Record-breaking salinities in the middle Adriatic during summer 2017 and concurrent changes in the microbial food web
Introduction
The Adriatic Sea, the semi-enclosed quasi-rectangular northernmost part of the Mediterranean Sea (Fig. 1), is known for: (1) its cyclonic circulation (Poulain and Cushman-Roisin, 2001), where warm and salty ultraoligotrophic Eastern Mediterranean waters (Krom et al., 1991, Krom et al., 2004), including Levantine Intermediate Water (LIW), enter along its eastern coast (Zore-Armanda, 1963, Zore-Armanda, 1991, Orlić et al., 1992, Artegiani et al., 1997a); (2) a large freshwater load in the northernmost part of the basin, primarily from the Po River (Raicich, 1996), which flows near the surface as the Western Adriatic Coastal Current (Orlić et al., 1992); (3) dense water formation in both the shallow northern Adriatic (Vilibić and Supić, 2005, Mihanović et al., 2013, Benetazzo et al., 2014) and the 1200-m deep South Adriatic Pit (Gačić et al., 2002, Vilibić and Šantić, 2008), bringing oxygen to deep layers and depressions; and (4) dense water outflow towards the deep and abyssal plains of the Eastern Mediterranean (Robinson et al., 1992). All these processes contribute to basin-wide thermohaline circulation (Orlić et al., 2006), confirmed by the application of indirect (Zore, 1956, Artegiani et al., 1997b, Hopkins et al., 1999) and direct current estimations (Poulain, 2001). Advection of the LIW has a strong interannual and decadal variability (Grbec and Morović, 1997, Matić et al., 2017), interplaying with the advection of Western Mediterranean waters driven via reversals in the North Ionian circulation from anticyclonic to cyclonic, and vice-versa, controlled mainly by internal dynamics such as the Adriatic-Ionian Bimodal Oscillating System (BiOS, Gačić et al., 2010). A strong decadal variability in the water masses advected into the Adriatic is recognizable in nutrient content variability (Vilibić et al., 2012). Plankton community composition and abundance also vary, indicating the origin of the advected water mass (Grbec et al., 2009, Civitarese et al., 2010, Batistić et al., 2014).
Alongside these complex processes, the entire Mediterranean Sea has been recognized as a hotspot and sensitive ocean region for climate change (Gualdi et al., 2013). Centurial measurements in the Adriatic Sea indicate warming of both surface and deep layers (Lipizer et al., 2014), while basin-wide salinity is also increasing due to increased evaporation and decreased precipitation and river runoff observed and projected for the area (Adloff et al., 2015). Temperature increase has also been recorded in the eastern Adriatic coastal area (Grbec et al., 2018). Long-term measurements in the middle Adriatic revealed weakening of thermohaline circulation (Vilibić et al., 2013) and decreased deep dissolved oxygen content (Vilibić et al., 2012). According to climate projections, anomalous periods with increased air temperature and decreased precipitation are expected to be more frequent over the Adriatic in the future climate (Zampieri et al., 2012, Branković et al., 2013), with the main changes projected during summer periods (Branković et al., 2012).
Marine microorganisms are an important part of all major biogeochemical cycles, fluxes and processes occurring in marine systems. Heterotrophic bacteria (HB), autotrophic picoplankton (APP) (Prochlorococcus (PROC), Synechococcus (SYN) and picoeukaryotes (PICO)) and heterotrophic nanoflagellates (HNF) as the most important picoplankton predators, represent the major components of the microbial food web (MFW). These microorganisms play a significant role in carbon production (up to 90%), assimilation of dissolved organic matter and production of new biomass, decomposition of organic matter and transformation of inorganic compounds into forms suitable for primary producers, and transfer of energy towards higher trophic levels (Li et al., 1983, Ducklow et al., 1986, Cole et al., 1988, Stockner, 1988, Campbell et al., 1994). Their role is particularly important in oligotrophic environments (Chisholm et al., 1992, Magazzu and Decembrini, 1995, Li, 1998, Zubkov et al., 2000, Li and Harrison, 2001, Grob et al., 2007) such as the eastern coast of the middle Adriatic Sea (Šolić et al., 2009, Šantić et al., 2013). In many oligotrophic ecosystems, these microorganisms located at the lower levels of the food web are responsible for strong bottom-up processes that control the structure and dynamics of upper trophic levels (Lassalle et al., 2011). Therefore, it is possible that even small changes at the base of the food web could be amplified through trophic chains, consequently affecting different aspects of the structure and functioning of marine ecosystems (e.g. Edwards and Richardson, 2004, Wiltshire et al., 2008, Montoya and Raffaelli, 2010, Sarmento et al., 2010). Recent studies in the Adriatic Sea have shown that local and regional effects of global warming may alter the structure and functioning of the MFW, which is then reflected in the carbon cycle and energy flow in the ecosystem (Šolić et al., 2017, Šolić et al., 2018a).
The year 2017 in the Adriatic can be considered anomalous in both physical, particularly salinity, and microbial properties. Subsurface temperatures were up to 4 °C above average, and salinity was also above average throughout the entire water column, with a maximum in the surface layer. We hypothesize that recorded high salinity was the result of interactions between local and remote processes operating at different temporal and spatial scales. We also hypothesize that the extreme increase in salinity may have caused significant changes in the MFW, thus impacting the whole food web, which is particularly sensitive in ultraoligotrophic environments such as the Adriatic Sea. In order to test these hypotheses, we used atmospheric reanalysis and climate products for quantification of the atmospheric anomaly (in air temperature and water mass budget), while the thermohaline and microbial properties were assessed by analysing long-term measurements carried out on a monthly basis at the Stončica station in the central Adriatic (Fig. 1). The results of the Regional Ocean Modeling System (ROMS, Shchepetkin and McWilliams, 2005, Shchepetkin and McWilliams, 2009) and calculations of Lagrangian Coherent Structures (LCS) via finite-time Lyapunov exponent (FTLE) were used to elucidate the relative importance of local and remote processes for the conditions documented in the middle Adriatic during summer 2017. Section 2 presents the data collected at the Stončica station, description of high-frequency (HF) radar measurements, ROMS model setup and FTLE calculations. Section 3 quantifies the thermohaline and MFW properties, both for 2017 and for the climate periods (1961–2016 for temperature and salinity, 2008–2016 for MFW parameters) and includes analyses of the water mass budget (evaporation, precipitation) over the central Adriatic and ROMS model results. Section 4 discusses the local and remote physical processes and their consequences on the MFW, while the fifth and final section gives the main conclusions.
Section snippets
Collection of temperature, salinity and inorganic nutrient data
Oceanographic data were collected at the Stončica station (43°N; 16° 20′E, Fig. 1), situated off the island of Vis. The station is located at the boundary between the open Adriatic and eastern Adriatic coastal waters, where the latter affect surface layers at the station due to freshwater river load (Buljan and Zore-Armanda, 1976, Grbec et al., 2007). The station has been surveyed regularly, on an almost monthly basis. Measurements of thermohaline and several chemical parameters date back to
Thermohaline properties and air-sea water fluxes
Temperature conditions during 2017 at the Stončica station followed an average seasonal cycle at the surface (0 m) (Fig. 2D). However, subsurface layers (10, 20, 30 m) had temperatures up to 4 °C higher than the long-term averages during the summer season (June–September), revealing heat accumulation and no substantial stratification in the upper part of the water column (Fig. 2D, E). Due to the higher than average surface salinity (Fig. 2A and 3), summer surface density was above
On the physical setup in the atmosphere and ocean
Summer 2017 was extremely hot and dry (MHS, 2017), with the largest water mass loss in the last ten years. In addition, due to low precipitation, eastern Adriatic rivers had below-average discharges during most of the year (MHS, 2017; Fig. 7). Atmospheric and hydrological conditions strongly impacted the eastern part of the middle Adriatic. Consequently, subsurface temperatures at the permanent oceanographic station Stončica were up to 4 °C above the long-term average (1961–2016), and surface
Conclusions
This paper documents the unique thermohaline and microbial observations in the central Adriatic Sea during 2017. Extremely high salinities were observed in the entire water column at a representative CTD station sampled regularly over a long-term period. Moreover, an ‘inverse’ salinity profile was recorded in August with record-breaking surface values surpassing 39.0. The typical annual salinity course with spring surface minimum was missing. The observed salinity distributions were a result of
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We are indebted to the crew members of R/V BIOS DVA and technicians engaged in data collection and laboratory analyses. NCEP/NCAR data were taken from the ESRL NOAA webpage at https://www.esrl.noaa.gov/psd/data/gridded/data.ncep.reanalysis.html. We thank INGV modelling group for providing boundary conditions from Adriatic Forecasting System (AFS) for the ROMS model. The comments provided by two anonymous reviewers are greatly appreciated. This study was supported by the Croatian Science
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