Original Research
27 July 2022
DOI 10.3389/fmars.2022.958924
TYPE
PUBLISHED
OPEN ACCESS
EDITED BY
Tomaso Fortibuoni,
Istituto Superiore per la Protezione e
la Ricerca Ambientale (ISPRA), Italy
REVIEWED BY
Dimitris Velaoras,
Hellenic Centre for Marine Research
(HCMR), Greece
Milena Menna,
Istituto Nazionale di Oceanografia e di
Geofisica Sperimentale, Italy
Maurizio AZZARO di Rosamarina,
National Research Council (CNR), Italy
*CORRESPONDENCE
T. Ozer
tal@ocean.org.il
B. Herut
barak@ocean.org.il
Relationship between
thermohaline and biochemical
patterns in the levantine upper
and intermediate water masses,
Southeastern Mediterranean Sea
(2013–2021)
T. Ozer *, E. Rahav, I. Gertman, G. Sisma-Ventura,
J. Silverman and B. Herut *
Israel Oceanographic and Limnological Research, National Institute of Oceanography, Haifa, Israel
SPECIALTY SECTION
This article was submitted to
Marine Fisheries, Aquaculture and
Living Resources,
a section of the journal
Frontiers in Marine Science
01 June 2022
29 June 2022
PUBLISHED 27 July 2022
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CITATION
Ozer T, Rahav E, Gertman I, SismaVentura G, Silverman J and Herut B
(2022) Relationship between
thermohaline and biochemical
patterns in the levantine upper and
intermediate water masses,
Southeastern Mediterranean Sea
(2013–2021).
Front. Mar. Sci. 9:958924.
doi: 10.3389/fmars.2022.958924
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© 2022 Ozer, Rahav, Gertman, SismaVentura, Silverman and Herut. This is an
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these terms.
Frontiers in Marine Science
The relationships between the interannual variations of the Levantine
intermediate water (LIW) core properties and the corresponding biochemical
variations in the euphotic zone were systematically studied in the Southeastern
Mediterranean during 2013–2021 and since 2002 based on a previous study.
Salinity and temperature interannual fluctuations in the LIW continue to follow
the Adriatic–Ionian Bimodal Oscillating System (BiOS) mechanism, with salinity
and temperature peaks in the years 2008–2010, 2014–2015, and 2018–2019
coinciding with periods of anticyclonic circulation of the North Ionian Gyre
(NIG). During these anticyclonic periods, the transport of Atlantic Water into the
Levant is reduced together with the transport of LIW out of the basin. These
interannual fluctuations are superimposed on a long-term warming trend
clearly evident from previous studies, showing a maximal temperature in
2018–2019, higher than the previously mentioned temperature peaks by
~0.7°C and ~0.4°C. The enhanced warming in 2018–2019 has caused a
decrease in density (sigma) values of the LIW core, which gave way to the
shallowest record of this water mass (~110-m depth), bringing it well within the
lower photic zone. We suggest that a higher level of nutrients became available,
supporting the observed long-term rise of the intergraded chlorophyll a (Chl.a)
(0.89 mg m−2 year−1), with a maximum recorded during 2018–2019. The longterm record of the mixed layer depths shows no significant change; thus, the
uplift of nutrients during winter mixing cannot support the trend and variations
of the integrated Chl.a. Additional biological parameters of specific picophytoplankton populations and integrated bacterial production and
abundance were measured in 2013–2021, but the measurements were too
sparse to follow a clear interannual dynamics. Yet significantly higher average
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10.3389/fmars.2022.958924
levels for integrated primary production and bacterial abundances were
observed during the anticyclonic period (as for Chl.a). The combined impacts
of the BiOS mechanism and global warming, and hence the increase in LIW
residence time and buoyancy, may impact the primary producers’ biomass at
the photic zone. This latter feedback may slightly counter the enhanced
oligotrophication due to enhanced stratification.
KEYWORDS
Mediterranean Sea, thermohaline, water masses, Levantine, biochemical, nutrients,
chlorophyll, phytoplankton
Introduction
years, a surface circulation scheme accommodating both the
along-slope cyclonic circulation (as in Millot and TaupierLetage, 2005) and the Mid Mediterranean Jet of Robinson and
Golnaraghi (1993) was demonstrated for the EMS using drifter
and altimetry data (Menna et al., 2012; Menna et al., 2020).
Based on a high-resolution simulation for the period of 2011 to
2020, Estournel et al. (2021) described seasonal variations of the
cyclonic, along-slope current as being stronger and more stable
in winter, while in summer, it tends to be interrupted, and the
continuity of the circulation is maintained by a train of eddies.
LIW formation occurs mainly in the Rhodes Gyre area
(Lascaratos and Nittis, 1998; Lascaratos et al., 1999), yet
compelling evidence is given to additional formation sources
along the Turkish and Israeli coasts (Kubin et al., 2019; Fach
et al., 2021), as well as the entire basin (Lascaratos et al., 1993;
Ozsoy et al., 1993). An additional established source
of intermediate water in the EMS is the South Aegean
Sea producing the Cretan Intermediate water (CIW)
(Georgopoulos et al., 1989; Schlitzer et al., 1991; Velaoras
et al., 2014; Velaoras et al., 2019). LIW generally flows
westward spreading from the Levantine Basin to the Ionian
Basin (IB) and then through the Sicily Channel into the Western
Basin, eventually exiting the MS through the Strait of Gibraltar
below the AW layer (Lascaratos et al., 1999; Tanhua et al., 2013;
Malanotte-Rizzoli et al., 2014). The pathways of LIW within the
EMS have high variability but can be generally described as
follows. LIW flow along the coast south of Crete, with part of the
LIW flowing through the straits of the eastern Cretan Arc at
intermediate depths into South Aegean to exit with the CIW
through the western straits. The LIW flows in the Ionian
bifurcates, one track circulating in the Ionian and the other
headed toward the Sicily Channel (Malanotte-Rizzoli et al., 1999;
Millot and Taupier-Letage, 2005). An additional important
feature of the LIW flow feeds the Southern Adriatic Sea,
introducing high-salinity masses into the Adriatic, and is
considered to be a preconditioning factor for the formation of
Adriatic Dense Water (Gacic et al., 2010; Gacic et al., 2011;
The Mediterranean Sea (MS) is dominated by an antiestuarine thermohaline circulation driven by the salinity
differences between the inflowing low-salinity Atlantic Water
(AW) and mainly the outflowing highly saline Levantine
intermediate water (LIW). The basin-scale circulation is
broadly described in terms of a surface flow of AW from the
Atlantic Ocean entering through the Strait of Gibraltar and
proceeding to the eastern basin through the Strait of Sicily, and a
return flow of LIW, originating in the Levantine Basin (LB),
proceeding toward Strait of Gibraltar and finally exiting into the
Atlantic (Tanhua et al., 2013; Malanotte-Rizzoli et al., 2014 and
references therein).
Following early works on the surface circulation in the
Eastern Mediterranean Sea (EMS) (Nielsen, 1912; Wust, 1961;
Ovchinnikov, 1966; Bethoux, 1980), the observations achieved in
the framework of the Physical oceanography of the Eastern
Mediterranean (POEM) program (Malanotte-Rizzoli and Hecht,
1988) provided an important stepping stone in the
understanding of the EMS circulation and yielded many
studies elucidating on basin-scale circulation and sub-basin
scale and mesoscale circulation patterns (Robinson et al., 1991;
Ozsoy et al., 1991; POEM Group, 1992; Malanotte-Rizzoli et al.,
1997). The resulting updated comprehensive description was of
a set of sub-basin gyres connected by a system of jet currents
(Robinson et al., 1991; Robinson and Golnaraghi, 1993). The
AW coming into the EMS through the Sicily Channel follows an
anticyclonic path through the southern Ionian, continuing
thereon toward the Levantine to form the Mid-Mediterranean
Jet, which flows from southwest to northeast in the center of the
basin and joins the Asia Minor Current (Malanotte-Rizzoli et al.,
1997). Later publications affirmed the previously described
along-slope basin-wide circulation and gave attention to the
unstable nature of the southern along-slope current developing
anticyclonic eddies, which disperse part of the AW northward
(Millot and Taupier-Letage, 2005; Hamad et al., 2006). In recent
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(e.g., integrated nutrients, alkalinity, dissolved oxygen, Chl.a,
picoplankton populations, and primary and bacterial
production) at the Southeastern Mediterranean Sea. For this
purpose, we make use of data collected in three deep-water
stations (1,100–1,600 m) in the eastern LB, which was visited
two to three times annually. The thermohaline and Chl.a
datasets represent ~20 years (2002–2021), while the additional
biological data represent the last 9 years (2013–2021). We use
Mediterranean Sea Physical Reanalysis data (Escudier et al.,
2020; https://doi.org/10.25423/CMCC/MEDSEA_
MULTIYEAR_PHY_006_004_E3R1) to examine the
relationship of our findings to variations of the mixed layer
depths (MLDs) and the volume of AW in the southeastern MS.
Recent results (Fedele et al., 2022; Menna et al., 2022) support
the advantage of using LIW to describe the long-term warming
and salinization and the interannual BiOS mechanism, which is
less sensitive to the seasonal cycle but is yet shallow enough to
reflect surface layer and photic zone dynamics.
Schroeder et al., 2012). Seasonality in the LIW flow regime was
recently presented (Pinardi et al., 2019; Lyubartsev et al., 2020;
Estournel et al., 2021; Menna et al., 2021) as well as their water
mass properties in the East Mediterranean (Gacic and Bensi,
2020; Fedele et al., 2022 and references therein; Hayes et al.,
2019). Estournel et al. (2021) outline the rim current of the
Rhodes Gyre dispersing the LIW throughout the eastern
Levantine in winter, while in summer, anticyclonic circulation
that occupies the southeast of the basin redistributes LIW toward
the south of the Levant. This LIW circulation of relatively high
salinity and nutrient levels plays an important role in the deepwater formation in both the eastern and western basins
(Robinson et al., 2001; Schneider et al., 2014) and the
biogeochemistry of the MS (Malanotte-Rizzoli et al., 2014;
Powley et al., 2014).
The LB is significantly influenced by the water exchange with
the IB via the Cretan passage. The Adriatic–Ionian Bimodal
Oscillating System (BiOS), thoroughly described in Gacic et al.,
2011; Gacic et al. (2010 and experimentally by Rubino et al.
(2020), controls the trajectory of the AW flow after passing
through the Sicily Straits to both the Southern Adriatic (SA) and
the LB, which correspond to quasi-decadal reversals in the North
Ionian Gyre (NIG). The BiOS mechanism has been shown to
have a significant effect on the physical and chemical dynamics
in the SA (Civitarese et al., 2010; Gacic et al., 2010; Lavigne et al.,
2018; Mihanovic et al., 2020; Menna et al., 2022; Placenti et al.,
2022) as well as in the LB (Ozer et al., 2017). These studies
proposed that the BiOS mechanism is a feedback mechanism
between changes in the thermohaline structure of SA waters and
the IB. In periods of cyclonic NIG, high-salinity LIW is injected
into the SA, while the transport of AW is diverted to the LB. This
results in buoyancy loss in the SA, which is thought to be a
preconditioning factor for the formation of Adriatic Dense
Water (Gacic et al., 2010; Gacic et al., 2011). During the
anticyclonic NIG, AW intrusion into the Ionian and Adriatic
Basins increases at the expense of the LB, and the formation of
Adriatic Dense water is minimized. In accordance with these
variations, Gacic et al. (2011) showed that during cyclonic NIG,
surface salinity in the SA and IB increases and co-varies with
nitrate levels in both the SA and IB in opposite phases
(Civitarese et al., 2010). Ozer et al. (2017) described the
magnitude of the long-term and superimposed thermohaline
interannual variations and corresponding changes in nutrient
and chlorophyll a (Chl.a) levels in the upper water masses of the
LB (LSW and LIW), attributing them to the long-term climate
change and the interannual BiOS mechanism, respectively.
The variability in physical and biogeochemical properties
observed in the Mediterranean through the last few decades
(Malanotte-Rizzoli et al., 2014; Von Schuckmann et al., 2020)
calls for more systematic monitoring of this basin. Here we
explore the relationships between the interannual variations of
the LIW thermohaline properties and its vertical position with
the corresponding biochemical variations in the euphotic zone
Frontiers in Marine Science
Materials and methods
Sampling/cruise data
The presented data are composed mostly of new 17 Haifa
Section (HaiSec) cruises extending 90 km to the northwest of the
Carmel Headland, northern Israel, which were conducted during
the period 2013–2021, including only deep stations H04, H05,
and H06 (>1,000-m water depth) (Figure 1). Additional data
from previous years (since 2002) at the same stations are
included (Ozer et al., 2017), as well as 10 CTD casts at station
H05. All surveys were carried out by the Israel Oceanographic
and Limnological Research Institute (IOLR). The cruises were
conducted aboard the R/V Shikmona until 2015 and since 2016
aboard the new Israeli R/V Bat-Galim. A Sea-Bird SBE911plus
CTD system, interfaced to an SBE Carousel, was used to collect
continuous profiles (24 Hz) of pressure, temperature, salinity,
dissolved oxygen, and fluorescence. The manufacturer reported
that the precision of the SBE911plus CTD is ±0.0025 for salinity
(inferred from the ±0.0003 S/m conductivity precision) and
±0.001°C for temperature. Throughout the period covered by
this dataset, the pressure, conductivity, and temperature sensors
were calibrated by the manufacturer periodically every 2 years
(as described in Ozer et al., 2020). CTD data were processed
using the Sea-Bird data processing software following the
manufacturer’s recommendations. The CTD data validation
procedure included lowering an additional autonomous
SBE19/SBE19plus CTD (factory calibrated within the last year)
parallel to the onboard SBE9plus in order to obtain duplicate
casts, ensuring that any non-conformities remained within the
sensors’ precision. Samples of dissolved oxygen and Chl.a
(described below) were used to calibrate the dissolved oxygen
profiles from the CTD.
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FIGURE 1
Map of hydrographic stations visited during the IOLR Haifa Section deep stations (blue dots, performed biannually). Station H05 was additionally
visited in 10 cruises. Domain of CMEMS physical reanalysis used for MLD, and AW volume estimate is marked by the dotted red rectangle. IOLR,
Israel Oceanographic and Limnological Research Institute; CMEMS, Copernicus Monitoring Environment Marine Service; MLD, mixed layer
depth; AW, Atlantic Water.
temperature and 37.8 to 39.5 with a 0.01 interval for salinity,
representing the complete range of thermohaline values found in
the dataset. The reanalysis data were then filtered through, and
the volume of each data point was accumulated in the relevant
q–S space position, based on its rounded temperature and
salinity values. For the evaluation of the total AW volume in
the domain, we summed up all the matrix cells with
temperatures above 15°C and salinities below 38.9, and finally,
we calculated the percentage of the domain volume occupied by
AW for each time step (i.e., month). The choice of these
threshold values can be contested, mainly for salinity, thus
changing the total volumes achieved through this method. For
this reason, several iterations, with the salinity limit ranging
from 38.85 to 39.95 (with 0.01 interval), were tested and gave
similar trends (not presented). Thus, we considered these results
to be a strong proxy for the overall volume of AW in the Levant
basin, so that the variability is well presented, not the absolute
volume values.
Atlantic water volume and mixed layer
depth variability
The products of monthly salinity, potential temperature, and
MLD from the MS physical reanalysis provided by the E.U.
Copernicus Monitoring Environment Marine Service (CMEMS)
(Escudier et al., 2020) were obtained for the southeastern MS
(30.7° to 36°N and 32° to 36.2°E, Figure 1) for the period of
January 2002 to May 2020. The reanalysis data had a horizontal
grid resolution of 1/24° (ca. 4–5 km) and 141 unequally spaced
vertical levels. The MLD data were averaged over the complete
domain in order to eliminate the sensitivity of the data to
mesoscale activity and attain a general estimate for this part of
the basin.
In order to quantify the volume of AW, we performed a
volumetric statistical analysis (VSA) introduced by Cochrane
(1958); Montgomery (1958), and Pollak (1958) and more
recently used for the Aegean by Gertman et al. (2006). This
approach is based on assigning temperature (>15°C) and salinity
(<38.9) ranges, which are considered to be characteristic of AW.
For each time step of the reanalysis model, the volume occupied
by AW (where thermohalines values match those of AW
characteristics) is summed up over the entire domain, and its
percentage of the domain is calculated. In order to achieve this,
we first calculated the volume (in m3) of each data point,
considering the spatial and vertical distribution of the data, as
follows:
Levantine intermediate water and photic
zone investigation
In order to minimize the effects of mesoscale phenomena on
our analysis, we only examined the core values of LIW, which are
less affected by diapycnal mixing and more controlled by
isopycnal processes. The vertical position of the LIW core was
identified by finding the maximal salinity value of each cast
within the depth range of intermediate water (100 and 350 m;
Ozer et al., 2017). Subsequently, the physical and chemical data
of the LIW core depth were averaged for all the stations of each
cruise, and finally, the resultant time series was smoothed, using
a moving average with a time window of 1 year. Additionally, the
contemporaneous biological parameters were integrated over the
photic zone (0–200 m) using water column sampling and
Vlat,lon,z = dlat *dlon* Zði+1Þ − Zði−1Þ = 2
where V is the volume of a specific grid point in m3; dlat and
dlon are the constant latitude and longitude distances of 4,620,
and 4,010 m, respectively; Z is the depth level in meters. Next, a
matrix of potential temperature and salinity (q–S space) was
created with the ranges of 13°C to 30°C with a 0.1°C interval for
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Pico-phytoplankton abundance was determined by flow
cytometry. Briefly, seawater samples (1.8 ml) were fixed with
glutaraldehyde (0.02% v:v, Sigma-Aldrich, St. Louis, MO, USA;
G7651) at room temperature for 10 min and frozen in liquid
nitrogen. The abundance of autotrophic pico-eukaryotes,
Synechococcus and Prochlorococcus, was determined using an
Attune ® Acoustic Focusing Flow Cytometer (Applied
Biosystems, Foster City, CA, USA).
Primary productivity was determined following the Steemann
Nielsen (1952) protocol. Specifically, triplicate water samples from
each depth (50 ml) were spiked with 5 mCi of NaH14CO3
(PerkinElmer, Waltham, MA, USA; specific activity 56 mCi
mmol −1 ) and incubated for 24 h under in situ natural
illumination and temperature in a flow-through tank on deck.
Measurements for the added activity and dark controls were also
performed. The incubations were terminated by filtering the
seawater through GF/F filters and acidifying them overnight in 5ml scintillation vials containing 50 μl of 32% hydrochloric acid to
remove excess 14C. Lastly, 5 ml of an Ultima-Gold scintillation was
added to the filters, and the radioactivity was measured using a TRICARB 2100 TR (Packard) liquid scintillation counter.
For measurements of bacterial abundance, heterotrophic
bacteria were stained (300 ml of the initial sample) with SYBR
Green Fluorescent Nucleic Acid Stain (Applied Biosystems) and
enumerated by discrimination based on green fluorescence (530
nm) and side scatter (Marie et al., 1997). Bacterial production
was estimated using the 3H-leucine incorporation method.
Triplicate samples (1.7 ml) were incubated with ~100 nmol
hot leucine L−1 for 4–7 h (PerkinElmer; specific activity 100 Ci
mmol−1). ‘Kill’ treatments in which seawater was added with 100
μl of 100% trichloroacetic acid (TCA; 4°C) along with 3Hleucine were also carried in triplicates from representing
depths (surface water was usually used). The incubations were
terminated with TCA and were later processed following the
micro-centrifugation technique (Smith et al., 1992) and added
with 1 ml of an Ultima-Gold scintillation cocktail. The samples
were counted using a TRI-CARB 2100 TR (Packard) liquid
scintillation counter. A conversion factor of 1.5 kg C mol−1 per
mol leucine incorporated was used (Simon et al., 1989).
analyses, while the Chl.a profiles and integrated values were
obtained from the calibrated CTD fluorescence measurements.
Dissolved oxygen, alkalinity, and
inorganic nutrients analysis
Water samples for dissolved oxygen and inorganic nutrients
were collected at sampling depths based on the thermohaline
structure of the water column, representing the different water
masses. Water samples for dissolved oxygen were sampled and
measured in duplicates onboard immediately after sampling
following the modified Winkler method (Carpenter–Winkler
titration procedure Carpenter, 1965), using an automated
Metrohm Titrando 905 titration system. Duplicate samples for
nutrient analysis were collected in 15-ml acid-washed plastic
scintillation vials and immediately frozen.
Total alkalinity (TA) was measured by potentiometric
titration with a Metrohm, 848 Titrino plus system using the
Gran method to calculate it from acid volumes and
corresponding pH measurements between pH 3.3 and 3.8
(Ben-Yaakov and Sass, 1977). The titration acid was 0.05 M of
HCl, which was verified and adjusted using certified reference
seawater supplied by the Certified Reference Materials
Laboratory, Scripps Institution of Oceanography, CA (Dickson
et al., 2003). Duplicate measurements were made for each
sample, and the precision error was ±1 μmol kg−1.
Nutrients were measured with a Seal Analytical AA-3 system
(Sisma-Ventura et al., 2022). The limits of detection (LODs),
estimated as three times the standard deviation of 10
measurements of the blank (low nutrient aged seawater
collected from the off-shore surface at the Levantine Basin) for
PO4, Si(OH)4, NO2+NO3 (NOx), and NH4, were 8, 80, 80, and
90 nM, respectively. The reproducibility of the analyses was
determined using certified reference materials (CRMs): MOOS 3
(PO4, NOx, NH4, and Si(OH)4), VKI 4.1 (NOx), and VKI 4.2
(PO4 and Si(OH)4). The sample analysis results were accepted
when measured CRMs were within ±5% of the certified values.
Quality control of the nutrient measurements over the years was
performed with the use of internal and certified reference
standards and by participation in international laboratory
performance exercises (QUASIMEME).
Results and discussion
The averaged salinity and temperature time series of the LIW
core present a good agreement with the presiding circulation pattern
of the north Ionian, the BiOS mechanism (Civitarese et al., 2010;
Gacic et al., 2010; Lavigne et al., 2018; Menna et al., 2022; Placenti
et al., 2022). Periods of anticyclonic circulation (tinted in red in
Figure 2) are characterized by a positive tendency in salinity and
temperature, while cyclonic periods (tinted in blue) are accompanied
by a decrease in the thermohaline values of LIW. In our display
(Figures 2–4, Supplementary Figure S1), we extend the final cyclonic
period starting in 2019 (Menna et al., 2022) through the end of the
Biological analyses
Seawater samples (500 ml) for chlorophyll a determination
were filtered through GF/F filters that were then wrapped in
aluminum foil and frozen (−20°C). At the lab, the chlorophyll a
pigment was extracted from the filters using acetone (90%)
overnight and determined by the non-acidification method
(Welschmeyer, 1994) using a Turner Designs (Trilogy) fluorometer.
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FIGURE 2
Time series of salinity (A; yellow), Atlantic Water volume percentage (A; black), temperature (B; red), depth (C; black), density (Sigma-Theta; C;
orange), and mixed layer depth (MLD; D; black) performed in the core of the LIW water mass (ca. 130 m< z< 350 m) during the Haifa Section
cruises (2002–2021). Time series of integrated chlorophyll a at the photic zone (0–200 m) (D; green). Station-specific values are presented in
dots, the moving average is presented in a solid line, and the standard error ranges are indicated with a light-colored area. Light blue dotted line
and formula show the calculated chlorophyll a trend. Periods of anticyclonic circulation (tinted in red in the salinity panel) and cyclonic periods
(tinted in blue) (Menna et al., 2022; Placenti et al., 2022).
the Levant is reduced according to the BiOS theory (Gacic et al.,
2010), there is indeed a significant reduction in the volume of
AW in the EMS by up to two orders of magnitude. The opposite
occurs in reported periods of cyclonic circulation in the north
Ionian, which are characterized by high AW volume. The AW
VSA results are also in the opposite phase of the LIW salinity
time series, providing important evidence of the link between the
variability of the Ionian circulation to the water fluxes coming in
and out of the LB and through this mechanism influencing the
thermohaline and nutrient values of the LIW.
The total alkalinity concentrations (Supplementary Figure
S1) are in accord with concentrations recorded in the
Mediterranean Sea (~2,600 mmol kg−1), showing relatively
high levels (Kolker et al., 2021). We observed a peak in the
total alkalinity concentration coinciding with the 2018 salinity
peak (Supplementary Figure S1), yet the existing data for 2013–
2021 are too small to draw a firm behavior and display
concentrations, which follow the conservative behavior (linear
trend) of total alkalinity with salinity (Kolker et al., 2021, and
references therein).
presented time series, as our data support it with the continuation of a
negative trend in thermohaline values. The long-term warming and
salinification trends are clearly evident in the presented data in
agreement with previously published studies (Ozer et al., 2017;
Ozer et al., 2022). The annual average LIW core depth variates
from 130 to 270 m (average values) over the examined period were
mostly affected by the density (Sigma-Theta) values of this water mass
(Pearson’s correlation value of 0.6). This relationship is most evident
in 2018, where LIW core reached a record low of sigma of ~28.6 kg
m−3, while its average core depth decreased significantly and reached
~110 m (annual average 130 m) (Figure 2), the shallowest depth
recorded here along the 20 years’ time series (2002–2021). It should
be noted that although the LIW reached a high-salinity content at this
time (2018), which is similar to the 2008 salinity peak, it has reached a
maximal temperature value of 17.7°C, attributed to the long-term
warming trend, permitting a minimal density as described above.
The AW volume variability, as achieved through the VSA,
closely follows the cyclonic–anticyclonic regime of the north
Ionian as described thoroughly by Menna et al. (2022). In the
periods of anticyclonic circulation, when the water exchange in
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photic zone (Figures 2, 3). The Chl.a time series partly coincides
with the periods of anticyclonic and cyclonic circulations, not
always in union with the thermohaline exact peaks and lows,
demanding further investigation. The maximal winter MLD
values from the CMEMS physical reanalysis product do not
seem to correspond with the observed integrated Chl.a
variations or its general increasing trend (Figure 2). Therefore,
the supply of nutrients from deeper water due to the annual deep
winter mixing does not support the general increasing trend and
interannual variability of the integrated Chl.a.
The rise in the buoyancy of LIW core in 2018–2019 through
its reduced sigma value gave way to the shallowest record of this
water mass (~110-m depth), bringing it well within the lower
photic zone. The LIW core in 2018–2019 is shallower by ~50 m
as compared to the 2008–2010 peak (Figure 2) and as expected
shows lower AOU values at the shallower depth (Figure 3).
Nevertheless, in contrast to the expected AOU behavior, both
periods contain similar concentrations of NO 3 , showing
relatively enriched concentrations in the 2018–2019 LIW core
(Figure 3). Thus, the mechanism of warming and shallowing the
Dissolved oxygen values correspond closely with the LIW
core depth and can be related to enhanced ventilation of this
water mass, as it becomes shallower and has higher oxygen
demand due to organic material decomposition as it becomes
deeper (Figure 3). The apparent oxygen utilization (AOU) time
series behaves out of phase with the nutrient concentrations
(Figure 3), reflecting the degree of organic matter degradation/
oxidation. In addition, the nutrients (NO3+NO2 and PO4) time
series (Figures 3C) present a mirror image of the thermohaline
and LIW depth data (Figures 2, 3), as they are presumably
depleted from the LIW water mass when it becomes shallower
and more available for primary production and is then
replenished when LIW core deepens.
The integrated Chl.a time series also presents a general longterm positive trend. We observe a significant long-term rise in
the integrated Chl.a of 0.89 mg m−2 year−1 for the years 2002 till
2021 (Figure 2), superimposed by interannual variations. At
three distinct times at the start of a shallowing period of the LIW
core, at the beginning of 2007, the end of 2013, and the middle of
2016, there is a clear rise of the integrated Chl.a levels in the
FIGURE 3
Time series of dissolved oxygen (A; blue), Apparent oxygen utilization (AOU; B; black), dissolved PO4 concentrations (C; orange), and dissolved
NO3+NO2 concentrations (D; purple) were performed in the core of the LIW water mass (ca. 130 m< z< 350 m) during the Haifa Section cruises
(2002–2021). Station-specific values are presented in dots; the moving average is presented in a solid line, and the standard error ranges are
indicated with a light-colored area. Circulation periods are presented as in Figure 2. LIW, Levantine intermediate water.
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10.3389/fmars.2022.958924
FIGURE 4
Time series of salinity (A; yellow) as presented in Figure 1 for the 2013–2021 time slot and time series of integrated Chl.a (B; green), integrated
primary production (C; orange), and integrated bacterial production (D; brown) performed at the photic zone (0–200 m) during the Haifa
Section cruises (2013–2021). Station-specific values are presented in dots, the moving average is presented in a solid line, and the standard
error ranges are indicated with a light-colored area (for salinity and Chl.a). The bold black segmented lines and the thin dotted side lines in
panels (C) and (D) represent the average and standard deviation range, respectively. Circulation periods are presented as in Figure 2.
delayed response of the biological cycle to the observed
physical changes in LIW core properties. Nonetheless,
considering the above two general periods, a significant (p<
0.05) change in the average integrated values for primary
production and bacterial abundance (as for Chl.a) shows
higher levels after 2017, during the anticyclonic period and
afterward (Figure 4). Other integrated biological parameters
measured during this period are too sparse to follow detailed
int erannual variat ions ( Supplementary Figure S1).
Specifically, data on the abundance of pico-phytoplankton
populations (autotrophic pico-eukaryotes, Synechococcus and
Prochlorococcus) and integrated bacterial production were
too sparse, preventing any clear statistical significance
(Supplementary Figure S1). Further observations are
required to better assess the response of such picophytoplankton populations.
The changes in buoyancy, consequent of the changes in the
thermohaline values, are the main mechanism controlling the
LIW core due to its increased buoyancy enabled a higher level of
nutrients to become available to the photic zone from below,
supporting the observed rise of the intergraded Chl.a (or algae
biomass), with a maximum recorded during 2018–2019.
Accordingly, we further suggest that this mechanism of
warming and shallowing the LIW core may explain the
general long-term rise of the integrated Chl.a (Figure 2) as the
LIW core becomes gradually more available for
photosynthetic activity.
The 2013–2021 time series shows two distinct periods of
BiOS, mainly cyclonic (2011–2016; Placenti et al., 2022) and
mostly anticyclonic (2017–2019; Menna et al., 2022). It is
expected that the biological response to BiOS is complex and
exhibits certain delay and thus does not coincide with the
detailed thermohaline interannual variations. Pearson lag
correlations for the above time series presented maximal
values of ~0.82 with the integrated Chl.a lagging ~22
months behind the thermohaline parameters, attesting to the
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10.3389/fmars.2022.958924
vertical position of LIW in the SE Levantine Basin. The vertical
uplift of the nutrient-rich LIW water is an important and
significant pathway of nutrients into the photic zone driving
the primary production in this oligotrophic area, especially
during anticyclonic periods, which prolong the residence time
of the LIW due to its reduced outflow from the LB. Thus, global
warming in combination with the BiOS mechanism, and hence
LIW residence time and buoyancy, may impact the primary
producers’ biomass at the photic zone and hence somewhat
reduce the degree of oligotrophic state. This latter feedback may
slightly counter the enhanced oligotrophication due to the
warming effect on enhanced stratification and mixing depths.
Further observations are needed to better understand and assess
these processes.
Acknowledgments
We thank the captain and crew of the R/V Bat-Galim
operated by the Israel Oceanographic and Limnological
Research Institute (IOLR). We thank the maritime crew,
electrical lab, and research assistants at the physical
oceanography, marine chemistry, and biology departments at
IOLR for their dedicated efforts.
Conflict of interest
The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Data availability statement
Publisher’s note
The datasets presented in this study can be found in online
repositories (physical updated and chemical in process). The
names of the repository/repositories and accession number(s)
can be found at: Israel Marine Data Center–https://isramar.
ocean.org.il/isramar2009/.
All claims expressed in this article are solely those of the
authors and do not necessarily represent those of their affiliated
organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteed
or endorsed by the publisher.
Author contributions
Conceptualization: BH and TO. Data acquisition: TO, IG,
ER, GS-V, BH, and JS. Formal analysis: TO, IG, ER, GS-V, JS,
and BH. Project administration: BH. Writing—original draft:
TO and BH with the help of IG, ER, GS-V, and JS. All authors
approved the submitted version.
Supplementary material
The Supplementary Material for this article can be found
online at: https://www.frontiersin.org/articles/10.3389/
fmars.2022.958924/full#supplementary-material
SUPPLEMENTARY FIGURE 1
Funding
Time series of alkalinity (A, red), Synechococcus (B, blue),
Prochlorococcus (C, orange) pico-eukaryotes (D, green) and integrated
bacterial production (E, grey) performed at the photic zone (0-200m)
during the Haifa Section cruises (2013–2021). Station-specific values are
presented in dots and the moving average is presented in a solid line.
Circulation periods are presented as in Figure 2.
This study was supported by the Israel Ministries of Energy
and Environmental Protection through the National Monitoring
Program of Israel’s Mediterranean waters.
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