Trophic Ecology of Deep-Sea Megafauna in the Ultra-Oligotrophic Southeastern Mediterranean Sea

Introduction

Deep-sea ecosystems cover much of the oceans seafloor and play a major role in large-scale biogeochemical cycles (Walsh, 1991; Drazen and Sutton, 2017). They provide ecosystem services that are important to humans, including carbon sequestration, nutrient recycling and burial, waste accumulation and fisheries production (Danovaro et al., 2008; Mengerink et al., 2014; Thurber et al., 2014). Recent studies have shown that an increasing number of stressors, including climate change (warming), deoxygenation, ocean acidification, as well as, overfishing, and natural resource extraction (e.g., Stramma et al., 2008; Yasuhara et al., 2008; Stramma et al., 2010; Helm et al., 2011; Tecchio et al., 2015) are expanding into deep environments, thus threatening the diversity and stability of deep-sea ecosystems. Consequently, studying the status of deep-sea communities and describing deep-sea ecosystem structures are currently gaining more and more attention.

Continental slopes account for ~11% of the total ocean floor (Ramirez-Llodra et al., 2010), connecting the shallow shelf productive areas with the abyssal plains along steep seabed gradients. Covering large bathymetric ranges (~ 200 – 2000 m), these dynamic habitats exhibit strong spatial differences in temperature, salinity, nutrient concentrations, sedimentological features, like organic carbon content, and consequently, in habitat suitability (Koslow, 1993; Gordon et al., 1995; Neat et al., 2008; Bergstad, 2013; Pajuelo et al., 2016). Bathyal habitats also support diverse deep-sea fauna (Gordon and Swan, 1997; Kelly et al., 1998; Menezes et al., 2006; Neat et al., 2008), even in ultra-oligotrophic basins, such as the easternmost Mediterranean Sea (Goren et al., 2008). In deep-sea benthic ecosystems, fish can play key ecological and biogeochemical roles (Drazen and Sutton, 2017) by regulating nutrient limitation and zooplankton populations (Hopkins and Gartner, 1992; Pakhomov et al., 1996).

Deep-sea benthic ecosystems largely rely on particulate organic matter (POM) that passively sinks from the surface waters or by lateral transport as a primary source of nutrients (Tecchio et al., 2013). Marine organisms that carry out vertical diel migrations through the water column (Trueman et al., 2014) and occasional sink of large animal carcasses is another important food source to deep-sea ecosystems (Smith and Baco, 2003). Each of these primary food sources may carry a distinct isotopic signature that reflects its origin, resulting from different chemo-physical processes. Thus, by knowing the isotopic composition of the food sources that fuels a specific food web, it is possible to reconstruct the trophic structure and dynamics of specific habitats (Post, 2002).

Stable isotope analysis (SIA) has been used successfully to study trophic level, important prey types, and trophic niche breadth in deep-sea ecosystems (e.g., Boyle et al., 2012; Shipley et al., 2017a). Nitrogen stable-isotope composition (δ¹⁵N) is used to determine the trophic position of an animal, as it preferentially fractionates as a function of its diet, where the heavy isotopes are retained in the consumers in respect to their prey by 2 – 4‰ (Post, 2002). Carbon stable isotopes (δ¹³C) fractionate much less with each trophic step (<1‰), but can be effectively used to infer basal sources of carbon. Moreover, SIA provides an integrated view of an organism’s diet over time-scales relevant to tissue turnover rates rather than digestion rates (Peterson and Fry, 1987; Post, 2002), thereby providing estimates of the trophic position of an organism within a specific food web.

Knowledge of food web structure and dynamics is key to our understanding of ecological communities and their functioning (Polis and Strong, 1996; Winemiller and Polis, 1996). This fundamental information is, however, lacking in many oceanographic regions, including the Southeastern Mediterranean Sea (hereafter, SEMS) (Parzanini et al., 2019) — one of the most oligotrophic, nutrient-impoverished marginal basin, worldwide (Kress et al., 2014). This basin exhibits extremely low open water primary production (~60 g C m⁻² y⁻¹) merely half of that measured in other oligotrophic areas of the ocean (Hazan et al., 2018), resulting in limited energy sources to its deep-sea habitats (Rahav et al., 2019). The greatest fraction of particulate flux to the SEMS deep-seafloor is transported laterally from the continental shelf at intermediate depths (Katz et al., 2020) and is considered to be highly refractory (Rubin-Blum et al., 2022). The SEMS, therefore, provides a miniature model of processes occurring in vast oligotrophic marginal seas, an ideal location to study food web structure and functioning under sever nutrient limitation. Furthermore, the SEMS is one of the regions where sea surface temperatures are rising at the fastest rates under recent climate changes (Sisma-Ventura et al., 2014; Ozer et al., 2017) and is one of most vulnerable marine regions to species invasions (Rilov and Galil, 2009), which have been also reported from deep-sea habitats (Galil et al., 2019). Understanding deep-sea community structure and functioning is of prime importance for developing better predictions regarding the ecological effects of future climate change. The main objective of this study was to elucidate the energy sources that sustain the deep-sea food-webs of the SEMS.

To date, much of the research describing the trophic ecology of the Eastern Mediterranean Sea has focused on zooplankton groups (Koppelmann et al., 2003; Koppelmann et al., 2009; Hannides et al., 2015; Protopapa et al., 2019), shallow rocky reefs (Fanelli et al., 2015), and on anthropogenically-influenced coastal environments (Grossowicz et al., 2019), while less attention has been paid to deep-sea fishes and crustaceans that occupy higher trophic levels. Here we used bulk carbon and nitrogen stable isotopes (δ¹³C and δ¹⁵N) of demersal and bathybenthic fishes and crustaceans from the southeast Mediterranean continental slope and rise. We explored potential factors that may explain the variability in stable isotope values across species. These data offer insights into the carbon sources and trophic complexity of deep-sea ecosystems in oligotrophic marginal seas.

Materials and Methods

Study Sites and Sampling Design

Sampling campaigns were conducted in the course of three oceanographic cruises during 2017 – 2019, as part of the national deep-water monitoring program of the Israeli Mediterranean Sea performed by Israel Oceanographic and Limnological Research (IOLR). Sampling sites were divided to three major benthic habitats: (1) the end of the continental shelf, with an average depth of 200 m; (2) the continental slope with depth range of 500 – 600 m; and (3) the deep bathyal plateau (continental rise) with depth range of 1000 – 1400 m (Figure 1). Specimens were collected onboard the R/V Bat-Galim, using a semi-balloon trawl net with an opening of eight meters and mesh size of 10 mm. Once the trawls were retrieved, specimens were sorted, enumerated, weighted and visually identified to species level. The total length (cm) of each specimen was recorded. Specimens for SIA were selected and frozen whole at –20°C until processed at the IOLR.

FIGURE 1

Figure 1 Map of sampling sites in the SEMS. The locations of POM samples are presented in black circles, and locations of fishes and crustaceans by trawl net are presented in black lines.

POM was collected during three research expeditions in winter 2018, summer 2020, and winter 2021, across the shelf, slope and rise of the SEMS (Figure 1 and Table 1). POM samples were collected throughout the water column using 8-L Niskin bottles. Water samples were then filtered on pre-combusted 47-mm glass fiber filters (Whatman) in duplicates at low pressure and dried at 60°C for 24 h prior to isotope analysis.

TABLE 1

Table 1 Sample descriptions and bulk δ¹³C and δ¹⁵N isotope data (mean ± SD).

Stable Isotopes Analysis

SIA was conducted on 86 fish and 46 crustacean specimens as well as 77 POM samples (Table 1). White muscle tissue for SIA was dissected from the dorsal musculature of fishes and from the abdominal segment of the crustaceans. Samples were rinsed with deionized water, frozen, and lyophilized for 48 h. Freeze-dried samples were homogenized using a mortar and pestle, weighed, and shipped to the Stable Isotope Facility at Cornell University (USA) for SIA analysis. The isotopic composition of organic carbon and nitrogen was determined by the analysis of CO₂ and N₂ continuous-flow produced by combustion on a Carlo Erba NC2500 connected on-line to a DeltaV isotope ratio mass spectrometer coupled with a ConFlo III interface.

Measured stable isotope ratios are reported in the δ-notation, i.e., as the deviation in per mill (‰) from the international standards:

$${\delta }_{Sample=\left(\frac{R_{Sample}}{R_{s\tan dard}}-1\right)\times {10}^3}$$

where, R represents the ¹⁵N/¹⁴N or ¹³C/¹²C ratio. Stable isotope data are expressed relative to international standards of Vienna PeeDee belemnite and atmospheric N₂ for carbon and nitrogen, respectively. The analytical precision for the in-house standard was ± 0.04‰ [1σ] for both δ¹³C and δ¹⁵N. The C/N ratios of fishes and crustaceans in this study were low (species mean C/N ranged between 2.33 – 4.48; where in 97% of individuals C/N< 4.0, see Supplementary Figures 1, 2), suggesting that lipids did not significantly affect the δ¹³C interpretation (Post et al., 2007). Therefore, all data analyses were performed on uncorrected δ¹³C values. To determine if the isotopic signatures of POM samples changed with depth, we used collection depth to classify POM samples as epipelagic (0 – 200 m), mesopelagic (200 – 800 m), or bathypelagic (>800 m).

Data Analysis

We estimated and compared modal trophic position (TP) and 95% credibility interval (i.e., 95% of modeled estimates of TP) for each species using the R package tRophicPosition (version 0.7.7; Quezada-Romegialli et al., 2018) according to the following equation:

$${\text{δ}}^{15}{N}_c={\text{δ}}^{15}{N}_b+\Delta N\left(TP-\text{λ}\right)$$

Where δ¹⁵N_c corresponds to the nitrogen stable isotope value from the consumer that the TP is estimated, δ¹⁵N_b represents the nitrogen stable isotope value of the baseline consumer; ΔN corresponds to the trophic discrimination factor (TDF) for nitrogen and λ the TP from baseline consumer. We used the average δ¹⁵N in zooplankton (3.9 ± 1.8‰) measured by Koppelmann et al. (2009) in the Eastern Levantine Basin as the baseline ( λ=2) using the oneBaseline model option and applied the trophic discrimination factor &xutri;^15N of 3.15 ± 1.28‰, which was previously used to calculate the trophic level of meso- and bathypelagic fish (Valls et al., 2014; Richards et al., 2018).

Least-squares linear regression analysis was conducted for each species to explore the relationship between fish length and the δ¹³C and δ¹⁵N values. Spatial variation in δ¹³C and δ¹⁵N of both fishes and crustaceans was investigated using least-squares linear regression between stable isotopic values and depth. All statistical analyses were performed in R v. 4.0.5 (R Core Team, 2020).The trophic breadth of each species (n ≥5) and trophic similarity among species were assessed by calculating Standard Ellipse Area (SEA) using the R package SIBER v. 2.1.6 (Jackson et al., 2011; Jackson and Parnell, 2021). Size-corrected SEAs (SEAc) and Bayesian estimate of SEAs (SEA_B) were calculated for each species, which adjusts for underestimation of ellipse area at small sample sizes and allows for inter-study comparison of ellipse sizes (Jackson et al., 2011). Fish and crustacean community metrics were calculated based on Layman et al. (2007).

Bayesian mixing models were applied using R package MixSIAR v. 3.1.12 (Stock et al., 2018; Stock et al., 2021) to estimate the relative contribution of shelf, slope, and deep-basin surface vs. bottom POM to each species. These models are sensitive to variable discrimination factors (Bond and Diamond, 2011; Olin et al., 2013), which may be influenced by diet (Caut et al., 2009), tissue type (Malpica-Cruz et al., 2012), temperature (Britton and Busst, 2018), and species-specific metabolic rates (Pecquerie et al., 2010). Since the modeled species are predators and do not feed directly on POM, the total trophic fractionation per species was calculated as follows:

$$TE{F}_{species}=TE{F}_{TL}\times \left(T{L}_{species}-T{L}_{source}\right)$$

Where, TEF_species is the total trophic fractionation in the consumer relative to its basal source, TEF_TL is the mean enrichment per trophic level, TL_species is the trophic position of the consumer, and TL_source is the trophic position of the source. To evaluate the contribution of the basal sources to the studied species, we have assigned to POM TL_source =1.0, since POM-δ¹³C values are compatible of the lowest size fraction (pico-phytoplankton) measured in the Western Mediterranean Sea (Hunt et al., 2017).

To calculate the enrichment factors from POM to the top consumers included in this study, we have used two discrimination factor levels — from POM to zooplankton, and from zooplankton to the studied species. Based on average Δ¹³C and Δ¹⁵N between POM to zooplankton measured in the Western Mediterranean Sea, we set the basal enrichment factors of 1.40 ± 1.15‰ for δ¹⁵N and 4.10 ± 1.63‰ for δ¹³C (Hunt et al., 2017). The enrichment from zooplankton to the studied species was done using discrimination factors of 3.15 ± 1.28‰ for δ¹⁵N and 0.97 ± 1.08‰ for δ¹³C (Sweeting et al., 2007), which have been previously used to study the trophic structure of meso- and bathypelagic fishes in the Gulf of Mexico (Richards et al., 2018) and in the Western Mediterranean Sea (Valls et al., 2014).

Each model was run with identical parameters (number of MCMC chains = 3; chain length = 300000; burn in = 200000; thin = 100), and model convergence was determined using Gelman-Rubin and Geweke diagnostic tests (Stock et al., 2018).

Results

Stable Isotopes

Species-specific mean δ¹³C values ranged from -20.85 to -16.89‰ for fish and from -18.54 to -16.38‰ for crustaceans. Fish mean δ¹³C values differed by 3.96‰, separating the most depleted (Macrorhamphosus scolopax: -20.85 ± 0.46‰, sampling depth of 200 m) and the most enriched species (Centrophorus granulosus and Conger conger: -16.89 and -16.57‰, respectively, sampling depth of ~1000m) (Table 1 and Figure 2). Crustaceans species-specific mean δ¹³C varied by 2.18‰, where the most depleted species was Aristeus antennatus (-18.54 ± 0.17‰, sampling depth of 600 m) and the most enriched species was Polycheles typhlops (-16.38 ± 0.21‰, sampling depth of ~1400 m). Species-specific differences in δ¹³C and δ¹⁵N were significant for both fish (MANOVA, F_13,144 = 19.73, p< 0.001) and crustaceans (MANOVA, F_5,78 = 14.62, p< 0.001).

FIGURE 2

Figure 2 Isotope biplot of δ¹³C and δ¹⁵N values of decapod crustaceans (circles) and fishes (triangles), and POM (squares) from the shelf (200-250m), slope (400-800m) and deep-basin (1000-1400m) of the Southeastern Mediterranean Sea. Data points represent means and error bars represent ± SD.

Species-specific mean δ¹⁵N values varied from 7.91 ± 0.36‰ (M. scolopax, 200 m depth) to 11.36 ± 0.39‰ (Nezumia sp., 1100 m depth) in fish and from 5.96 ± 0.24‰ (Plesionika edwardsii; 200 m depth) to 7.73 ± 0.46‰ (Aristeus antennatus; 1100 – 1400 m depth) in crustaceans. Fish mean δ¹⁵N values positively correlated with the δ¹³C values (r² = 0.6, p< 0.001, Figure 2 and Supplementary Figure 1) and varied among species (ANOVA, F_13,72 = 24.22, p< 0.001). Crustaceans, however, did not show this correlation between δ¹⁵N and δ¹³C (r² = 0.002, p > 0.05, Figure 2 and Supplementary Figure 2), observed in fish from similar depths. Due to limited spatial coverage within each species (the specimens of most species were sampled from the same depth), spatial variation could not be tested within each species, and therefore, spatial trends were tested by addressing all fish species together. Fish δ¹³C values positively varied with bottom depth (r² = 0.42; P< 0.01, Figure 3), where the most enriched samples were found at the continental rise (> 1000 m) and the most depleted at the shallow slope (200 m) at the edge of the shelf. This pattern was less clear in the case of fish δ¹⁵N values (Figure 4), where species-specific mean values seem more variable in the continental rise (> 1000 m). Crustaceans mean δ¹⁵N values positively correlated with depth (r² = 0.76, p = 0.053, Figure 4), while their mean δ¹³C values showed no such correlation (Figure 3).

FIGURE 3

Figure 3 Correlations between mean δ¹³C (‰) and depth (m) in Levantine deep-sea decapod crustaceans (left) and fishes (right). Dash lines represent Least-squares regression line.

FIGURE 4

Figure 4 Correlations between mean δ¹⁵N (‰) and depth (m) in Levantine deep-sea decapod crustaceans (left) and fishes (right). Dash lines represent Least-squares regression line.

POM collected from depths ranging from 0 to 1135 m over the continental shelf, slope and rise exhibited a wide δ¹³C range (-27.72 to -21.36‰) and δ¹⁵N range (-3.25 to 12.76‰), with POM samples generally becoming more enriched in ¹⁵N and more depleted in ¹³C at bottom depths (Figure 5). Significant differences in POM δ¹³C and δ¹⁵N among the zones and depths were observed (MANOVA, F_5,98 = 7.15, p< 0.001). POM-δ¹³C and C/N ratio exhibited a significant negative correlation (Pearson correlation, r = -0.566, p< 0.001, Supplementary Figure 3), which was not observed in POM-δ¹⁵N and C/N ratio.

FIGURE 5

Figure 5 Boxplots showing POM-δ¹⁵N (‰), POM-δ¹³C (‰) and POM-C/N ratios collected from the surface and bottom of the continental shelf (200-250m), slope (400-800m) and deep-basin (1100-1400m) in the Southeastern Mediterranean Sea during 2018-2021.

Trophic Position Estimates

We used the average δ¹⁵N value of Eastern Levantine zooplankton (3.9 ± 1.8‰) obtained from Koppelmann et al. (2009) as a baseline (λ=2.0) for estimating species-specific TL. Based on the low δ¹⁵N values of zooplankton in the eastern Mediterranean, it was assumed that the primary food source, namely smaller zooplankton, phytoplankton and particles have a δ¹⁵N value around zero (Koppelmann et al., 2009). Large mesozooplankton (333-µm mesh size, upper water column) δ¹⁵N values in the EMS showed an enrichment trend across a west-east transect (SE Crete mean δ¹⁵N value ~2.0‰ and SE Cyprus mean δ¹⁵N value ~4.0‰, Koppelmann et al., 2009). Using these data to set the baseline, fish modal TL ranged from 3.17 (M. scolopax; 200 m depth) to 4.19 (C. conger; 1000 m depth), while the average modal TL of all fish species was 3.62 ± 0.31 (Figure 6). Crustaceans- δ¹⁵N values yielded modal TLs between 2.66 (P. edwardsii; 200-600 m depth) and 3.11 (A. antennatus; 600 – 1400 m), with an average of 2.94 ± 0.18 (Figure 6).

FIGURE 6

Figure 6 Trophic level (TL) Bayesian estimates based on δ¹⁵N data of deep-sea Levantine decapod crustacean (orange, n=6) and fish (blue, n=14) species using zooplankton of the Eastern Levantine Basin (Koppelmann et al., 2009) as an isotopic baseline. Error bars denote 95% confidence intervals.

Of the species examined, only few enabled an estimation of ontogenetic effect (Figure 7). This is due to the low range of body size within individual species that were sampled in this study. Nevertheless, the crustaceans A. eximia (r² = 0.82; p< 0.001) and P. edwardsii (r² = 0.72; p< 0.05) exhibited a positive relationship between length and δ¹⁵N values. Size and δ¹³C values did not yield significant correlations. Positive relationship between size and δ¹⁵N values was also observed for the fish D. macrophthalmus (r² = 0.59; p< 0.05).

FIGURE 7

Figure 7 Least-squares regression analysis between total length (cm) and δ¹⁵N values in the decapod crustaceans A. eximia (n=10) and P. edwardsii (n=6), and the fish D. macrophthalmus (n=7).

Trophic Niche Breadth

Isotopic niche breadth, calculated using size-corrected standardized ellipse area SEA_C (Supplementary Table 1 and Figure 8), was largest for the fish collected from the shallow continental slope C. caelorhincus (SEA_C = 2.04), D. macrophthalmus (SEA_C = 0.94) and M. scolopax (SEA_C = 0.66), and for the shrimps A. antennatus (SEA_C = 0.63) and A. eximia (SEA_C = 0.56), both opportunistic carnivores. The smallest isotopic niche breadth belonged to the deep-water rose shrimp P. longirostris (SEA_C = 0.07). Fish and crustacean assemblage metrics (Table 2A) showed a contrasting trend of isotopic niche size with depth, where fish isotopic niche size was largest in the shelf assemblage (SEA_C = 1.81) and crustaceans isotopic niche size was largest in the deep assemblage (SEA_C = 1.43). As a trophic guild (Table 2B), the fish showed higher convex hull area (TA = 7.37) than the crustaceans (TA = 0.81), indicating a larger trophic community width (Layman et al., 2007).

FIGURE 8

Figure 8 Trophic niche breadth of Levantine fishes and decapod crustaceans (n≥5) estimated by size-corrected standard ellipse area (SEA_C) boxplots (showing 95, 75 and 50% credibility intervals). Black circles represent means; red x symbols represent the maximum likelihood estimates of SEA. Ae , Acanthephyra eximia; Pe , Plesionika edwardsii; Aa , Aristeus antennatus; Pl , Parapenaeus longirostris; Ns , Nezumia sp.; Hd , Helicolenus dactylopterus; Hm , Hoplostethus mediterraneus; Cc , Coelorinchus caelorhincus; Dm , Dentex macrophthalmus; Ms , Macroramphosus scolopax; Lc , Lepidotrigla cavillone; Se , Scorpaena elongata.

TABLE 2

Table 2 Metrics for estimating assemblage and community (trophic guild) isotopic niche size in fish and decapod crustaceans from the Levantine deep-sea.

Bayesian Mixing Models

The results of the mixing models indicated variable sources sustaining the deep-sea fish and crustacean consumers included in this study (Figure 9). The contribution of deep bathypelagic POM was highest in the decapod crustaceans A. eximia (74.8 ± 10.8%), A. antennatus (63.3 ± 9.5%) and P. typhlops (43.1 ± 1.7%), and in the rattail fish Nezumia sp. (66.3 ± 8.0%). The contribution of pelagic POM to the deep bathypelagic fauna spanned 26 ± 4%, increasing in the slope, varying between 24 and 61% (including both the shelf and slope surface POM). Whereas, the models showed an increased contribution of benthic POM to the deep-sea fauna (Figures 9G–O). For example, the benthic contribution to the red shrimp A. antennatus was 20 ± 18.9% in the slope (Figure 9A) versus 63.3 ± 9.5% in the rise (Figure 9I). Therefore, the model results support a shift from pelagic to benthic source with increasing depth, i.e. with distance from shore.

FIGURE 9

Figure 9 Estimated relative contributions (%) of POM collected from the surface and bottom depths of the continental slope and rise (400-800, 1100-1400 m, respectively) to Levantine fish and decapod crustaceans, based on Bayesian mixing models. (A–F). Species collected from the continental slope (400-600m). (G–O). Species collected from the continental rise (1000-1400m). Bars represent mean contributions and error bars represent ± SD.

Discussion

This is the first attempt to elucidate the trophic ecology of deep-sea fish and crustacean species in the SEMS. The knowledge gained in this study provides insights into the main energy sources sustaining deep-sea food webs in one of the most oligotrophic, nutrient-improvised marine basins, worldwide. However, insights gained in this study are not limited to the SEMS alone, and can be relevant to many oligotrophic basins with limited carbon and nutrient sources.

Our δ¹³C and δ¹⁵N values varied across fish species and as a function of depth, suggesting that depth and diet are controlling the trophic positions inferred from our stable isotope data. As expected, top predators such as the European conger eel C. conger, occupied the highest trophic position. The rattail Nezumia sp., a small macrourid fish that was collected from similar depths of >1000 m, yielded similar high δ¹⁵N values. Both species occupied a maximum trophic position of 4.14 – 4.19 (modal TL). Polunin et al. (2001) found similar trophic position of 4.4 for both the shark Centroscymnus coelolepsis and Nezumia aequalis in the continental slope of the Balearic Islands. High δ¹⁵N values of Nezumia (11.09 ± 0.58‰ and 11.31‰) were also recorded by Fanelli and Cartes (2010) in the Archipelago of Cabrera (Algerian Basin) and by Papiol et al. (2013) in the Balearic Islands (Catalan Sea, West Mediterranean), respectively, and were attributed to the suprabenthic crustaceans and polychaetes that constitute the diet of this macrourid. Our TL data also agree well with that of benthic carnivorous fish from Bay of Banyuls-sur-Mer (northwest Mediterranean, France; Carlier et al., 2007). Among the fish, the lowest trophic position (3.17) was found in the snipefish M. scolopax, which feeds on hyperbenthic demersal zooplankton during daytime (Carpentieri et al., 2016). This was also inferred from the results of the mixing models, indicating a relatively high contribution of mesopelagic POM to the diet of M. scolopax. Relatively to the fish, the bathybenthic crustaceans measured in this study occupied lower trophic positions — between 2.66 and 3.11, in agreement with the TL of deep benthic invertebrates of the Western Mediterranean (Carlier et al., 2007; Zorica et al., 2021).

The δ¹⁵N values of the deep-sea decapods A. eximia and P. edwardsii increased significantly with length indicating an ontogenetic effect. Such trend was found in A. eximia from the Catalan Sea (Western Mediterranean), where gut content analysis indicated a dietary shift from scavenging and detritivory in small individuals to active predation in larger individuals (Cartes, 1993). Smaller sized A. eximia were suggested to be better adapted to regions where resources are scarce (Thiel, 1983; Pérès, 1985). Similar dietary preferences were observed in P. edwardsii (Cartes, 1993). The lower δ¹⁵N that we measured in the smaller individuals of these decapods may indicate a detritivorous mode of feeding (Polunin et al., 2001). We found a similar ontogenetic effect in the demersal fish D. macrophthalmus. A gut analysis of this sparid fish off Angola and Namibia (South Atlantic Ocean) supports our finding, as the smaller fish tended to feed almost exclusively on polychaetes and euphausiids, but the larger fish preferred fish prey (Kilongo et al., 2007).

In the fish species examined here, mean δ¹⁵N values spanned 3.45‰, about 1.1 TL, while in the crustacean species mean δ¹⁵N values spanned 1.77‰, about 0.6 TL (assuming trophic enrichment factor of 3.15‰). Our observed ranges of estimated trophic levels are in line with other studies examining Mediterranean (1.1 TL, Valls et al., 2014), Pacific (1.6 TL, Choy et al., 2015), and the Gulf of Mexico (0.62 TL, Richards et al., 2018). Different feeding strategies as well as different migration habits may explain wider range of δ¹⁵N (Shipley et al., 2017a; Richards et al., 2020). Despite of the reliance on similar basal production, mesopelagic fishes from the Western Mediterranean were segregated by trophic position, between 2.9 for the small bristlemouth Cyclothone braueri to 4.0 for the lanternfish Lobianchia dofleini (Valls et al., 2014), and bathyal fishes off the Balearic Islands appeared to be foraging over two to three full trophic levels (Polunin et al., 2001). Our results support a much narrower trophic range for bathyal fish and bathybenthic decapod crustaceans in the SEMS. We attribute this narrow range to the ultra-oligotrophic state of the SEMS, resulting in limited carbon sources to sustain the deep-sea food webs, reflected by a general increase of δ¹³C in fish as function of bottom depth. This pattern could be driven by a number of factors including shifting production sources, or shifts in community composition and feeding strategies, and or switching from benthic to pelagic prey (Fanelli et al., 2011; Trueman et al., 2014). For example, ¹³C became more depleted in individuals captured at greater depths in the deep-sea island slope system of the Exuma Sound, the Bahamas (Shipley et al., 2017b). Inshore-to-offshore depletion in ¹³C values were also apparent in epipelagic fishes in the northern California Current, where copepods, gelatinous zooplankton, and nekton showed a significant linear decrease in δ¹³C with distance offshore (Miller et al., 2008). Our results show a different trend of increase in fish δ¹³C as function of bottom depth, i.e., distance offshore.

The major carbon sources supporting deep-sea food webs are poorly defined, aside from oligotrophic open-ocean gyres, where sinking phytoplanktonic-POM is considered the main energy source (Shipley et al., 2017b). This was observed by a narrow range of δ¹³C in meso- and bathypelagic predatory fishes in the Gulf of Mexico, indicating an exclusive epipelagic carbon source (Richards et al., 2018). Differently, the results of our mixing-model show increased contribution of bathypelagic POM and a reduction in the epipelagic source with increasing depth, i.e. distance offshore. This pattern agrees well with the extremely low primary production and carbon flux from the surface open water of the SEMS to the deep-seafloor (Katz et al., 2020). While most of the flux to the deep seabed is transported laterally.

Indeed, the majority of carbon supporting the species examined in this study is not derived from epipelagic sources. An alternative hypothesis is that the source of carbon in the deep-sea originates from the shelf. A significant proportion of neritic-derived primary production may be transported into deep-sea systems by currents (Suchanek et al., 1985; Sanchez-Vidal et al., 2012; Efrati et al., 2013), or via lateral transport (Fahl and Nöthig, 2007), and once assimilated into the food web, more enriched ¹³C values are to be expected (Polunin et al., 2001; Fanelli et al., 2011). Katz et al. (2020) used deep-sea sediment traps in the Israeli Southeastern Mediterranean Sea and showed that lateral transport from the continental margin contributes the greatest fraction of particulate flux to the seafloor. Therefore, we suggest that lateral transport constitutes the main source of carbon to the deep-sea food web in the Southeastern Mediterranean Sea. Our mixing model results and the relative decrease of C:N ratio in fish with increasing depth, indicating lower lipid content in deep-sea fish, further support a shift from pelagic to regenerated benthic carbon sources with depth. Given that the δ¹³C of POM slightly vary between the different foraging habitats, it is likely that this shift in δ¹³C occurs in the sediments water interface, by the enhanced bacterial regeneration of organic matter. This is likely driven by the high temperatures of the SEMS deep water near the seafloor (~13-14°C), compared to much lower temperatures of ~4°C at similar depths in most oceanic basins and despite the relatively low organic content of the SEMS sediments <1% (Ogrinc et al., 2007).

Since the carbon signature of primary producers can significantly vary between macroalgae and different phytoplankton groups (Fanelli et al., 2011; Grossowicz et al., 2019), food webs that show a linear relationship between δ¹⁵N and δ¹³C values are suggestive of a single food source (Polunin et al., 2001; Carlier et al., 2007). Generally weak δ¹³C–δ¹⁵N correlations were found in deep-sea macrozooplankton and micronekton off the Catalan slope likely due to the consumption of different kinds of sinking particles (e.g. marine snow, phytodetritus). Multiple recycling of POM constituted an enrichment effect on the δ¹³C and δ¹⁵N values of deep-sea macrozooplankton and micronekton (Fanelli et al., 2011). Our results yielded significant positive correlation between fish δ¹⁵N and δ¹³C values, further supporting a single food source.

Previous studies have shown that δ¹³C fractionates less than 1.0‰ for each trophic position. The Δ¹³C between the mean water column POM-δ¹³C (-24.13 ± 1.56‰) and fish/crustaceans δ¹³C (-18.10 ± 0.93‰) of the SEMS amounted to 6.04‰ (equal to at least six trophic positions), and therefore, cannot be attributed to trophic enrichment alone, but could be partly linked to the regeneration of benthic carbon sources, which may be relevant for detritus feeding animals, including all of the crustacean and some of the fish studied here Moreover, our δ¹³C-C/N data support the potential effect of microbially degraded phyto-detritus resulting in higher isotopic values of nitrogen and carbon in deep benthic food webs compared with pelagic food webs (Papiol et al., 2013; Romero-Romero et al., 2021).

Deep-sea ecosystems are subjected to exacerbating anthropogenic stressors, including overfishing, chemical pollution, mining, dumping, litter, plastics, and climate change (Davies et al., 2007). In oligotrophic environments such as the ultra-oligotrophic SEMS, deep-sea ecosystems are further vulnerable to reduced food availability (Kröncke et al., 2003). Regeneration of benthic carbon sources, supported by this study, provides oligotrophic deep-sea food webs with a greater ability to endure carbon limitation. Benthic carbon sources originating in lateral transport from the shallow shelf to the deep-sea, as indicated here, may hold important implications for marine spatial planning and the establishment of Marine Protected Areas (MPAs) in the SEMS exclusive economic zones (EEZ), promoting the extension of protected areas from the shelf to the deep-sea in a continuum rather than the establishment of MPAs that are disconnected from the continental shelf and slope. Furthermore, lateral transport from the shelf to the deep sea may carry detrimental implications to the ecosystem via pollutant accumulation and biomagnification (Liu et al., 2020). This is particularly important in marginal seas that are prone to anthropogenic pollution (Kim et al., 2019; Shoham-Frider et al., 2020). Continuous studies should be undertaken to further unveil the implications of lateral transport and benthic carbon regeneration to deep-sea food webs.

Data Availability Statement

The datasets presented in this study can be found in: Guy-Haim, Tamar; Stern, Nir; Sisma-Ventura, Guy (2022): Bulk stable isotopes of deep sea fish and crustaceans from the Southeastern Mediterranean Sea. PANGAEA, https://doi.org/10.1594/PANGAEA.945321.

Ethics Statement

The animal study was reviewed and approved by Israel National Institute of Oceanography Ethics Committee.

Author Contributions

GS-V and TG-H conceived this study. GS-V, NS, and TG-H collected the data. NS provided species identification and measurements. GS-V and TG-H analyzed and modeled the stable isotope data. All co-authors contributed substantially to drafting the manuscript, and approved the final submitted manuscript.

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.

Publisher’s Note

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.

Acknowledgments

We wish to thank Mor Kanari for map preparation, and the captain and crew of R/V Bat-Galim, including onboard technical and scientific personnel for assistance in sampling. We also thank the two reviewers for critically reading the manuscript and suggesting substantial improvements. This work was supported by the National Monitoring Program of the Israeli Mediterranean waters.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmars.2022.857179/full#supplementary-material

References

Bergstad O. (2013). North Atlantic Demersal Deep-Water Fish Distribution and Biology: Present Knowledge and Challenges for the Future. J. Fish. Biol. 83, 1489–1507. doi: 10.1111/jfb.12208

PubMed Abstract | CrossRef Full Text | Google Scholar

Bond A. L., Diamond A. W. (2011). Recent Bayesian Stable-Isotope Mixing Models are Highly Sensitive to Variation in Discrimination Factors. Ecol. Appl. 21, 1017–1023. doi: 10.1890/09-2409.1

PubMed Abstract | CrossRef Full Text | Google Scholar

Boyle M., Ebert D., Cailliet G. (2012). Stable-Isotope Analysis of a Deep-sea Benthic-Fish Assemblage: Evidence of an Enriched Benthic Food Web. J. Fish. Biol. 80, 1485–1507. doi: 10.1111/j.1095-8649.2012.03243.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Britton J. R., Busst G. M. (2018). Stable Isotope Discrimination Factors of Omnivorous Fishes: Influence of Tissue Type, Temperature, Diet Composition and Formulated Feeds. Hydrobiologia 808, 219–234. doi: 10.1007/s10750-017-3423-9

CrossRef Full Text | Google Scholar

Carlier A., Riera P., Amouroux J.-M., Bodiou J.-Y., Grémare A. (2007). Benthic Trophic Network in the Bay of Banyuls-sur-Mer (Northwest Mediterranean, France): An Assessment Based on Stable Carbon and Nitrogen Isotopes Analysis. Estuarine. Coast. Shelf. Sci. 72, 1–15. doi: 10.1016/j.ecss.2006.10.001

CrossRef Full Text | Google Scholar

Carpentieri P., Serpetti N., Colloca F., Criscoli A., Ardizzone G. (2016). Food Preferences and Rhythms of Feeding Activity of Two Co-Existing Demersal Fish, the Longspine Snipefish, Macroramphosus Scolopax (Linnaeus 1758), and the Boarfish Capros Aper (Linnaeus 1758), on the Mediterranean Deep Shelf. Mar. Ecol. 37, 106–118. doi: 10.1111/maec.12265

CrossRef Full Text | Google Scholar

Cartes J. (1993). Feeding Habits of Oplophorid Shrimps in the Deep Western Mediterranean. J. Mar. Biol. Assoc. United. Kingdom. 73, 193–206. doi: 10.1017/S0025315400032720

CrossRef Full Text | Google Scholar

Caut S., Angulo E., Courchamp F. (2009). Variation in Discrimination Factors (Δ15N and Δ13C): The Effect of Diet Isotopic Values and Applications for Diet Reconstruction. J. Appl. Ecol. 46, 443–453. doi: 10.1111/j.1365-2664.2009.01620.x

CrossRef Full Text | Google Scholar

Choy C. A., Popp B. N., Hannides C. C., Drazen J. C. (2015). Trophic Structure and Food Resources of Epipelagic and Mesopelagic Fishes in the North Pacific Subtropical Gyre Ecosystem Inferred from Nitrogen Isotopic Compositions. Limnology. Oceanogr. 60, 1156–1171. doi: 10.1002/lno.10085

CrossRef Full Text | Google Scholar

Danovaro R., Dell’anno A., Corinaldesi C., Magagnini M., Noble R., Tamburini C., et al. (2008). Major Viral Impact on the Functioning of Benthic Deep-Sea Ecosystems. Nature 454, 1084–1087. doi: 10.1038/nature07268

PubMed Abstract | CrossRef Full Text | Google Scholar

Davies A. J., Roberts J. M., Hall-Spencer J. (2007). Preserving Deep-Sea Natural Heritage: Emerging Issues in Offshore Conservation and Management. Biol. Conserv. 138, 299–312. doi: 10.1016/j.biocon.2007.05.011

CrossRef Full Text | Google Scholar

Drazen J. C., Sutton T. T. (2017). Dining in the Deep: The Feeding Ecology of Deep-Sea Fishes. Annu. Rev. Mar. Sci. 9, 337–366. doi: 10.1146/annurev-marine-010816-060543

CrossRef Full Text | Google Scholar

Efrati S., Lehahn Y., Rahav E., Kress N., Herut B., Gertman I., et al. (2013). Intrusion of Coastal Waters Into the Pelagic Eastern Mediterranean: In Situ and Satellite-Based Characterization. Biogeosciences 10, 3349–3357. doi: 10.5194/bg-10-3349-2013

CrossRef Full Text | Google Scholar

Fahl K., Nöthig E.-M. (2007). Lithogenic and Biogenic Particle Fluxes on the Lomonosov Ridge (central Arctic Ocean) and their Relevance for Sediment Accumulation: Vertical vs. Lateral Transport. Deep. Sea. Res. Part I.: Oceanogr. Res. Papers. 54, 1256–1272. doi: 10.1016/j.dsr.2007.04.014

CrossRef Full Text | Google Scholar

Fanelli E., Azzurro E., Bariche M., Cartes J. E., Maynou F. (2015). Depicting the Novel Eastern Mediterranean Food Web: a Stable Isotopes Study Following Lessepsian Fish Invasion. Biol. Invasions. 17, 2163–2178. doi: 10.1007/s10530-015-0868-5

CrossRef Full Text | Google Scholar

Fanelli E., Cartes J. E. (2010). Temporal Variations in the Feeding Habits and Trophic Levels of Three Deep-Sea Demersal Fishes from the Western Mediterranean Sea, Based on Stomach Contents and Stable Isotope Analyses. Mar. Ecol. Prog. Ser. 402, 213–232. doi: 10.3354/meps08421

CrossRef Full Text | Google Scholar

Fanelli E., Cartes J. E., Papiol V. (2011). Food Web Structure of Deep-Sea Macrozooplankton and Micronekton Off the Catalan Slope: Insight From Stable Isotopes. J. Mar. Syst. 87, 79–89. doi: 10.1016/j.jmarsys.2011.03.003

CrossRef Full Text | Google Scholar

Galil B. S., Danovaro R., Rothman S., Gevili R., Goren M. (2019). Invasive Biota in the Deep-Sea Mediterranean: an Emerging Issue in Marine Conservation and Management. Biol. Invasions. 21, 281–288. doi: 10.1007/s10530-018-1826-9

CrossRef Full Text | Google Scholar

Gordon J. D., Merrett N. R., Haedrich R. L. (1995). “Environmental and Biological Aspects of Slope-Dwelling Fishes of the North Atlantic,” in Deep-Water Fisheries of the North Atlantic Oceanic Slope ( Dordrecht, Springer), 1–26.

Google Scholar

Gordon J., Swan S. (1997). “Deep-Water Demersal Fishes: Data for Assessment and Biological Analysis. Final Report of European Commission”. EUROPEAN COMMISSION.

Google Scholar

Goren M., Mienis H., Galil B. (2008). Not so Poor—More Deep-Sea Records From the Levant Sea, Eastern Mediterranean. Mar. Biodiversity Records (Cambridge University Press; Cambridge) 1, 1–4. doi: 10.1017/S1755267206005203

CrossRef Full Text | Google Scholar

Grossowicz M., Sisma-Ventura G., Gal G. (2019). Using Stable Carbon and Nitrogen Isotopes to Investigate the Impact of Desalination Brine Discharge on Marine Food Webs. Front. Mar. Sci. 6, 142. doi: 10.3389/fmars.2019.00142

CrossRef Full Text | Google Scholar

Hannides C. C., Zervoudaki S., Frangoulis C., Lange M. A. (2015). Mesozooplankton Stable Isotope Composition in Cyprus Coastal Waters and Comparison with the Aegean Sea (Eastern Mediterranean). Estuarine. Coast. Shelf. Sci. 154, 12–18. doi: 10.1016/j.ecss.2014.12.009

CrossRef Full Text | Google Scholar

Hazan O., Silverman J., Sisma-Ventura G., Ozer T., Gertman I., Shoham-Frider E., et al. (2018). Mesopelagic Prokaryotes Alter Surface Phytoplankton Production During Simulated Deep Mixing Experiments in Eastern Mediterranean Sea Waters. Front. Mar. Sci. 5, 1. doi: 10.3389/fmars.2018.00001

PubMed Abstract | CrossRef Full Text | Google Scholar

Helm K. P., Bindoff N. L., Church J. A. (2011). Observed Decreases in Oxygen Content of the Global Ocean. Geophys. Res. Lett. 38, 1–6.doi: 10.1029/2011GL049513

CrossRef Full Text | Google Scholar

Hopkins T., Gartner J. (1992). Resource-Partitioning and Predation Impact of a Low-Latitude Myctophid Community. Mar. Biol. 114, 185–197. doi: 10.1007/BF00349518

CrossRef Full Text | Google Scholar

Hunt B. P., Carlotti F., Donoso K., Pagano M., D’ortenzio F., Taillandier V., et al. (2017). Trophic Pathways of Phytoplankton Size Classes Through the Zooplankton Food Web Over the Spring Transition Period in the North-West M Editerranean Sea. J. Geophys. Research.: Oceans. 122, 6309–6324. doi: 10.1002/2016JC012658

CrossRef Full Text | Google Scholar

Jackson A. L., Inger R., Parnell A. C., Bearhop S. (2011). Comparing Isotopic Niche Widths Among and Within Communities: SIBER–Stable Isotope Bayesian Ellipses in R. J. Anim. Ecol. 80, 595–602. doi: 10.1111/j.1365-2656.2011.01806.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Jackson A., Parnell A. (2021). Package ‘SIBER’. R Package Version 2.1.4.

Google Scholar

Katz T., Weinstein Y., Alkalay R., Biton E., Toledo Y., Lazar A., et al. (2020). The First Deep-Sea Mooring Station in the Eastern Levantine Basin (DeepLev), Outline and Insights Into Regional Sedimentological Processes. Deep. Sea. Res. Part II.: Topical. Stud. Oceanogr. 171, 104663. doi: 10.1016/j.dsr2.2019.10466

CrossRef Full Text | Google Scholar

Kelly C., Connolly P., Clarke M. (1998). The Deep Water Fisheries of the Rockall Trough: Some Insights Gleaned From Irish Survey Data. CES CM. O:40, 22 pp.

Google Scholar

Kilongo K., Barros P., Diehdiou M. (2007). Diet of Large-Eye Dentex Macrophthalmus (Pisces: Sparidae) Off Angola and Namibia. Afr. J. Mar. Sci. 29, 49–54. doi: 10.2989/AJMS.2007.29.1.4.69

CrossRef Full Text | Google Scholar

Kim H., Lee K., Lim D.-I., Nam S.-I., Hee Han S., Kim J., et al. (2019). Increase in Anthropogenic Mercury in Marginal Sea Sediments of the Northwest Pacific Ocean. Sci. Total. Environ. 654, 801–810. doi: 10.1016/j.scitotenv.2018.11.076

PubMed Abstract | CrossRef Full Text | Google Scholar

Koppelmann R., Böttger-Schnack R., Möbius J., Weikert H. (2009). Trophic Relationships of Zooplankton in the Eastern Mediterranean Based on Stable Isotope Measurements. J. Plankton. Res. 31, 669–686. doi: 10.1093/plankt/fbp013

CrossRef Full Text | Google Scholar

Koppelmann R., Weikert H., Lahajnar N. (2003). Vertical Distribution of Mesozooplankton and its δ15N Signature at a Deep-sea Site in the Levantine Sea (Eastern Mediterranean) in April 1999. J. Geophys. Research.: Oceans. 108, 1–11. doi: 10.1029/2002JC001351

CrossRef Full Text | Google Scholar

Koslow J. A. (1993). Community structure in North Atlantic Deep-Sea Fishes. Prog. Oceanogr. 31, 321–338. doi: 10.1016/0079-6611(93)90005-X

CrossRef Full Text | Google Scholar

Kress N., Gertman I., Herut B. (2014). Temporal Evolution of Physical and Chemical Characteristics of the Water Column in the Easternmost Levantine Basin (Eastern Mediterranean Sea) from 2002 to 2010. J. Mar. Syst. 135, 6–13. doi: 10.1016/j.jmarsys.2013.11.016

CrossRef Full Text | Google Scholar

Kröncke I., Türkay M., Fiege D. (2003). Macrofauna Communities in the Eastern Mediterranean Deep Sea. Mar. Ecol. 24, 193–216. doi: 10.1046/j.0173-9565.2003.00825.x

CrossRef Full Text | Google Scholar

Layman C. A., Arrington D. A., Montaña C. G., Post D. M. (2007). Can Stable Isotope Ratios Provide for Community-Ide Measures of Trophic Structure? Ecology 88, 42–48. doi: 10.1890/0012-9658(2007)88[42:CSIRPF]2.0.CO;2

PubMed Abstract | CrossRef Full Text | Google Scholar

Liu M., Xiao W., Zhang Q., Shi L., Wang X., Xu Y. (2020). Methylmercury Bioaccumulation In Deepest Ocean Fauna: Implications For Ocean Mercury Biotransport Through Food Webs. Environ. Sci. Technol. Lett. 7, 469–476. doi: 10.1021/acs.estlett.0c00299

CrossRef Full Text | Google Scholar

Malpica-Cruz L., Herzka S. Z., Sosa-Nishizaki O., Lazo J. P. (2012). Tissue-Specific Isotope Trophic Discrimination Factors And Turnover Rates In A Marine Elasmobranch: Empirical And Modeling Results. Can. J. Fisheries. Aquat. Sci. 69, 551–564. doi: 10.1139/f2011-172

CrossRef Full Text | Google Scholar

Menezes G. M., Sigler M. F., Silva H. M., Pinho M. R. (2006). Structure And Zonation Of Demersal Fish Assemblages Off The Azores Archipelago (Mid-Atlantic). Mar. Ecol. Prog. Ser. 324, 241–260. doi: 10.3354/meps324241

CrossRef Full Text | Google Scholar

Mengerink K. J., Van Dover C. L., Ardron J., Baker M., Escobar-Briones E., Gjerde K., et al. (2014). A Call For Deep-Ocean Stewardship. Science 344, 696–698. doi: 10.1126/science.1251458

PubMed Abstract | CrossRef Full Text | Google Scholar

Miller T. W., Brodeur R. D., Rau G. H. (2008). Carbon Stable Isotopes Reveal Relative Contribution Of Shelf-Slope Production To The Northern California Current Pelagic Community. Limnology. Oceanogr. 53, 1493–1503. doi: 10.4319/lo.2008.53.4.1493

CrossRef Full Text | Google Scholar

Neat F., Burns F., Drewery J. (2008). The Deepwater Ecosystem Of The Continental Shelf Slope And Seamounts Of The Rockall Trough: A Report On The Ecology And Biodiversity Based On Frs Scientific Surveys. Fisheries. Res. Serv. Internal Rep. 1–30.

Google Scholar

Ogrinc N., Monperrus M., Kotnik J., Fajon V., Vidimova K., Amouroux D., et al. (2007). Distribution Of Mercury And Methylmercury In Deep-Sea Surficial Sediments Of The Mediterranean Sea. Mar. Chem. 107, 31–48. doi: 10.1016/j.marchem.2007.01.019

CrossRef Full Text | Google Scholar

Olin J. A., Hussey N. E., Grgicak-Mannion A., Fritts M. W., Wintner S. P., Fisk A. T. (2013). Variable Δ15n Diet-Tissue Discrimination Factors Among Sharks: Implications For Trophic Position, Diet And Food Web Models. PloS One 8, e77567. doi: 10.1371/journal.pone.0077567

PubMed Abstract | CrossRef Full Text | Google Scholar

Ozer T., Gertman I., Kress N., Silverman J., Herut B. (2017). Interannual Thermohaline, (1979–2014) And Nutrient, (2002–2014) Dynamics In The Levantine Surface And Intermediate Water Masses, Se Mediterranean Sea. Global Planetary. Change 151, 60–67. doi: 10.1016/j.gloplacha.2016.04.001

CrossRef Full Text | Google Scholar

Pajuelo J. G., Seoane J., Biscoito M., Freitas M., González J. A. (2016). Assemblages Of Deep-Sea Fishes On The Middle Slope Off Northwest Africa (26–33 N, Eastern Atlantic). Deep. Sea. Res. Part I.: Oceanogr. Res. Papers. 118, 66–83. doi: 10.1016/j.dsr.2016.10.011

CrossRef Full Text | Google Scholar

Pakhomov E., Perissinotto R., Mcquaid C. (1996). Prey Composition And Daily Rations Of Myctophid Fishes In The Southern Ocean. Mar. Ecol. Prog. Ser. 134, 1–14. doi: 10.3354/meps134001

CrossRef Full Text | Google Scholar

Papiol V., Cartes J. E., Fanelli E., Rumolo P. (2013). Food Web Structure And Seasonality Of Slope Megafauna In The Nw Mediterranean Elucidated By Stable Isotopes: Relationship With Available Food Sources. J. Sea. Res. 77, 53–69. doi: 10.1016/j.seares.2012.10.002

CrossRef Full Text | Google Scholar

Parzanini C., Parrish C. C., Hamel J.-F., Mercier A. (2019). Reviews And Syntheses: Insights Into Deep-Sea Food Webs And Global Environmental Gradients Revealed By Stable Isotope (Δ 15 N, Δ 13 C) And Fatty Acid Trophic Biomarkers. Biogeosciences 16, 2837–2856. doi: 10.5194/bg-16-2837-2019

CrossRef Full Text | Google Scholar

Pecquerie L., Nisbet R. M., Fablet R., Lorrain A., Kooijman S. A. (2010). The Impact Of Metabolism On Stable Isotope Dynamics: A Theoretical Framework. Philos. Trans. R. Soc. B.: Biol. Sci. 365, 3455–3468. doi: 10.1098/rstb.2010.0097

CrossRef Full Text | Google Scholar

Pérès J. (1985). History Of The Mediterranean Biota And The Colonization Of The Depths. Western. Mediterr. 1, 198–232.

Google Scholar

Peterson B. J., Fry B. (1987). Stable Isotopes In Ecosystem Studies. Annu. Rev. Ecol. systematics. 18, 293–320. doi: 10.1146/annurev.es.18.110187.001453

CrossRef Full Text | Google Scholar

Polis G. A., Strong D. R. (1996). Food Web Complexity And Community Dynamics. Am. Nat. 147, 813–846. doi: 10.1086/285880

CrossRef Full Text | Google Scholar

Polunin N., Morales-Nin B., Pawsey W., Cartes J. E., Pinnegar J. K., Moranta J. (2001). Feeding Relationships In Mediterranean Bathyal Assemblages Elucidated By Stable Nitrogen And Carbon Isotope Data. Mar. Ecol. Prog. Ser. 220, 13–23. doi: 10.3354/meps220013

CrossRef Full Text | Google Scholar

Post D. M. (2002). Using Stable Isotopes To Estimate Trophic Position: Models, Methods, And Assumptions. Ecology 83, 703–718. doi: 10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2

CrossRef Full Text | Google Scholar

Post D. M., Layman C. A., Arrington D. A., Takimoto G., Quattrochi J., Montana C. G. (2007). Getting To The Fat Of The Matter: Models, Methods And Assumptions For Dealing With Lipids In Stable Isotope Analyses. Oecologia 152, 179–189. doi: 10.1007/s00442-006-0630-x

PubMed Abstract | CrossRef Full Text | Google Scholar

Protopapa M., Koppelmann R., Zervoudaki S., Wunsch C., Peters J., Parinos C., et al. (2019). Trophic Positioning Of Prominent Copepods In The Epi-And Mesopelagic Zone Of The Ultra-Oligotrophic Eastern Mediterranean Sea. Deep. Sea. Res. Part II.: Topical. Stud. Oceanogr. 164, 144–155. doi: 10.1016/j.dsr2.2019.04.011

CrossRef Full Text | Google Scholar

Quezada-Romegialli C., Jackson A. L., Hayden B., Kahilainen K. K., Lopes C., Harrod C. (2018). Trophicposition, An R Package For The Bayesian Estimation Of Trophic Position From Consumer Stable Isotope Ratios. Methods Ecol. Evol. 9, 1592–1599. doi: 10.1111/2041-210X.13009

CrossRef Full Text | Google Scholar

Rahav E., Silverman J., Raveh O., Hazan O., Rubin-Blum M., Zeri C., et al. (2019). The Deep Water Of Eastern Mediterranean Sea Is A Hotspot For Bacterial Activity. Deep. Sea. Res. Part II.: Topical. Stud. Oceanogr. 164, 135–143. doi: 10.1016/j.dsr2.2019.03.004

CrossRef Full Text | Google Scholar

Ramirez-Llodra E., Brandt A., Danovaro R., Mol B. D., Escobar E., German C. R., et al. (2010). Deep, Diverse And Definitely Different: Unique Attributes Of The World’s Largest Ecosystem. Biogeosciences 7, 2851–2899. doi: 10.5194/bg-7-2851-2010

CrossRef Full Text | Google Scholar

R Core Team (2020). “R: A Language and Environment for Statistical Computing” (Vienna, Austria: R Foundation for Statistical Computing).

Google Scholar

Richards T. M., Gipson E. E., Cook A., Sutton T. T., Wells R. D. (2018). Trophic Ecology Of Meso-And Bathypelagic Predatory Fishes In The Gulf Of Mexico. ICES. J. Mar. Sci. 76, 662–672. doi: 10.1093/icesjms/fsy074

CrossRef Full Text | Google Scholar

Richards T. M., Sutton T. T., Wells R. (2020). Trophic Structure And Sources Of Variation Influencing The Stable Isotope Signatures Of Meso-And Bathypelagic Micronekton Fishes. Front. Mar. Sci. 7, 876. doi: 10.3389/fmars.2020.507992

CrossRef Full Text | Google Scholar

Rilov G., Galil B. (2009). “Marine Bioinvasions In The Mediterranean Sea–History, Distribution And Ecology,” In Biological Invasions In Marine Ecosystems (Berlin Heidelberg, Springer-Verlag), 549–575.

Google Scholar

Romero-Romero S., Miller E. C., Black J. A., Popp B. N., Drazen J. C. (2021). Abyssal Deposit Feeders Are Secondary Consumers Of Detritus And Rely On Nutrition Derived From Microbial Communities In Their Guts. Sci. Rep. 11, 1–11. doi: 10.1038/s41598-021-91927-4

PubMed Abstract | CrossRef Full Text | Google Scholar

Rubin-Blum M., Sisma-Ventura G., Yudkovski Y., Belkin N., Kanari M., Herut B., et al. (2022). Diversity, Activity, And Abundance Of Benthic Microbes In The Southeastern Mediterranean Sea. FEMS Microbiol. Ecol. 98, fiac009. doi: 10.1093/femsec/fiac009

PubMed Abstract | CrossRef Full Text | Google Scholar

Sanchez-Vidal A., Canals M., Calafat A. M., Lastras G., Pedrosa-Pàmies R., Menéndez M., et al. (2012). Impacts On The Deep-Sea Ecosystem By A Severe Coastal Storm. PloS One 7, e30395. doi: 10.1371/journal.pone.0030395

PubMed Abstract | CrossRef Full Text | Google Scholar

Shipley O. N., Brooks E. J., Madigan D. J., Sweeting C. J., Grubbs R. D. (2017a). Stable Isotope Analysis In Deep-Sea Chondrichthyans: Recent Challenges, Ecological Insights, And Future Directions. Rev. Fish. Biol. Fisheries. 27, 481–497. doi: 10.1007/s11160-017-9466-1

CrossRef Full Text | Google Scholar

Shipley O. N., Polunin N. V., Newman S. P., Sweeting C. J., Barker S., Witt M. J., et al. (2017b). Stable Isotopes Reveal Food Web Dynamics Of A Data-Poor Deep-Sea Island Slope Community. Food Webs. 10, 22–25. doi: 10.1016/j.fooweb.2017.02.004

CrossRef Full Text | Google Scholar

Shoham-Frider E., Gertner Y., Guy-Haim T., Herut B., Kress N., Shefer E., et al. (2020). Legacy Groundwater Pollution As A Source Of Mercury Enrichment In Marine Food Web, Haifa Bay, Israel. Sci. Total. Environ. 714, 136711. doi: 10.1016/j.scitotenv.2020.136711

PubMed Abstract | CrossRef Full Text | Google Scholar

Sisma-Ventura G., Yam R., Shemesh A. (2014). Recent Unprecedented Warming And Oligotrophy Of The Eastern Mediterranean Sea Within The Last Millennium. Geophys. Res. Lett. 41, 5158–5166. doi: 10.1002/2014GL060393

CrossRef Full Text | Google Scholar

Smith C. R., Baco A. R. (2003). “Ecology Of Whale Falls At The Deep-Sea Floor,” in Oceanography and Marine Biology, An Annual Review, Volume 41 (Florida, CRC Press), 319–333.

Google Scholar

Stock B. C., Jackson A. L., Ward E. J., Parnell A. C., Phillips D. L., Semmens B. X. (2018). Analyzing Mixing Systems Using A New Generation Of Bayesian Tracer Mixing Models. PeerJ 6, e5096. doi: 10.7717/peerj.5096

PubMed Abstract | CrossRef Full Text | Google Scholar

Stock B., Semmens B., Ward E., Parnell A., Jackson A., Phillips D. (2021). “Package ‘MixSIAR’,” in Bayesian Mixing Model s in R, Version 3, 1.12.

Google Scholar

Stramma L., Brandt P., Schafstall J., Schott F., Fischer J., Körtzinger A. (2008). Oxygen Minimum Zone In The North Atlantic South And East Of The Cape Verde Islands. J. Geophys. Research.: Oceans. 113, 1–15. doi: 10.1029/2007JC004369

CrossRef Full Text | Google Scholar

Stramma L., Schmidtko S., Levin L. A., Johnson G. C. (2010). Ocean Oxygen Minima Expansions And Their Biological Impacts. Deep. Sea. Res. Part I.: Oceanogr. Res. Papers. 57, 587–595. doi: 10.1016/j.dsr.2010.01.005

CrossRef Full Text | Google Scholar

Suchanek T. H., Williams S. L., Ogden J. C., Hubbard D. K., Gill I. P. (1985). Utilization Of Shallow-Water Seagrass Detritus By Carribbean Deep-Sea Macrofauna: δ13C evidence. Deep. Sea. Res. Part A. Oceanogr. Res. Papers. 32, 201–214. doi: 10.1016/0198-0149(85)90028-7

CrossRef Full Text | Google Scholar

Sweeting C., Barry J., Barnes C., Polunin N., Jennings S. (2007). Effects Of Body Size And Environment On Diet-Tissue Δ15n Fractionation In Fishes. J. Exp. Mar. Biol. Ecol. 340, 1–10. doi: 10.1016/j.jembe.2006.07.023

CrossRef Full Text | Google Scholar

Tecchio S., Coll M., Sardà F. (2015). Structure, Functioning, And Cumulative Stressors Of Mediterranean Deep-Sea Ecosystems. Prog. Oceanogr. 135, 156–167. doi: 10.1016/j.pocean.2015.05.018

CrossRef Full Text | Google Scholar

Tecchio S., Van Oevelen D., Soetaert K., Navarro J., Ramírez-Llodra E. (2013). Trophic Dynamics Of Deep-Sea Megabenthos Are Mediated By Surface Productivity. PloS One 8, e63796. doi: 10.1371/journal.pone.0063796

PubMed Abstract | CrossRef Full Text | Google Scholar

Thiel H. (1983). Meiobenthos and nanobenthos of the deep sea. in: G. rowe (ed.), Deep-Sea Biololgy. Wiley, New York. pp. 167–230

Google Scholar

Thurber A. R., Sweetman A. K., Narayanaswamy B. E., Jones D. O., Ingels J., Hansman R. (2014). Ecosystem Function And Services Provided By The Deep Sea. Biogeosciences 11, 3941–3963. doi: 10.5194/bg-11-3941-2014

CrossRef Full Text | Google Scholar

Trueman C., Johnston G., O’hea B., Mackenzie K. (2014). Trophic Interactions Of Fish Communities At Midwater Depths Enhance Long-Term Carbon Storage And Benthic Production On Continental Slopes. Proc. R. Soc. B.: Biol. Sci. 281, 20140669. doi: 10.1098/rspb.2014.0669

CrossRef Full Text | Google Scholar

Valls M., Olivar M. P., De Puelles M. F., Molí B., Bernal A., Sweeting C. (2014). Trophic Structure Of Mesopelagic Fishes In The Western Mediterranean Based On Stable Isotopes Of Carbon And Nitrogen. J. Mar. Syst. 138, 160–170. doi: 10.1016/j.jmarsys.2014.04.007

CrossRef Full Text | Google Scholar

Walsh J. J. (1991). Importance Of Continental Margins In The Marine Biogeochemical Cycling Of Carbon And Nitrogen. Nature 350, 53–55. doi: 10.1038/350053a0

CrossRef Full Text | Google Scholar

Winemiller K. O., Polis G. A. (1996). “Food Webs: What Can They Tell Us About The World?” in Food Webs (New York, NY: Springer), 1–22.

Google Scholar

Yasuhara M., Cronin T. M., Demenocal P. B., Okahashi H., Linsley B. K. (2008). Abrupt Climate Change And Collapse Of Deep-Sea Ecosystems. Proc. Natl. Acad. Sci. 105, 1556–1560. doi: 10.1073/pnas.0705486105

CrossRef Full Text | Google Scholar

Zorica B., Ezgeta-Bali&cacute; D., Vidjak O., Vuletin V., Šestanovi&cacute; M., Isajlovi&cacute; I., et al. (2021). Diet Composition And Isotopic Analysis Of Nine Important Fisheries Resources In The Eastern Adriatic Sea (Mediterranean). Front. Mar. Sci. 8, 183. doi: 10.3389/fmars.2021.609432

CrossRef Full Text | Google Scholar