Living (stained) foraminifera in the Lesser Syrtis (Tunisia): influence of pollution and substratum

Cluster A and B: polluted environment

These two clusters can be considered together as the only difference between the two is the abundant T. conica in Cluster A (which is composed by only one sample, GBS-06) and a different substratum (Fig. 3), Facies G3 for GBS-06, and Facies G4 for all stations of Cluster B. These two clusters group the majority of the stations in the Gulf of Gabes (Figs. 2 and 3).

The dominant foraminiferal species is E. scaber (Table 3). Murray (2006) described this species as infaunal, detritivore and typical of shelf environments. Bouchet (2007) suggests that the sedimentary detrital organic matter represents the main food resource for this species. Dessandier et al. (2016) studied the distribution of E. scaber along the Portuguese coast, highlighting its preference for environments characterized by high-quality of the organic matter (e.g., high chlorophyll-a to phaeopigment ratio and available amino acids). Murray (2013) reported that E. scaber is sensitive to salinity not exceeding 24 psu and oxygen depletion (<0.5 ml/L), and that it is tolerant to fluctuations in temperature and heavy metal pollution. Other highly contributing species of Cluster A and B are B. elegantissima and B. striatula, two stress-tolerant species able to survive in polluted environmental conditions and under oxygen depletion (e.g., Murray, 2006; Dimiza et al., 2019, and references therein). Martins et al. (2016a) documented the preference of B. striatula for high quality organic matter enriched in proteins, carbohydrates and chlorophyll -a.

In general, taxa which are tolerant to such conditions are typically associated with muddy substrates that can accumulate high amounts of organic matter (e.g., Van der Zwaan et al., 1999 and reference therein). This is evident as Cluster B includes stations from Facies G4 (clay with centimetric biogenic fragments). For Cluster B, the SIMPER analysis additionally identified the stress-tolerant species A. tepida and B. marginata (e.g., Dimiza et al., 2019; Jorissen et al., 2018), as well as Haynesina depressula, and Nonionoides grateloupi, which are classified as “indifferent species” by Jorissen et al. (2018). The relatively high contribution of A. mamilla in Cluster B (Table 3), in addition to its high abundances in samples from Clusters A and B (Supplemental Information S1), is not consistent with its life strategy from the literature. Murray (2013) described this species as epifaunal clinging on large detrital fragments or on marine vegetation. Dimiza et al. (2016) show the negative correlation between abundances of A. mamilla and the percent of mud. Is the quality of the organic matter playing a role on the abundance of this species? The abundance of this species may be, indeed, linked to the high quality of the organic matter, whose δ¹³C signature corresponds to marine phytoplankton, along the Gabes transect (Supplemental Information S2; El Kateb et al., 2018b; El Kateb et al., 2020). Alternatively, the centimetric bioclasts characterizing Facies G4 may provide a suitable ecological niche for A. mamilla (Fig. 3, Table 2).

The LINKTREE (Fig. 5) shows that stations grouped in Cluster A and B separate based on the relatively high (in relation the Djerba samples) values of TOC (≤3.34 wt. %), As (≤1.26 µg/L), Cd (0.73-1.19 µg/L) and phosphorus both in the sediments (87.1 > Ptot > 28.7 µmol/g ) and sea water (P > 144 µg/L).

In conclusion, the living (stained) benthic foraminifera assemblages from Clusters A and B are interpreted to reflect high sedimentary organic matter supply, in a stressed environment due to heavy metals and phosphorus contamination deriving from the Gabes industry.

Cluster C: polluted Environment characterized by physicochemical variability

Major contributors of this cluster (exceeding 13%) are T. inflata and R. vilardeboana (Table 3). It groups only two stations (GBS-04 and -05) which are characterized by sandy carbonate sediments and large biogenic fragments (Facies G3 in Table 2, El Kateb et al., 2018b) that may represent an ideal habitat for R. villardeboana. This species is described as stress-tolerant in culturing experiments (Hintz et al., 2004) and has been reported living in shallow water (Erginal et al., 2013), similarly to station GBS-04, with a water depth not exceeding 12 m (El Kateb et al., 2018b). Trochammina inflata is a species known to be highly tolerant to physicochemical variability (Murray, 2006; Martins et al., 2016b). It is a cosmopolitan epifaunal or infaunal, euryhaline marsh species, living down to 60 m of water depth and with a general preference for muddy substrates (Usera et al., 2002; Murray, 2006; Benito et al., 2016). The abundance of T. inflata within these samples may be due to the physicochemical variability linked to the tides that in this region reach the highest variations (up to 2 m, Aloulou, EllEuch & Kallel, 2012). Other species of this cluster are the stress-tolerant B. striatula, B. elegantissima and C. involvens, attributed to group 3 third-order opportunists, tolerant to and favoured by the first stages of organic enrichment (Alve et al., 2016; Jorissen et al., 2018). Rare specimens of Q. laevigata and T. conica (not exceeding 3 and 13 specimens, respectively) also occur, these species are considered as “sensitive” by Jorissen et al. (2018).

Cluster C is characterized by low species and low specimen numbers. In the LINKTREE (Fig. 5) it groups with Cluster A and B with relatively high TOC (≤3.34 wt. %), As (≤1.26 µg/L), Cd (0.73–1.19 µg/L) and high phosphorus concentrations both in the sediments (87.1 < Ptot >  8.7 µmol/g) and the sea water (P > 144 µg/L). In summary, the living (stained) benthic foraminifera assemblages from Cluster C represent a stressed environment under the impact of heavy metal and phosphorus contamination deriving from the Gabes industry. This is in combination with unstable physicochemical conditions that may account for the presence of more sensitive species.

Cluster D and E: Seagrass meadows and “pristine” sites

These clusters group all stations from the Djerba transect (Figs. 2 and 3). The living (stained) foraminifera assemblages of Clusters D and E show significant differences in comparison to the other clusters (Fig. 3, Table 3), highlighted by the consistent presence of sensitive species such as A. lessonii. Amphisteginids are large symbiont-bearing foraminifera widely used as bioindicators to assess water quality due to their fast response to environmental changes, e.g., water temperature and photo-oxidation (e.g., Emrich, Martínez-Colón & Alegria, 2017, De Freitas Prazeres, Martins & Bianchini, 2012; Hallock et al., 2006; Spezzaferri et al., 2018). Water transparency is an essential factor for Amphistegina spp. because these organisms host symbionts and, as such, are light dependent (Hallock, 1981). El Kateb et al. (2018c) suggest that the presence of P. oceanica meadows along the Djerba transect promotes the development of A. lessonii. This species is also very sensitive to heavy metals pollution because these pollutants directly affect its symbiotic algae. Furthermore, De Freitas Prazeres, Martins & Bianchini (2011) demonstrated, in culture, that zinc exposure causes visual alteration such as bleaching and/or dark brown areas in the test.

Cluster D is characterized by A. lessonii and to a lesser extent by R. villardeboana, P.  mediterranensis and R. macropora and includes two samples DJB-01 collected in the P. oceanica meadow (Facies D1) and DJB-12 (Facies D3, well-preserved biogenic fragments of bivalves, calcareous algae, gastropods and bryozoans), characterized by abundant degraded algae. R. vilardeboana is especially abundant at station DJB-01, where P. oceanica traps the sediments in its rhizomes to form small barriers. Planorbulina mediterranensis is epifaunal clinging on hard substrata and/or seagrass (Villanueva Guimerans & Cervera Currado, 1999). Mateu-Vicens et al. (2010) mentioned high abundances of this species in P. oceanica meadows, which is corroborated at station DJB-01 where the seagrass is densely covering the sea floor (El Kateb et al., 2018b). As an epifauna foraminifera, R. macropora is generally associated with sandy and vegetated substrate (Vidović et al., 2014 and references therein). Elshanawany et al. (2011) proposed R. macropora to be a species relatively sensitive to pollution.

Cluster E is characterized primarily by R. macropora, R. villardeboana in addition to the species B. striatula, A. lessonii, A. mamilla, P. pertusus. It includes all the remaining samples from Djerba covering a variety of Facies, from D1 to D3, ranging from P. oceanica meadows to fine sediment with biogenic clasts of various sizes. Similarly to the epibenthic and sensitive A. lessonii, P. pertusus is also a symbiont-bearing species and needs high light intensities (Samir & El-Din, 2001 and references therein). Amao, Kaminski & Setoyama (2016) suggested that this species is associated with the presence of marine flora. There are no investigations showing the pollution impact on this species but as a symbiont-bearing foraminifer, it can be considered as sensitive to anthropogenic-related stressors such as heavy metals. Within this cluster the occurrence of A. mamilla, R. vilardeboana and R. macropora seems to be linked to P. oceanica meadows, which provides them with an ideal substratum. Brizalina striatula is an infaunal species relatively tolerant to oxygen depletion and feeding on organic detritus (e.g., Murray, 2006). El Kateb et al. (2018a) documented abundant B. striatula linked to P. oceanica meadows, indicating that the remains of P. oceanica may represent a potential food resource for this species.

All the Djerba sites are characterized by the highest species numbers, specimen numbers and Shannon diversities (Supplemental Information S1). They separate in the LINKTREE (Fig. 5) based on the lowest values of P, Ptot and Cd (<17.6 µg/L, <0.62 µmol/g and 23.5 µg/L, respectively) confirming the more negative association of the species, identified in the SIMPER analysis for Clusters D and E, with lower levels of pollution.

In summary, benthic foraminifera of Cluster D and E seem to be linked to P. oceanica meadows. Sensitive species such as A. lessonii and peneroplidae suggest relatively “pristine” environments where anthropogenic stress is minor (Triantaphyllou et al., 2005; Koukousioura et al., 2012).

Cluster F: Major industrial impact

This cluster groups Sample GBS-01, −02 and −09. The first two samples are located in front of the industrial complex at Gabes and are the closest to the pollution source, whereas sample GBS-09 is located further away. Sample GBS-02 was collected in the industrial sludge consisting of dark siliciclastic sediments (Facies G1, Fig. 3, Table 3), where concentrations of TOC and heavy metals reach the highest values in both seawater and marine sediments (Supplemental Information S2; El Zrelli et al., 2015; El Zrelli et al., 2018; Ayadi, Aloulou & Bouzid, 2015; El Kateb et al., 2018b). Major contributors to this cluster are A. tepida and B. striatula, two stress-tolerant species. In particular, A. tepida is well known to tolerate pollution and elevated concentrations of TOC (e.g., Samir & El-Din, 2001; Armynot du Châtelet, Debenay & Soulard, 2004; Dimiza et al., 2019). This cluster is characterized by the lowest species numbers, specimen numbers and Shannon diversities (Supplemental Information S1). The grouping of Sample GBS-09 with -01 and -02 is possibly due to the fine nature of the sediments that favors the accumulation of organic matter resulting in high TOC concentrations (Facies G5, Table 3, Figs. 3 and 5) (e.g., Tyson, 1995; Bergamaschi et al., 1997). Samples GBS-02 and −01 are still distinguished by their strong relation to high concentrations of Ptot, As and Cd (>282 µmol/g, >2.9 µg/L and 2.61 µg/L, respectively).

The living benthic foraminifera of Cluster F can be interpreted as a stress-tolerant assemblage related to high pollution levels (P, As, Cd) in a eutrophic setting.