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Article

Determining the Fluxes and Relative Importance of Different External Sources and Sinks of Nitrogen to the Israeli Coastal Shelf, a Potentially Vulnerable Ecosystem

by
Tal Ben Ezra
1,*,
Anat Tsemel
1,
Yair Suari
2,
Ilana Berman-Frank
3,
Danny Tchernov
1 and
Michael David Krom
1,4
1
Morris Kahn Marine Station, Department of Marine Biology, Leon H. Charney School of Marine Sciences, University of Haifa, Haifa 3103301, Israel
2
The Faculty of Marine Sciences, Ruppin Academic Center, Michmoret 4025000, Israel
3
Department of Marine Biology, Leon H. Charney School of Marine Sciences, University of Haifa, Haifa 3103301, Israel
4
School of Earth and Environment, University of Leeds, Leeds LS2 9JT, UK
*
Author to whom correspondence should be addressed.
Water 2024, 16(18), 2585; https://doi.org/10.3390/w16182585
Submission received: 4 August 2024 / Revised: 4 September 2024 / Accepted: 5 September 2024 / Published: 12 September 2024
(This article belongs to the Special Issue Research on Coastal Water Quality Modelling)
Browse Figures
Versions Notes

Abstract

:
While the biogeochemical properties of the Israeli coastal shelf (ICS) are similar to adjacent pelagic waters, the external sources of inorganic nitrogen (N) are very different. The main source of ‘new’ N to the pelagic zone is deep winter mixing, with minor contributions from atmospheric deposition and eddy diffusion across the nutricline. For the ICS, major N sources include offshore water advection (260 × 10⁶ mol N y−¹), atmospheric input (115 × 10⁶ mol N y−¹), and riverine input (138 × 10⁶ mol N y−¹), which primarily consists of treated wastewater and stormwater runoff. Direct pollutant discharge from sewage outfalls and submarine groundwater discharge are relatively minor. Key N sinks are new production (420 × 10⁶ mol N y−¹) and sediment deposition and uptake (145 × 10⁶ mol N y−¹). Inputs of nitrate and ammonium were similar and dominant in winter. Unlike temperate shelves, where riverine input is dominant, here it was only slightly higher than atmospheric input, with net N advection onto the shelf being significant. External N inputs did not change net primary production (NPP) by more than ~30% or affect dominant pico and nanophytoplankton genera, except in localized patches. This study offers baseline values for future climate and environmental change assessments.

1. Introduction

The Eastern Mediterranean (EMS) is a highly unusual inland sea that has been used as a natural laboratory to study globally important biogeochemical processes, especially those related to oligotrophic areas of the ocean which are P depleted [1]. Many studies exist to investigate nutrient and phytoplankton dynamics in offshore Eastern Mediterranean Sea (EMS; [2,3,4,5,6,7]), while such processes on the coastal shelves have remained relatively understudied [8,9,10,11,12,13,14]. This is especially the case for the Israeli coastal shelf (ICS; [15,16]). Many of the studies of coastal shelves of the EMS deal with understanding the nature and effect of specific point sources of pollution such as discharges from rivers [17,18] or industrial or domestic wastewater discharges [19] or to set eutrophication standards [20,21]. There have been very limited previous studies to determine the relative importance of various anthropogenic and natural discharges to the overall nutrient supply to an EMS coastal shelf region.
The coastal zone of most regions of the world is very different from the adjacent offshore marine ecosystem. Typically, there are higher fluxes and concentrations of nutrients, which result in higher primary productivity and phytoplankton biomass, which in turn result in increased fisheries, but can also result in eutrophication and, nowadays, often hypoxic areas [22,23,24]. This high level of productivity on temperate coastal shelves is caused by a combination of high external nutrient supply from discharging rivers and wastewater outfalls, together with recycling of nutrients from underlying sediments and upwelling of nutrient-rich offshore waters. Similar studies in the ICS have generally been restricted to shallow water and targeting pollution “hot spots” [25,26]. These studies and the few studies examining processes across the entire coastal shelf [15,16,27,28,29] show that the ICS is generally oligotrophic and similar in many ways to the adjacent pelagic offshore.
In this study, we have carried out a detailed budget for all the major sources and sinks of N to and from the ICS. The aim of this study was to determine the relative importance of the different inorganic N sources to the ICS. Where available, we also determined the seasonality of the inputs to the ICS to explain why the timing and magnitude of the major biogeochemical processes on the shelf are similar to those offshore, despite the fact that the immediate processes supplying bioavailable nutrients to the ICS are very different from those known to occur offshore.

2. Materials and Methods

For a detailed description of the methods used to determine the physical structure (temperature and salinity), nutrient dynamics, primary productivity and chlorophyll measurement procedures shown as figures in Supplementary Materials, see Ben Ezra et al., (2023) [29]. For a detailed definition of the ICS see Appendix A.

3. Results and Discussion

3.1. Nutrient Dynamics across the Israeli Coastal Shelf (ICS)

The seasonal changes in nitrate and nitrite (N + N) and dissolved inorganic phosphate (DIP) at the edge of the ICS, at sampling locations across the shelf and at the offshore pelagic station sampled at 1450 m water depth, were similar throughout 2018–2019 (Figure 1; [29] and Figures S1 and S2). It is characteristic of the upper water column of the S.E. Levantine basin that deep mixing in winter results in excess N + N accumulating in the water column, which decreases to low values during the period of seasonal water column stratification [7]. Unusually, there is essentially no DIP measured in the photic zone throughout the year. This is because cyanobacteria, which are an important component of the phytoplankton community, have the capability of taking up DIP into their periplasm very efficiently [30,31,32]. What is measured is a balance between this uptake and recycling processes.

3.2. Seasonal Changes in Primary Productivity and Phytoplankton Biomass on the ICS

The seasonal changes in monthly primary productivity (PP) are consistent with the nutrient dynamics across the ICS to the offshore, with the highest values during winter decreasing after the water column becomes seasonally stratified (Figure S5; [29]). The integrated annual gross PP at the outer shelf station and at the offshore pelagic station were 30 g C m−2 y−1 and 28 g C m−2 y−1, respectively, and both were in the range of gross PP data previously measured on the ICS (10–20 g C m−2 y−1) [33]. The phytoplankton community on the ICS is dominated by Synechococcus, Prochlorococcus and picoeukaryotes, as is the offshore pelagic community [34]. There is very limited data on the important but quantitively minor eukaryote community. Keuter et al. (2022) [35] showed some minor systematic differences in the coccolith community between the pelagic station offshore and that on the edge of the ICS [35]. Rahav and Berman-Frank (2023) [36] found minor differences between other eukaryote groups (e.g., diatoms, dinoflagellates, etc.) between the pelagic and ICS [36]. Local studies have shown higher phytoplankton activity at specific locations on the ICS, such as adjacent to locations with measurable submarine groundwater discharge [26] or due to sewage discharge [37]. It is also likely that the pulses of water from the micro-estuaries flushed out during storms will also result in short term changes in the phytoplankton communities [38]. While the satellite-derived data show a very similar temperature profile between the outer coastal station and the offshore pelagic station, the chlorophyll in the upper layers at the coastal station was more scattered and somewhat higher (Figure 2). Pearson r cross-correlation analysis showed a stronger correlation with a shorter lag time at the pelagic station (r = −0.783; lag = ~25 days) compared to the coastal station (r = −0.487; lag = ~50 days). Considering that Chl levels are influenced by factors such as mixing depth and nutrient fluxes, in addition to temperature, this confirms that different driving forces are at play between the pelagic and coastal shelf environments.

3.3. Sources and Sinks of Nutrients to the ICS

In the pelagic ecosystem, the principal driver of the winter phytoplankton bloom is deep winter mixing from the major reservoir of nutrients below the nutricline [7,39]. Although the coastal shelf has a similar winter increase in net PP and autotrophic phytoplankton (Figure S5), there is no major reservoir of nutrients immediately below the photic zone. This raises the question of why the seasonal nutrient pattern and the timing of the bloom are similar on the ICS and the pelagic station (Figure 2).
To understand better the similarities and differences between the ICS and the pelagic, an inorganic N budget was calculated of the sources and sinks to the ICS. Given that the ecosystem becomes N and P co-limited during the summer [3,40], understanding the N sources and sinks also defines the new production on the ICS. A similar attempt at determining N budget across the ICS was made by Townsend et al. (1988) [15]. However, they made a conceptual error in which they compared the measured gross PP (which includes both new production, supported by external nutrients, and recycled production) with estimates of the (new) nutrient (N) fluxes to the shelf.
In Townsend et al. (1988) [15], and indeed in this more comprehensive study, it is not possible to directly determine the new production, which is normally calculated in oceanic systems as the nitrate supplied externally to the photic zone [39,41]. Such a calculation does not work on the shelf because both nitrate and ammonium are supplied externally (Table 1).
However, we have shown (Figure S3) that the gross PP on the pelagic station (30 g C m−2 y−1) was similar to the gross PP for the coastal station (28 g C m−2 y−1). We have also shown how similar the nutrient dynamics, the chlorophyll content, and other measures of phytoplankton biomass and production are between the ICS and the pelagic offshore station [29]. It is thus considered a reasonable assumption that the ratio of export (new) production to gross production on the ICS was proportional to that at the pelagic station. Since the calculated export production at the pelagic station was 172 mmoles N m−2 y−1 [7], which is 46% of the gross PP using a Redfield conversion factor of 6.6 (C:N), then the calculated new production on the ICS would be 161 mmoles N m−2 y−1. Integrating that new production over the entire area of the ICS (2558 × 106 m2) results in a total annual value of 420 × 106 Moles N yr−1. Although the dissolved N:P ratio in this region is different than the classical Redfieldian ratio [1,7], the measured value of C:N on the ICS was 7.2, determined from a limited number of samples of particulate matter from the transect samplings. Therefore, we assume the use of Redfield ratio on uptake calculations is justified. It was, in addition, considered reasonable that, like the adjacent offshore EMS, there was minimal N fixation [42] and denitrification in the water column and/or sediment [43]. Based on these assumptions, it is possible to use a calculated external N budget to the ICS to quantify the relative importance of different N sources in supporting the productivity on the shelf.
In Table 1, the average of two estimates is presented for each source and sink as explained in the text and the value ± range is given. Where available, the ratio of nitrate–ammonium in the sources/sinks are given.
Table 1. Calculated net sources and sinks of N to the Israeli coastal shelf.
Table 1. Calculated net sources and sinks of N to the Israeli coastal shelf.
Source of N to ICSAverage ± Range (106 mol N y−1) Nitrate–Ammonium RatioReference
Atmospheric supply1157:5[7]
Submarine groundwater discharge8–3819:1[44,45]
Direct wastewater discharge60 ± 20Dominantly ammonium [46]
Riverine input123.51:1.6 [38]
Total external sources316
Sinks of N from ICS
Sediment145 ± 15N.A.[16]
Net primary productivity420N.A.This study
Fishing activity13N.A.
Total sinks on the ICS575
Advection = Sum of sinks− sources259 (45%)Advection is dominantly nitrate and mainly in winterThis study
Notes: Table 1 Calculated net sources and sinks of N to the Israeli coastal shelf (in units of 106 mol N y−1). The average values (rounded to nearest 5 or 10) ± range are given. See Section 3.3. for the assumptions made in each of the nutrient flux estimates. The difference between the integrated N consumed and the integrated N supplied is assumed to be the annual flux of N advecting onto the shelf from the pelagic plus the recycled PP. The references are for flux data and also for nitrate–ammonium ratio where given. N.A. stands for data Not Available.

3.3.1. Atmospheric Input

The atmospheric flux of nutrients to the EMS has been determined by a series of studies from coastal stations around the EMS [47,48,49]. Ben Ezra et al. (2021) [7] measured the monthly integrated flux of atmospheric input of N to a sampling station at Tel Shikmona, close to Haifa, during February 2018–January 2019, the period of sampling covered in this study. Defining ICSA as the surface area of the ICS (see Figure 1c), which is 2558 × 106 m2, the annual atmospheric flux of N to ICS is calculated in Equation (1) as follows:
44.6 mmol N + N m−2 y−1 × ICSA m2 = 115 × 106 mol N y−1
The nitrate–ammonium ratio in the atmospheric supply was 7:5 during this period. Most of the deposition occurred in winter (February–March and November–January; 5 months) resulting in 57% of the total annual deposition. This was due mainly to the winter rains which are characteristic of the region. Indirect evidence of atmospheric input of nitrate (and ammonium) exists from our transect measurements in summer, when the water column is seasonally stratified, there are occasionally surface samples with high N + N and ammonium [29].

3.3.2. Input from Submarine Groundwater Discharge (SGD)

It is known that nutrients are supplied by submarine groundwater discharge (SGD) into the Mediterranean [45]. The Israeli coast is underlain with sedimentary rocks (carbonate and sandstones) which are known to contain large amounts of groundwater, some of which release SGD into the adjacent offshore [44]. However, while there have been estimates of the N flux per m of coast at specific locations known to have high SGD (e.g., the flux of N at the Dor beach is ~500 mol N y−1 m−1; Weinstein et al., 2011 [44]), there are no regional estimates of the total annual flux into the ICS.
Powley et al. (2017) [5] calculated the flow of SGD into the entire eastern Mediterranean Sea, based on the literature values, as 2.21 × 109 mol N y−1 into the EMS. It is assumed here that the flux of SGD from the ICS is typical of the EMS coastline. Here, we use the ratio of the atmospheric input to the ICS (115 × 106 mol N y−1) to the atmospheric input to the entire EMS (33.6 × 109 mol N y−1; [46,48]), and use that ratio to calculate the fraction of the total SGD supplied to the ICS (i.e., what fraction of 2.21 × 109 mol N y−1 is supplied by local SGD to the ICS). By this calculation, the SGD supply to the Israeli coastal shelf was 7.6 × 106 mol N y−1.
The net annual flux of N from SGD into the ICS is calculated in Equation (2) as follows:
115 × 106 (mol N y−1) × 2.21/33.6 = 7.6 × 106 mol N y−1
An alternative estimate is based on the regional study of the flux of DIN into the entire Mediterranean Sea (MS) by Rodellas et al. (2015) [45], in which they estimated the DIN flux to be in a range of values from 20 to 1500 × 109 mol N y−1. The higher values are incompatible with N budgets carried out in the EMS [43], which calculated a net flux of <10 × 109 mol N y−1 passing through the Straits of Sicily without any SGD. Rodellas et al., (2015) [45] also presented a conservative estimate for the flux of fresh SGD based on water flux from Zektser et al. (2006) [50]. Their concentration of DIN in fresh SGD resulted in an estimate flux of 30 × 109 mol N y−1 for the entire MS. Using the ratio of DIN from SGD to the WMS/SGD to the EMS [5] results in an annual SGD flux of N to the entire EMS of 11.2 × 109 mol N y−1 to the EMS. Here, we use the same calculation involving the well-defined atmospheric inputs, locally and over the entire EMS as above, to prorate the SGD for the ICS to the total EMS.
The net annual flux of N from SGD into the ICS is calculated in Equation (3) as follows:
115 × 106 (mol N y−1) × 11.2/33.6 = 38.3 × 106 mol N y−1
Using these two values, we calculate an average SGD to the ICS of 23 ± 15 × 106 mol N y−1.
Weinstein et al. (2011) [44] determined that 95% of SGD supplied to the ICS was as nitrate. To our knowledge, there are no studies on the seasonality of the flux of SGD into the EMS. It is however likely that the flux in late winter, when the local groundwater had been recharged by winter rains and before it had been substantially pumped, would yield the highest SGD flow rate into the coastal waters.

3.3.3. Direct Discharge of Wastewater into the ICS

In a study of wastewater inputs to the Mediterranean, Powley et al. (2016) [46] assembled data of wastewater discharges via submarine outfalls from three Israeli towns: Herzliya, Acre and Nahariyah. These towns discharge effluent from secondary sewage treatment. The estimated values are 54 (41–76) × 106 mol N y−1. It is generally assumed that most of the DIN input directly from sewage discharges is as ammonium, which can be converted to nitrate by nitrification if the receiving body of water is oxic.

3.3.4. Riverine Input

In many coastal shelves, an important source of nutrients is from local river input. Indeed for the EMS as a whole, Krom et al. (2010) [43] estimated that rivers provide ~30% of the total N flux. However, there are no major rivers flowing into the ICS. Even for the several streams that once flowed, almost no natural water flow remains [51]. Freshwater is a valuable resource in Israel and is trapped in reservoirs and used for domestic and/or agricultural use. What limited baseflow does exist is mainly treated sewage effluent and other aqueous discharges such as agricultural irrigation waters, except in those streams (Yarkon and Kishon) where there is limited water flow to maintain some discharge through nature reserves, etc. [52]. As part of the Israeli National Monitoring Program, IOLR has carried out nutrient measurements in the outlets of all the main Israeli streams [53]. They have calculated an annual flux of nutrients from the main streams into the ICS by multiplying the concentration measured in their March sampling by the annual water flux discharged from each stream, as determined by the Israeli Water Authority. These data are presented in Table S1 as fluxes in units of 106 mol N y−1. The average total input of dissolved inorganic N over the past 10 years was thus 132 × 106 mol N y−1.
However, the streams of Israel are characterized by two distinct discharge states, the normal baseflow and periodic storms in winter, which have much higher flows but lower dissolved nutrient contents [54]. These storms flush out nutrients from the streams together with their surficial sediments into the adjacent ICS. In a detailed study of Alexander Stream, which is considered a typical Israeli stream, monthly measurements of baseflow at five locations were carried out, as well as hourly sampling of storm flow when the water flow rate was greater than 2 m3 s−1 [54]. They calculated that the stormwater discharge contained 62% of the annual water flow to the ICS, while the concentration of DIN during storms was 55% of the typical baseflow concentration. Using this calculation, the total DIN discharged to the ICS from the Alexander Stream was 89% of the value estimated using the IOLR procedure. In addition, there is a further 2% of particulate N (PN) discharged, which was not included in the IOLR estimate [53]. Assuming that the Alexander Stream is a typical Israeli stream, then the total flux of all streams to the ICS is thus 91% of the IOLR value (123.5 × 106 mol N y−1), and the IOLR estimate is increased to include PN and is now 138 × 106 mol N y−1. Here, we use these two values as the possible range of values for the riverine flux into the ICS.
The dominant N species flowing out of the Alexander Stream is ~1.6:1 ammonium–nitrate.

3.4. Sinks of N on the ICS

3.4.1. Flux of N across the Sediment–Water Interface

Christensen et al. (1988) [16] determined the flux of nutrients across the sediment–water interface of the ICS. Typically on coastal shelves, the sediment is a source of nutrients to the shelf from decomposing labile organic matter in the upper layers of the sediment [24]. However, Christensen et al. (1988) [16] found the opposite. They found that there was little or no ammonium between 0 and 4 cm depth and concluded that no ammonium escaped from the sediment. Although a small amount of nitrate did flux out of the sediment (0.43–0.57 μmol m−2 h−1), this was only sufficient to support 2% of the phytoplankton N demand. Thus, the total net N flux across the sediment–water interface is the sum of the benthic productivity and N burial (5.5 μmol N m−2 h−1) plus total denitrification (0.67–1.60 μmol N m−2 h−1). Christensen et al. (1988) [16] estimated that this represented ~25% of the total autotrophic N demand.
Thus, to calculate the net flux into the sediment, we used the calculated higher value for PP (625 × 106 mol N y−1) and assumed that an additional 25% of N had been supplied to the ICS but removed by sedimentary processes, i.e., 160 × 106 mol N y−1.
The minimum calculation used the integrated estimate of denitrification of 0.67–1.60 μmol N m−2 h−1 (average value of 1.14) and sedimentary burial of 5.5 μmol N m−2 h−1. We then assumed that these processes took place over half of the ICS (2558 × 106 m2 × 0.5) to take account of the fact that these high rates of burial and diagenesis are likely to be dominant only in finer grained sediment and not in sand [55].
This calculation for the outer shelf resulted in a flux of N removed by the sediment, which was obtained using Equation (4) as follows:
6.60 (μmol N m−2 h−1) × ICSA (m2) × 0.5 × 24 × 365 = 74 × 106 mol N y−1
For the inner half of the shelf, an average sedimentation rate of 0.36 cm yr−1 is used [56], a porosity of 40%, a density for quartz sand of 2.65, and an average carbon content of 0.1%. It is assumed that the C:N molar ratio of the organic matter is 6.6:1. This results in a total burial flux of N of 60 × 106 mol N yr−1.
This value is added to the lower flux estimate, resulting in a total flux of 130 × 106 mol N yr−1.

3.4.2. N Consumed by Net Primary Productivity

As described above, this was calculated assuming the same ratio of export production to gross productivity as measured on the pelagic shelf for the same year (2018–2019; [7,34]). Using the value of 30 g C m−2 y−1 for the GP on the shelf, 172 mmoles N m−2 y−1 for export/new production and a Redfield ratio of 6.6 (C:N), the calculated new production on the ICS for 2018–2019 was 420 × 106 Moles N yr−1.

3.4.3. Fishing Activity on the ICS

The total fishing activity on the ICS was 2100 tons of fish in 2021 [57]. Assuming that the fish is 50% organic C and has a C:N ratio of 6.6, the total amount of fish-N removed from the ICS is 13 × 106 Moles N yr−1.

3.4.4. Advection onto the ICS

The missing N in this budget is that supplied by net advection of N by waters transferred onto the shelf. The calculated net N flux advected onto the shelf is 259 × 106 mol N y−1 (~45% of the total). Since the net water flow is by definition zero, this means that the N concentration must be higher in the water transferred onto the shelf than in the water flowing off the shelf. This excess N flux will dominantly occur in winter. This results from both a higher flux of water from the offshore in winter and higher concentrations of N + N in the surface waters during and soon after winter mixing. This is also the time when there was the largest increase in N + N in the deep water at 100 m on the outer shelf.

4. Implications on Biogeochemical Processes and Seasonality across the ICS and Pelagic EMS

4.1. Implication of the Total N Budget for Biogeochemical Processes on the Shelf

4.1.1. The Relative Importance of Different Sources and Sinks of N on the Shelf

The calculated external DIN input to the ICS is 0.13 Moles N M−2 y−1, which is very similar to 0.15 Moles N M−2 y−1 of total N estimated for the entire EMS [58]. In previous attempts to calculate the nutrient budget for the entire EMS [43,58], the coastal shelves were deliberately excluded from the calculation because there were no suitable studies of N fluxes onto and through EMS coastal shelves. The results of this study show that for the ICS, the external N flux per unit area is actually very similar to the rest of the EMS. The determined external flux of DIN to the ICS is roughly half the calculated flux (0.36 Moles N M−2 y−1) for the Baltic Sea [59]. The biological effects of this higher flux are drastically different with the EMS and ICS being ultra-oligotrophic [29,60], while the Baltic Sea is characterized by eutrophication and even hypoxia [59].
Atmospheric sources and riverine sources to the ICS are approximately similar in magnitude at ~30% each of the total N external input. This is not the case for many other systems. In the Baltic Sea, 70% of the N supplied comes from riverine input with 30% from atmospheric sources [61]. Pätsch and Kühn (2008) [62] estimated the atmospheric source to the North Sea was 35–50% of the riverine sources. Artioli et al. (2008) [59], using modelled data, calculated that the contemporary external N input to coastal shelves was dominantly from river inputs compared with the atmospheric inputs: 92% for the Northern Adriatic, 78% for the coastal North Sea and 97% for the NW Shelf of the Black Sea, with atmospheric sources constituting the remainder.
In Europe, the input of mainly anthropogenic nutrients into rivers and thus into coastal regions, is relatively higher than the calculated percentage of riverine input to the ICS because in Europe, the continuous flow of river water is used as the medium to discharge wastewater, which is diluted sufficiently to be acceptable downstream. By contrast, the natural water which used to flow into the streams of Israel (and similar other countries around the basin) is used almost entirely for domestic and agricultural supply with very little remaining net flow. In addition, since the Israeli stream estuaries are often tourist locations and the amount of wastewater discharge is limited, the net N flux to the coast is relatively low [52]. Thus, the riverine flux is relatively lower compared with other areas of Europe. An exception to this was the Kishon river, which for many years was effectively a chemical sewer for the waste from the chemical industry of Haifa until the discharges were drastically reduced mainly between 1994 and 2000 [63,64].
Another difference between the temperate coastal shelves of Europe and the ICS is that there is a net export of N to the offshore pelagic sea from the northern Adriatic, the North Sea, and the NW shelf of the Black sea [59], in contrast to the ICS, where there was a net import of DIN from offshore. These differences are likely due to the contrasting physical circulation patterns, which is estuarine of the European coastal shelves, with fresher surface water flowing out, carrying both externally supplied nutrients and nutrients upwelled onto the shelf, while the circulation on the ICS is anti-estuarine, with dominantly surface waters flowing onto the shelf and downwelling before flowing off the shelf.
Other land-based sources of N to the shelf are relatively minor. In particular, although SGD can be an important source in certain local areas, its overall contribution to the N budget of the ICS is rather small (2–11%) of the total external sources. This is also typically true for the EMS, since the net flux of N through the Straits of Sicily without SGD is in balance at 180 × 109 Moles N y−1 [43], and thus SGD cannot be at the higher range of the estimate (1500 × 109 Moles N y−1) to the EMS presented by [45].

4.1.2. Why Is the Seasonality of Nutrient Dynamics on the ICS Similar to the Dynamics in the Pelagic?

The seasonality of the EMS pelagic system is driven mainly by deep mixing during winter storms bringing nutrients up from below the nutricline with lesser inputs from atmospheric sources, which are also higher in winter and eddy diffusion across the nutricline [7,39]. In 2018–2019, more than 60% of the total N input came from winter mixing of N from below the nutricline, while 57% of the atmospheric input came between November and January (25% of the year). In the pelagic system, during spring and summer, nitrate is gradually lost by phytoplankton uptake and subsequent sedimentation and/or excretion by zooplankton below the nutricline [29].
Although the flux of nutrients into the water column on the shelf is also higher in winter, the seasonality of different sources is less well known and more complex. Physical oceanographic data obtained at a 135 m station off the Israeli coast showed that advection from offshore is an important process for this system [65]. The advected water onto the shelf carries a similar nutrient signal as the pelagic waters, which are relatively nitrate-rich in winter, with a decreasing concentration and, hence, lower advected flux of N (mainly nitrate) in summer. The other external input of nutrients, particularly nitrate, to the ICS are also higher in winter. The atmospheric N flux to the ICS (like the pelagic) is higher in winter compared with summer, mainly because of rainfall, which only occurs in winter in a Mediterranean climate. The normal flow of the streams during the year is low with occasional periods of winter floods with much greater volume and nutrient flux [54]. Both SGD and domestic waste discharge are likely to be somewhat higher in winter, though there is no direct data available to confirm this. However, the inputs of nutrients to the ICS are more variable in both time and space than deep winter mixing offshore, which may partially explain why the primary productivity is patchier on the ICS (e.g., Figure 2 and Figure S5).

5. Conclusions

Despite the direct and indirect external sources of N to the ICS, overall the trophic status is oligotrophic and similar to that of the offshore system [29]. The unusual oligotrophic status of the ICS compared with coastal shelves in more temperate regions is driven to a considerable extent by the same anti-estuarine circulation, which causes the entire EMS to be ultra-oligotrophic, i.e., there is very little freshwater flow from the land; thus, in contrast to coastal shelves in many temperate regions, the net physical oceanographic flow is relatively nutrient depleted, and high salinity surface waters flows onto the shelf, become increasingly saline (especially during the hot dry summer) and then downwelling and flow offshore.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/w16182585/s1, Figure S1: Physical structure of water column at THEMO stations; Figure S2: Physical structure of water column at MMT; Figure S3: Dissolved inorganic phosphorus and nitrate and nitrite distribution at THEMO stations; Figure S4: Dissolved inorganic phosphorus and nitrate and nitrite distribution at MMT; Figure S5: Primary productivity at THEMO stations; Table S1: Locations of sampling stations used in this study; Table S2: Annual nutrient flux from Israeli streams to the sea as determined by IOLR (References [5,7,34,53] are cited in the Supplementary Materials).

Author Contributions

Conceptualization, M.D.K.; formal analysis, T.B.E. and A.T. and Y.S.; investigation, T.B.E. and A.T. and Y.S.; resources, M.D.K. and I.B.-F.; data curation, T.B.E. and A.T.; writing—original draft preparation, M.D.K. and T.B.E.; writing—review and editing, M.D.K. and I.B.-F. and Y.S. and A.T.; visualization, T.B.E.; supervision, M.D.K. and D.T. and I.B.-F.; funding acquisition, M.D.K. and D.T. and I.B.-F. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

The original data presented in this study are openly available in the Morris Kahn Marine Research Station database website at https://med-lter.haifa.ac.il/data-base/ (accessed on 1 January 2021).

Acknowledgments

The study is part of the Ph.D. work of Tal Ben Ezra. This study was conducted with support during data collection and analysis from the staff at the Morris Kahn Marine Research Station. We acknowledge the support from the Helmholtz-funded International Laboratory: The Eastern Mediterranean Sea Centre—An Early-Warning Model System for our Future Oceans: EMS Future Ocean REsearch (EMS FORE). The manuscript was submitted under the umbrella of ocean@leeds.

Conflicts of Interest

The authors declare no conflicts of interest.

Appendix A

Definition of the Israeli Coastal Shelf: The Mediterranean shoreline of Israel is made up mainly of Nile sand eroded from the delta and transported by long-shore drift. Offshore, there is a rather wide continental shelf with gradually decreasing grain size from the coarse sand near the shoreline to silt at the shelf break, which is generally at a depth of 100–130 m [55]. Berman and co-workers, in their studies of biogeochemical processes on the ICS, measured transects to a depth of 150 m [15,16,28]. Haifa University, in collaboration with Texas A&M University, has recently set up two ocean observatory systems, one coastal and the other pelagic. THEMO1 is located off the northern Israeli coast at 130 m, while THEMO2 is located at 1450 m (Figure 1). In this study, we consider the monthly sampling at THEMO1 (130 m) to represent the outer coastal shelf, and the transects from 10 to 100 m off the coast from Maagan Michael (MMT) to represent the rest of the ICS (Figure 1).

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Water 16 02585 g001
Figure 1. (a) S.E. Levantine basin of the Eastern Mediterranean Sea. (b) Location of sampling stations across the Israeli coastal shelf in the S.E. Levantine basin. Station THEMO1, the outer coastal shelf station, was at a bottom depth of 135 m, while THEMO2, the offshore station, was at a bottom depth of 1450 m. The ICS was sampled in a series of transects from 10 m to 100 m bottom depth off the coast of Maagan Michael. (c) Shows in gray stripes the extent of the Israeli coastal shelf to 130 m, which we have used to carry out an annual nutrient (N) budget. It has an area of 2558 × 106 m2 and a length of 199 km. The Israeli coast is the boundary to the right of the sampling box area.
Figure 1. (a) S.E. Levantine basin of the Eastern Mediterranean Sea. (b) Location of sampling stations across the Israeli coastal shelf in the S.E. Levantine basin. Station THEMO1, the outer coastal shelf station, was at a bottom depth of 135 m, while THEMO2, the offshore station, was at a bottom depth of 1450 m. The ICS was sampled in a series of transects from 10 m to 100 m bottom depth off the coast of Maagan Michael. (c) Shows in gray stripes the extent of the Israeli coastal shelf to 130 m, which we have used to carry out an annual nutrient (N) budget. It has an area of 2558 × 106 m2 and a length of 199 km. The Israeli coast is the boundary to the right of the sampling box area.
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Water 16 02585 g002
Figure 2. Seasonal changes in satellite-derived temperature (blue) and Chlorophyll-a at the outer coastal station (135 m; THEMO1) and, for comparison, at the pelagic (1450 m; THEMO2) station over a period of three years. The sampling period of 2018–2019 is marked as light brown shading (reproduced from Ben Ezra et al., 2023) [29].
Figure 2. Seasonal changes in satellite-derived temperature (blue) and Chlorophyll-a at the outer coastal station (135 m; THEMO1) and, for comparison, at the pelagic (1450 m; THEMO2) station over a period of three years. The sampling period of 2018–2019 is marked as light brown shading (reproduced from Ben Ezra et al., 2023) [29].
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Ben Ezra, T.; Tsemel, A.; Suari, Y.; Berman-Frank, I.; Tchernov, D.; Krom, M.D. Determining the Fluxes and Relative Importance of Different External Sources and Sinks of Nitrogen to the Israeli Coastal Shelf, a Potentially Vulnerable Ecosystem. Water 2024, 16, 2585. https://doi.org/10.3390/w16182585

AMA Style

Ben Ezra T, Tsemel A, Suari Y, Berman-Frank I, Tchernov D, Krom MD. Determining the Fluxes and Relative Importance of Different External Sources and Sinks of Nitrogen to the Israeli Coastal Shelf, a Potentially Vulnerable Ecosystem. Water. 2024; 16(18):2585. https://doi.org/10.3390/w16182585

Chicago/Turabian Style

Ben Ezra, Tal, Anat Tsemel, Yair Suari, Ilana Berman-Frank, Danny Tchernov, and Michael David Krom. 2024. "Determining the Fluxes and Relative Importance of Different External Sources and Sinks of Nitrogen to the Israeli Coastal Shelf, a Potentially Vulnerable Ecosystem" Water 16, no. 18: 2585. https://doi.org/10.3390/w16182585

APA Style

Ben Ezra, T., Tsemel, A., Suari, Y., Berman-Frank, I., Tchernov, D., & Krom, M. D. (2024). Determining the Fluxes and Relative Importance of Different External Sources and Sinks of Nitrogen to the Israeli Coastal Shelf, a Potentially Vulnerable Ecosystem. Water, 16(18), 2585. https://doi.org/10.3390/w16182585

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