3.2. Sediment Transport and Modern Sedimentation
3.2.1. Historic Changes in River Deltas and Sediment Supplies
The deltaic complex of Gallikos, Axios, Loudias and Aliakmonas is a prominent feature along the northern coast of TG (
Figure 1b). Sediment and freshwater inflows have changed significantly during the last century due to direct and indirect human interventions. Axios river had two mouths that were periodically active: the presently active mouth at Cape Kavoura (current delta) and the now abandoned Palaiomana mouth, located around 15 km to the NE (22.86
oE, 40.59
oN;
Figure 1b). The active mouth was at Cape Kavoura prior to 1900, after which the main flow shifted to Palaiomana, which remained as the active mouth until the artificial diversion of the flow back to the main tributary (outflowing to Cape Kavoura) in 1934, with discharges from the abandoned Palaiomana mouth thereafter only during floods (Kapsimalis et al., 2005). This diversion was part of a major reclamation project in the deltaic plain (1925-1933), during which the routes of Axios, Aliakmonas, Gallikos and Loudias were rearranged, and artificial banks were constructed along their straightened (after the works) distributary channels (Poulos et al., 1994).
Historical data indicate significant accretion in the deltaic zone of Axios and Aliakmonas during the 20th century, with net gains of 175 km2 and 139 km2 between 1850 and 1987 (Poulos et al., 1994). Kapsimalis et al. (2005) identified three main phases in the deltaic system evolution since 1850: a) natural evolution between 1850 and 1916, with the system delivering a net sediment supply of 130·106 m3 to the TG; b) accretive phase from 1916 to 1956, during which the artificial realignment of the main river channels, and drainage and reclamation projects in the coastal plain, increased the sediment outflow to 900·106 m3 (28·106 t/yr) and led to coastal progradation at the active mouths of Axios and Aliakmonas; and c) erosional phase after 1956 (1956-2000), due to human-induced (dam construction) reduction of sediment supplies (by 2.5·106 m3/yr or 4·106 t/yr), leading to coastline retreat at the deltas. Coastal erosion was tackled locally with hard coastal protection measures (1960-1974), like the construction of a 22 km long and 2.5 m high seawall along the abandoned Palaiomana mouth of Axios, equipped with five pumping stations to drain the agricultural plain (Kapsimalis et al., 2005). The limitation of freshwater and sediment discharge has led to erosion of the protected deltas and shoreline retreat in more recent years. Petropoulos et al. (2015) estimated losses of 1.26 km2 in Axios and 0.63 km2 in Aliakmonas between 1984 and 2009, while the observed subsidence rate in the deltaic plane since the 1960s is around 10 cm/yr (Kapsimalis et al., 2005; Poulos et al., 1994). Considering that these areas are low-lying, the risk of intensification of the coastal retreat and flooding under rising sea level in the future is very high and could entail severe environmental and socioeconomical impacts (Androulidakis et al., 2023b). Regarding Pinios river, numerous paleochannels can be identified across the flood-plain of the delta, with two major former river mouths north of the presently active (since 1955) mouth, and two more south from it (Karymbalis et al., 2016). Recent coastline changes shift from progradation around the presently active mouth to erosion over the coastal stretch of around 10 km (around 50% of the deltaic coastline) along the abandoned river mouths, with rates that range from +7.5 m/yr to -3.5 m/yr between 1955 and 2013 (Karymbalis et al., 2016).
The present-day morphometric characteristics of the deltas indicate the dominance of fluvial processes in the north (Axios and Aliakmonas) and wave dominance in the south (Pinios) (Poulos et al., 1993). Axios, Aliakmonas and Pinios provide the bulk of freshwater and fine sediment discharge in the gulf, while Loudias River has a sporadic contribution (Karageorgis and Anagnostou, 2003; Kombiadou and Krestenitis, 2012). While historic data estimate the average total riverine sediment influx to Thermaikos at 3-5·106 t/y (Lykousis and Chronis, 1989; Poulos et al., 2000), by the end of the 20th century the total supply of suspended solids by the rivers had decreased to around 0.63·106 t/y (10.7% from Axios, 1.1% from Aliakmonas, 1.0% from Loudias and 87.2% from Pinios; Karageorgis and Anagnostou, 2003).
3.2.2. Seasonal Patterns of Suspended Sediments
Riverine sediments entering the TG marine environment comprise very fine silt to clay, with mean diameters between 2 and 4 μm (Kourafalou et al., 2004). Due to the low settling rates, riverine sediments show high suspension times in the domain, often confined above the pycnocline and near the surface due to the stratification of the water column (Karageorgis and Anagnostou, 2003; Kombiadou and Krestenitis, 2012). Elevated suspended Particulate Matter Concentrations (PMCs) near the bed are attributed to associated current activity, either inhibiting settling or causing resuspension (Poulos et al., 2000).
The distribution of suspended PMCs over the TG was investigated by various oceanographic campaigns. Among these, campaigns that covered the entire Central and Outer TG, extending southwards until the Sporades basin, were conducted in the framework of projects EURECOMARGE (1 survey: June 1987; Durrieu de Madron et al., 1992), Metro-Med (4 surveys: May 1997, Jul. 1997, Feb. 1998 and Sep. 1998; Karageorgis and Anagnostou 2001; 2003) and INTERPOL (3 surveys: Sep. 2001, Oct. 2001 and Feb. 2002; Zervakis et al., 2005). More recent, monthly monitoring campaigns (Thermaikos 2004, 2006; Tsompanoglou et al., 2017), were restricted to the Inner and Central TG. Satellite imagery have also been used to sense suspended PMCs in the surface waters, using Landsat (Karageorgis et al., 2000; Balopoulos et al 1986) and MERIS (Monachou et al., 2014; Alexandridis et al, 2015). The main conclusions of these studies regarding seasonal patterns of suspended particulate matter in the area are discussed in unison below.
Elevated PMCs are often concentrated near the surface and the seabed, forming Surface and Bottom Nepheloid Layers (SNL and BNL, respectively). The seasonal patterns of SNL formation in the gulf are mainly controlled by suspended sediment influx, stratification and surface circulation, while the BNL structure is due to resuspension of loosely consolidated sediments by near-bottom currents (Karageorgis and Anagnostou, 2003). PMCs are typically lower in the rest of the column, with less pronounced, or even absent, Intermediate Nepheloid Layers (INLs). Overall, under non-stratified conditions, INLs follow the distribution and magnitude of the SNL under non-stratified conditions, while under stratified conditions PMCs of INLs are significantly reduced. Winter conditions, with high influx of solids by the rivers and strong haloclines, are typically characterised by well-defined SNLs (PMCs>0.5 mg/l) that extend southwards from the Central TG and the deltaic zone in the north, along the western coast of the Outer TG (
Figure 7a), driven by the predominant cyclonic circulation (
Figure 6a). INLs, when present, show lower PMC maxima and are confined closer to the north and west coasts. BNLs during this period (
Figure 7b) can be extensive, with high suspended PMCs (>0.5 mg/l) covering most of the Outer TG, apart from its eastern part along the coast of Chalkidiki peninsula. Higher PMCs (>1 mg/l) within the BNL can be found throughout the west coastal stretch and locally elevated concentrations can also be present near the river deltas. Extraordinary dynamics and transport conditions near the bed, like density currents, can influence the BNL structure. Such conditions might be observed during winter when dense water masses can be formed in the Inner TG and slowly travel toward the Aegean Sea (
Figure 6a; see
Section 3.1.3), altering the BNL structure in its wake (Estournel et al., 2005; Tragou et al., 2005). This has been observed in the field, with a peak in PMC of the winter BNL offshore the Pinios mouth (measured in February 2002) linked to a DWF event that had taken place 2 weeks prior (Zervakis et al., 2005). Spring conditions can be associated with a very prominent SNL, with elevated maximum PMCs near all river mouths (3-7 mg/l), as well as throughout the Central TG and along the western coasts and the Inner TG (>1 mg/l; dashed lines in
Figure 7a). A reversal of the surface circulation near the southwestern part of the Outer TG can observed due the occasional shift of the Sporades eddy from predominantly cyclonic in winter to anticyclonic in other seasons (Kontoyiannis et al., 2003; Kourafalou and Tsiaras, 2007), which can lead to northward expansion of the Pinios SNL plume. High PMCs (>0.5 mg/l) in the spring BNL can cover the entire domain, with even higher concentrations (>1 mg/l) along the western half of the Outer TG (dashed lines in
Figure 7b). Suspended PMCs are reduced during summer, due to reduced influx by the rivers; under southerly winds the sediment can be confined to the north and transported toward the Inner TG, with high PMCs (>1 mg/l) in the SNL northwest from Cape Megalo Emvolo (
Figure 7c) and with very low values in the rest of the domain. The BNL can be more pronounced, with high PMCs (>1 mg/l) over the western part of the shelf and near the river mouths, as well as the Inner TG (
Figure 7d). Autumn conditions (dashed lines in
Figure 7c) are mostly characterized by higher outflows than summer and cyclonic circulation, leading to a more typical SNL formation in the domain, with higher PMCs (0.5-1 mg/l) along the river outflows in the north and with the sediment-laden plumes extending southwards along the west coast. Autumn surveys show that the BNL can often extend eastwards from the river mouths, with high PMCs (>1 mg/l) throughout the entire Central TG and extending along the east coast well south from Cape Epanomi (dashed lines in
Figure 7d).
3.2.3. Near-Bed Processes and Sedimentation Patterns
TG acts as a sediment trap, with the bulk of the riverine sediment (~90%) depositing within the bounds of the domain (Kombiadou and Krestenitis, 2012; Lykousis and Chronis, 1989). Sedimentation in the deltaic zone of TG has been associated with seaward dispersion of the river outflow and settling of the suspended material, dominated by differential settling near the river mouth and by flocculation further offshore (Poulos et al., 1996). Sediment cores indicate that fine-grained sediments are frequently resuspended on the Thermaikos shelf, by natural (storm) or anthropogenic (intense trawling activities) forcing, while there is no evidence of erosion of the bed (Karageorgis et al., 2005a; Zervakis et al., 2005). Numerical modeling and oceanographic observations indicate that nearshore currents are not able to resuspend sediment (Poulos et al., 1994), while wave-induced resuspension can be an important factor over low depths near the coast (Paphitis and Collins, 2005). The trawling activity taking place in the area has been shown to contribute to the BNL concentrations in the Outer TG (Tragou et al., 2005; Zervakis et al., 2005). In fact, trawling was estimated to increase BNL concentrations over the shelf by 2 to 3 times (Price et al., 2005). Similarly, using numerical modeling, Kombiadou and Krestenitis (2011) estimated that the sediment entering suspension due to trawling over the trawling season can supersede the annual influx by the rivers. Resuspended particles are removed rapidly from the system by sinking and/or horizontal advective processes (Muir et al., 2005). Overall, mechanically eroded sediment moves in the vicinity of the bed (3-6 m), contributing to the BNLs in the area, and resettle onto the bed shortly after (1-5 days; Kombiadou and Krestenitis, 2011).
Surface sediments over the Inner TG and the western half of the shelf (Central and Outer TG) comprise muds and sandy muds that transition to muddy sands in the eastern part of the shelf (Lykousis et al., 1981; Lykousis and Chronis, 1989; Poulos et al., 2000). Sedimentation over the western shelf is dominated by the riverine water and sediment outflows, while sand fraction is high (>50%) over the eastern shelf, with values that reach 60-85% along a relatively narrow band along the eastern shoreline of the Outer TG (Poulos et al., 2000). These coarser sediments are interpreted as relict sands that remain uncovered (or partly mixed) by modern sedimentation, due to the predominant cyclonic transport (Karageorgis and Anagnostou, 2001). Sedimentation rates near the river mouths were measured at 8.8 mm/yr for Axios and 1.8 mm/yr for (Karageorgis et al., 2005a). Corresponding modeled values are 18, 7 and 3 mm/yr near the mouths of Aliakmonas, Axios and Pinios, respectively (Kombiadou and Krestenitis, 2012). The same study indicated the following sedimentation patterns: Axios is the main sediment supplier for the Inner TG; Axios and Aliakmonas contribute equally to the Central TG, with the sediments from the former showing higher dispersal in the domain and sediment from the latter depositing mainly southwards along the western coastline; matter from Pinios settles along the west coast of the Outer TG, with a higher sediment accumulation north from the delta.
3.3. Marine Pollution and Biogeochemical Properties
TG is influenced by human activities (sewage and industrial discharges, agricultural runoff, shipping, airborne litter, hydrocarbon refueling, and harbour operations) while the five large rivers discharge substantial loads of nutrients, heavy metals and other compounds, after drainage resulting from human activities within their watersheds. Axios River has been recognized as the major supplier of suspended particulate matter even during the dry summer season (Tsompanoglou et al., 2017; see
Section 3.2) and a source of heavy metals to the coastal environment of the gulf (Karageorgis et al., 2003). The influence of the rivers, the Thessaloniki metropolitan area, and the diverse sedimentological background contribute to the formation of a spatially varying and patchy distribution of major and minor elements in the surface sediments of TG. In Thessaloniki Bay and Central Gulf of Thessaloniki, the geochemical characteristics of the sediments are substantially influenced by the domestic and industrial effluents that were released partly treated for several decades resulting in high levels of organic carbon and contaminant elements (Cu, Zn, As and Pb).
3.3.1. Heavy Metals
Metal enrichment is mainly detected in the northernmost part of the TG (Inner TG), and to a lesser extent close to the river mouths; then, the heavy-metal content gradually decreases towards the open sea (Karageorgis et al., 2005b). Several other studies have also reported increased concentrations of heavy metals in sediments adjacent to the rivers, the industrial zone, the port of Thessaloniki and the sewage outfall of the Wastewater Treatment Plant (WTP) (
Figure 1a; e.g. Vasilikiotis et al., 1982; Fytianos and Vasilikiotis, 1983; Voutsinou-Taliadouri and Satsmadjis, 1983; Voutsinou-Taliadouri and Varnavas, 1995; Zabetoglou et al., 2002; Christophoridis et al., 2009; Violintzis et al., 2009; Kapsimalis et al., 2010; Christophoridis et al., 2019).
The sediments in the western part of the TG’s continental shelf are dominated by major and minor elements of terrigenous origin that are transported by the rivers, reflecting the lithology of their catchment areas where abundant metal-rich formations, mainly ophiolites, are present. In addition, Axios river carries suspended matter enriched in metals, due to mining and industrial activities in the upper catchment, while the Aliakmonas and the Pinios rivers have no significant industrial activity in their drainage basins. The geochemical signature of each river is identified by the supply of certain heavy metals: a) Zn and Pb for the Axios river, b) Cr, Co, Ni, Cu and As for the Aliakmonas river, and c) V, Co, Ni and Cu for the Pinios river. In the central and eastern parts of the shelf, the presence of relict sands (see
Section 3.2.3) controls the sediments’ geochemistry causing a substantial dilution of heavy metals concentration (Karageorgis et al., 2005b).
The pollution status of marine sediments in the coastal area of Thessaloniki Bay (
Figure 1b) was evaluated by employing enrichment factors and comparing with sediment quality guidelines (Violintzis et al., 2009; Christophoridis et al., 2009; 2019). For Zn, Cu, Pb, As and Ag significant contribution from human-related sources was found, particularly in the inner part of the Bay (Violintzis et al., 2009). The sediments from the area near the Thessaloniki port exhibited the highest impact of anthropogenic heavy metals, revealing the cumulative effect of anthropogenic load from the industrial and shipping activities operating for many decades in the area (Christophoridis et al., 2019). Most heavy metal concentrations were found at levels that could adversely affect marine biota, while sites at the inner part of the Bay could be considered of medium-low and medium-high priority in terms of toxicity potential (Violintzis et al., 2009).
The dissolved fraction of heavy metals in TG’s water column corresponds to 33% up to 90% of the total metal load. The ratio of dissolved trace metal concentrations in the Inner TG, based on data collected from 1995 to 2003, showed three-fold enrichment in Cd, Cu and Ni compared to the north Aegean, for Pb the enrichment was seven times higher, whereas for Mn the ratio was less than 1 (Dassenakis et al., 2005). Zeri and Hatzianestis (2005) measured the dissolved Cu and Ni and reported that the maximum concentrations of both metals were encountered in front of the Axios and Aliakmonas rivers deltas. Stronger binding of both Cu and Ni with organic ligands of terrestrial origin was also observed than with those of marine origin, underlining the important role of riverine dissolved organic matter in metal complexation at least during winter. Data on dissolved trace metals (Cd, Co, Cu, Hg, Ni, Pb, Zn), collected from 2012 to 2019 in the framework of the national monitoring for the implementation of the European Union Water Framework Directive (WFD), have shown no systematic metal enrichment. However, the adjacent estuaries and lagoons at TG were classified as above background concentration water bodies for several metals, indicating that metal contamination is localized within these areas and does not extend extensively across the broader expanse of the gulf (Tzempelikou et al., 2021).
The mineralogical composition of particulate matter has been found to be fairly homogeneous over the Inner TG, consisting of clay minerals, quartz, plagioclase, K-feldspar and calcite. The geochemical analyses of the PMC showed the predominance of Al, Si, Fe, Ti, K, V, Mg, and Ba indicating their terrigenous origin i.e. aluminosilicate detrital material. The increased Al concentration at the surface suggested that river inputs constitute the main source of Al in the study area. Si and Ca are of terrigenous origin but also originate from autochthonous biogenic fraction (Tsompanoglou et al., 2017). Fe is predominantly held in the structure of aluminosilicate minerals, while Mn is mainly controlled by the resuspension of the surficial sediments, by redox recycling, as a result of organic matter degradation and biogeochemical processes (Price et al., 2005). The increased concentrations of particulate Co, Ni and Cr are attributed to riverine inputs produced from the weathering of the mafic and ultramafic rocks in the drainage basin of Axios and Aliakmon watersheds. Enhanced Cu and Zn concentrations in Thessaloniki Bay and the southwestern part of the Central Gulf of Thessaloniki (
Figure 1b) imply that a portion of the two trace metals, derived from partially treated domestic and industrial effluents (Tsompanoglou et al., 2017). Similarly, Pb and Cd were attributed to anthropogenic sources, derived from the rivers and the city of Thessaloniki (Price et al., 2005).
3.3.2. Organic Pollutants
Pesticides, Polychlorinated Biphenyls (PCBs) and hydrocarbons are among the organic pollutants commonly found in the marine environment, entering the sea both indirectly and directly through a range of diffuse and point sources including sewage and industrial discharges, agricultural and urban runoff, ship transportation and dry deposition from the atmosphere.
Agricultural activities in the river catchment areas seem to be the source of various pesticides like the herbicide Triazine Atrazine (ATR) and its Transformation Products (TPs) and the organochlorine insecticides like DDT and its metabolites, lindane and dieldrin. The major organochlorine pesticides identified in surface sediments collected in 1995 at Inner TG were p,p'-DDT and its metabolites p,p'-DDE and p,p'-DDD, while the rest of the organochlorine compounds, namely lindane and dieldrin were found at quite low concentration levels (Hatzianestis et al., 2000; 2001). These results confirm the findings of previous relevant studies (Fytianos et al., 1985; Larsen and Fytianos, 1989). The maximum value of ΣDDTs (sum of concentrations of DDT, DDE and DDD) was found inside the Thessaloniki port, while high levels of ΣDDTs were also measured close to the WTP sewage outfall and near the city of Thessaloniki. Moreover, the ratio DDE/DDT was consistently higher than one, suggesting the absence of “fresh” DDT inputs in the gulf. The vertical distribution of ΣDDTs concentrations in a sediment core showed the highest value 30 cm down-core, probably attributed to the banning of DDT use in Greece since 1972 and corroborating the absence of new DDT inputs in Inner TG (Hatzianestis et al., 2000; 2001). Despite the ATR ban within the European Union in 2004, ATR and its TPs were still detected in seawater and sediments of TG collected during sampling campaigns in 2010 and 2011 (Nödler et al., 2013), although at relatively lower concentrations than in the period before the ban of ATR use (Albanis et al., 1992; Readman et al., 1993). However, the detection frequency of the compound was 100%, probably due to leaching from agricultural soils where significant amounts were applied in the past and its slow degradation in the marine ecosystem. In parallel, terbuthylazine, which is an active substance replacing ATR, was detected at rather low concentrations except for one exceptionally high concentration that was observed in the western part of Thessaloniki Bay close to the estuary of Gallikos river (Nödler et al., 2013).
The occurrence of phenolic compounds (nitro- and chlorophenols) in the seawater was studied along the western coastline of the Outer TG for one year (October 2003-September 2004). Considering the dominant activities in the wider area, urban, industrial, and agricultural sources, as well as natural loading, are the main contributors to the presence of these compounds. The detected concentrations were higher than the levels set by the European Union for bathing waters, particularly for pentachlorophenol and 2,4-dichlorophenol, but do not appear to pose a threat to the aquatic environment of the area (Dimou et al., 2006). Arditsoglou and Voutsa (2012) also conducted a study to determine the presence of phenolic and steroid Endocrine-Disrupting Compounds (EDCs), in all elements of the marine environment of Inner and Central TG (seawater, suspended particulate matter, sediments, mussels), based on findings of previous studies that showed the presence of EDCs in inland waters (rivers and streams), sewage effluents and industrial wastewaters discharged into the gulf (Pothitou and Voutsa, 2008; Arditsoglou and Voutsa, 2010). Phenolic compounds were detected in all samples, with nonylphenol and its ethoxylates being the dominant pollutants. Nonylphenol occurred in sediments in relatively high concentrations, posing a significant risk to biota, while mussels exhibited low bioconcentration factors for nonylphenol and octylphenol.
Organophosphate Esters (OPEs), a group of chemical compounds used as additives into plastic materials/products, were determined in samples originating from the coastal area of the Inner TG, as well as from rivers and streams outflowing into the Gulf during 2019-2020. OPEs were ubiquitous in the aquatic environment, with higher concentration levels in streams. Alkyl-OPEs were the dominant group of the dissolved fraction, contributing in more than 50% in all samples from rivers and seawater, followed by Aryl-OPEs and Chlorinated-OPEs. Risk assessment did not show a potential threat due to OPEs to aquatic species although certain streams exhibited relatively higher risk (Pantelaki and Voutsa, 2021).
Hatzianestis et al. (2000; 2001) using the same sediment samples analyzed for DDT and its metabolites, conducted a parallel study to determine seven PCB congeners. The sum of the concentrations of the seven PCB congeners (ΣPCBs) presented a spatial distribution similar to that found for DDTs with maximum ΣPCBs values in the vicinity of the city of Thessaloniki. The congener distributions were generally dominated by hexachloro- and heptachloro-substituted compounds, as in the commercial products Arochlor and Clophen. Interestingly, the less volatile heptachloro-substituted compounds were present at very low levels or even absent in the more distant stations, indicating that are more easily removed from the atmosphere and are partitioned close to the pollution sources.
The same sediment samples were also analyzed to determine hydrocarbons (Hatzianestis et al., 2000; 2001). In surface sediments, the aliphatic hydrocarbon composition was dominated by petroleum-related constituents and according to the observed concentration levels the Inner TG can be characterized as moderately polluted with petroleum compounds. The evaluation of the gas chromatograms of the aliphatic hydrocarbons indicated the widespread presence of important petroleum-related residues in sediments with a distinctive decreasing trend offshore (Hatzianestis et al., 2000). Polycyclic Aromatic Hydrocarbons (PAH) were also determined in the upper 60 cm of one core. PAH concentrations in the sediment core were relatively low, however the proportion of petrogenic PAH (compounds found mainly in petroleum) over the other fractions was increasing in the deeper parts of the core, implying a long-lasting petroleum contamination history in the area (Hatzianestis et al., 2001).
The concentrations of different organic contaminants (i.e. PAHs, PCBs, organochlorine pesticides and polybrominated diphenylethers) were measured at three sites of Inner and Central TG not only in surface seawater but also in the air in summer (July) 2012 (Lammel et al., 2015). The results showed that the concentrations of PAHs, PCBs and some organochlorine pesticides (hexachlorocyclohexane-HCHs and DDT and its degradation products) in surface seawater were by a factor of 2–10 higher than in the Cretan sea (Southern Aegean). Furthermore, the spatial variation of seawater pollution across the three sites was remarkable with the highest PAHs levels recorded at a residential coastal site (Michaniona), the highest levels of organochlorine pesticides measured at Loudias River estuary implying influence from agricultural activities, whereas the highest levels of PCBs and polybrominated diphenylethers were recorded off-shore possibly indicating a shift of contaminant partitioning from particle-bound to dissolved, corresponding to a negative gradient of suspended particulate matter concentration, or influence from shipping activities.
3.3.3. Nutrient Pressures
TG is one of the most disturbed Hellenic coastal areas regarding anthropogenic nutrient enrichment (Pagou, 2005). Environmental pressures of human origin, from urban, agricultural, industrial, commercial, marine and aquaculture activities, have led to increased nutrient concentrations in the water column of TG that exhibit significant seasonal and annual variations (e.g., Samanidou et al. 1987; Balopoulos and Friligos, 1994; Pavlidou, 2012; Zachioti et al., 2022). More specifically the Inner and Central TG receives domestic, stormwater, agricultural and industrial effluents, not only through the four rivers and their tributaries, but also from the treated wastewater discharges and the sewerage network overflows of the Thessaloniki metropolitan area. Large volumes of domestic and industrial wastewater have been directed for decades to the TG and especially to the northernmost part, Thessaloniki Bay promoting the occurrence of eutrophication conditions (e.g., Friligos and Koussouris, 1984; Friligos et al., 1997). From 1992 and on, Level I wastewater treatment was applied, while since 2001, Level II wastewater treatment is implemented (Krestenitis et al., 2012), with a 92% performance degree, in order to reduce the contribution of urban effluents to eutrophication events (e.g., Moncheva et al., 2001; see
Section 3.4).
In general, the nutrients distribution shows significant spatial variability, with high concentrations of nutrients (e.g., nitrates, phosphates, nitrites, ammonia) near the west coastline of the Inner TG, in the proximity of the river estuaries and the aquacultures, as well as in Thessaloniki Bay (port and sewage outfall area) (Pavlidou et al., 2005; Pagou, 2005). A timeseries (1995-2007) analysis of nutrients data from Thessaloniki Bay and the area near the Axios river delta showed that nutrient concentrations were generally lower in Thessaloniki Bay than those near the river estuary, except for ammonia during the period 1995-2000 (Zachioti et al., 2022). The seasonal variability of nutrient concentrations is controlled by several factors acting synergistically, such as the seasonality of the quantity and quality of both the treated and untreated wastewater effluents, the fluctuation of the flow rate of the main rivers discharging into the study area and the mesoscale and sub-mesoscale ocean circulation in conjunction with the prevailing meteorological conditions (Androulidakis et al., 2021). This latter study has shown that localized-scale ocean dynamics may reduce the renewal of the Gulf with clear waters of Aegean origin (see
Section 3.2) or induce advection of the nutrient-rich waters from the rivers to the northern part of the Gulf enhancing the eutrophic characteristics of the Gulf (see
Section 3.4).
Among the rivers, Axios is the most polluted in terms of nutrient concentrations characterized by a clear seasonal signal of high flow rate in spring and low in late summer, contrary to Aliakmonas river, where the existence of dams along its waterway determines the temporal variability of the outflow with high to maximum discharge in summer due to the peak of hydropower production (Skoulikidis, 2009). In view of these differences, Aliakmon shows an increase in nitrate concentration with discharge, indicating the prevalence of agricultural land flashing, while Axios shows a nitrate decrease with discharge, indicating the prevalence of dilution processes (Skoulikidis, 2009). Regarding long-term nutrient variation, Axios presents an increase in nitrate concentration during the 1980s that can be attributed to agricultural intensification. After a subsequent decrease, nitrate concentration increased again to reach the multi-year maximum in 1997–98 and since then gradually diminished (Skoulikidis, 2009; Tsiaras et al., 2014). On the other hand, in Axios, phosphate concentration remained particularly high and slightly increased until 2000 due to increased inputs from industrial and urban waste point sources in the Former Yugoslavian Republic of Macedonia (North Macedonia now) which includes almost 80% of the river’s drainage basin (Karageorgis et al., 2005c; Skoulikidis, 2009; Tsiaras et al., 2014). Accordingly, phosphate loads are unbalanced in relation to nitrate loads resulting to decreased values of N:P ratios, lower than the theoretical Redfield stoichiometry (N:P = 16:1), implying a possible nitrogen deficiency, in the coastal river-influenced environment.
Analysis of nutrients data time-series (1995-2002) in the Inner TG (including Thessaloniki Bay), has revealed that nitrate, nitrite, and ammonium concentrations showed a statistically non-significant decrease, nitrate showed a statistically non-significant increase, phosphate did not follow any trend, whereas ammonium showed a statistically significant (pvalue<0.05) decrease. This has resulted in a decrease in the N:P ratio which may cause indirect effects of eutrophication, like the blooming of certain harmful dinoflagellate species (Pagou et al., 2003; Pagou, 2005; Pavlidou, 2012). The above results were confirmed by Zachioti et al. (2022) who found that the N:P ratio was constantly below 10, highlighting the strong N-limitation in the inner part of the Gulf, also demonstrated in other previous studies (e.g. Nikolaidis et al., 2006; Pavlidou, 2012; Pavlidou et al., 2015; Simboura et al., 2016). However, based on weekly nutrient measurements in Thessaloniki Bay during March 2017 - February 2018, the mean inorganic nutrient ratios were 25.1 for N:P, 0.70 for Si:N and 18.4 for Si:P. The average N:P ratio in 2017-2018 was much higher (mean 25) compared to the N:P ratio (6.40) of the period 1995–2007 (Pavlidou, 2012). The high N:P ratio in combination with the extreme NH4 concentrations measured during 2017-2018, may be linked to the relatively high contribution of dinoflagellates, such as Noctiluca scintillans and Spatulodinium pseudonoctiluca, to plankton community biomass and increased red tides (Genitsaris et al. 2019). Similarly, the N:P ratio was high (19.5) during the years 2020 -2022 (Kourkoutmani et al., 2023) indicating nitrogen pollution.
3.3.4. Other Biogeochemical Characteristics
Particulate organic matter (POM) in TG is a mixture of terrigenous organic material, autochthonous biomass derived from planktonic and benthic organisms and inputs from anthropogenic activities. In the period from June 2004 to June 2005, the highest particulate organic carbon (POC) concentrations were recorded at the surface of Thessaloniki Bay and Central Gulf of Thessaloniki, during spring-early summer linked to the development and decline of the spring phytoplankton bloom (see
Section 3.4.2). The distribution of particulate nitrogen and phosphorus was similar to that of POC (Tsompanoglou et al., 2017). Furthermore, POC and the nitrogen content of the particles were significantly correlated and the C:N ratio of the POM ranged between 5 and 12, with high values systematically observed over the river deltas and in Thessaloniki Bay and Central Gulf of Thessaloniki. C:N ratios > 7 that have been calculated at different depth layers suggest that carbonaceous compounds were selectively accumulated in bulk POM resulting in carbon enrichment. Nevertheless, the C:N ratio was close to the theoretical stoichiometric analogy of marine plankton (C:N = 106:16 = 6.6) implying that autochthonous biomass is the main component of particulate organic matter. In another study conducted from April 2000 to May 2001 (Strogyloudi et al., 2023), low ratios of POC:chl-a were recorded in the mussel-farms area close to the rivers estuaries the high participation of chl-a to POC that was also supported by the strong positive correlation between total chl-a and POC in the Inner TG’s stations. In addition, a short-term deployment of sediment traps in the spring of 2003 showed that the proportion of phytoplankton carbon in the POC vertical flux was up to 45% (Zervoudaki et al., 2014).
Inner TG characterized by high loads of organic and mineral particles, as well as inorganic nitrogen compounds, provided ideal conditions either for the production of nitrous oxide (N2O) by nitrification and denitrification, or the production of methane (CH4) by methanogenesis that consequently may be released to the atmosphere (Marty et al., 2001 and references therein). Thus the concentrations of the two greenhouse gases and the bacterial processes involved in their production (nitrification and denitrification for N2O, and methanogenesis for CH4), were determined in surface waters in April 1998. High concentrations of both gases were recorded in the surface waters of the Inner TG. However, no direct relationship was found between the concentration and the production of the biogases, as they may also be produced in deep water or bottom sediment in shallow areas or derived from anthropogenic activity or ship contamination in polluted areas. Whatever their origin, the presence of extremely high concentrations of these two greenhouse gases in surface seawater suggests that Inner TG could act as a significant source of atmospheric N2O and CH4 (Marty et al., 2001).
In a study performed during May 1997 data of the CO2-carbonate system of the Inner TG was obtained for the first time (Krasakopoulou et al., 2006). Surface concentrations of total Dissolved Inorganic Carbon (DIC) were lower than those recorded close to the bottom. The positive relatively good correlation between DIC and both the Apparent Oxygen Utilisation (AOU) and phosphate at the last sampling depth confirmed the regenerative origin of a large proportion of DIC. The decomposition of the organic material, imported directly from external sources (rivers, sewage) and produced in situ in the Gulf, increased the concentration of dissolved inorganic carbon, particularly in the bottom layer. The correlations between surface fugacity of CO2 (fCO2), calculated from the total alkalinity (AT) and DIC measurements, and chl-a as well as AOU revealed that the carbon dioxide fixation through biological activity was the principal factor modulating the variability of fCO2. A rough first estimate of the magnitude and direction of the air-sea CO2 exchange showed that in May 1997, the Inner TG acted as a weak sink for atmospheric CO2 at a rate between -0.60 and -1.43 mmolm-2d-1, depending on which formula for the gas transfer velocity was used, and in accordance to recent reports regarding other temperate continental shelves.
3.4. Biological Elements of the Water Column - Plankton
Plankton - named from the Greek “πλαγκτόν”, meaning to “wander“- is a vital component of the marine environment. Bacterioplankton comprising the highest abundance of pelagic biota, has key roles in global processes, influencing ecosystem structure and functioning as well as biogeochemical cycles. Marine phytoplankton contributes approximately 50% of global primary production plays a crucial role in removing CO2 from the elevated atmospheric levels via carbon pumping to the deep sea. Protozooplankton is highly important for carbon and energy transfer in the microbial loop and plankton food web. Metazoan zooplankton is an important component of the pelagic food web, contributing to many ecosystem functions, such as the transfer of primary production to higher organisms.
3.4.1. Bacterioplankton
Although the view on ecology of marine plankton has changed remarkably since the 1980’s (Azam et al., 1983, Fenchel, 1988) recognizing the significant role of bacteria in plankton food-webs (microbial loop), there is a lack of publications on bacterioplankton structure and dynamics in the TG. The first relevant work in the Inner TG (Mihalatou and Moustaka-Gouni, 2002) indicated high numbers of bacteria (from 0.9 to 6.8·106 cells mL-1), reaching maximums in May, within the water layer between 50% and 20% of the incident Photosynthetic Active Radiation (PAR). This bacterial maximum coincided with high primary productivity (13.0 mg C m-3h-1) indicating strong trophic coupling of bacterioplankton and phytoplankton. Another work, recently published by Genitsaris et al. (2023), aimed at the response of bacterioplankton communities from the Inner and the Outer TG to PAHs’ exposure under experimental conditions (mesocosms). No negative effects of the contaminants were apparent in the experiments and net growth rates of both bacterioplankton communities were always positive. The bacterioplankton community composition was also examined for the first time. High Operational Taxonomic Unit (OTU) numbers were observed in both communities. In total, 841 and 693 OTUs were retrieved from the Inner and Outer TG, respectively. A high functional-response diversity of PAHs degrading OTUs reflected a high potential for acute mitigation responses of bacteria in TG. The Outer TG contained bacterioplankton communities with higher resistance sustaining bottom-up ecosystem stability.
3.4.2. Phytoplankton
Several studies on phytoplankton in the TG have been carried out, although long timeseries are lacking. The existing studies provide important information on phytoplankton composition, abundance and biomass, seasonal and spatial distributions, molecular diversity, and Harmful Algal Blooms (HABs). The earlier studies on phytoplankton have focused on composition, abundance and biomass. Diatoms and dinoflagellates were the richest groups in morphospecies of the diverse phytoplankton community of the Inner TG (Nikolaides and Moustaka-Gouni, 1990). The phytoplankton seasonal succession was dominated by Leptocylindrus, Chaetoceros, Skeletonema, Pseudo-nitzschia, Thalassiosira, Cylindrotheca, Cerataulina (diatoms) and Gymnodinium, Prorocentrum, Scrippsiella, Gonyaulax, Heterocapsa (dinoflagellates) species forming phytoplankton biomass peaks up to 6.7 mgL
-1. Focusing on spatial phytoplankton distribution in the entire TG, Gotsis-Skretas and Friligos (1990) showed a spatial variation of phytoplankton along the pollution gradient with maximal total abundance of 7,600 cells mL
-1. Most of the dominant phytoplankters of the Inner TG, mentioned above, also dominate the phytoplankton communities of the broader TG. New findings from works spanning the entire Aegean Sea (including TG), indicate that circulation patterns leading to broad-scale compartmentalization, might also have an important impact on the diversity and composition of phytoplankton assemblages in the coastal system of Thermaikos (Spatharis et al., 2019). Androulidakis et al. (2021) indicated that the phytoplankton species of the different habitat communities of the Inner, Central and Outer TG were highly connected via circulation (see
Section 3.1), while the largest species pool, including nutrient opportunists, was recorded in the phytoplanktonic community of a station located closest to the river deltas (see
Section 3.3).
Genitsaris et al. (2020), based on an eDNA analysis, showed that the temporal scale rather than the small-spatial scale, was the main signal for shaping phytoplankton assemblages in the Inner TG. This metabarcoding analysis has detected phytoplankton groups frequently observed in the Inner TG, dominated by diatoms and dinoflagellates. The most abundant molecular species were Chaetoceros tenuissimus, Chaetoceros cf. wighamii, Skeletonema pseudocostatum, Thalassiosira sp., (diatoms), Scrippsiella trochoidea, Gonyaulax fragilis, Alexandrium margaelefii (dinoflagellates), the cryptophyte Teleaulax sp., the pico-chlorophyte Micromonas pusilla and the haptophyte Haptolina sp. Dominant OTUs were closely related to species known to form harmful blooms and mucilage aggregates, together with rare taxa having potential negative impacts on human health not detectable with traditional microscopy. Among the potentially harmful species of the TG’s phytoplankton (Genitsaris et al., 2019), Dinophysis species was found responsible for mussel intoxication in aquaculture areas (Koukaras and Nikolaidis, 2004; Varkitzi et al., 2013). Dinophysis bloom occurrence had been documented several decades ago (Athanassopoulos, 1931; Gotsis-Skretas and Friligos, 1990; Nikolaides and Moustaka-Gouni, 1990; Nikolaidis and Evagelopoulos, 1997). Cysts of potentially toxic dinoflagellate species, such as Alexandrium cf. tamarense, A. cf. affine, A. cf. minutum, as well as Gymnodinium catenatum, were detected in the sediment of the Central and Outer TG (Giannakourou et al., 2005).
Comprehensive long-term studies on red tides and algal blooms are scarce. The first study that examined the seasonal shift and described the responsible phytoplankton for the formation of these phenomena in the Inner, Central and Outer TG was conducted by Petala et al. (2018). By applying traditional microscopy, they divided Thermaikos into two subregions based on phytoplankton abundance and, hence, the eutrophic status. The study estimated significantly higher abundance in the Inner and Central TG compared to the Outer TG. Algal bloom and red tides formation (
Figure 8) by several mucilaginous diatoms (i.e. Chaetoceros sp., Cylindrotheca closterium etc.) and dinoflagellates (i.e. Gonyaulax fragilis) including the heterotrophic dinoflagellate Noctiluca scintillans (
Figure 9) and its relative Spatulodinium pseudonoctiluca were observed. Furthermore, the study found considerably lower plankton abundance in the Outer TG, demonstrating its oligotrophic state. A thorough study documenting the weekly phytoplankton species succession and identifying the responsible taxa for the formation of phytoplankton blooms and red tides at the urban marine environment of the Inner TG was conducted by Genitsaris et al. (2019). The study classified this subregion of Thermaikos as heavily eutrophic, indicating persistent phytoplankton blooms that were dominated by known mucilaginous species such as C. closterium, Chaetoceros spp., Leptocylindrus spp. and Skeletonema costatum (
Figure 9). The accumulation of the organic mucilaginous material from the successive algal blooms and red tides resulted in the formation of an excessive mucilage aggregate phenomenon in June and July 2017 (
Figure 8), extending from the Inner to the Outer TG (Genitsaris et al., 2019), attributed to the same mucilage-producing diatoms, together with the mucilaginous haptophyte Phaeocystis sp. and the dinoflagellate G. fragilis.
The trophic conditions of TG were assessed using the multiparametric Eutrophication index (E.I.; Primpas et al., 2010) by some studies. Based on nutrients and chlorophyll-a (chl-a) data of the period 1995-2007 an improvement in the trophic status of Thessaloniki bay and of the area near the Axios river estuary was observed. The trophic status of both areas which was classified as “Poor” till 2000, was improved and classified as “Moderate” in 2007 (Zachioti et al., 2022). In addition, data collected in five samplings during 2012–2014 for the implementation of the WFD showed that the “Moderate” trophic status of the two areas is maintained (Pavlidou et al., 2015).
Figure 8.
Eutrophication events in Thermaikos Gulf (TG) in July 2017 (Photo courtesy: Eurokinissi.gr), February 2017 (Photo courtesy: Thes.gr), March 2017, and December 2017. The plankton species associate with the red tide events in March and December 2017 are also shown.
Figure 8.
Eutrophication events in Thermaikos Gulf (TG) in July 2017 (Photo courtesy: Eurokinissi.gr), February 2017 (Photo courtesy: Thes.gr), March 2017, and December 2017. The plankton species associate with the red tide events in March and December 2017 are also shown.
Several studies in the prism of monitoring activities in the framework of the implementation of WFD 2000/60/EC (WFD) and Marine Strategy Framework Directive 2008/56/EU (MSFD), evaluated the Inner TG, and particularly the Thessaloniki Bay, with “Moderate” or “Poor” status (Pavlidou et al., 2012; 2015; Simboura et al., 2016). Recently, a study on eutrophication assessment of TG capitalized on current advances in remote sensing, and employed satellite image analysis in order to evaluate the spatial distribution of chl-a levels (Androulidakis et al. 2021). In order to have more accurate evaluation of chl-a levels, the authors combined microscopy with satellite ocean color image analysis and attempted to associate the chl-a with the “actual” plankton biomass during eutrophication events in the TG. It was found that chl-a concentrations evaluated using satellite imagery correlated well with phytoplankton biomass, measured with the time consuming microscopy, revealing similar patterns. Thus, they concluded that by coupling the two methods it is possible to determine the extent, as well as the responsible taxa, for the formation of these eutrophication phenomena. For instance, they found that during an annual cycle, chl-a peaked at 45 mgm
-3 in December 2017 (
Figure 8) under the prevalence of southerly winds (weak renewal;
Section 3.1), when an extensive red tide caused by the photosynthetic ciliate Mesodinium rubrum expanded throughout the Inner and Central TG (Androulidakis et al., 2021). On the contrary, low chl-a levels were detected during periods with northerly winds that enhanced the renewal of the enclosed basins.
Figure 9.
Micrographs of common planktonic organisms of TG as seen by microscopy. Epifluorescence micrographs were taken by UV excitation for (A) DAPI-fluorescence cells or by green excitation (B) and blue excitation for (C) Chl-a red auto-fluorescence. Light - phase contrast (D, E, F, G) micrographs. (A) Heterotrophic bacteria. (B) Pico- cyanobacteria. (C) Pico-chlorophytes. (D) The diatoms Chaetoceros sp. and Leptocyllindrus sp. along with the dinoflagellate Ceratium cf. horridum. (E) The red-tide forming ciliate Mesodinium rubrum. (F) The bloom forming dinoflagellate Karenia with other plankton species. (G) Cells of the red-tide forming heterotrophic dinoflagellate Noctiluca scintillans along with the pelagic tunicate Oikopleura dioica. Scale bars in μm.
Figure 9.
Micrographs of common planktonic organisms of TG as seen by microscopy. Epifluorescence micrographs were taken by UV excitation for (A) DAPI-fluorescence cells or by green excitation (B) and blue excitation for (C) Chl-a red auto-fluorescence. Light - phase contrast (D, E, F, G) micrographs. (A) Heterotrophic bacteria. (B) Pico- cyanobacteria. (C) Pico-chlorophytes. (D) The diatoms Chaetoceros sp. and Leptocyllindrus sp. along with the dinoflagellate Ceratium cf. horridum. (E) The red-tide forming ciliate Mesodinium rubrum. (F) The bloom forming dinoflagellate Karenia with other plankton species. (G) Cells of the red-tide forming heterotrophic dinoflagellate Noctiluca scintillans along with the pelagic tunicate Oikopleura dioica. Scale bars in μm.
3.4.3. Protozooplankton
Protozooplankton community is underappreciated in plankton studies in the TG. The early study by Mihalatou and Moustaka-Gouni (2002) focused on protozooplankton components (heterotrophic nanoflagellates, heterotrophic dinoflagellates and ciliates) as grazers of bacteria. The ciliate M. rubrum as member of protozooplankton was assigned to the photosynthetic functional category, supported by organelle robbery. Several heterotrophic dinoflagellates (e.g., species of the genera Protoperidinium, Gyrodinium) even the red-tide forming omnivorous feeder N. scintillans, have been considered members of phytoplankton community in earlier plankton studies (Nikolaides and Moustaka-Gouni, 1990; Gotsis-Skretas and Friligos, 1990). Investigating the underexplored diversity of marine unicellular eukaryotes, Genitsaris et al. (2020) identified phytoplankton heterotrophic unicellular eukaryotes frequently observed in TG. In addition, they also revealed protozooplankton taxonomic groups previously undetected in the area (MALVs, MAST and Cercozoa). The protozooplankton community showed temporal patterns rather than small-scale spatial separation responding to the variability of physical and chemical environmental factors. The specific functional characterization of protozooplankton, that had previously been taxonomically characterized by 18S rRNA gene amplicon sequencing, showed a diverse range of trophic preference of picograzers, nanograzers, micrograzers, phagotrophs, decomposers and parasites (Genitsaris et al., 2020).
3.4.4. Metazooplankton
The metazooplankton community of TG is also poorly known resulting to lack of data on trophic interactions occurring in the pelagic food web and the resource efficiency of zooplankton in relation to phytoplankton richness and harmful blooms. An early study on zooplankton (Siokou-Frangou and Papathanasiou, 1991) indicated that the spatial-temporal variability in the Gulf is highly affected by riverine water inflow, pollution and ocean circulation. Copepods and cladocerans were the most abundant groups, with high numbers of copepods in the Inner TG. The dominant species were Acartia clausi followed by Oithona nana and Podon polyphernoides. In the Central TG, dominant species were Acartia clausi followed by Paracalanus parvus and Penilia avirostris. Appendicularians were well represented, in terms of species richness and number of individuals, in the Outer and Central TG. Another early study on metazooplankton focused on the annual cycle of neritic cladocera (Alvanou, 1999). The distribution of mesozooplankton resting eggs was studied in the sediments of TG and indicated higher abundance of eggs at locations close to the river mouths, with water column rich in zooplankters (Siokou-Frangou et al., 2005). Recent research on metazooplankton reported the presence of the non-indigenous calanoid copepod Pseudodiaptomus marinus (Kourkoutmani and Michaloudi, 2022). One of the very few studies dealing with marine rotifers across the Mediterranean Sea investigates the temporal distribution patterns of four coexisting Synchaeta species in the Inner TG. This work contributed to our understanding of the dynamics of this group of micrometazoans, previously underestimated among marine zooplankton, given that rotifers are lost when using larger mesh size nets in sampling (Kourkoutmani et al., 2023).
3.4.5. Planktonic Response to Climate Change and Pollutants
During the last decade, Inner TG unicellular plankton community has been used in mesocosm experiments to explore the species response to multiple variables of climate change (Stefanidou et al., 2018a), and phytoplankton response to pollutants discharged in the seawater from exhaust gas cleaning systems on ships, known as scrubbers (Genitsaris et al., 2023). In regard to the climate change variables, the impacts of elevated temperature (see
Section 4.2) in the form of an intense heat shock, together with changes in salinity, were examined on the natural phytoplankton community of TG and demonstrated adverse effects on species diversity, resource use efficiency and productivity (Stefanidou et al., 2018a). The lower productivity and resource use function after the heat shock and the changes in salinity were supported by the lower inferred activity of the major phytoplankton taxonomic groups, as evidenced by the lower ratio of rRNA sequences to rDNA sequences (rRNA : rDNA) under these circumstances (Stefanidou et al., 2018b), which has been used as a proxy of metabolic activity in the literature. The major outcome of these studies was the synergistic negative effects on phytoplankton community caused by the elevated temperature and increased salinity, which was also confirmed by measurements of physical properties by Androulidakis et al. (2023). Taking into consideration that climate change is associated with concurrent shifts in several variables, besides temperature and salinity, in the marine environment, it could also lead to more intensified and complex effects on primary producers; this may modify the energy flow and consequently the biogeochemical cycles, therefore impacting ecosystem functioning. The potential impacts of scrubber effluents, containing several chemical compounds such as PAHs and metals, and particularly vanadium and nickel, was examined in mesocosms using natural phytoplankton communities of the Inner and Outer TG. Adverse effects were observed only under high, 10% (v/v) dilutions of scrubber effluent exposure while no adverse effects were observed in communities exposed at 1% dilutions. Effluent discharge at 50 m along the ships’ wake is diluted 2000 times for vessels with established open-loop scrubbers sailing in open sea (Genitsaris et al., 2023).
3.5. Benthic Fauna: Diversity, Ecological Quality and Environmental State
Despite the significance of zoobenthos in the assessment of the environmental status of marine ecosystems through biodiversity and food web descriptors, few studies have been conducted, so far, in TG (see
Section 2). Relevant attempts are almost exclusively limited to the research efforts of the Marine and Terrestrial Animal Diversity (LMTAD) and Ichthyology laboratories of the Biological Department of the Aristotle University of Thessaloniki (AUTh), the Laboratory of Environmental Chemistry and Ecology of the Department of Environmental Engineering of the International Hellenic University (IHU), and the field studies of the Hellenic Centre of Marine Research (HCMR). More specifically, the first research effort about benthic fauna of Thermaikos Gulf was about the diversity of extant mollusks (Sakellariou, 1957). Quite a few years later, in the 1970s, the first scientific research program devoted to the benthic bionomy of the north Aegean Sea and funded by the United Nations Environment Programme/Mediterranean Action Plan (UNEP/MAP) has been carried out by AUTh.
3.5.1. Benthic Communities
The seabed of TG is dominated by various soft substrata types, which are locally covered by seagrass meadows of the species Posidonia oceanica and Cymodocea nodosa (Haritonidis et al., 1990; Panayotidis et al., 2022). In the unvegetated sedimentary bottom, muddy sands constitute the predominate type (Poulos et al., 2000). The proportion of sand increases eastward and to shallower depth, whereas the amount of silt and clay balance in deeper waters and along the western coast, which is influenced by the transitional waters and terrigenous inputs of the Axios-Loudias-Aliakmonas deltaic system. Based on the European Nature Information System (EUNIS) typology (2022) of natural habitats
4, 20 types of benthic communities occur in TG, exhibiting a large variety of different facies, according to prevailing fauna (
Appendix B). In many cases, the structure of the zoobenthos diverges from the typical one described in EUNIS, and this may be due to either the transitional stage of the studied communities, being under high pressure from various anthropogenic factors influencing the area, or the fact that the description was based on data derived from the western Mediterranean. In very shallow (around 3 m depth) waters, a narrow rocky platform exists, which together with the various artificial constructions (i.e., docks, marinas, aquaculture facilities, etc.) along the gulf represent the hard substrata type of the seabed. The hard substrata is covered by periwinkles, limpets and barnacles in the supralittoral and mediolittoral zone, respectively (Kitsos, 2003), whereas in the sublittoral zone four different facies of the photophilic algae community develop, depending on prevailing environmental factors (Chintiroglou et al., 2004; Antoniadou and Chintiroglou, 2009; Antoniadou et al., 2011; Ganias et al., 2023).
Seven out of the 20 biocenoses found in natural habitats of TG are considered as threatened at the European level, according to the International Union for Conservation of Nature (IUCN) Red list assessment (EUNIS, 2022). More specifically, the photophilic algae community, the Cymodocea nodosa meadows on muddy sands in sheltered waters, and the littoral muddy sands and muds in lagoons and estuaries are assessed as Endangered (EN) in European waters. The Posidonia oceanica meadows, the sublittoral muddy detritic bottoms, the euryhaline/eurythermal muddy estuaries and the mediolittoral sands as Vulnerable (VU), whereas the lower mediolittoral rock and the infralittoral mixed sediments are classified as near Threatened (NT). Apart from the above habitats that demand specific management plans to improve their conservation status, two facies of the stony coral Cladocora caespitosa on rocky and mixed sediments, and one facies of the sea pen Crassophyllum thessalonicae should also be considered as threatened, since both species are assessed as endangered according to the regional assessment of Mediterranean anthozoans (Otero et al., 2017).
3.5.2. Benthic Diversity and Species of Community Interest
Overall, 1,368 benthic invertebrate species have been reported from the faunistic studies that have been carried out in TG since the 1957, with the vast majority belonging to the phylum Mollusca (57%). Annelida (18%) and Arthropoda (16%) are the next most speciose phyla (
Figure 10). At the class or order level, Gastropoda prevail, followed by Polychaeta, Bivalvia, Peracarida, Eucarida, Demospongiae and Anthozoa (
Figure 11). This increased diversity of the benthic invertebrate fauna emerges from the relevant diversity in habitat types (see
Section 3.5.1) and to the extensive taxonomic studies focusing in particular to the phylum Mollusca (Manousis et al., 2010; 2012; Manousis and Galinou-Mitsoudi, 2014; 2022). Among the reported invertebrate species, some are commercially exploited, such as the clams Venus verrucosa, Callista chione, the scallops Pecten jacobaeus and Flexopecten spp., the prawns Penaus kerathurus, Parapenaeus longirostris, the mud and mantis shrimps Upogebia tipica and Squilla mantis, the crabs Callinectes sapidus and Maja squinado, and the sea-cucumbers Holothuria tubulosa and H. poli (Damianidis et al., 2016; Kevrekidis and Thesslaou-Legaki, 2011; Kevrekidis and Antoniadou, 2018; Vafidis and Antoniadou, 2023), raising concerns on the future viability of natural stocks and habitats.
Other species, however, face direct threats as the endangered corals Crassophyllum thessalonicae (
Figure 12a) and Cladocora caespitosa (
Figure 12b) and the critically endangered fan mussel Pinna nobilis (
Figure 12c). The soft coral C. thessalonicae, originally described in by Vafidis and Koukouras (1991), lives exclusively in TG, where it forms sparse populations (0.5 to 4 colonies/20 km) on the silty sediments of the Central TG. The species habitat is heavily disturbed by bottom trawling, urbanization, and pollution (Otero et al., 2017). There are no active protection measures, so far, for the sea pen, whose population remains out of the established Special Areas of Conservation (SACs) of TG. The pillow coral C. caespitosa forms moderately dense populations on coarse sedimentary and rocky habitats, especially along the eastern coast of the gulf (Ganias et al., 2023). Climate change and fisheries mainly threaten the species (Otero et al., 2017), whereas in areas influenced by sewage treatment plants, siltation constitute an additional threat, as the polyps of the colonies are buried within the silty sediment. Cladocora caespitosa is an ecosystem-engineering species due to the provision of biogenic habitat that constitutes an important biodiversity reservoir (Antoniadou et al., 2023). Although there are no specific conservation measures for the species, a part of its population in Thermaikos is protected within the SAC GR1220005. Thermaikos Gulf hosted the denser population of the fan-mussel P. nobilis in the Greek Seas (Vafidis et al., 2014) with densities reaching 1.04 individuals/m2 (Galinou-Mitsoudi et al., 2006). Unfortunately, the species have been affected by haplosporidia parasites and mycobecteria that caused Mass Mortality Events (MMEs) that totally devastated the population (Zotou et al., 2020). Until nowadays, only dead eroded shells heavily colonized by epiphytes and sessile invertebrates (
Figure 12c) may be found in TG, including the designated SACs in the region.
3.5.3. Ecological Quality Based on Benthic State
According to European Union directives, MSFD and WFD, the monitoring of coastal and transitional marine waters is mainly assessed through biological quality elements under an integrative approach that uses physicochemical data as supporting variables. Among the four proposed biological quality elements (i.e. Phytoplankton, Phytobenthos, Zoobenthos, and Fish), the zoobenthos, which includes all animal organisms living in the benthic zone, is the most promising tool to develop appropriate indices to assess the ecological quality status and the seabed integrity. This is due to their widespread and abound presence in both species’ richness and number of individuals within marine habitats, also to the rather limited natural variability in the synthesis of their biotic communities, and lastly to their fundamental life traits. They are relatively long-lived, sessile or discretely motile organisms that do not perform large-scale migrations, and accordingly, their synthesis reflects the cumulative environmental conditions over time in a specific site. Moreover, the different species have different tolerance limits and are able to respond to various stress factors, such as eutrophication, organic pollution, mechanic disturbance of substrata, and heavy metal load. They also play a main role to food webs, nutrient cycling and energy flow in benthic-pelagic coupling. Several biotic indices have been developed to assess the ecological quality of marine waters based on benthic invertebrates, in full compliance with the WFD. Among the various proposed indices, the BENTIX index originally developed by Simboura and Zenetos (2002) has been successfully inter-calibrated between European countries to be used over Mediterranean coastal waters and the M-AMBI index (Borja et al., 2004; Muxica et al., 2007) for transitional waters (Simboura and Reizopoulou 2008).
The National Monitoring Water Network (NMWN
5) estimates the ecological quality of coastal and transitional waters in TG by analyzing the synthesis of benthic macroinvertebrates and applying the BENTIX and M-AMBI indices, respectively. The operational program has been, so far, implemented along three periods: an initial reference period (2000-2008), a first (2012-2014) and a second (2018-2022) implementation period. According to relevant reports, the ecological quality in the Inner and Central TG has been assessed as moderate in the reference and the first implementation period and improved to good in the second one (YPEKA, 2012; 2017; 2023). In the Outer TG, the ecological quality state -originally assigned as good (YPEKA, 2012)- has degraded to moderate (YPEKA 2017; 2023); however, the latest assessment has not been based on biological samplings, but to an extrapolation of the previous evaluation. Considering the transitional waters, the state has been steadily assessed as moderate (YPEKA, 2017; 2023).
Based on the few studies that have applied the BENTIX index in TG (Antoniadou et al., 2004; Antoniadou and Chintiroglou, 2005; Chintiroglou et al., 2006; 2007; Simboura and Reizopoulou, 2007; Antoniadou and Chintiroglou 2009; Simboura et al., 2014; HCMR, 2015; AUTh 2018a; 2018b; 2019; 2020a; 2020b; 2023), the ecological quality state alternates from moderate to good according to the specific geographic area and the sampling period, revealing increased spatiotemporal variability in ecological quality status. A spatial trend of decreased state in the Inner TG together with an improved state in the Outer TG emerges, whereas in the Central TG, the eastern shores appears in better state that the western ones, which are influenced by the estuarine systems of Axios-Loudias-Aliakmonas. Seasonal assessment in three sampling stations in the Inner and the Central TG during the period 2017-2020 (AUTh, 2018a; 2018b; 2019; 2020a) revealed a gradual improvement in the quality of the western shores but a deterioration in the eastern ones, where ecological quality state shifted from moderate to good and vice-versa, respectively. In the transitional waters of Thermaikos all relevant studies report moderate quality in Loudias and Aliakmonas estuarine systems (AUTh, 2020b; 2023) and good quality along the western coasts of the Outer TG (AUTh, 2023).