trend in total biomass of target demersal fishes;- decreasing trend in small pelagic fish (e.g. anchovy) catches;- reduction of the average trophic level of fish community;

On the whole, these changes are indicative of an oligo-trophication process, similarly to what happen in other Europeanseas like the Danish Straits (Carstensen et al., 2006), the Scheldtestuary (Soetaert et al., 2006), the northwestern Black Sea(McQuatter-Gollop et al., 2009). This oligotrophication processcoupled with overfishing could severely impact different level ofthe trophic web.

It is extremely difficult to forecast the interplay of humanactivities and climatic factors. The ongoing warming trend,including an increasingly frequency of extreme events, couldenhance the stratification and, together with reductions in thewater exchange, increase the turnover time of the NAd waters. Inthese conditions, the sensitivity of the NAd ecosystem to eutro-phication and acidification processes would enhance, notwith-standing the ongoing oligotrophication. Moreover the increasingtemperature in shallow water can significantly accelerate thedegradation of organic matter and, consequently the oxygenconsumption, as well as the plankton and benthos communitystructures.

The eutrophication trend which occurred in the XX centurysustained an increased fish productivity which partially balancedthe effect of the significant increase in fishing effort, up to partiallymasking first evidences of overfishing. However, changes in fishcommunity structure did occur, possibly decreasing the ecosystem

efficiency and resilience. The reversal in the eutrophication trend,and the consequent reduction in plankton productivity, altered thisbalance, possibly increasing the risk of collapse of fisheries andincreasing the probability of occurrence of major changes inecosystem structure and functioning. The increasingly frequentoutbreaks of jellyfishes (Kogov�sek et al., 2010), the endangermentof key-stone species, the replacement of top predator species, thedecrease in small pelagic catches are examples of such changes.Also the fact that the demersal/pelagic ratio has not beenincreasing, despite the reductions in the eutrophication processesand in the frequency of hypoxia events might be seen as a symptomof the lack of resilience of the system.

Nonetheless, the evident effort of the scientific communityover the last decades to include in the long term ecologicalstudies also the microbial compartment, many parametersfundamental to describe the functioning of the ecosystems in theNAd, as primary production, respiration, temporal variation of thesedimentewater fluxes are still undersampled both spatially andtemporally.

Acknowledgments

The compilation of this paper was supported by the PerseusFP7-OCEAN-2011-287600 Project, the MEDSEA FP7-ENV-2010-265103 Project, and the Croatian Ministry of Science project0982705-2731. The data to update the long time series were kindlyprovided by CMR Rovinj and ARAP Emilia Romagna (Po River flow).

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