Prevention is better than cure: Persian Gulf biodiversity vulnerability to the impacts of desalination plants

1 INTRODUCTION

Desalination of seawater is one of the most promising ways (and often the only way) to provide drinking water in arid and semiarid regions. The industrial, global production of fresh water is rapidly increasing (Lattemann & Höpner, 2008a), and although seawater desalination provides a range of economic, social, and health benefits, numerous potential negative effects associated with the chemical and condensed compounds released into the environment can occur (Roberts, Johnston, & Knott, 2010). Given that most desalination plants (DPs) extract water from local sources, environmental degradation near the plants can occur. In general, impingement (IPM) and entrainment (ETM) processes include the removal of marine organisms during the intake system operation of DPs. Impingable organisms include larger organisms with active swimming ability (such as juveniles and adult organisms) and retained by a mesh with a max opening of 14.2 mm. Entrainable organisms are defined as small organisms with limited to no swimming ability, and lacking the ability to avoid intake flow, and which also can pass through the 14.2 mm mesh (Missimer & Maliva, 2018). The effects of IPM (mortality of marine organisms on the intake screens) and ETM (mortality of microscopic organisms, fish eggs and larvae, and small crustaceans during salt water processing) caused by DPs have been assessed for mostly freshwater intake systems, while mortality in seawater intake systems is not well documented (Gille, 2003; Miri & Chouikhi, 2005). Impingement and ETM of marine species are influenced by intake design and operation, intake location, water quality parameters such as temperature and dissolved oxygen, as those impact the mobility of organisms and ambient hydraulics (Hogan, 2015). Death of plankton can have serious food web consequences, as these organisms are the base of the marine food web; without these microorganisms much of the local aquatic life will be at risk.

One of the most important emerging issues in the Persian Gulf is that DPs will alter biodiversity and jeopardize ecosystem services. Given that marine invertebrates and fishes are ectotherms (Sunday, Bates, & Dulvy, 2011), the impacts of DP discharges on aquatic fauna may be serious. Water temperature and salinity are critical to the growth and survival of all aquatic species, especially larval forms, and sudden changes in these may endanger numerous species. Increases in temperatures and salinities can push marine fauna close to their upper tolerances; consequently, these changes can be expected to affect species distributions and cause changes in recruitment success, fecundity, and growth rate (Lattemann & Höpner, 2008a; Pörtner & Farrell, 2008). Biodiversity in semienclosed bodies of water such as Persian Gulf is vulnerable to anthropogenic activities such as discharges from DPs. That is not to say that other environmental features do not threaten marine life. Indeed, impacts from shipping ports and hydrocarbon loading facilities can be substantial, given the sensitive nature of Persian Gulf fauna. The Persian Gulf is facing with many threats resulting from natural changes and anthropogenic pressures. Marine species diversity, ecosystem health, and fisheries are currently threatened by multiple stressors such as industrial effluents, reclamation and dredging, oil pollution, overfishing, and other natural and anthropogenic factors (Figure 1; Daliri, Kamrani, Jentoft, & Paighambari, 2016; Kamrani, Sharifinia, & Hashemi, 2016; Sharifinia, Daliri, & Kamrani, 2019; Sharifinia, Taherizadeh, Namin, & Kamrani, 2018). Despite the potential effects of DPs on marine ecosystems and their services, there is a lack of research on the impact of brine discharges from DPs on Persian Gulf biodiversity. We summarize the literature to assess the knowledge of DP discharges and their impacts on marine organisms from fish to microbes, discuss the potential effects of DPs on the Persian Gulf biodiversity, and describe an achievable and practical management plan to mitigate the impacts of DPs.

2 SEAWATER DESALINATION TECHNIQUES

Desalination plant systems depend on energy sources, and these can be classified as thermal, mechanical, electrical, and chemical energy sources. Reverse osmosis (RO), multi-effect distillation (MED), and multi-stage flash (MSF) are the three most globally applied desalination systems (Miller, Shemer, & Semiat, 2015). Figure 2a,b shows the classification of the main desalination techniques and contribution of each desalination technology to water production around the world. According to Alkaisi, Mossad, and Sharifian-Barforoush (2017), 62% of the installed global desalination capacity is based on RO, while MED and MSF account for 14% and 10%, respectively. The widespread use of the RO system is due to its lower costs and energy demands and improved membrane durability. In the RO system, dynamic pressure was used to overcome the osmotic pressure of salt solution and leads to water-selective permeation from the saline waterside of a membrane to the freshwater side (Semiat, 2000). In MSF distillation, evaporation of seawater takes place by reduction in the pressure of the heated water. The energy efficiency is obtained by regenerative heating and also preheating of the incoming seawater using the condensing water vapor. In MED, the process takes place in a series of evaporators and operates on the reducing principle of the ambient pressure in each component. Generation of a secondary steam at a lower pressure conducted by the primary steam is fed to the next component where the process is repeated (Miller et al., 2015; Semiat, 2000). The advantages and disadvantages of some desalination processes are shown in Table 1.

3 DISTRIBUTION OF DPs IN THE WORLD AND PERSIAN GULF COUNTRIES

Water from DPs has been used to supply freshwater in arid and semiarid areas of the world for decades. The highest numbers of DPs have been constructed in the Middle East, North America, Asia, Europe, and Africa (Figure 3a; Gorjian & Ghobadian, 2015; Lattemann & Höpner, 2008a; Shatat, Worall, & Riffat, 2013). Given the arid nature of the region, threat to the Persian Gulf environment from DPs (and also by other human activities) will be greater in the future, and there is an urgent need for more research on reducing the effects of DPs on this system. Thermal evaporation and membrane-based separation are the two main techniques used in seawater desalination in the Persian Gulf (Elimelech & Phillip, 2011). Additionally, the Iranian government envisages massive investments in DPs to bring water from the southern Iranian coastal waters to the interior of the country. Currently, 213 active seawater DPs are operating in the Persian Gulf, with 51 plants planned, under construction, or being installed. Saudi Arabia and Kuwait have the highest and lowest numbers of DPs among the Persian Gulf countries (Figure 3b). The daily capacity of these plants for all of the Persian Gulf countries is about 11 million m³ per day, which is approximately equal to half the global production (Gorjian & Ghobadian, 2015; Sharifinia et al., 2019). Lattemann and Höpner (2008a) reported that 81% of the desalinated water in the Persian Gulf countries is produced by MSF and 13% by MED, but only 6% by reverse osmosis. In contrast, the most applied technique in Iranian DPs are RO and MED, respectively (Figure 3c; Gorjian & Ghobadian, 2015).

4 BIODIVERSITY VULNERABILITY TO ENVIRONMENTAL IMPACTS OF DP DISCHARGES

Given the increasing rates of development of urban areas and coastal construction in the Persian Gulf region, anthropogenic activities and climate change will be important threats to the future of biodiversity in marine ecosystems (Griffith, Strutton, & Semmens, 2018; Henson et al., 2017; Kamrani et al., 2016; Segan, Murray, & Watson, 2016; Sharifinia et al., 2018, 2019; Sharifinia, Penchah, Mahmoudifard, Gheibi, & Zare, 2015; Taherizadeh & Sharifinia, 2015). The impacts of DPs on marine biodiversity include decreases in sensitive species, reductions in plankton abundance, decreases in hard substrate epifauna, and growth rate decreases of seagrasses (Roberts et al., 2010). Although there already is a variety of environmental impacts, DPs will continue to have an increased negative impact on biodiversity in marine ecosystems in the future. There are several means that a rapid change in anthropogenic pressures may intensify or limit the ability of a species to respond to DP impacts. For example, brine discharges from DPs induce morphological and physiological changes in a variety of species, which in turn may limit the ability of a species to resist additional environmental stresses (Roberts et al., 2010). Owing to extreme evaporation (1.54 m/year; Brewer & Dyrssen, 1985) and low precipitation rates (0.03–0.11 m/year), the Persian Gulf is highly saline (average salinity for the entire region is more than 37; Moaddab, Khabazi, & Roosta, 2017). The rapid increase in the number of DPs will lead to ecological stresses by increasing water temperatures and salinities throughout the region, decreasing dissolved oxygen concentrations, and increasing heavy metal concentrations (Sharifinia et al., 2019). Despite the documented impacts of DP discharges on marine species, the Persian Gulf region suffers from a lack of research on the regional impacts, with limited research that addresses environmental issues of DPs in general (de la Ossa-Carretero et al., 2016a; Lattemann & Höpner, 2008a; Roberts et al., 2010).

Semienclosed and shallow ecosystems such as Persian Gulf (with a mean and maximum depth of 50 and 89 m) with a high diversity of marine species, are generally more sensitive to brine discharges than open-ocean systems (Lattemann & Höpner, 2008a). The impacts of desalination processes and applied pretreatments on the physicochemical properties of DP discharges were discussed by Lattemann and Höpner (2008a). Discharges from DPs on salinity and temperature (having been defined by Tettelbach & Rhodes 1981 and O'Connor & Lawler 2004 as ‘master factors’ for several marine organisms) and other contaminants around outfalls can be considerable (Table 2). Autecological studies have indicated that development, growth, and survival of marine organisms are affected by salinity and temperature (Kinne, 1964; O'Connor & Lawler, 2004; Tettelbach & Rhodes, 1981).

Increases in seawater salinity and temperature due to anthropogenic activities and climate change will continue to occur in the coming century (Pires, Figueira, Moreira, Soares, & Freitas, 2015), particularly in coastal areas (Cardoso, Raffaelli, & Pardal, 2008; Pires et al., 2015; Reid, Soudant, Lambert, Paillard, & Birkbeck, 2003). Studies that assess the impacts of salinity and temperature changes on marine organisms are increasing, because these changes can have harmful and lasting effects. For example, Pires et al. (2015) reported that salinity increases have a significant negative impact on the regenerative capacity of polychaete Diopatra neapolitana, and found that under higher salinities complete regeneration was significantly delayed. The toxicological effects of DP discharges on seagrasses, fish, macrofauna, meiofauna, zooplankton, and phytoplankton exposed to effluents in areas surrounding the outlets are summarized in Table 3.

Given that brine discharges from DPs are more dense than ambient seawater, outfall water tends to remain at the bottom rather than getting mixed within the water column (Gacia, Invers, Manzanera, Ballesteros, & Romero, 2007; Purnama, Al-Barwani, & Smith, 2005; Roberts et al., 2010). Therefore, benthic species are more likely to be initially affected by brine discharges rather than planktonic and pelagic species, and most studies have examined the impact of DPs on benthic organisms. Gacia et al. (2007) investigated the effects of DP brine discharges on the seagrass Posidonia oceanica. They suggested that discharges result in increasing nitrogen content in tissues and decreasing carbohydrates. Seagrass meadows in the Persian Gulf include Halodule uninervis, Halophila stipulacea, and Halophila ovalis and are responsible for high primary production, high biodiversity of associated flora and fauna, and serve as nursery and feeding grounds for many marine organisms. Persian Gulf seagrasses are subject to very large changes in salinity (from 38 to 70) and temperatures (from 10 to 39°C; Price, Sheppard, & Roberts, 1993). Halophila stipulacea and H. ovalis are more sensitive to increases in salinity, so the distribution of these species is more limited spatially than that of the H. uninervis (Erftemeijer & Shuail, 2012; Green, Short, & Frederick, 2003). The available evidence indicates that H. uninervis in the Persian Gulf can tolerate hypersaline conditions (Erftemeijer & Shuail, 2012; Green et al., 2003), but further research into the impacts of the DP brine discharges on seagrass species distribution and growth in the region is needed.

Salinity and temperature are the main factors controlling growth, photosynthesis, and survival of corals (Baird & Hughes, 2000; Ferrier-Pages, Gattuso, & Jaubert, 1999; Kuanui, Chavanich, Viyakarn, Omori, & Lin, 2015). Most marine organisms adapt to modest changes from optimal salinity and temperature conditions, but are unable to tolerate these changes for long time periods (Lattemann & Höpner, 2008a). Research on the relationship between environmental variables and coral distributions suggests that coral reefs only grow within narrow ranges of salinity and temperature. Despite the importance of salinity and temperature to coral reefs physiological processes, the effects of changes in theses parameters due to DP discharges remains incompletely studied.

Salinity is a critical factor regulating the distribution of coral species and reef-building potential (Riegl & Purkis, 2012). Corals appear to have lower thresholds, as a 5% salinity increase causes reduced growth and/or death (Birkeland, 2015; Hughes et al., 2017; van der Merwe et al., 2014). Generally, most scleractinian corals can survive only within a small range of salinity, and death occurs when salinity increases above 40 (Muthiga & Szmant, 1987). Other studies found that sudden changes in salinity had a negative effect on coral reproduction, photosynthesis of algal symbionts, and respiration (Porter, Lewis, & Porter, 1999; Richmond, 1993). Disruption in the symbiotic relationship between coral and alga due to salinity stress will have a severe effect on coral metabolism (Muthiga & Szmant, 1987). It has also been shown that salinity variations disrupt optimal cellular electrochemical processes, enzyme kinetics and nerve conduction, and cause metabolic drain (Vernberg & Vernberg, 2012). Ferrier-Pages et al. (1999) reported that the growth rates of Stylophora pistillata decreased if salinity changed by 2–4 from optimal levels, and the coral is particularly sensitive to hypersaline conditions. Furthermore, other studies indicated that rapid changes in salinity can effect zooxanthellae photosynthesis and may induce coral death by reducing the amount of energy transferred to corals (Manzello & Lirman, 2003; Muthiga & Szmant, 1987). Petersen et al. (2018) investigated the potential impacts of brine discharge on reef-building corals S. pistillata, Acropora tenuis, and Pocillopora verrucosa. They found that there was an overall reduction in coral performance and variations in physiology of corals and suggested that the DP brine discharge can lead to coral tissue loss due to decreases in Symbiodinium abundance and reduction in protein synthesis.

The best development and growth of corals occur in offshore areas of the Persian Gulf, and is limited due to the extremes in temperature, salinity, and other physical parameters (Sheppard et al., 2010). Despite these difficult environmental conditions, coral species show remarkable resilience and vitality in the region. Tolerance ranges of different corals to the salinity in the Persian Gulf are shown in Table 4. Sheppard, Price, and Roberts (1992) found Cyphastrea serailia and Porites harrisoni growing in salinities >42 in the Persian Gulf with large heads of Porites spp. flourishing at 48. However, most corals die or suffer damage at salinities above 48. Although Persian Gulf corals are adapted to high salinities, corals may be vulnerable to exposure to DP discharges, and there is a need for systematic studies on the effects of brine discharges on coral reefs and their abilities to acclimate to increased salinities.

5 WHAT WILL HAPPEN TO BIODIVERSITY IF WE EXPAND DESALINATION PLANTS IN THE PERSIAN GULF?

The direct impacts of DP discharges on the Persian Gulf biodiversity presently remain unknown, and little is known about how these releases impact present and future ecosystem functioning and services. Beaumont et al. (2007) and Hein, Koppen, Groot, and Ierland (2006) classified goods and services provided by marine ecosystems into four categories: Provisioning services (fisheries, bioprospecting, building materials), supporting services (life cycle maintenance for both fauna and flora, primary and secondary production, nutrient cycling), regulating services (carbon sequestration and storage, erosion prevention, wastewater treatment, moderation of extreme events), and cultural services (touristic, recreational, esthetic, and spiritual benefits). It is difficult to evaluate Persian Gulf services and goods, because the same ecosystem can have a local, regional, and global impact (Pendleton, Thébaud, Mongruel, & Levrel, 2016). Despite the great loss of biodiversity (e.g., coral reef deterioration), ecosystem goods and services are more greatly valued today than 20 years ago. In the Persian Gulf, several systems such as mangroves forests, seagrasses, and marshes are potentially important for carbon sequestration (Sharifinia et al., 2019). Furthermore, the Persian Gulf ecosystem sustains the livelihoods of millions of people through fisheries and tourism (Daliri et al., 2016; Madani, Ahmadian, KhaliliAraghi, & Rahbar, 2012; Nouri, Danehkar, & Sharifipour, 2008; Sharifinia et al., 2019). Coral reefs and mangrove forests provide coastal protection to nearby Persian Gulf villages, towns, and cities, an increasingly important service owing to sea level rise (Sale et al., 2011; Sharifinia et al., 2019). It is possible that the adverse impacts of DPs will modify or impair the provided goods and services by Persian Gulf in the future. As such, there is a pressing-need for further research into the impacts of discharges on marine biodiversity.

The potential impacts of DPs on all species in the system result from their exposure, adaptive capacity, and sensitivity. However, there is a growing evidence that DPs have begun to affect survival, reproduction, diversity, and distribution of marine organisms (Chang, 2015; Petersen et al., 2018; Roberts et al., 2010). Brine discharges (and other associated environmental disturbances) by DPs into the Persian Gulf will impact physicochemical parameters. Therefore, due to accumulation of brine discharges in and around the DPs, the bottom dwelling species will be strongly impacted (Feary et al., 2013). With such a high number of existing DPs and a scarcity of research on the effects of DPs on biodiversity, we used the results from other parts of the world to predict and suggest the future potential impacts of DP discharges on the Persian Gulf fauna and flora (Figure 4).

We conclude that increasing the input of brine discharges from DPs will cause a reduction in plankton biomass, species diversity, and richness in the Persian Gulf. High levels of brine discharges into the Persian Gulf may have the following impacts: alter phytoplankton photosynthesis due to increases in water turbidity that reduce light penetration; increase benthic mortality due to cell dehydration and subsequent turgor reduction, and over long time periods, alter the nature of the benthic habitat; change chloroplast ultrastructure, decrease in chlorophyll content, enzyme activity, and electron flow inhibition in photosynthetic organisms; alter larval development and individual growth, larval survival rate and generation time, species reproduction and reproductive traits in a variety of organisms; and result in a loss of fishery resources and economic activity due to biomass and reproductive reductions in marine species.

6 MITIGATION PLANS FOR DP ECOLOGICAL IMPACTS

Mitigation plans for DP facilities are necessary to maintain the aquatic vitality and productivity (‘prevention is better than the cure’) and should be evaluated prior to and during the construction of new DPs in the Persian Gulf. The effects of DPs on the environment depend on factors such as plant size, type of desalinizing process, use of chemicals during desalination, and the specific ecological and hydrographical characteristics of the site (Lattemann & Höpner, 2008b). To mitigate the negative impacts of DP discharges on Persian Gulf biodiversity, we propose measures to achieve a balance between marine ecological conservation and generation of needed freshwater. To mitigate the impingement and entrainment of larger plankton in intakes, a low through-screen velocity (lower than 0.15 m/s), small screen openings (less than 22 cm), and suitable fine screen mesh size (less than 9 mm) should be used to reduce the impact on plankton, fish eggs and larvae. One common mitigation strategy to reduce impacts is to use modern surface water intake designs or a subsurface intake. In particular, subsurface intakes can virtually eliminate IPM and ETM, as seawater is taken from beneath the sea floor. Three additional mitigation plans that can be useful and effective in reducing impacts include creation of marine wetland areas or other marine habitats allowing greater areas for spawning of fish and invertebrates, paying a fee based on calculating the IPM and ETM losses, and restocking the marine impacted habitat with fish and invertebrates’ eggs, larvae, juvenile, and small adult forms (Missimer & Maliva, 2018). Furthermore, the intake inlet should be placed outside the littoral zone in deeper waters and away from sensitive productive areas. Locating intake inlets at least 300 m from shoreline and installing them in water at least 20 m, where organism abundances are lower, could minimize effects associated with intake operations (WateReuse-Association, 2011). The adverse effects of chemicals can be reduced by treatment before discharge such as replacing hazardous substances, as well as through the use of alternative treatment options. Biocides such as chlorine that can acutely affect organisms at the discharge site, should be replaced or treated before discharge. Chlorine can be removed from the effluent by using efficient chemical substances such as sodium bisulfite (NaHSO₃), as practiced in RO plants, while sulfur dioxide (SO₂) and hydrogen peroxide (H₂O₂) have been suggested to treat thermal plant stream effluents (Lattemann & Höpner, 2008a). Cleaning solutions should be treated on-site in special treatment facilities, while waters from filter backwash should be treated by sedimentation, land deposition, and dewatering. In summary, environmental impacts of DPs could be mitigated by preventing and replacing damaging chemicals such as heavy metals and chlorine used during treatment, diluting and dispersing the salt, heat, and any contaminants using hydrological conditions and shoreline morphology (sandy and rocky shorelines exposed to strong currents are suggested), eliminating plant construction in areas of high biological importance (near coral reefs, mangroves, and nesting habitats for sea turtles), and avoiding plant construction in areas that are important to biodiversity and productivity, (nursery, feeding, and harvesting grounds). Appropriately sited, designed, operated, and well-planned DPs can minimize ecological impacts on the marine life. By using current developments in impingement and entrainment reduction technology, both nationally and internationally, marine biodiversity and local ecosystems will be preserved with minimal environmental impacts.

7 CONCLUDING REMARKS

Desalination plants are a potentially serious threat to biodiversity in marine environments. A better understanding of the impacts will increase the breadth of mitigation plans to deal with their negative effects on marine systems. Information on the impacts of DP brine discharge on marine biota is available, but there is a pressing need for further research to explore footprints of DPs in the Persian Gulf and on regional impacts. We propose that new efforts in six categories are necessary: (a) Understanding the vulnerability of species to DPs releases for designing effective mitigation strategies; (b) Use of both field monitoring and laboratory experiments to assess DP impacts on the biodiversity in the Persian Gulf; (c) Provide data on positive or negative responses of each species to brine discharges for use in future plan construction efforts; (d) Conduct a comprehensive Environmental Impact Assessment before and after each desalination project to understand all ecological impacts of DP construction; (e) Develop collaborative research projects to prevent the negative impacts of DPs and other activities on the Persian Gulf biodiversity; and (f) Creation of a joint task force on how to protect the regional environment, or establishing a forum for Persian Gulf countries to reach a consensus. Such a system will allow the development of reasonable scenarios of future environmental impacts of DPs and marine biodiversity.

CONFLICT OF INTEREST

The authors declare that they have no conflict of interest.

ETHICAL APPROVAL

No animals are involved in the study.