Physicochemical system
Seasonal salinas fallow during winter and produce salt only during the summer, when climate conditions are favourable. They are found in climates with warm, dry summers, and where 65 to 80% of the annual rainfall occurs during winter months (e.g., shores of Atlantic Europe, the Black Sea and Mediterranean Sea, Namibia, South Africa, Yellow Sea, San Francisco Bay) [20, 25]. For Portuguese salinas, salt production is restricted to a period, from spring to autumn [16]. After this period, the sluices are opened during high tide, and the salina is flooded. It stays flooded until March or April, when temperatures rise and atmospheric precipitation decreases [11]. In the non-productive season, the salinity in the whole system approaches that of the supply water, i.e. ≤ 35 ppt, while water depths vary per compartment. During this season water depth in the supply ponds, evaporation ponds and crystallizers is approximately 70 cm, 80 cm and 100 cm, respectively [29]. When the productive season begins, the ponds are emptied and prepared for a new cycle of salt production [11]. It is necessary to proceed with specific works on the salt ponds bottoms, which include the reparation of the separation dikes, replacement of damaged woodwork and preparation of the tools for salt production. Once all these works are concluded, it is necessary to clean the crystallization basins. Well-maintained and carefully prepared basins are essential for the production of high quality salt [19]. In June, the ponds are filled again. They are subsequently supplied with new sea water every 15 days, during spring tides. A slight level gradient between the supply and crystallizer ponds provides a water flow by gravity [30]. The passage of water must be regulated and timed, so that it flows into each following tank more concentrated, reaching saturation in sodium chloride on arrival at the crystallizers. During the productive season, water depths in the supply, evaporation and crystallizer ponds is about 20 cm to 100 cm, 10 cm to 50 cm, and a few centimetres, respectively. The salinity is generally below 70 ppt in the supply ponds, varies between 70 ppt and 290 ppt in the evaporators and is very high in the crystallizer ponds, reaching more than 300 ppt. It is in the evaporation ponds that seawater is concentrated up to the saturation point of NaCl, and where the various salts crystallize which are less soluble than NaCl, such as Fe2O3, CaCO3, BrO3 and CaSO4, which precipitate at salinities of approximately 95 ppt, 95 ppt, 130 ppt and 160 ppt, respectively [11, 29]. The high surface-to-volume ratio in the ponds promotes evaporation as the brine slowly flows to each succeeding, more saline pond in the series. The aim of this form of brine management is to allow precipitation of the less soluble marine minerals ahead of the crystallizers, so that only NaCl precipitates in these ponds [31].
When the water volume is reduced to 1/10 of its initial volume in the evaporation ponds, the brine flows into the crystallizers. There it stays until reaching 1/40 of its volume in order to obtain the precipitation of NaCl on the bottom at 220 ppt, followed by the more soluble salts in the brine, such as MgSO4 (260 ppt), MgCl2 (275 ppt) NaBr (284 ppt) or KCl (294 ppt) [11, 29]. The supernatant liquid (bittern), rich in compounds of magnesium, potassium chlorides and sulphates, is removed and the deposited salt (the crop) is harvested [25]. In the salinas of Aveiro, salt (NaCl) harvesting (Figure 3) takes place in the crystallizers ("meios de baixo") and only exceptionally (i.e. in very hot summers) in the condensers ("meios de cima"), originally created to obtain purer sodium chloride.
The salt deposit on the floor of the crystallizers is very consistent and compact. During the harvest this salt has to be released, broken and washed (with the crystallizer brine). Some care has to be taken not to mix the salt with the sediment. The harvested salt is piled up on wooden boards next to the crystallizer pond, and left to dry. When thoroughly dried the salt is stored, after removal of the upper layer of the heap, which has become dirty due to its exposition to dust (this salt is returned to the crystallizer ponds to contribute to the following harvest). During the warm months salt production is continuous. At Aveiro, the crystallizers are supplied with brine at 3-day intervals.
Some artisanal salinas, including those in Aveiro, also produce fleur de sel; a salt rich in minerals, with a particular taste and high market value. As the water volume is reduced to the required fraction (1/40) of the supplied sea water, the fleur de sel, which consists of sodium chloride and traces of different salts, begins to form on the crystallizer ponds' water surface. This floating salt is collected once or even twice a day (except when it does not form due to heavy winds or when humidity is high). Fleur de sel does not undergo any form of processing. It is directly packaged and commercialized.
Importance of physicochemical and biological systems in salt production
Salinas are mostly closed systems, exposed to annual drainage and drying. Contrary to natural brackish environments (lagoons, estuaries and inland seas) and as a result of the annual cycle of salt production, seasonal salinas present two ecologically distinct periods (production and non-production) with distinct physicochemical and biological conditions. During the non-productive season, when the salinas are flooded, environmental factors do not show important variations and the systems are more stable for living organisms [11], holding high fauna and flora diversity, distributed over all of the ponds, with the deeper supply ponds showing the highest diversity of organisms. During the salt production season, characteristic biota, adapted to different salt concentrations, inhabit the salina ponds along the salinity gradient [32]. The increase of the proportion of salts dissolved in the brine causes a reduction in the specific diversity, with less-eurihaline organisms being eliminated [26].
The living organisms in the brine of a salina constitute a biological system or ecosystem essential to the salt production process, which is intimately linked to the system's physicochemical phenomena [24, 33]. The exchanges with the sea, the hydrology, salinity and nutrients play an important role in the development of the biological communities [34]. Depending on its type and development, the ecosystem's performance is often responsible for the degree of success (i.e. product quality and output) of a salina [33].
The aim of every solar saltwork or salina with seawater intake is the achievement of a continuous and economic production of high quality salt (sodium chloride). One way to maintain or increase the salt production in the Aveiro salinas and to improve its quality is to simultaneously manage and coordinate the physicochemical and the biological systems in the salina ponds, from the inlet channel to the crystallizer ponds [31, 35]. Therefore, continuous collection, display and utilization of information are required, which indicate the physicochemical and biological status of the salt field, efficiency of the harvest and wash processes, and concentrations of critical ions and insolubles in the washed salt. Such information allows manipulation of control features, to make routine adjustments, anticipate and obviate developing problems, and enable optimum and harmonious performance of the physical and biological systems [24].
"Balanced", "inadequate" and "unbalanced" biological systems
The salina's biological system, composed mainly of microscopic organisms suspended in the water (the planktonic community) and attached to ponds floor (benthic communities forming mats), can aid or harm the salt production [24]. Knowledge of the ecology of these communities is therefore of utmost importance for salt production. Each community consists of: producer organisms (algae, cyanobacteria, and certain bacteria) that manufacture organic substances from light energy, carbon dioxide, and inorganic nutrients (through photosynthesis) and power the entire biological system; and, consumer organisms (Artemia, brine flies, bacteria, ciliates, crustaceans, molluscs, nematodes), which use organic substances to power their physical activities, growth and reproduction [34].
Three types of biological systems with different characteristics can be considered in salinas: "balanced", "inadequate" and "out of balance" biological systems. It is well known that a "balanced" biological system in salt ponds is essential for salt production, whereas an "inadequate" or "unbalanced" system creates problems for salt precipitation [33, 36]. A "balanced" biological system produces optimum quantities of organic materials properly distributed between plankton and bottom communities living in a salina, promoting the production of high quality salt. The planktonic community of such a system (which includes algae, bacteria, protozoa, and brine animals suspended in the brine) contributes to salt production, colouring the brine and increasing solar energy absorption and water evaporation [33, 37]. The benthic community (which consists of microorganisms, small molluscs and nematodes growing on the floor of the ponds as mats and deposits) favours salt production promoting the development and maintenance of mats firmly attached to the pond floor, which sustain the desired thicknesses, preserve biodiversity, remove and permanently retain nutrients from the overlying water, seal ponds against brine leakage and fresh groundwater infiltration, and help prevent dominance of undesirable mucilage producers [20, 33, 34].
An "inadequate" biological system lacks sufficient organic productivity; salinas with these systems experience insufficient brine colouring and evaporation, and leaking ponds. An "unbalanced" biological system, caused by a sub-optimal distribution of organic materials between the planktonic and benthic communities, can result in mucilaginous brine, decreased evaporation, and a low-quality product (particularly in terms of colour, insolubles and sulphate content, and crystal size of the salt) [33].
Even when salinas have functioned successfully for a number of years, their biological systems are sensitive to internal and external ecological changes that can lead to serious problems [33]. Microbiological problems in the salinas (e.g. poor mat development and slime production) may be anticipated based on a regular monitoring program of nutrient analyses, plankton and mat evaluations [31]. Hence, knowledge about the variability of the ecological factors is necessary to be able to maintain or increase the salt production and improve its quality, proceeding with a careful biomanipulation of the system, when necessary.
Biological spatial organization in salina ponds with a "balanced" biological system
During the salt production season, a biological spatial organization consisting of ecological entities that can be relatively autonomous and stable forms along the salinity gradient, in the consecutive salina compartments. The formation of such biological entities along the gradient, which ranges from seawater in the supply ponds to extreme hypersaline environments in the crystallizing ponds, gives salinas a high eco-physiological and ecological value [35]. From low to high salinities: 1) the benthic community changes from loosely organized mats of many species to leathery mats of several layers dominated by fewer species; 2) the composition of planktonic community gradually changes from low levels of diverse groups of species (kinds) to high concentrations of few important species; 3) photosynthetic production of new organic substances that exceed consumption gradually changes to consumption surpassing production; and 4) concentrations of dissolved and particulate organic substances increase in the water [34]. The later increase is due to brine concentration by evaporation and due to the inability of bacteria in the downstream ponds to breakdown organic matter as fast as it arrives. Salinity increase also introduces a succession of organisms that allow reuse of essential minerals and organic matter. Thus, when organisms flow from lower to higher-salinity ponds, they die making their minerals and organic matter available to a new set of organisms [33].
The supply ponds display the greatest organism diversity, biological productivity of organic matter and ecological stability of the entire system [33]. In these ponds the variety and concentration of microorganisms suspended in the water column are similar to the plankton of the nearby marine environment. Seagrasses, seaweeds, fish, and other large marine life are also well represented in the supply ponds [24].
In the evaporation ponds, where salinity during the production season is 3 to 7 times higher than that of sea water, specific diversity decreases though the density of some species may be slightly higher [27]. Specialized biota develop in these ponds, but most noteworthy is the plankton component consisting of cyanobacteria, brine flies and brine shrimp. In a "balanced" biological system, non mucilage producing planktonic cyanobacteria thrive, conferring dark colours to the brine. In a salina whose ecosystem is out of balance, often caused by excessive nutrients and severe brine dilution, the planktonic cyanobacteria Aphanothece halophytica may predominate and harm the salina [25, 33]. Disturbances cause A. halophytica to reproduce at high rates, excluding competing species (e.g. Artemia sp.) and secreting abundant polysaccharide slime [34, 38]. When this polysaccharide material reaches the crystallizer ponds downstream, this may result in an increase in brine viscosity and the production of soft, poor-quality salt crystals [38]. In the crystallizers, effects of high viscosity include: decreased effectiveness of the red halophilic Archaea; crops or salt floors unable to support machinery (in industrial salterns); harvests of small and hollow crystals that bind or retain dissolved and crystalline contaminants; and, increased development of Dunaliella salina populations [24, 38]. These green algae are generally of great importance, being part of the diet of Artemia and contributing to the increase of solar radiation absorption. Disturbances, however, may cause D. salina to reproduce massively, and release damaging quantities of organic substances that are highly detrimental to salt production [24, 25, 34].
Depending on the intake water of the salina, brine fly larvae and brine shrimp feed on organisms and debris produced in the low salinity ponds [33]. Brine shrimp Artemia thrive in the highly saline evaporation ponds, but their numbers and activity decline sharply in the crystallizers due to a variety of environmental factors (e.g., the metabolic cost of osmoregulation in strong brines, elevated brine temperatures and low oxygen levels) [25, 31]. Brine shrimp living in the evaporation ponds synthesize more haemoglobin, expend greater amounts of energy and thus consume more food than they would require at lower salinities, because of the extra osmoregulation effort needed for survival. This "forced" feeding by brine shrimp is of particular value to solar salinas [33]. Brine shrimp ingest suspended calcium sulphate (gypsum) crystals, and efficiently utilize much of the microplankton and other organic substances they consume. These shrimps deposit their wastes in membrane-bound faecal pellets that fall to the floor and become incorporated into the benthic community. These activities clear the water, aid maintenance of the mat, prevent recycling of nutrients, control phytoplanktonic Aphanothece halophytica and Dunaliella salina populations, and assist the delivery of high-quality, nutrient-depleted brine, to the downstream ponds. Artemia may ingest but not utilize A. halophytica but ingest and utilize D. salina [24, 25].
In the crystallizers, the salinity reaches values exceeding the tolerance limits of Artemia and brine fly larvae. These organisms die, sink and stay deposited at the bottom in large quantities, constituting the main protein source for the resident red halophilic Archaea which are the key biological component of the crystallizer ponds [22, 33, 39, 40]. Red halophilic Archaea are heterotrophs that thrive on the dissolved organic carbon, which passively increases by concentration as the water flows downstream to the crystallizers [32]. In these ponds the few species that exist are often present in high concentrations [41]. The plankton, mostly several genera of red halophilic Archaea (Halobacteriaceae), reaching or exceeding 108 cells ml-1, feed on dissolved organic substances and colour the brine pink to bright red because they contain 50-carbon bacterioruberin carotenoids in their cell membrane, and sometimes also retinal proteins (bacteriorhodopsin, halorhodopsin) [23, 24]. By consuming significant quantities of organic substances, and by absorbing heat energy from the sun, high concentrations of the red halophilic Archaea decrease organic substances in the brine, improve evaporation, increase the quality of the salt, and improve crystal characteristics [24]. When excessively high concentrations of nutrients reach the evaporation and crystallizer ponds, Dunaliella salina, rich in β-carotene, may form populations sufficiently dense to colour the brine red-orange [20]. It was recently recognized that a rod-shaped, extremely halophilic representative bacterium of the phylum Bacteroidetes (Salinibacter) may also be present in significant numbers in those environments in which red halophilic Archaea thrive, such as the crystallizer ponds. This bacterium contributes to the brine coloration (orange-red) due to the presence of the pigment salinixanthin (an unusual acylated C40- carotenoid glucoside). The carotenoids of the bacterioruberin group of the members of the family Halobacteriaceae appear however to be the main factor causing the characteristic red colour of hypersaline brines worldwide [23].