Solar Salterns and Pollution: Comparison
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Solar salterns and salt marshes are unique ecosystems with special physicochemical features and characteristic biota. There are very few studies focused on the impacts of pollution on these economic and ecological systems. Unfortunately, diversified pollution (metals, Polycyclic Aromatic Hydrocarbons, etc.) has been detected in these complex ecosystems. These hypersaline environments are under increasing threat due to anthropogenic pressures.

  • solar salterns
  • biota
  • pollution
  • bioremediation

1. Introduction

Solar salterns have considerable economic, ecological, and scientific value. They are distributed globally along tropical and subtropical coasts in arid and semiarid regions [1,2][1][2]. They are mainly distributed in Mediterranean regions, where the climate is characterized by long dry periods in the summer, during which evaporation of seawater in ponds is accentuated [3]. Multi-pond salterns are human-controlled semi-artificial coastal systems designed to harvest NaCl from seawater for human consumption. In this system, seawater is pumped through a series of separate shallow ponds (Figure 1) that are typically less than 0.5 m in depth [4], in which it is gradually driven to ponds of greater salinities, ranging from seawater to sodium chloride saturation and sometimes even beyond [5]. Salterns are well known as continuous or semi-continuous systems because each set of ponds is characterized by a distinct range of salinity and biogeochemical attributes [6,7][6][7]. These thalassohaline environments are operated in repeated cycles of feeding with natural saltwater, increasing salt concentration due to water evaporation, and, finally, salt precipitation. Hence, they have certain attributes of semi-closed chemostats [6].
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Figure 1. Water flow in solar salterns: the direction of the water circulation is indicated by the arrows.

2. Physicochemical Parameters

Salterns are hypersaline extreme ecosystems with unique abiotic features, including a wide range of salinities, low oxygen, and intense ultraviolet radiation [1,7][1][7]. The physicochemical properties of seawater change due to evaporation in the flow-through multi-pond system. Although the pH of seawater is slightly alkaline, owing to carbonate buffering systems, the pH of saline water in salterns is generally close to neutral in ponds with biota [3,8,9,10,11,12][3][8][9][10][11][12]. The pH of ponds in salterns can be regulated via the salinity, temperature, and amount of carbonate ions [2]. It was shown to gradually decrease, along the distinct ponds, from 8.3 for seawater to 5.8 for magnesium chloride solutions as measured in the Sfax solar saltern in Tunisia [13] and exhibits little seasonal variation [14]. The nutrient concentrations found in solar salterns depend on a variety of parameters. Geographic factors influencing nutrients include the proximity to rivers, urban pollution, the nutrient status of the incoming seawater, and climate change [15]. The nature and extent of the fauna and flora, the season of productivity, and management practices also influence nutrient concentration [15]. According to Kobbi-Rebai [16], the internal recycling processes such as the release from sediment and the mineralization of organic matter are the key drivers of phosphorous concentrations in ponds. However, these concentrations are mainly impacted by the seawater inflow in the first pond [16]. Total phosphorus (TP) would be one of the most suitable chemical parameters from which to propose a methodology for the determination of trophic status in solar salterns [17]. Among solar salterns, both oligotrophic [18,19][18][19] and eutrophic systems [11,20,21,22,23,24][11][20][21][22][23][24] have been described. However, nutrients are concentrated in first ponds and decrease with increases in the salt concentration [22]. Nitrate and nitrite concentrations are influenced by halophilic bacteria activity [25]. Extremely halophilic denitrifying bacteria in hypersaline environments reduce nitrate to nitrite, nitrous oxide, and even dinitrogen [26].

3. Biota

The biota of the salterns are not only of great scientific interest, but also have a direct impact on the quality and the quantity of the salt produced via evaporation and precipitation [6,27][6][27]. Solar salterns are inhabited by highly specialized extremophiles (Figure 2). Many ecological changes happen throughout the salinity gradient. Biodiversity decreases with the increase in salinity [9,11,28,29,30[9][11][28][29][30][31],31], with the zonal biological community structure ranging from marine to extreme halophilic communities [9,32,33,34][9][32][33][34]. Archaea and Bacteria are the two components of the microbial community in solar salterns [28,35,36][28][35][36]. These organisms are generally members of the archaeal Halobacteria class and in the bacterial family of Salinibacteraceae (Rhodothermia class) [37,38][37][38]. Nevertheless, relatively high species richness is noted within each class [39]. Analysis of prokaryotic communities’ compositions in solar salterns in Mexico, Spain, Tunisia, and Turkey showed that the most highly represented genera were Haloquadratum, followed by Halorubrum, Haloarcula, and Halonotius [40,41,42,43][40][41][42][43]. In the crystallizer ponds, which have very low prokaryotic diversity with Archaea making up the dominant fraction [44[44][45],45], the most abundant Archaea observed were Haloquadratum walsbyi and Halorubrum sp. [5]. Salinibacter phylotypes and other Bacteroidetes are highly abundant in the microbial community [44,46,47][44][46][47]. However, in lower salinity ponds, a more diverse assemblage of Archaea and Bacteria was detected [47].
The phytoplankton community of Dinophyta and Diatomeae found in lower salinities was replaced by a community of Dunaliella and Cyanobacteria adapted to higher salt concentrations [9,11,22,48,49,50][9][11][22][48][49][50]. A shift was observed from Diatomeae to Dinophyta dominance along the salinity gradient (from 38 to 86 psu), as exemplified in the Sfax solar saltern in Tunisia [51]. This salinity gradient was negatively correlated with the amount of Diatomeae, while it was positively correlated with the amount of Dinophyta [51]. The Chlorophyta Dunaliella salina and the Cyanobacteria Aphanothece sp. and Phormidium sp. dominated the phytoplanktonic community in the saltiest ponds from 190 to 476 psu [9]. Dunaliella salina is the most ubiquitous eukaryotic microorganism in hypersaline environments [15]. The phytoplankton community in the crystallizer ponds (TS > 300 psu) was entirely composed by D. salina (for the Sfax solar saltern, see [9,30][9][30]). Dunaliella salina release enzymes and nitrogen compounds into the water which favor the growth of halophilic bacteria and, in turn, accelerate evaporation [31]. According to Elloumi et al. [9], the Ciliophora community is dominated by Oligotrichida (Strobilidium sp., Strombidium sp., Tintinnides sp.) at salinities from 41 psu to 46.9 psu. The Prostomatida Urotricha sp. became the dominant taxon at salinity values of 45.6–146.8 psu, but from 184 to 203.2 psu the Ciliophora shifted to a dominance of Heterotrichida (Fabrea salina and Blepharisma sp.), Hymenostomata (Uronema sp.), and Gymnostomatida (Encheylodon sp.).
Among zooplankton groups, Artemiidae (Branchiopoda) and Copepoda are the most abundant groups in hypersaline ecosystems [14,52,53,54,55,56][14][52][53][54][55][56]. In keeping with their fluctuations in abundance along the salinity gradient in the Sfax solar saltern, Copepoda species are split into thalassophilic species (species whose abundance decreases with increasing salinity) and halophilic species (species whose abundance increases with increasing salinity) [12,16,34,51,56][12][16][34][51][56]. At salinities from 157 to 312 psu, the euryhaline Artemia spp. is the only zooplanktonic taxon [14,54,56,57][14][54][56][57].
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Figure 2. Distribution of the dominant living beings (plankton and heterotrophic prokaryotes) along the salinity gradient in solar salterns.

4. Pollution Diversity in Solar Salterns

Hypersaline environments, including solar salterns and salt marshes, are often polluted with various contaminants [59,60][58][59]. They are fragile econiches and are very susceptible to disturbances [61][60]. Knowledge of pollution existing in solar salterns is not generalizable to every site and the completion of analyses of a great number of sites remains to be achieved (Table 1).
The metal (Cd, Cu, Pb, and Zn) concentrations in the salt marsh sediments of the Karnaphuli River coast (Bangladesh) are related to contamination from domestic and industrial discharges [62][61] (Table 1). The metal concentrations in the sediments were: 105.0 ppm for Zn, 26.70 ppm for Pb, 45.79 ppm for Cu, and 0.43 ppm for Cd [62][61]. The Ribandar solar salterns (India) are fed by the Mandovi Estuary and are, in turn, vulnerable to metal effluent influxes from ferromanganese ore mining activity, barge traffic, and sewage disposal, affecting the water and sediment quality in the salt pan and its inhabitant organisms [63][62]. Sediment quality indicates that the Ribandar solar saltern sediments were moderately contaminated by Co, Fe, Mn, Ni, Pb, and Zn during the salt-making seasons [63][62]. The concentrations of heavy metals in the sediments ranged from a minimum of 1.7 ± 0.1–2.6 ± 0.7 ppm Pb to a maximum of 44 ± 21.6–62.8 ± 23.6 ppm Zn [63][62] (Table 1).
In the Pomorie brine salterns (the Black Sea, Bulgaria), the distribution of Pb and Cu in the three constituents of the brine system, the salt solution, colloidal particles, and biota (Halobacterium salinarium and microalgae Dunaliela salina), showed the highest percentages in biota, at 45% and 48%, respectively [64][63]. However, Cd and Bi have not been detected in biota and are uniformly distributed between the salt solution and colloidal particles [64][63] (Table 1).
A comparison of the concentrations of trace metals in the sediments of three salt marshes (Tinto, Odiel, and Piedras) in Huelva, Spain showed that the Tinto sediments were the most polluted, with high amounts of As (600 ppm), Cu (3300 ppm), and Zn (2500 ppm) [65][64] (Table 1). On the other hand, the Piedras estuary had not been affected by anthropogenic inputs and was the least polluted estuary [65][64].
As an example of pollution and dysfunction in the hypersaline ecosystem, wresearchers present the case of the Sfax solar saltern in Tunisia. Since the 1950s, there has been rapid industrialization and urbanization along the coastal area near the solar saltern. Thus, the treated domestic wastewater (pH 8.3) and the untreated industrial wastewater released diversified pollutants. For example, near the Sfax solar saltern (Tunisia), the phosphate treatment plant, SIAPE, and the gypsum water produced from the lixiviation of SIAPE phosphogypsum deposits are sources of heavy metals which are rapidly precipitated in marine sediments [66,67,68,69][65][66][67][68]. Such a mixture of effluents, which has a pH of 3, facilitated the dissolution of heavy metals, thus enhancing the movement of the bioavailable ionic forms of these metals in seawater.
The brine metal concentrations in the Sfax solar saltern vary from 0.065 to 1.57 mg L−1 for Zn, 0.002–0.034 mg L−1 for Cd, 0.006–0.064 mg L−1 for Cu, and 0.002–0.128 mg L−1 for Pb. The analysed metals are present in the following order: Zn > Pb > Cu > Cd. The computed enrichment factors (EFs) showed significant brine contamination due the impact of industrial particulate fallout highly enriched with heavy metals [70][69]. In fact, concentrations of trace metals in surface sediment samples have shown Fe varying from 8750 to 8889 ppm of dry weight, Zn from 39.92 to 574.89 ppm of dry weight, Pb from 18.98 to 233.46 ppm of dry weight, Ni from 17.47 to 160.92 ppm of dry weight, Cu from 13 to 98 ppm of dry weight, and Cd from 4.86 to 37.42 ppm of dry weight [69][68]. The highest metal concentrations have been found in sites frequently subject to local pollutant sources and in sites often saturated by high-tide marine water which drains industrial waste from the port area. This agrees with the findings of Amdouni [71][70], who reported the presence of a variety of metals (Al, Cd, Cu, Pb, and Zn) in crystallization ponds.
According to Amdouni [72][71], the concentrations of trace elements in brines are affected by the evaporation phenomenon in the same way as those of the major elements. Initially, the evaporation effect is very limited and the behavior of trace elements is under the direct influence of the biological activities which colonize the first ponds of the saline saltern. Thus, the evolution of trace element concentration seems to be controlled only by the evaporation–salt precipitation antagonist effect in the more concentrated brine where biological activity is absent or very limited. However, the concentrations of trace metals such as mercury, copper, zinc, lead, and cadmium in cysts and biomasses of Artemia (Branchiopoda) originating from the Sfax solar saltern are lower than those recorded in other strains, i.e., those from other localities that are already commercialized and used in larval fish feeding [73][72]. The lowest bioaccumulation of trace elements in Artemia was observed at the highest salinity (190 psu) [74][73]. In fact, the bioavailability of elements often decreases with increasing salinity due to trace element complexation [75][74]. Compared to studies carried out at various solar salterns around the world, the presence of Ni seems to be a characteristic novelty, and the order of abundance of the metal concentration is not entirely similar either [62,63][61][62].
Solar salterns and salt marshes may be also contaminated by aliphatic and aromatic hydrocarbons. A hydrocarbon analysis performed in the Sfax solar saltern allowed for the detection of aliphatic hydrocarbons and n-alkanes [76][75]. The total aliphatic hydrocarbon concentrations varied from 92.5 mg. L−1 in the first pond, which has marine characteristics, to 661.1 mg. L−1 in the crystallizer pond [76][75]. The use of n-alkane distribution indices coupled with environmental factors permitted for the assertion of the assumption that a major proportion of the hydrocarbons resulted from eukaryotic and prokaryotic communities and a low proportion of the hydrocarbons might be petrogenic [76][75]. Hydrocarbon extraction and analysis from the Sfax coastal region near the solar saltern showed that the sediments are contaminated by petrogenic aliphatic and aromatic hydrocarbons [77,78,79][76][77][78]. The transportation of oil, shipping and industrial activities, urban runoff, and waste water discharge are the main sources of hydrocarbon contamination in the Sfax coastal zone [77][76].
Table 1. Contaminants recorded in solar salterns.
Contaminants Solar Saltern Fraction References
Trace metals Sfax solar saltern (Tunisia) Surface sediments [69,80][68][79]
Water [70,72][69][71]
Biota: Artemia salina [73][72]
Ribandar solar saltern (India) Surface sediments [63][62]
Porteresia Bed, Karnafully coastal area (Bangladesh) Surface sediments [62][61]
The Black Sea brine Pomorie salterns, Burgas (Bulgaria) Water [64][63]
Biota

Halobacterium salinarium and microalgae Dunaliela salina [64][63]
Colloidal particles [64][63]
Tinto,

Odiel, and Piedras salt marshes in Huelva (Spain).		 Surface sediments [65][64]
Hydrocarbons Sfax solar saltern (Tunisia) Surface sediments [76][75]
  Water [76][75]

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