water Article Phytoplankton–Macrophyte Interaction in the Lagoon of Venice (Northern Adriatic Sea, Italy) Fabrizio Bernardi Aubry *, Francesco Acri, Gian Marco Scarpa and Federica Braga National Research Council—Institute of Marine Sciences (CNR—ISMAR), Arsenale Tesa 104, Castello 2737/F, 30122 Venice, Italy; [email protected] (F.A.); [email protected] (G.M.S.); [email protected] (F.B.) * Correspondence: [email protected] Received: 7 August 2020; Accepted: 7 October 2020; Published: 10 October 2020 Abstract: The coexistence of phytoplankton and macrophytes in the Lagoon of Venice (Northern Adriatic Sea, Italy) was investigated using in situ data collected monthly as part of International Long Term Ecosystem Research (LTER), together with satellite imagery for the period 1998–2017. The concentrations of chlorophyll a and hydrochemical parameters were measured in three areas of the lagoon, where the expansion of well-developed stands of submerged vegetation was observed by remote sensing. Our results suggest interaction between phytoplankton and macrophytes (macroalgae and seagrasses) in the last few years of the time series, evidenced by decreasing chlorophyll a concentrations in the vicinity of the macrophyte stands. The integration of LTER and remotely sensed data made it possible to evaluate the interaction of macrophytes and phytoplankton at the ecosystem scale for the first time in the Lagoon of Venice. Keywords: phytoplankton and macrophytes; water quality; multiannual variation; International Long Term Ecosystem Research (LTER); remote sensing; Lagoon of Venice 1. Introduction Coastal lagoons are characterized by strong spatial heterogeneity, widely fluctuating hydrological variables and seasonal patterns [1–3]. In these ecosystems, the pronounced heterogeneity of the habitat and the shallow waters allow the development of a range of trophic conditions. This, in turn, gives rise to a very diverse community of primary producers on multiple functional levels, such as macroalgae, marine phanerogams, benthic microalgae and phytoplankton. Macrophytes (macroalgae and seagrasses) respond univocally to environmental stressors in aquatic environments and thus represent sensitive indicators of water quality and the ecological status of transitional waters [4–6]. They play a key role in primary production, regulating the nutrient cycles and contributing to water oxygenation [7]. Water clarity tends to be enhanced by submerged vegetation, because it prevents sediment resuspension and erosive processes [8], and, by attenuating current and wave energy, it also traps suspended particles. On the other hand, the distribution of submerged vegetation is controlled by light availability [9,10]. In very turbid waters, light cannot penetrate to the bottom, leading to a decline in macrophyte growth and distribution, while phytoplankton become the only primary producers [6]. In transitional waters, light attenuation can be due to both natural and human-driven processes such as (i) the physical characteristics of the area (water depth, sea-floor properties, tidal currents, freshwater run-off and associated sediment delivery from the drainage basin and wind- and wave-driven sediment resuspension), (ii) human activities (increased nutrient and sediment loading from runoff and sewage disposal leading to eutrophication and algal blooms, ship and boat wakes, fishing and clam harvesting, dredging and coastal engineering works), and (iii) regional weather patterns (e.g., extreme storms and altered rainfall patterns) [10–12]. These factors play a crucial Water 2020, 12, 2810; doi:10.3390/w12102810 www.mdpi.com/journal/water Water 2020, 12, 2810 2 of 22 regulating role in the competition between macrophytes and phytoplankton for light and nutrients, and their interaction is difficult to unravel in practice, also considering the positive water clarity feedback of the development of aquatic submerged vegetation. At the regional scale, both changes in temperature and precipitation may influence aquatic ecosystems and are expected to have consequences for the competition between submerged macrophytes and phytoplankton, but, as different effects may counteract each other, the overall result is difficult to predict [13]. Macrophytes and phytoplankton, together with macrobenthic and fish fauna, represent Biological Quality Elements (BQEs) in the Water Framework Directive (WFD 2000/60/EC). The quali-quantitative assessment of BQEs and their alternation or coexistence is necessary for gauging the overall state of water bodies and the long-term changes affecting them [14–16], and it is also useful in the design of future studies in conjunction with various types of impact assessment. In the last fifty years, several changes have been observed in the composition of primary producers in the Lagoon of Venice (LoV). Since 1960, the seagrass meadows (Zostera, Cymodocea), which originally covered the whole lagoon, have almost completely disappeared [17,18], while until 1990, much of the lagoon was extraordinarily covered in monospecific meadows of Ulva rigida C. Ag., with standing crops of up to 550,000 tons in wet weight, overall net primary production exceeding 1.5 million tonnes and gross primary production 5–6 times higher [19]. After 1990, Ulva receded [20] owing to a combination of climate conditions [21] and lower nutrient inputs [22]. The lowest values were observed 2 in the late 1990s, with mean macroalgal biomasses of 0.27, 0.18 and 0.66 kg fwt m− in the northern, central and southern areas of the lagoon, respectively [23]. However, other studies have demonstrated that in recent years, seagrass beds have increased again, covering several areas of the lagoon close to the three inlets [18,24]. Facca and co-workers [23] reported average seagrass biomasses of 0.63 2 and 1.99 kg fwt m− , respectively, in the central and southern basin of the LoV. As for microalgae, the period from 1970 to the late 1990s saw frequent phytoplankton blooms, mainly in the central and 1 northern basins [19,25–29]. In 1984, a massive Cryptomonas sp. bloom (chlorophyll a > 500 µg L− ) and 1 a Peridinium foliaceum bloom (chlorophyll a > 150 µg L− ) were observed [30]. Since the start of the century, there has been a decrease in the number of blooms and, more generally, in phytoplankton biomass in lagoon waters [29]. The last 20 years (1998–2017) have seen a general improvement in the ecological condition of the LoV: water transparency has increased due to several factors including declining river discharge [31], a reduction in clam harvesting and the resurgence of macroalgae and seagrasses [32]. Furthermore, mean relative oxygen has increased considerably, while concentrations of ammonia and nitrates have decreased significantly [31]. Concentrations of chlorophyll a have decreased significantly due to lower nitrogen inputs, as well as the competition for nutrients between phytoplankton and the macrophytes (macroalgae and seagrasses) that have recently recolonized the lagoon [31]. Satellite remote sensing can complement in situ sampling by providing useful information and tools to support the long-term analysis of ecological patterns and environmental changes in aquatic ecosystems. Specifically, remotely sensed data have been used extensively for mapping the extent and spatial distribution of submerged aquatic vegetation in lacustrine and coastal environments. Recent reviews of the various methods for assessing bottom cover types in tropical and temperate latitudes were published [33–35]. The suitability of multispectral sensors for large-scale habitat mapping in shallow waters and, specifically, the long data series from Landsat satellites, which provide the only means of investigating retrospective long-term changes in submerged vegetation cover since 1972, were assessed [36–38]. In this study, we analysed the evolution of the trophic state, phytoplankton biomass and macrophyte coverage on the basis of a 20-year time series of in situ and satellite data at three sampling stations in the Lagoon of Veniceused for Long Term Ecosystem Research (LTER) activities [31]. The main aims of this study were (i) to investigate, by means of remote sensing images, patterns of macrophyte colonization and interannual spatial variations based on data recorded in late spring–summer; (ii) to analyse the relationship between macrophyte-colonized areas and phytoplankton biomass; Water 2020, 12, 2810 3 of 22 (iii) to ascertain how lagoon trophic trends influence phytoplankton and macrophyte coexistence and interaction. 2. Area of Studies The LoV (Northern Adriatic Sea, Mediterranean Sea; Figure1) is the largest wetland (550 km 2) in Water 2020, 12, x 3 of 22 the Mediterranean Sea [39]. It is surrounded by densely inhabited and industrial areas and affected by a high touristic2. Area of pressure, Studies as well as intensive fishing and aquaculture. It has an average depth of 1 m and is morphologicallyThe LoV (Northern characterized Adriatic Sea, by Mediterranean the presence Sea; of largeFigure shallow 1) is the largest areas wetland (tidal and (550subtidal km2) flats) and a networkin the Mediterranean of deeper (5–10 Sea [ m)39]. channels.It is surrounded The by LoV densely is connected inhabited and tothe industrial sea through areas and three affected inlets, Lido, Malamoccoby a and high Chioggia, touristic pressure which, divideas well as the intensive lagoon fishing itself intoand aquaculture. three morphological It has an average basins: depth north, of central 1 m and