Open access peer-reviewed chapter

Evaluation of the Water Quality and the Eutrophication Risk in Mediterranean Sea Area: A Case Study of the Gulf of Gabès

Written By

Neila Annabi-Trabelsi, Mohammad Ali, Genuario Belmonte, Habib Ayadi and Wassim Guermazi

Submitted: 09 October 2023 Reviewed: 12 December 2023 Published: 29 December 2023

DOI: 10.5772/intechopen.114108

From the Edited Volume

Marine Ecosystems - Biodiversity, Ecosystem Services and Human Impacts

Edited by Ana Marta Gonçalves

Chapter metrics overview

43 Chapter Downloads

View Full Metrics

Abstract

The Gulf of Gabès, located in southern Tunisia, is a distinct and ecologically significant area in the Mediterranean Sea. Unfortunately, this dynamic marine ecosystem is experiencing cultural eutrophication, a process where water enrichment with nutrients like phosphorus and nitrogen salts leads to excessive algae growth, disrupting the ecological equilibrium and degrading water quality. In the Gulf of Gabès, key sources of nutrient pollution include industrial discharges, urbanization and agriculture. Eutrophication’s effects here include harmful algal blooms, oxygen depletion, and declining water quality, upsetting the marine ecosystem’s balance and impacting both fish and aquatic life. Nutrient enrichment interacts with trace metal pollution, overfishing and climate change. Future research must acknowledge and consider the complex interactions among these variables. Efforts in the Gulf of Gabès to address eutrophication involve tighter industrial regulations, enhanced agriculture and improved wastewater management, all crucial for preserving the marine environment’s integrity and ensuring sustainability for the future.

Keywords

  • eutrophication
  • phosphorus
  • phytoplankton
  • zooplankton
  • algal blooms

1. Introduction

Cultural eutrophication poses a severe environmental and economic challenge in coastal marine ecosystems across the globe [1, 2, 3]. According to the European Union’s definition, cultural eutrophication involves enriching water with nutrients, especially compounds of nitrogen and phosphorus, causing an accelerated growth of algae and higher forms of plant life to produce an undesirable disturbance to the balance of organisms present in the water and to the quality of the water concerned [4]. This kind of pollution by nutrients is resulting from anthropogenic activities including industry, agriculture and sewage disposal [5]. The repercussions of cultural eutrophication extend to coastal ecosystem biodiversity and the services they give to society such as protection from coastal erosion and flooding, or fish production [6]. Eutrophication is mostly accompanied by hypoxia and an increase in the biomass of nuisance algal taxa [7]. In fact, eutrophication is an important factor contributing to the increased frequency and diversity of harmful algal blooms [8] and shifts in the zooplankton community [7]. Despite the fact the Mediterranean Sea is generally considered of good quality [9, 10] and classified as nutrient-poor and oligotrophic [11], eutrophication problems began emerging in the 1960s [12], mainly situated in areas of encircled gulfs and bays near big cities, in estuarine areas and near ports [13, 14, 15, 16, 17]. The Gulf of Gabès, situated on the southeastern coast of Tunisia, faces pollution from anthropogenic and industrial activities, and its coastal area showed signs of eutrophication [18]; continuous and increasing deterioration of the coastal waters of the Gulf was reported since the industrialization [19, 20, 21].

Advertisement

2. The Gulf of Gabès: main characteristics

Situated in southeastern Tunisia, the Gulf of Gabès, also known as “Petite Syrte”, stretches from 9.5 to 12°E in longitude and from 33 to 35.5°N in latitude. It extends from “Ras Kapoudia” in the north to the Tunisian–Libyan border in the south, encompassing a coastline exceeding 400 km (Figure 1). It shelters various islands (Kerkenneh, Kneiss and Jerba) and lagoons (Boughrara and El Bibane).

Figure 1.

Localization of the Gulf of Gabès.

It is characterized by a semiarid Mediterranean climate, shallow waters, weak currents, high salinity and high temperature. The Gulf’s circulation is predominantly influenced by tides and anticyclonic winds [22].

The Gulf has the highest tidal range in the Mediterranean Sea (maximum >2 m), essentially due to the low slope of the continental shelf and the shallow depth, which maintains its horizontal dimensions close to the resonance phenomena [22, 23].

Since industrialization in 1970, the Gulf of Gabès has been heavily impacted by industrial wastes and described as one of the most human-impacted coastal areas in the Mediterranean Sea [21]. Diverse untreated pollutants from liquid and solid wastes discharged from industrial and domestic activities (crude phosphate treatment, chemical processing plants, tanneries and textile mills) have severely degraded the Gulf of Gabès [24, 25]. The phosphate fertilizer industry is mediated as the major source of pollution. The most important phosphate industry group (Tunisian Chemical Group: TCG) was set in Gabès city. Two other companies (SIAPE and GRANUPHOS) are located in Sfax city, and recently, another one (SIAPE II) has been launched in Skhira. The unregulated disposal of phosphogypsum (PG), a byproduct of the phosphate fertilizer industry, into the Gulf of Gabès at a daily rate ranging from 1000 to 13,000 tons, stands as the primary factor responsible for the deterioration of this ecosystem [26, 27].

Advertisement

3. Causes of eutrophication in the Gulf of Gabès

Phosphogypsum (PG) industrial effluents released into the Gulf of Gabès are notably acidic and carry elevated levels of fluoride and phosphate. Additionally, they contain variable concentrations of heavy metals such as cadmium, chromium, copper, zinc and lead, along with radionuclides [28, 29]. The study of El Kateb et al. [30] clearly established that the substantial discharge of PG is a leading cause of eutrophication in the Gulf of Gabès.

While phosphorus is an essential element in the marine ecosystem, its excessive enrichment poses various challenges to biota, elevates the growth of organic matter, and consequently reinforces eutrophication [31, 32]. The high availability of inorganic phosphate along the coast of Gabès is also associated with agricultural use of land along the coast [33]. For phosphates, eutrophication is identified by phosphate levels exceeding 0.68 μmol l−1 [34]. Very high concentrations of phosphates are recorded in coastal areas of the Gulf of Gabès and reflect a eutrophic state. In fact, phosphate concentrations ranged from 0.51 to 8.52 μmol L−1 (mean ± SD = 2.98 ± 2.44 μmol L−1) in the southern coast of Sfax [35]. They fluctuated between 1.25 to 2.97 μmol L−1 (mean ± SD = 2.07 ± 0.62 μmol L−1) in the northern coastal area of Sfax [36]. In the coastal waters of Gabès, phosphate concentrations ranged from 1.7 to 6.7 μmol L−1 (mean ± SD = 3.74 ± 1.65 μmol L−1) [17].

The application of an Eutrophication Index (E.I.) [37] was used by [17] in order to assess the eutrophication status of the coastal waters of Gabès. This index takes into consideration nitrites, nitrates, ammonium, phosphates and Chlorophyll-a. If E.I. is above 1.51, water quality is bad. Values of E.I. calculated in the Gulf of Gabès were > 2.16, indicating a high ecological alteration of the marine ecosystem [17].

Ammonium stands out as the predominant form of dissolved inorganic nitrogen, followed by nitrates, in the coastal waters of the Gulf of Gabès [17, 35, 36]. This dominance is a typical characteristic of untreated anthropogenic wastewater input [38].

The range (min–max) and mean values of dissolved inorganic nitrogen forms (ammonium, nitrates and nitrites) recorded in the Gulf of Gabès are given in Table 1, confirming the widespread status of eutrophication in the coastal waters of the Gulf of Gabès.

Southern coast of Sfax [35]Northern coast of Sfax [36]Coast of Gabès city [17]
Ammonium (μmol L−1)3.47–38.06 (13.26 ± 1.85)2.99–7.75 (5.01 ± 1.71)2.8–20.6 (8.73 ± 5.41)
Nitrates (μmol L−1)1.09–26.53 (7.56 ± 1.5)1.71–11.44 (3.07 ± 2.95)3.1–6.0 (0.6 ± 0.1)
Nitrites (μmol L−1)0.02–4.83 (0.82 ± 1.29)0.04–2.64 (0.37 ± 0.8)0.4–0.7 (3.07 ± 2.95)

Table 1.

Minimum, maximum and mean values of dissolved inorganic nitrogen forms in the Gulf of Gabès ± standard deviation from previous studies.

Eutrophication is recognized for ammonium when values are above 2.2 μmol L−1 [34].

Eutrophication is recognized for nitrates when values are above 1.19 μmol L−1 [34].

Advertisement

4. Signs of eutrophication in the Gulf of Gabès

Eutrophication yields a range of consequences impacting water quality, ecosystems, human health and economic activities [39].

Changes in coastal ecosystem states due to coastal eutrophication include:

  • Presence of low dissolved oxygen and formation of hypoxic or “dead” zones (oxygen-depleted waters) particularly on the bottom [6, 40]. Hypoxia and anoxia significantly affect living resources and can cause severe damage to fisheries [41].

  • A shift in the composition of phytoplankton species toward more tolerant and opportunistic species [42], creating favorable conditions for the proliferation of harmful algal blooms [43].

  • A decrease in zooplankton diversity [44] as larger-sized taxa are replaced by smaller ones [45, 46].

  • Loss of marine biodiversity of the aquatic community [47, 48] and the dominance of gelatinous organisms [49, 50].

  • A reduction in subaquatic vegetation due to excessive macroalgae and microalgae growth reduces light penetration [40, 51].

The Gulf of Gabès has exhibited these characteristic signs of eutrophication exacerbated by trace metals pollution over the last decades.

4.1 Degradation of water quality in the Gulf of Gabès

The seawater temperature range from 13°C during winter to 26°C in the summer [52]. The mean annual salinity is notably high, around 38 psu, and may surpass 39 psu during summer [53]. The lowest recorded salinity (36 psu) and pH (7.6) were observed in the spring in areas adjacent to discharges from TCG and urban wastewaters [17].

Various studies have highlighted deteriorations in water quality, including turbidity [18, 30, 54] and depletion in seawater oxygen levels [30, 55].

4.2 Decline of Posidonia oceanica in the Gulf of Gabès

The characterization and evaluation of specific responses to eutrophication in seagrasses offer a valuable tool for detecting changes in water quality in coastal areas, especially considering they are among the most widespread organisms in coastal waters [56, 57]. Eutrophication has been cited as a primary factor leading to the global decline of seagrass populations [58]. Therefore, Posidonia oceanica is suggested for use as a bioindicator to assess the health status of coastal habitats [59, 60]. The surface alkaline phosphatase activity in the seagrass P. oceanica can be used as a biomarker of eutrophication [57].

At the beginning of the twentieth century, the littoral beds of the endemic Mediterranean seagrass P. oceanica almost entirely covered the sea floor in Gulf of Gabès [61]. However, the present condition of P. oceanica indicates an ongoing decline in its meadows and its localized disappearance from multiple areas within the central part of Gabès Gulf [62]. Consequently, a noticeable decline in associated fish production has been consistently observed since 1990 [63]. The loss of the native vegetation cover in the Gulf of Gabès is estimated at 90%, with the P. oceanica beds being replaced by the opportunistic green algae Caulerpa prolifera in deeper zones [64]. This decline is a global phenomenon and is supposed to be primarily induced by eutrophication [65]. In addition to the effects of eutrophication, the warming of the sea may lead to synergistic effects and an increased rate of loss for these valuable ecosystems [66, 67]. The decline of P. oceanica in the Gulf of Gabès is linked to pollution from the phosphate industries [33, 62].

4.3 Phytoplankton and harmful microalgae blooms in the Gulf of Gabès

In the coastal region of the Gulf of Gabès, the phytoplankton community is composed of seven major groups: Dinophyceae (108 taxa), Bacillariophyceae (58 taxa), Cyanobacteria (5 taxa), Dictyochophyceae (1 taxon), Euglenophyceae (1 taxon), Coccolithophorideae (1 taxon) and Chlorophyceae (1 taxon) [68]. Within the identified species, ten have been recognized as potentially toxic, including Alexandrium minutum, Coolia monotis, Karenia selliformis, Protoceratium reticulatum [68], Amphidinium carterae, Dinophysis caudata, Prorocentrum lima, Prorocentrum minimum, Pseudonitzchia sp. [17] and Ostreopsis cf. ovata [69].

Since 1990, multiple blooms of toxic dinoflagellates have been detected in the Gulf of Gabès [70, 71, 72, 73]. Harmful algal blooms (HABs) of A. minutum formed in areas subjected to anthropogenic eutrophication such as Sfax Harbor and in confined lagoons in the Gulf [71]. The sudden A. minutum blooms along the nearshore of the Gulf of Gabès are complex, but phosphorus appears to be the key driving factor [71].

In 1994, K. selliformis was responsible for a significant intensive fish kill, estimated at 200 tons in the Gulf of Gabès [74, 75]. The occurrence of this taxon in the Gulf is related to high nitrate levels and is supported by elevated temperatures [76]. Typically, late summer and autumn are the periods of high bloom frequency of this taxon [70].

The abundance of Cyanobacteria in the Gulf of Gabès was positively correlated with inorganic nitrogen [70]. Blooms of Trichodesmium erythraeum were initially observed in July 1988 [77]. T. erythraeum blooms occurred approximately 2.11 times per year during the period from 1988 to 2013 [78]. Damages resulting from the toxic algal blooms cannot be considered resolved by reducing their populations. Indeed, numerous toxic Dinophyceae produce cysts at their blooming, successively accumulating in the sediments where they wait for the return of favorable conditions to germinate [79]. The encystment phenomenon is regular and frequent in the Gulf of Gabès but affects a low variety of species. During two decades of monitoring, eight different groups of cysts were recorded in the Gulf, with the dominance of ones of potentially toxic species [80, 81]. Even in the absence of algal inoculation from neighboring geographic areas, such toxic species can re-appear by the germination of the cysts in the sediments each time the conditions are favorable. Thus, the management of coastal areas has to carefully consider this “potential” harmful injection, even in the absence of algal blooms in the water column for many years.

4.4 Copepoda in the Gulf of Gabès

Zooplankton assemblages in the Gulf of Gabès were primarily dominated by copepods, accounting for 69–83% of the total zooplankton abundance [82]. A total of 52 species of Calanoida, 30 Cyclopoida and 11 Harpacticoida species were reported in the Gulf of Gabès [83, 84]. Notably, Cyclopoida, particularly Oithonidae (mainly Oithona nana), dominated copepod communities in the Gulf of Gabès [17, 35, 36, 82, 85]. We suggest that with increasing eutrophication over decades, a general shift to smaller-sized Copepoda with egg sacs, particularly the cyclopoid Oithona nana, was observed in the Gulf of Gabès. The success of Oithona spp. in eutrophicated and disturbed ecosystems is mainly due to their remarkable adaptability to changing environments than other species [86] as they are typical ecological generalists [83, 84]. In fact, the dominance of this species can be linked to a change in the food spectrum (and/or the fact that it does not spawn eggs into the water column). The possession of egg sacs is considered as an advantage in eutrophicated ecosystems that evolve hypoxic/anoxic bottom waters [7]. Spawned eggs that fall into the sediments may be prevented from hatching due to reduced oxygen levels. Therefore, the combination of a successful reproductive strategy, an omnivorous diet, and lower metabolic demands likely underlines the prominence of Oithona in the Gulf of Gabès [85, 87].

Advertisement

5. Conclusion

As documented by a number of investigations, eutrophication is a serious problem for the biodiversity in the Gulf of Gabès. However, since the Gulf also experienced chemical pollution by trace metals, and overfishing, eutrophication may not have been the only factor. The enrichment of nutrients, especially phosphorus, interacts with these factors and, in addition, with climate change. Due to cumulative anthropogenic pressures, integrated management of the coastal marine environment of the Gulf of Gabès remains necessary to re-direct the ecosystem functioning toward a healthier status and a restoration of ecosystem services [88, 89] possibly compromised. Efforts in the Gulf of Gabès to contain eutrophication involve a policy of environmentally sustainable development, with tighter industrial regulations, enhanced agriculture and improved wastewater management. The heavy socio-economic impact of such a policy is only apparent. In fact, the decision should be sustained by detailed studies on the economic convenience of such an approach, with a precise monetization of what the present situation subtracts in terms of ecosystem services to society. The restoration of good environmental status, in addition, would not be a cost for managers because open gulfs (such as the Gabès one) should be easily re-populated. Living organisms, in fact, can go elsewhere when local conditions are adverse or can undergo a lethargic condition, waiting for the return of suitable conditions in the sediments for years [90, 91]. The re-covering of a good environmental status (and the re-launch of ecosystem services) could be, consequently, a fast process.

References

  1. 1. Smith VH. Using primary productivity as an index of coastal eutrophication: The units of measurement matter. Journal of Plankton Research. 2006;29(1):1-6
  2. 2. Chen X, Wang Y, Cai Z, Zhang M, Ye C. Response of the nitrogen load and its driving forces in estuarine water to dam construction in Taihu Lake, China. Environmental Science and Pollution Research International. 2020;27(25):31458-31467
  3. 3. Wurtsbaugh WA, Paerl HW, Dodds WK. Nutrients, eutrophication and harmful algal blooms along the freshwater to marine continuum. WIREs Water. 2019;6(5):e1373
  4. 4. Directive EUW. Council directive of 21 May 1991 concerning urban waste water treatment (91/271/EEC). Journal of European Communities. 1991;34:40
  5. 5. Schindler DW. Eutrophication and recovery in experimental lakes: Implications for lake management. Science. 1974;184(4139):897-899
  6. 6. Malone TC, Newton A. The globalization of cultural eutrophication in the coastal ocean: Causes and consequences. Frontiers in Marine Science. 2020;7:670
  7. 7. Marcus N. An overview of the impacts of eutrophication and chemical pollutants on copepods of the coastal zone. Zoological Studies. 2004;43(2):211-217
  8. 8. Glibert PM, Burford MA. Globally changing nutrient loads and harmful algal blooms: Recent advances, new paradigms, and continuing challenges. Oceanography. 2017;30(1):58-69
  9. 9. Primpas I, Karydis M. Scaling the trophic index (TRIX) in oligotrophic marine environments. Environmental Monitoring and Assessment. 2011;178(1-4):257-269
  10. 10. Karydis M, Kitsiou D. Eutrophication and environmental policy in the Mediterranean Sea: A review. Environmental Monitoring and Assessment. 2012;184:4931-4984
  11. 11. Group TM, de Madron XD, Guieu C, Sempéré R, Conan P, Cossa D, et al. Marine ecosystems’ responses to climatic and anthropogenic forcings in the Mediterranean. Progress in Oceanography. 2011;91(2):97-166
  12. 12. Unep/Map. State of the Mediterranean marine and coastal environment. In: United Nations Environment Programme/Mediterranean Action Plan (UNEP/MAP). Athens: Barcelona Convention; 2012. p. 96
  13. 13. Yilmaz A, Baesturk O, Ediger D, Ylmaz K, Hatipoglu E. Eutrophication in Iskenderun Bay, North-Eastern Mediterranean. In: Science of the Total Environment. Amsterdam: Elsevier; 1992. pp. 705-717
  14. 14. Moncheva S, Gotsis-Skretas O, Pagou K, Krastev A. Phytoplankton blooms in Black Sea and Mediterranean coastal ecosystems subjected to anthropogenic eutrophication: Similarities and differences. Estuarine, Coastal and Shelf Science. 2001;53(3):281-295
  15. 15. Pavlidou A, Simboura N, Rousselaki E, Tsapakis M, Pagou K, Drakopoulou P, et al. Methods of eutrophication assessment in the context of the water framework directive: Examples from the eastern Mediterranean coastal areas. Continental Shelf Research. 2015;108:156-168
  16. 16. Viaroli P, Nizzoli D, Pinardi M, Soana E, Bartoli M. Eutrophication of the Mediterranean Sea: A watershed—Cascading aquatic filter approach. Rendiconti Lincei. Scienze Fisiche e Naturali. 2015;26(1):13-23
  17. 17. Annabi-Trabelsi N, Guermazi W, Leignel V, Al-Enezi Y, Karam Q , Ali M, et al. Effects of eutrophication on plankton abundance and composition in the Gulf of Gabès (Mediterranean Sea, Tunisia). Water. 2022;14(14):2230
  18. 18. Katlane R, Nechad B, Ruddick K, Zargouni F. Optical remote sensing of turbidity and total suspended matter in the Gulf of Gabes. Arabian Journal of Geosciences. 2013;6(5):1527-1535
  19. 19. El Zrelli R, Rabaoui L, Alaya MB, Daghbouj N, Castet S, Besson P, et al. Seawater quality assessment and identification of pollution sources along the central coastal area of Gabes gulf (SE Tunisia): Evidence of industrial impact and implications for marine environment protection. Marine Pollution Bulletin. 2018;127:445-452
  20. 20. Rabaoui L, Balti R, Zrelli R, Tlig-Zouari S. Assessment of heavy metals pollution in the gulf of Gabes (Tunisia) using four mollusk species. Mediterranean Marine Science. 2013;15(1):45
  21. 21. El Zrelli R, Courjault-Radé P, Rabaoui L, Castet S, Michel S, Bejaoui N. Heavy metal contamination and ecological risk assessment in the surface sediments of the coastal area surrounding the industrial complex of Gabes city, Gulf of Gabes, SE Tunisia. Marine Pollution Bulletin. 2015;101(2):922-929
  22. 22. Sammari C, Koutitonsky VG, Moussa M. Sea level variability and tidal resonance in the Gulf of Gabes, Tunisia. Continental Shelf Research. 2006;26(3):338-350
  23. 23. Othmani A, Béjaoui B, Chevalier C, Elhmaidi D, Devenon JL, Aleya L. High-resolution numerical modelling of the barotropic tides in the Gulf of Gabes, eastern Mediterranean Sea (Tunisia). Journal of African Earth Sciences. 2017;129:224-232
  24. 24. Mezghani-Chaari S, Hamza A, Hamza-Chaffai A. Mercury contamination in human hair and some marine species from Sfax coasts of Tunisia: Levels and risk assessment. Environmental Monitoring and Assessment. 2011;180:477-487
  25. 25. Gargouri D, Gzam M, Kharroubi A, Jedoui Y. Use of sediment quality indicators for heavy metals contamination and ecological risk assessment in urbanized coastal zones. Environmental Earth Sciences. 2018;77:1-8
  26. 26. Kharroubi A, Gzam M, Jedoui Y. Anthropogenic and natural effects on the water and sediments qualities of costal lagoons: Case of the Boughrara Lagoon (Southeast Tunisia). Environmental Earth Sciences. 2012;67:1061-1067
  27. 27. Bejaoui B, Rais S, Koutitonsky V. Modélisation de la dispersion du phosphogypse dans le golfe de Gabès. INSTM Bulletin: Marine and Freshwater Sciences. 2004;31:113-119
  28. 28. Rutherford PM, Dudas MJ, Samek RA. Environmental impacts of phosphogypsum. Science of the Total Environment. 1994;149(1-2):1-38
  29. 29. Ajmal PY, Bhangare RC, Tiwari M, Sahu SK, Pandit GG. External gamma radiation levels and natural radioactivity in soil around a phosphate fertilizer plant at Mumbai. Journal of Radioanalytical and Nuclear Chemistry. 2014;300:23-27
  30. 30. El Kateb A, Stalder C, Rüggeberg A, Neururer C, Spangenberg JE, Spezzaferri S. Impact of industrial phosphate waste discharge on the marine environment in the Gulf of Gabes (Tunisia). PLoS One. 2018;13(5):e0197731
  31. 31. Correll DL. The role of phosphorus in the eutrophication of receiving waters: A review. Journal of Environmental Quality. 1998;27(2):261-266
  32. 32. Ngatia L, Grace JM III, Moriasi D, Taylor R. Nitrogen and phosphorus eutrophication in marine ecosystems. Monitoring of Marine Pollution. 2019;1:1-17
  33. 33. Brahim MB, Hamza A, Hannachi I, Rebai A, Jarboui O, Bouain A, et al. Variability in the structure of epiphytic assemblages of Posidonia oceanica in relation to human interferences in the Gulf of Gabes. Tunisia. Marine Environmental Research. 2010;70(5):411-421
  34. 34. Ignatiades L, Karydis M, Vounatsou P. A possible method for evaluating oligotrophy and eutrophication based on nutrient concentration scales. Marine Pollution Bulletin. 1992;24(5):238-243
  35. 35. Salem ZB, Drira Z, Ayadi H. What factors drive the variations of phytoplankton, ciliate and mesozooplankton communities in the polluted southern coast of Sfax, Tunisia? Environmental Science and Pollution Research. 2015;22:11764-11780
  36. 36. Drira Z, Kmiha-Megdiche S, Sahnoun H, Tedetti M, Pagano M, Ayadi H. Copepod assemblages as a bioindicator of environmental quality in three coastal areas under contrasted anthropogenic inputs (Gulf of Gabes, Tunisia). Journal of the Marine Biological Association of the United Kingdom. 2018;98(8):1889-1905
  37. 37. Primpas I, Tsirtsis G, Karydis M, Kokkoris GD. Principal component analysis: Development of a multivariate index for assessing eutrophication according to the European water framework directive. Ecological Indicators. 2010;10(2):178-183
  38. 38. Sahraoui I, Grami B, Bates SS, Bouchouicha D, Chikhaoui MA, Mabrouk HH, et al. Response of potentially toxic pseudo-nitzschia (Bacillariophyceae) populations and domoic acid to environmental conditions in a eutrophied, SW Mediterranean coastal lagoon (Tunisia). Estuarine, Coastal and Shelf Science. 2012;102:95-104
  39. 39. Hwang SJ. Eutrophication and the ecological health risk. International Journal of Environmental Research and Public Health IJERPH. 2020;17(17):6332
  40. 40. Rabalais NN, Cai WJ, Carstensen J, Conley DJ, Fry B, Hu X, et al. Eutrophication-driven deoxygenation in the coastal ocean. Oceanography. 2014;27(1):172-183
  41. 41. Karim MR, Sekine M, Ukita M. Simulation of eutrophication and associated occurrence of hypoxic and anoxic condition in a coastal bay in Japan. Marine Pollution Bulletin. 2002;45(1-12):280-285
  42. 42. McQuatters-Gollop A, Gilbert AJ, Mee LD, Vermaat JE, Artioli Y, Humborg C, et al. How well do ecosystem indicators communicate the effects of anthropogenic eutrophication? Estuarine, Coastal and Shelf Science. 2009;82(4):583-596
  43. 43. Brush MJ, Giani M, Totti C, Testa JM, Faganeli J, Ogrinc N, et al. Eutrophication, harmful algae, oxygen depletion, and acidification. In: Coastal Ecosystems in Transition: A Comparative Analysis of the Northern Adriatic and Chesapeake Bay. In: Malone TC, Malej A, Faganeli J, editors. Geophysical Monograph Series 256. American Geophysical Union. 1st ed. Hoboken, NJ, USA: John Wiley and Sons; 2020. pp. 75-104
  44. 44. Loanna S-F, Papathanassiou E, Lepretre A, Frontier S. Zooplankton assemblages and influence of environmental parameters on them in a Mediterranean coastal area. Journal of Plankton Research. 1998;20(5):847-870
  45. 45. Uye S-I. Replacement of large copepods by small ones with eutrophication of embayments: Cause and consequence. In: Hydrobiologia. Hamburg: Springer; 1994;292/293:513-519
  46. 46. Belmonte G, Moscatello S, Hajdëri E, Vaglio I, Denitto F. Composition and spatial distribution of mesozooplankton along confinement and anthropogenic-impact gradients in the gulf of Vlore (Albania). Journal of Coastal Research. 2018;34(1):174-184
  47. 47. Horta PA, Rörig LR, Costa GB, Baruffi JB, Bastos E, Rocha LS, et al. Marine eutrophication: Overview from now to the future. In: Häder DP, Helbling EW, Villafañe VE, editors. Anthropogenic Pollution of Aquatic Ecosystems. Cham: Springer; 2021. pp. 157-180. DOI: 10.1007/978-3-030-75602-4_8
  48. 48. Fetahi T. Eutrophication of Ethiopian water bodies: A serious threat to water quality, biodiversity and public health. African Journal of Aquatic Science. 2019;44(4):303-312
  49. 49. Richardson AJ, Bakun A, Hays GC, Gibbons MJ. The jellyfish joyride: Causes, consequences and management responses to a more gelatinous future. Trends in Ecology & Evolution. 2009;24(6):312-322
  50. 50. Hashim AR, Kamaruddin SA, Buyong F, Mat Nazir EN, Che Ismail CZ, Tajam J, et al. Jellyfish blooming: Are we responsible? In: ICAN International Virtual Conference 2022 (IIVC 2022) Proceedings–Navigating the VUCA World: Harnessing the Role of Industry Linkages, Community Development and Alumni Network in Academia. Arau, Malaysia; 2022. pp. 51-60
  51. 51. Adams JB, Taljaard S, Van Niekerk L, Lemley DA. Nutrient enrichment as a threat to the ecological resilience and health of south African microtidal estuaries. African Journal of Aquatic Science. 2020;45(1-2):23-40
  52. 52. Béjaoui B, Ben Ismail S, Othmani A, Hamida OBA-BH, Chevalier C, Feki-Sahnoun W, et al. Synthesis review of the Gulf of Gabes (eastern Mediterranean Sea, Tunisia): Morphological, climatic, physical oceanographic, biogeochemical and fisheries features. Estuarine, Coastal and Shelf Science. 2019;219:395-408
  53. 53. Mounir BB, Asma H, Sana BI, Lotfi M, Abderrahmen B, Lotfi A. What factors drive seasonal variation of phytoplankton, protozoans and metazoans on leaves of Posidonia oceanica and in the water column along the coast of the Kerkennah Islands, Tunisia? Marine Pollution Bulletin. Amsterdam: Elsevier; 2013;71(1-2):286-298
  54. 54. Darmoul B. Pollution Dans le Golfe de Gabès (Tunisie): Bilan de Six Années de Surveillance (1976-1981). Institut National des Sciences et Technologies de la Mer; 1988;15:61-84
  55. 55. Mosbahi N, Pezy JP, Dauvin JC, Neifar L. COVID-19 pandemic lockdown: An excellent opportunity to study the effects of trawling disturbance on macrobenthic Fauna in the shallow waters of the Gulf of Gabès (Tunisia, Central Mediterranean Sea). International Journal of Environmental Research and Public Health. 2022;19(3):1282
  56. 56. Spalding M, Taylor M, Ravilious C, Short FT, Green E. Global overview: The distribution and status of seagrasses. In: Green EP, Short FT, editors. World Atlas of Seagrasses. 1st edition. Berkeley: University of California Press; 2003. pp. 5-26
  57. 57. Martínez-Crego B, Romero J, Alcoverro T. The use of surface alkaline phosphatase activity in the seagrass Posidonia oceanica as a biomarker of eutrophication. Marine Ecology. 2006;27(4):381-387
  58. 58. Green EP, Short FT. World Atlas of Seagrasses. Prepared by the UNEP World Conservation Monitoring Centre. 1st ed. Berkeley, USA: University of California Press; 2003. pp. 1-324
  59. 59. Cannac M, Ferrat L, Pergent-Martini C, Pergent G, Pasqualini V. Effects of fish farming on flavonoids in Posidonia oceanica. Science of the Total Environment. 2006;370(1):91-98
  60. 60. Bonanno G, Di Martino V. Trace element compartmentation in the seagrass Posidonia oceanica and biomonitoring applications. Marine Pollution Bulletin. 2017;116(1-2):196-203
  61. 61. Zaouali J. Les peuplements benthiques de la petite Syrte, golfe de Gabès-Tunisie. Résultats de la campagne de prospection du mois de juillet 1990, Etude préliminaire: Biocénoses et thanatocénoses récentes. Life. 1990;3(1-2):47-60
  62. 62. El Zrelli R, Courjault-Radé P, Rabaoui L, Daghbouj N, Mansour L, Balti R, et al. Biomonitoring of coastal pollution in the Gulf of Gabes (SE, Tunisia): Use of Posidonia oceanica seagrass as a bioindicator and its mat as an archive of coastal metallic contamination. Environmental Science and Pollution Research. 2017;24:22214-22225
  63. 63. Hamza-Chaffai A, Pellerin J, Amiard JC. Health assessment of a marine bivalve Ruditapes decussatus from the Gulf of Gabès (Tunisia). Environment International. 2003;28(7):609-617
  64. 64. Ramos-Espla A, Ouergui A, Bayle JT, Ben Mbarek N, Fernanadez- Troquemada Y, Gallouza S, et al. Contribution à la caracterisation des herbiers à Posidonia oceanica (L.) Delile aux iles Kerkennah (est de la Tunisie, mediterranée orientale). In: Proceedings of the First Mediterranean Symposium on Marine Vegetation. Ajaccio, France; 2000. pp. 177-181
  65. 65. Touchette BW, Burkholder JM, Glasgow HB. Variations in eelgrass (Zostera marina L.) morphology and internal nutrient composition as influenced by increased temperature and water column nitrate. Estuaries. 2003;26:142-155
  66. 66. Lloret J, Marín A, Marín-Guirao L. Is coastal lagoon eutrophication likely to be aggravated by global climate change? Estuarine, Coastal and Shelf Science. 2008;78(2):403-412
  67. 67. Pazzaglia J, Santillán-Sarmiento A, Helber SB, Ruocco M, Terlizzi A, Marín-Guirao L, et al. Does warming enhance the effects of eutrophication in the seagrass Posidonia oceanica? Frontiers in Marine Science. 2020;7:564805
  68. 68. Feki-Sahnoun W, Hamza A, Béjaoui B, Mahfoudi M, Rebai A, Bel HM. Multi-table approach to assess the biogeography of phytoplankton: Ecological and management implications. Hydrobiologia. 2018;815:229-251
  69. 69. Abdennadher M, Zouari AB, Sahnoun WF, Alverca E, Penna A, Hamza A. Ostreopsis cf. ovata in the Gulf of Gabès (South-Eastern Mediterranean Sea): Morphological, molecular and ecological characterization. Harmful Algae. 2017;63:56-67
  70. 70. Drira Z, Hamza A, Belhassen M, Ayadi H, Bouaïn A, Aleya L. Dynamics of dinoflagellates and environmental factors during the summer in the Gulf of Gabes (Tunisia, eastern Mediterranean Sea). Scientia Marina. 2008;72(1):59-71
  71. 71. Abdenadher M, Hamza A, Fekih W, Hannachi I, Bellaaj AZ, Bradai MN, et al. Factors determining the dynamics of toxic blooms of Alexandrium minutum during a 10-year study along the shallow southwestern Mediterranean coasts. Estuarine, Coastal and Shelf Science. 2012;106:102-111
  72. 72. Walha LD, Hamza A, Keskes FA, Cibic T, Mechi A, Mahfoudi M, et al. Heavy metals accumulation in environmental matrices and their influence on potentially harmful dinoflagellates development in the Gulf of Gabes (Tunisia). Estuarine, Coastal and Shelf Science. 2021;254:107317
  73. 73. Feki-Sahnoun W, Njah H, Abdennadher M, Hamza A, Barraj N, Mahfoudi M, et al. A Naïve Bayesian network approach to determine the potential drivers of the toxic dinoflagellate Coolia monotis (Meunier, 1919) in the Gulf of Gabès, Tunisia. Euro-Mediterranean Journal for Environmental Integration. 2019;4:1-11
  74. 74. Hamza A, El Abed A. Les eaux colorées dans le golfe de Gabes. Bulletin de l’Institut National Scientifique et Technique d’Océanographie et de Pêche de Salammbo. 1994;21:66-77
  75. 75. Souâd T, El Abed A. On the presence of potentially toxic algae in the lagoons of Tunisia. Harmful Algae News. 2001;22:10
  76. 76. Feki W, Hamza A, Frossard V, Abdennadher M, Hannachi I, Jacquot M, et al. What are the potential drivers of blooms of the toxic dinoflagellate Karenia selliformis? A 10-year study in the Gulf of Gabes, Tunisia, southwestern Mediterranean Sea. Harmful Algae. 2013;23:8-18
  77. 77. Hamza A, Naceur BEN. Sur l’apparition du phénomène" d’eau rouge" dans le golfe de Gabès en été 1988. INSTM Bulletin: Marine and Freshwater Sciences. 1990;17:5-16
  78. 78. Sabeur HI, Wafa FS, Asma H, Malika BH. Long term characterization of Trichodesmium erythraeum blooms in Gabès gulf (Tunisia). Continental Shelf Research. 2016;124:95-103
  79. 79. Belmonte G, Rubino F. Cysts and resting eggs from marine zooplankton: Dimension of the phenomenon, physiology of rest, and ecological and biogeographic implications. In: Alekseev VR, Pinel-Alloul B, editors. Dormancy in Aquatic Organisms Theory, Human Use and Modeling [Internet], Monographiae Biologicae. Vol. 92. Cham: Springer International Publishing; 2019. pp. 71-94. Available from: http://link.springer.com/10.1007/978-3-030-21213-1_5
  80. 80. Keskes FA, Ayadi N, Atoui A, Mahfoudi M, Abdennadher M, Walha LD, et al. Dinoflagellates encystment with emphasis on blooms in Boughrara lagoon (South-Western Mediterranean): Combined effects of trace metal concentration and environmental context. Estuarine, Coastal and Shelf Science. 2020;237:106648
  81. 81. Abdelmouleh F, Hamza A, Mahfoudi M, Walha LD, Barraj N, Hassen MB. Encystment of dinoflagellate in tidal coasts of Gabes gulf (Tunisia): Analyse of long term observations. INSTM Bulletin: Marine and Freshwater Sciences. 2018;45:23-26
  82. 82. Drira Z, Belhassen M, Ayadi H, Hamza A, Zarrad R, Bouaïn A, et al. Copepod community structure related to environmental factors from a summer cruise in the Gulf of Gabès (Tunisia, eastern Mediterranean Sea). Journal of the Marine Biological Association of the United Kingdom. 2010;90(1):145-157
  83. 83. Annabi-Trabelsi N, Guermazi W, Ayadi H. Cyclopoida and Harpacticoida (crustacea: Copepoda) of the Gulf of Gabès: A review. Thalassia Salentina. 2020;2020(42):93-98
  84. 84. Annabi-Trabelsi N, Guermazi W, Ayadi H. Marine Calanoida (crustacea: Copepoda) of the Gulf of Gabes: A review. Thalassia Salentina. 2020;2020(42):99-106
  85. 85. Drira Z, Bel Hassen M, Ayadi H, Aleya L. What factors drive copepod community distribution in the Gulf of Gabes, eastern Mediterranean Sea? Environmental Science and Pollution Research. 2014;21(4):2918-2934
  86. 86. Chihoub S, Christaki U, Chelgham S, Amara R, Ramdane Z, Zebboudj A, et al. Coastal eutrophication as a potential driver of functional homogenization of copepod species assemblages in the Mediterranean Sea. Ecological Indicators. 2020;115:106388
  87. 87. Ben Ltaief T, Drira Z, Hannachi I, Bel Hassen M, Hamza A, Pagano M, et al. What are the factors leading to the success of small planktonic copepods in the Gulf of Gabes, Tunisia? Journal of the Marine Biological Association of the United Kingdom. 2015;95(4):747-761
  88. 88. Pepper IL, Gerba CP, Brusseau ML. Environmental and Pollution Science. Amsterdam: Elsevier; 2011
  89. 89. Costanza R, d’Arge R, De Groot R, Farber S, Grasso M, Hannon B, et al. The value of the world’s ecosystem services and natural capital. Nature. 1997;387(6630):253-260
  90. 90. Kerfoot WC, Weider LJ. Experimental paleoecology (resurrection ecology): Chasing Van Valen’s red queen hypothesis. Limnology and Oceanography. 2004;49(4 part 2):1300-1316
  91. 91. Belmonte G, Rubino F. Resting cysts from coastal marine plankton. Oceanography and Marine Biology. An Annual Review. In: Hawkins SJ, Allcock AL, Bates AE, Firth LB, Smith IP, Swearer SE, et al, editors. Boca Raton: CRC Press; Vol. 57. 2019. pp. 1-88

Written By

Neila Annabi-Trabelsi, Mohammad Ali, Genuario Belmonte, Habib Ayadi and Wassim Guermazi

Submitted: 09 October 2023 Reviewed: 12 December 2023 Published: 29 December 2023