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Received: 3 June 2019    Revised: 9 August 2019    Accepted: 11 August 2019

DOI: 10.1111/gcb.14808

RESEARCH REVIEW

Prevention is better than cure: Persian Gulf biodiversity


vulnerability to the impacts of desalination plants

Moslem Sharifinia1  | Zahra Afshari Bahmanbeigloo2 | Walker O. Smith Jr3,4 |


Chee Kong Yap5 | Mehrzad Keshavarzifard1

1
Shrimp Research Center, Iranian Fisheries
Science Research Institute, Agricultural Abstract
Research, Education and Extension Due to extremely high rates of evaporation and low precipitation in the Persian Gulf,
Organization (AREEO), Bushehr, Iran
2 discharges from desalination plants (DPs) can lead to ecological stresses by increasing
Faculty of Sciences, Hamedan Branch,
Islamic Azad University, Hamedan, Iran water temperatures, salinities, and heavy metal concentrations, as well as decreas‐
3
School of Oceanography, Shanghai Jiao ing dissolved oxygen levels. We discuss the potential ecological impacts of DPs on
Tong University, Shanghai, People's Republic
of China
marine organisms and propose mitigating measures to reduce the problems induced
4
Virginia Institute of Marine Science, College by DPs discharges. The daily capacity of DPs in the Persian Gulf exceeds 11 million
of William & Mary, Gloucester Point, VA, m3 per day, which is approximately half of global daily freshwater production; multi‐
USA
5 stage flash distillation (MSF) is the dominant desalination process. Results from field
Department of Biology, Faculty of
Science, Universiti Putra Malaysia, Serdang, and laboratory studies indicate that there are potentially serious and chronic threats
Selangor, Malaysia
to marine communities following exposure to DP discharges, especially within the
Correspondence zoobenthos, echinodermata, seagrasses, and coral reefs. DP discharges can lead to
Moslem Sharifinia, Shrimp Research Center,
decreases in sensitive species, plankton abundance, hard substrate epifauna, and
Iranian Fisheries Science Research Institute,
Agricultural Research, Education and growth rates of seagrasses. However, the broad applicability of any one of these
Extension Organization (AREEO), Bushehr,
impacts is currently hard to scale because of the limited number of studies that have
Iran.
Email: moslem.sharifinia@yahoo.com been conducted to assess the ecological impacts of DP discharge on Persian Gulf
organisms. Even so, available data suggest that appropriately sited, designed, and
Funding information
Iran National Science Foundation, Grant/ operated DPs combined with current developments in impingement and entrainment
Award Number: 97015984
reduction technology can mitigate many of the negative environmental impacts of
DPs.

KEYWORDS
brine discharge, corals, desalination plants, macrofauna, plankton, seagrasses

1 |  I NTRO D U C TI O N plants (DPs) extract water from local sources, environmental degra‐
dation near the plants can occur. In general, impingement (IPM) and
Desalination of seawater is one of the most promising ways (and entrainment (ETM) processes include the removal of marine organ‐
often the only way) to provide drinking water in arid and semiarid isms during the intake system operation of DPs. Impingable organ‐
regions. The industrial, global production of fresh water is rapidly isms include larger organisms with active swimming ability (such as
increasing (Lattemann & Höpner, 2008a), and although seawater de‐ juveniles and adult organisms) and retained by a mesh with a max
salination provides a range of economic, social, and health benefits, opening of 14.2 mm. Entrainable organisms are defined as small or‐
numerous potential negative effects associated with the chemical ganisms with limited to no swimming ability, and lacking the ability
and condensed compounds released into the environment can occur to avoid intake flow, and which also can pass through the 14.2 mm
(Roberts, Johnston, & Knott, 2010). Given that most desalination mesh (Missimer & Maliva, 2018). The effects of IPM (mortality of

Glob Change Biol. 2019;00:1–12. © 2019 John Wiley & Sons Ltd |  1
wileyonlinelibrary.com/journal/gcb  
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marine organisms on the intake screens) and ETM (mortality of mi‐ (MED), and multi‐stage flash (MSF) are the three most globally
croscopic organisms, fish eggs and larvae, and small crustaceans applied desalination systems (Miller, Shemer, & Semiat, 2015).
during salt water processing) caused by DPs have been assessed for Figure 2a,b shows the classification of the main desalination
mostly freshwater intake systems, while mortality in seawater intake techniques and contribution of each desalination technology
systems is not well documented (Gille, 2003; Miri & Chouikhi, 2005). to water production around the world. According to Alkaisi,
Impingement and ETM of marine species are influenced by intake Mossad, and Sharifian‐Barforoush (2017), 62% of the installed
design and operation, intake location, water quality parameters such global desalination capacity is based on RO, while MED and MSF
as temperature and dissolved oxygen, as those impact the mobility account for 14% and 10%, respectively. The widespread use of
of organisms and ambient hydraulics (Hogan, 2015). Death of plank‐ the RO system is due to its lower costs and energy demands and
ton can have serious food web consequences, as these organisms improved membrane durability. In the RO system, dynamic pres‐
are the base of the marine food web; without these microorganisms sure was used to overcome the osmotic pressure of salt solution
much of the local aquatic life will be at risk. and leads to water‐selective permeation from the saline water‐
One of the most important emerging issues in the Persian Gulf side of a membrane to the freshwater side (Semiat, 2000). In
is that DPs will alter biodiversity and jeopardize ecosystem ser‐ MSF distillation, evaporation of seawater takes place by reduc‐
vices. Given that marine invertebrates and fishes are ectotherms tion in the pressure of the heated water. The energy efficiency
(Sunday, Bates, & Dulvy, 2011), the impacts of DP discharges on is obtained by regenerative heating and also preheating of the
aquatic fauna may be serious. Water temperature and salinity are incoming seawater using the condensing water vapor. In MED,
critical to the growth and survival of all aquatic species, especially the process takes place in a series of evaporators and operates
larval forms, and sudden changes in these may endanger numerous on the reducing principle of the ambient pressure in each com‐
species. Increases in temperatures and salinities can push marine ponent. Generation of a secondary steam at a lower pressure
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 semien‐
closed bodies of water such as Persian Gulf is vulnerable to an‐
thropogenic 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 anthro‐
pogenic 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 po‐
tential effects of DPs on the Persian Gulf biodiversity, and describe
an achievable and practical management plan to mitigate the im‐
pacts of DPs.

2 |  S E AWATE R D E SA LI N ATI O N


TEC H N I Q U E S

Desalination plant systems depend on energy sources, and these


F I G U R E 1   The main threats to biodiversity in the Persian Gulf
can be classified as thermal, mechanical, electrical, and chemical (Daliri et al., 2016; Kamrani et al., 2016; Sharifinia et al., 2015,
energy sources. Reverse osmosis (RO), multi‐effect distillation 2018, 2019)
SHARIFINIA et al. |
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F I G U R E 2   Classification of (a) the main desalination techniques and (b) contribution of each desalination technology to the world water
production

TA B L E 1   Advantages and disadvantages of desalination technologies (Negewo, 2012)

Desalination
processes Advantages Disadvantages

RO • Easily adapts to local conditions. • Needs comprehensive pretreatments to be applied


• Plant size can be adjusted to meet short‐term increases in demand for high saline water.
and expanded incrementally as needed. • Membrane fouling.
• Can remove silica. • Complex configuration.
• Capital cost approximately 25% less than thermal options. • Needs experienced personnel for operation and
maintenance.
MED • Capability to operation between 0% and 100% capacity while MED • Antiscalants necessary to stop scale buildup on
unit is kept under vacuum and cold circulation. evaporating surfaces.
• Appropriate to mix with renewable energy sources that supply
intermittent energy.
MSF • Easy management and operation. • Cannot operate below 60% capacity.
• Capability to treat saline water up to 70,000 mg/L. • Not appropriate to mix with renewable energies
that have intermittent energy supplies.
• High energy use.
ED • Up to 94% recovery rate. • Capital intensive and costly compared to RO.
• Durable membranes (up to 15 years).
• Ability to combine with RO for higher water recovery (up to 98%).

Abbreviations: ED, Electrodialysis; MED, multi‐effect distillation; MSF, multi‐stage flash; RO, reverse osmosis.

conducted by the primary steam is fed to the next component region, threat to the Persian Gulf environment from DPs (and also by
where the process is repeated (Miller et al., 2015; Semiat, 2000). other human activities) will be greater in the future, and there is an
The advantages and disadvantages of some desalination pro‐ urgent need for more research on reducing the effects of DPs on this
cesses are shown in Table 1. 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
3 | D I S TR I B U TI O N O F D P S I N TH E WO R LD envisages massive investments in DPs to bring water from the south‐
A N D PE R S I A N G U LF CO U NTR I E S ern Iranian coastal waters to the interior of the country. Currently,
213 active seawater DPs are operating in the Persian Gulf, with 51
Water from DPs has been used to supply freshwater in arid and semi‐ plants planned, under construction, or being installed. Saudi Arabia
arid areas of the world for decades. The highest numbers of DPs have and Kuwait have the highest and lowest numbers of DPs among the
been constructed in the Middle East, North America, Asia, Europe, and Persian Gulf countries (Figure 3b). The daily capacity of these plants
Africa (Figure 3a; Gorjian & Ghobadian, 2015; Lattemann & Höpner, for all of the Persian Gulf countries is about 11 million m3 per day,
2008a; Shatat, Worall, & Riffat, 2013). Given the arid nature of the which is approximately equal to half the global production (Gorjian
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F I G U R E 3   The global distribution of


the existing desalination plants (DPs; a)
worldwide, (b) in the Persian Gulf, and
(c) relative frequency of desalination
techniques used in Iran, and the entire
Persian Gulf

& Ghobadian, 2015; Sharifinia et al., 2019). Lattemann and Höpner Gheibi, & Zare, 2015; Taherizadeh & Sharifinia, 2015). The impacts
(2008a) reported that 81% of the desalinated water in the Persian Gulf of DPs on marine biodiversity include decreases in sensitive species,
countries is produced by MSF and 13% by MED, but only 6% by re‐ reductions in plankton abundance, decreases in hard substrate epi‐
verse osmosis. In contrast, the most applied technique in Iranian DPs fauna, and growth rate decreases of seagrasses (Roberts et al., 2010).
are RO and MED, respectively (Figure 3c; Gorjian & Ghobadian, 2015). 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
4 |  B I O D I V E R S IT Y V U LN E R A B I LIT Y change in anthropogenic pressures may intensify or limit the ability
TO E N V I RO N M E NTA L I M PAC T S O F D P of a species to respond to DP impacts. For example, brine discharges
D I S C H A RG E S from DPs induce morphological and physiological changes in a variety
of species, which in turn may limit the ability of a species to resist
Given the increasing rates of development of urban areas and coastal additional environmental stresses (Roberts et al., 2010). Owing to ex‐
construction in the Persian Gulf region, anthropogenic activities and treme evaporation (1.54 m/year; Brewer & Dyrssen, 1985) and low
climate change will be important threats to the future of biodiversity precipitation rates (0.03–0.11 m/year), the Persian Gulf is highly sa‐
in marine ecosystems (Griffith, Strutton, & Semmens, 2018; Henson line (average salinity for the entire region is more than 37; Moaddab,
et al., 2017; Kamrani et al., 2016; Segan, Murray, & Watson, 2016; Khabazi, & Roosta, 2017). The rapid increase in the number of DPs
Sharifinia et al., 2018, 2019; Sharifinia, Penchah, Mahmoudifard, will lead to ecological stresses by increasing water temperatures and
SHARIFINIA et al. |
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salinities throughout the region, decreasing dissolved oxygen con‐ Given that brine discharges from DPs are more dense than ambient
centrations, and increasing heavy metal concentrations (Sharifinia seawater, outfall water tends to remain at the bottom rather than getting
et al., 2019). Despite the documented impacts of DP discharges on mixed within the water column (Gacia, Invers, Manzanera, Ballesteros,
marine species, the Persian Gulf region suffers from a lack of research & Romero, 2007; Purnama, Al‐Barwani, & Smith, 2005; Roberts et al.,
on the regional impacts, with limited research that addresses environ‐ 2010). Therefore, benthic species are more likely to be initially affected
mental issues of DPs in general (de la Ossa‐Carretero et al., 2016a; by brine discharges rather than planktonic and pelagic species, and most
Lattemann & Höpner, 2008a; Roberts et al., 2010). studies have examined the impact of DPs on benthic organisms. Gacia
Semienclosed and shallow ecosystems such as Persian Gulf (with et al. (2007) investigated the effects of DP brine discharges on the seagrass
a mean and maximum depth of 50 and 89 m) with a high diversity Posidonia oceanica. They suggested that discharges result in increasing
of marine species, are generally more sensitive to brine discharges nitrogen content in tissues and decreasing carbohydrates. Seagrass
than open‐ocean systems (Lattemann & Höpner, 2008a). The im‐ meadows in the Persian Gulf include Halodule uninervis, Halophila stipula‐
pacts of desalination processes and applied pretreatments on the cea, and Halophila ovalis and are responsible for high primary production,
physicochemical properties of DP discharges were discussed by high biodiversity of associated flora and fauna, and serve as nursery and
Lattemann and Höpner (2008a). Discharges from DPs on salin‐ feeding grounds for many marine organisms. Persian Gulf seagrasses
ity and temperature (having been defined by Tettelbach & Rhodes are subject to very large changes in salinity (from 38 to 70) and tem‐
1981 and O'Connor & Lawler 2004 as ‘master factors’ for several peratures (from 10 to 39°C; Price, Sheppard, & Roberts, 1993). Halophila
marine organisms) and other contaminants around outfalls can be stipulacea and H. ovalis are more sensitive to increases in salinity, so the
considerable (Table 2). Autecological studies have indicated that de‐ distribution of these species is more limited spatially than that of the
velopment, growth, and survival of marine organisms are affected H. uninervis (Erftemeijer & Shuail, 2012; Green, Short, & Frederick, 2003).
by salinity and temperature (Kinne, 1964; O'Connor & Lawler, 2004; The available evidence indicates that H. uninervis in the Persian Gulf can
Tettelbach & Rhodes, 1981). tolerate hypersaline conditions (Erftemeijer & Shuail, 2012; Green et al.,
Increases in seawater salinity and temperature due to anthro‐ 2003), but further research into the impacts of the DP brine discharges
pogenic activities and climate change will continue to occur in the on seagrass species distribution and growth in the region is needed.
coming century (Pires, Figueira, Moreira, Soares, & Freitas, 2015), Salinity and temperature are the main factors controlling
particularly in coastal areas (Cardoso, Raffaelli, & Pardal, 2008; Pires growth, photosynthesis, and survival of corals (Baird & Hughes,
et al., 2015; Reid, Soudant, Lambert, Paillard, & Birkbeck, 2003). 2000; Ferrier‐Pages, Gattuso, & Jaubert, 1999; Kuanui, Chavanich,
Studies that assess the impacts of salinity and temperature changes Viyakarn, Omori, & Lin, 2015). Most marine organisms adapt to mod‐
on marine organisms are increasing, because these changes can have est changes from optimal salinity and temperature conditions, but are
harmful and lasting effects. For example, Pires et al. (2015) reported unable to tolerate these changes for long time periods (Lattemann &
that salinity increases have a significant negative impact on the regen‐ Höpner, 2008a). Research on the relationship between environmen‐
erative capacity of polychaete Diopatra neapolitana, and found that tal variables and coral distributions suggests that coral reefs only
under higher salinities complete regeneration was significantly de‐ grow within narrow ranges of salinity and temperature. Despite the
layed. The toxicological effects of DP discharges on seagrasses, fish, importance of salinity and temperature to coral reefs physiological
macrofauna, meiofauna, zooplankton, and phytoplankton exposed to processes, the effects of changes in theses parameters due to DP
effluents in areas surrounding the outlets are summarized in Table 3. discharges remains incompletely studied.
Salinity is a critical factor regulating the distribution of coral spe‐
cies and reef‐building potential (Riegl & Purkis, 2012). Corals appear
TA B L E 2   Physicochemical properties of discharges from DPs to have lower thresholds, as a 5% salinity increase causes reduced
growth and/or death (Birkeland, 2015; Hughes et al., 2017; van der
Physicochemical
properties Effect Merwe et al., 2014). Generally, most scleractinian corals can survive
only within a small range of salinity, and death occurs when salinity
Salinity Increases of up to 50,000 mg/L in both RO and
increases above 40 (Muthiga & Szmant, 1987). Other studies found
thermal plants
that sudden changes in salinity had a negative effect on coral repro‐
Temperature In RO plants equal to ambient seawater while in
MSF plants increases from 5 to 15°C duction, photosynthesis of algal symbionts, and respiration (Porter,

Dissolved Below ambient seawater DO Lewis, & Porter, 1999; Richmond, 1993). Disruption in the symbiotic
oxygen (DO) relationship between coral and alga due to salinity stress will have a
Heavy metals Elevated levels of iron, chromium, nickel, and severe effect on coral metabolism (Muthiga & Szmant, 1987). It has
molybdenum in RO, and copper and nickel in also been shown that salinity variations disrupt optimal cellular elec‐
thermal plants (MSF) trochemical processes, enzyme kinetics and nerve conduction, and
Coagulants In RO may be present, while in MSF not present cause metabolic drain (Vernberg & Vernberg, 2012). Ferrier‐Pages
Antiscalants Low content below toxic levels et al. (1999) reported that the growth rates of Stylophora pistillata
Abbreviations: DO, dissolved oxygen; MSF, multi‐stage flash; RO, decreased if salinity changed by 2–4 from optimal levels, and the
reverse osmosis. coral is particularly sensitive to hypersaline conditions. Furthermore,
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TA B L E 3   The ecological and toxicological impacts of DP brine discharges on marine organisms

Reference Species/community Summary of findings

de la Ossa‐Carretero Echinoderms, Polychaetes and • BOPA (Benthic Opportunistic Polychaetes and Amphipods) index suc‐
et al. (2016a); Amphipods cessfully indicates the impacts of DPs brine discharges on macrofaunal
Fernández‐Torquemada, communities.
González‐Correa, and • Echinoderms disappeared, sensitive amphipods decreased, and tolerant
Sánchez‐Lizaso (2013) polychaete families increased at the station closest to the discharge.
• The combination of a sensitive group like amphipods and a tolerant group
such as some polychaeta families, allowed an evaluation of the impact of
brine discharge.
Raventós, Macpherson, and Macrofauna • Monitoring found no significant changes in macrofaunal related to DP
García‐Rubies (2006) brine discharges.
Ruso, Ossa Carretero, Macrofauna • Found changes in abundance, number of taxonomic groups, and diversity
Casalduero, and Lizaso in macrofaunal assemblages impacted by DP discharges.
(2007) • In the vicinity of DP outfall, diversity and the number of taxonomic
groups reduced, while the abundance of nematode, increased.
• Macrofaunal assemblages in stations with salinity values >39 (close to a
DP outfall) dominated by nematodes (up to 98%).
Riera, Tuya, Ramos, Macrofauna • Macrofaunal assemblages surrounding DPs directly impacted by brine
Rodríguez, and discharges.
Monterroso (2012) • Monitoring found significant differences in abundance, community struc‐
ture, and diversity of macrobenthic fauna.
• The amphipod Ampelisca brevicornis dominated, in stations located at 15
and 30 m away from brine discharge was abundant.
Riera et al. (2011) Meiofauna • Abundances and community structure of meiofauna clearly impacted by
brine discharges.
• Found decreased abundance of meiofauna, particularly, nematodes in
impacted stations by brine discharge.
• Recommended meiofauna as useful indicators for ecological monitoring
programs of DP impacts.
de la Ossa‐Carretero et al. Amphipods • Amphipods indicated high sensitivity to DP brine discharges.
(2016b) • Found reduced abundance and diversity of amphipods in station sur‐
rounding and closest to discharge, where salinity values are up to 53.
Yoon and Park (2011) Phytoplankton (Skeletonema • Reported different tolerance ranges of phytoplankton species to brine
costatum, Chlorella vulgaris, discharge.
Tetraselmis suecica, and Isochrysis • Found significant correlation between brine concentration and phyto‐
galbana) plankton growth inhibition of the four species tested.
Macroalgae (Ulva pertusa) • Growth rate of S. costatum, T. suecica, and I. galbana decreased over 45
Zooplankton (Brachinonus plicatilis, • Galbana was the most sensitive species to DP brine discharges.
Tigriopus japonicas) • Sporulation rate of green algae U. pertusa sharply reduced with the
Demersal fish (Olive flounder, increase in brine concentration.
Paralichthys olivaceus) • Brine concentrations lower than 60.0 induced <50% mortality and over
65.0 resulted in >50% mortality.
• Mortality rate of fish increased with increasing salinity.
• Difference of brine effect on Paralichthys olivaceus related to ecophysi‐
ological characteristics such as adaptation capacity, exposure time, and
origin of species.
• Survival rate reduced with the increase in brine concentration.
Portillo et al. (2014) Fish • Total mortality of Liza fish (Synodus synodus) occurred at sodium metabi‐
sulfite concentrations equal to or greater than 50 ppm.
• Dead individuals of Lizardfish and other soft‐bottom species (Bothus
podas, Microchirus azevia, and Trachinus draco) occurred over more than
2 ha.
Gacia et al. (2007); Seagrass • Shallow Posidonia oceanica meadows exposed to RO brine discharge;
Sanchez‐Lizaso et al. found P. oceanica very sensitive to high salinities.
(2008); Latorre (2005); • High epiphyte load and nitrogen content in the leaves, high frequen‐
Walker and McComb cies of necrosis marks, low total nonstructural carbohydrates, and low
(1990) glutamine synthetase activity in affected meadows observed.

(Continues)
SHARIFINIA et al. |
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TA B L E 3   (Continued)

Reference Species/community Summary of findings

Cambridge, Zavala‐Perez, Seagrass Posidonia australis • Salinity decreased maximum quantum yield of chlorophyll‐a fluorescence
Cawthray, Mondon, and emissions.
Kendrick (2017) • Elevated salinity negatively affected the leaf water potential and osmotic
potential, while turgor pressure unaffected.
• K+ and Ca2+ concentrations is reduced in meadow leaves, while sugars
mainly sucrose and amino acids increased.
• Leaf osmolarity, ion, sugar, and amino acids recommended as potential
bioindicators to assess impacts of DP brine discharge.
Iso, Suizu, and Maejima Fish (Pagrus major, Pleuronectes • The impacts of DP brine discharge on fertilized eggs, larvae, juveniles,
(1994) yokohamae) and adults.
• Incipient lethal high salinity and sensitivity in each organism were differ‐
ent in different species according to their ecological and morphological
characteristics.
• Pagrus major juveniles exposed to salinities of 70 died within 1 hr, with
some mortality at 50.
• Pleuronectes yokohamae larvae died at salinities of 55 after approximately
6 days of exposure.
• Hatchability of eggs was delayed at S = 60 and completely inhibited at 70.
Iso et al. (1994) Bivalve (Tapes philippinarum) • In salinities <50, Tapes philippinarum extended their siphons after 30 min.
• In salinities >50, T. philippinarum kept their shells closed. After 24 hr, they
opened the shell at S = 60 and 70.
• The first lethal effect observed at 48 hr in S = 60 and at 24 hr at 70.
del Pilar‐Ruso, Ossa‐ Polychaeta • Found different sensitivity of polychaete families to brine discharges;
Carretero, Giménez‐ Ampharetidae were the most sensitive, followed by Nephtyidae and
Casalduero, and Spionidae.
Sánchez‐Lizaso (2008) • Syllidae and Capitellidae exhibited some resistance, while Paraonidae
was shown to be a tolerant family.
Dupavillon and Gillanders Cuttlefish (Sepia apama) • Cuttlefish embryo survival rates reduced with increasing salinity, with no
(2009) embryos surviving in salinities >50.
• Mean weight and mantle length reduced with an increase in salinity.
• DP brine discharge introduced as a potential threat to the spawning ag‐
gregation of the Sepia apama.
Mandelli (1975) Oyster (Crassostrea virginica) • The effects of DP brine discharge on juvenile and adult Crassostrea virgi‐
nica were evaluated; they found that high copper concentrations in brines
was the most critical factor affecting survival and reproduction.
Petersen et al. (2018) Corals (Stylophora pistillata, • DP brine discharge adversely impacted scleractinian corals and associ‐
Acropora tenuis, and Pocillopora ated Symbiodinium and microbial communities.
verrucosa) • Increased salinity (10% above ambient) changed Stylophora pistillata,
Acropora tenuis, and Pocillopora verrucosa physiology.
• Found that the effects of DP brine discharge on hard corals is
species‐specific.
Frank, Rahav, and Bar‐Zeev Microbial communities • Microbial abundance decreased (up to 60%) at salinity levels >5% above
(2017) the surrounding environment.
• Elevated salinity increased the activity of bacterial metabolism.
Portillo et al. (2014) Seagrass (Cymodocea nodosa) • Monitoring shows high sensitivity to short‐term exposure to low sodium
metabisulphite (SMBS).
• Cymodocea nodosa were completely absent within the influence of the
salinity field connected with the brine discharge.
• Vitality and survival of the Cymodocea nodosa seedling exposure to
100 ppm SMBS concentrations decreased.

other studies indicated that rapid changes in salinity can effect zo‐ there was an overall reduction in coral performance and variations
oxanthellae photosynthesis and may induce coral death by reduc‐ in physiology of corals and suggested that the DP brine discharge
ing the amount of energy transferred to corals (Manzello & Lirman, can lead to coral tissue loss due to decreases in Symbiodinium abun‐
2003; Muthiga & Szmant, 1987). Petersen et al. (2018) investigated dance and reduction in protein synthesis.
the potential impacts of brine discharge on reef‐building corals S. The best development and growth of corals occur in offshore
pistillata, Acropora tenuis, and Pocillopora verrucosa. They found that areas of the Persian Gulf, and is limited due to the extremes in
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8       SHARIFINIA et al.

TA B L E 4   Tolerance range of different corals species to the for carbon sequestration (Sharifinia et al., 2019). Furthermore, the
salinity in the Persian Gulf Persian Gulf ecosystem sustains the livelihoods of millions of people

Salinity through fisheries and tourism (Daliri et al., 2016; Madani, Ahmadian,
KhaliliAraghi, & Rahbar, 2012; Nouri, Danehkar, & Sharifipour, 2008;
Coral species 46 48 50
Sharifinia et al., 2019). Coral reefs and mangrove forests provide
Cyphastrea serailia X     coastal protection to nearby Persian Gulf villages, towns, and cities,
Porites harrisoni X     an increasingly important service owing to sea level rise (Sale et al.,
Platygyra daedalea X X   2011; Sharifinia et al., 2019). It is possible that the adverse impacts
Favia pallida X X   of DPs will modify or impair the provided goods and services by

Favites chinensis X X   Persian Gulf in the future. As such, there is a pressing‐need for fur‐
ther research into the impacts of discharges on marine biodiversity.
Leptastrea purpurea X X  
The potential impacts of DPs on all species in the system result
Porites nodifera X X X
from their exposure, adaptive capacity, and sensitivity. However,
Cyphastrea microphthalma X X X
there is a growing evidence that DPs have begun to affect survival,
Siderastrea savignyana X X X
reproduction, diversity, and distribution of marine organisms (Chang,
2015; Petersen et al., 2018; Roberts et al., 2010). Brine discharges
temperature, salinity, and other physical parameters (Sheppard (and other associated environmental disturbances) by DPs into the
et al., 2010). Despite these difficult environmental conditions, Persian Gulf will impact physicochemical parameters. Therefore, due
coral species show remarkable resilience and vitality in the region. to accumulation of brine discharges in and around the DPs, the bot‐
Tolerance ranges of different corals to the salinity in the Persian tom dwelling species will be strongly impacted (Feary et al., 2013).
Gulf are shown in Table 4. Sheppard, Price, and Roberts (1992) With such a high number of existing DPs and a scarcity of research
found Cyphastrea serailia and Porites harrisoni growing in salinities on the effects of DPs on biodiversity, we used the results from other
>42 in the Persian Gulf with large heads of Porites spp. flourishing parts of the world to predict and suggest the future potential im‐
at 48. However, most corals die or suffer damage at salinities above pacts of DP discharges on the Persian Gulf fauna and flora (Figure 4).
48. Although Persian Gulf corals are adapted to high salinities, cor‐ We conclude that increasing the input of brine discharges from
als may be vulnerable to exposure to DP discharges, and there is a DPs will cause a reduction in plankton biomass, species diversity,
need for systematic studies on the effects of brine discharges on and richness in the Persian Gulf. High levels of brine discharges into
coral reefs and their abilities to acclimate to increased salinities. the Persian Gulf may have the following impacts: alter phytoplank‐
ton photosynthesis due to increases in water turbidity that reduce
light penetration; increase benthic mortality due to cell dehydration
5 |  W H AT W I LL H A PPE N TO and subsequent turgor reduction, and over long time periods, alter
B I O D I V E R S IT Y I F W E E X PA N D the nature of the benthic habitat; change chloroplast ultrastructure,
D E SA LI N ATI O N PL A NT S I N TH E PE R S I A N decrease in chlorophyll content, enzyme activity, and electron flow
G U LF ? inhibition in photosynthetic organisms; alter larval development and
individual growth, larval survival rate and generation time, species
The direct impacts of DP discharges on the Persian Gulf biodiver‐ reproduction and reproductive traits in a variety of organisms; and
sity presently remain unknown, and little is known about how these result in a loss of fishery resources and economic activity due to
releases impact present and future ecosystem functioning and ser‐ biomass and reproductive reductions in marine species.
vices. 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, bioprospect‐ 6 | M ITI G ATI O N PL A N S FO R D P
ing, building materials), supporting services (life cycle maintenance ECO LO G I C A L I M PAC T S
for both fauna and flora, primary and secondary production, nutri‐
ent cycling), regulating services (carbon sequestration and storage, Mitigation plans for DP facilities are necessary to maintain the
erosion prevention, wastewater treatment, moderation of extreme aquatic vitality and productivity (‘prevention is better than the cure’)
events), and cultural services (touristic, recreational, esthetic, and and should be evaluated prior to and during the construction of new
spiritual benefits). It is difficult to evaluate Persian Gulf services DPs in the Persian Gulf. The effects of DPs on the environment de‐
and goods, because the same ecosystem can have a local, regional, pend on factors such as plant size, type of desalinizing process, use
and global impact (Pendleton, Thébaud, Mongruel, & Levrel, 2016). of chemicals during desalination, and the specific ecological and hy‐
Despite the great loss of biodiversity (e.g., coral reef deterioration), drographical characteristics of the site (Lattemann & Höpner, 2008b).
ecosystem goods and services are more greatly valued today than To mitigate the negative impacts of DP discharges on Persian Gulf
20 years ago. In the Persian Gulf, several systems such as man‐ biodiversity, we propose measures to achieve a balance between ma‐
groves forests, seagrasses, and marshes are potentially important rine ecological conservation and generation of needed freshwater.
SHARIFINIA et al. |
      9

F I G U R E 4   Potential impacts of
desalination plant (DP) discharges on the
Persian Gulf ecosystem. DO, dissolved
oxygen

To mitigate the impingement and entrainment of larger plankton in land deposition, and dewatering. In summary, environmental impacts
intakes, a low through‐screen velocity (lower than 0.15 m/s), small of DPs could be mitigated by preventing and replacing damaging
screen openings (less than 22 cm), and suitable fine screen mesh size chemicals such as heavy metals and chlorine used during treatment,
(less than 9 mm) should be used to reduce the impact on plankton, fish diluting and dispersing the salt, heat, and any contaminants using
eggs and larvae. One common mitigation strategy to reduce impacts hydrological conditions and shoreline morphology (sandy and rocky
is to use modern surface water intake designs or a subsurface intake. shorelines exposed to strong currents are suggested), eliminating
In particular, subsurface intakes can virtually eliminate IPM and ETM, plant construction in areas of high biological importance (near coral
as seawater is taken from beneath the sea floor. Three additional reefs, mangroves, and nesting habitats for sea turtles), and avoiding
mitigation plans that can be useful and effective in reducing impacts plant construction in areas that are important to biodiversity and pro‐
include creation of marine wetland areas or other marine habitats al‐ ductivity, (nursery, feeding, and harvesting grounds). Appropriately
lowing greater areas for spawning of fish and invertebrates, paying a sited, designed, operated, and well‐planned DPs can minimize eco‐
fee based on calculating the IPM and ETM losses, and restocking the logical impacts on the marine life. By using current developments in
marine impacted habitat with fish and invertebrates’ eggs, larvae, ju‐ impingement and entrainment reduction technology, both nationally
venile, and small adult forms (Missimer & Maliva, 2018). Furthermore, and internationally, marine biodiversity and local ecosystems will be
the intake inlet should be placed outside the littoral zone in deeper preserved with minimal environmental impacts.
waters and away from sensitive productive areas. Locating intake in‐
lets at least 300 m from shoreline and installing them in water at least
20 m, where organism abundances are lower, could minimize effects 7 | CO N C LU D I N G R E M A R K S
associated with intake operations (WateReuse‐Association, 2011).
The adverse effects of chemicals can be reduced by treatment before Desalination plants are a potentially serious threat to biodiversity
discharge such as replacing hazardous substances, as well as through in marine environments. A better understanding of the impacts will
the use of alternative treatment options. Biocides such as chlorine increase the breadth of mitigation plans to deal with their negative
that can acutely affect organisms at the discharge site, should be re‐ effects on marine systems. Information on the impacts of DP brine
placed or treated before discharge. Chlorine can be removed from discharge on marine biota is available, but there is a pressing need
the effluent by using efficient chemical substances such as sodium bi‐ for further research to explore footprints of DPs in the Persian Gulf
sulfite (NaHSO3), as practiced in RO plants, while sulfur dioxide (SO2) and on regional impacts. We propose that new efforts in six cat‐
and hydrogen peroxide (H2O2) have been suggested to treat thermal egories are necessary: (a) Understanding the vulnerability of species
plant stream effluents (Lattemann & Höpner, 2008a). Cleaning solu‐ to DPs releases for designing effective mitigation strategies; (b) Use
tions should be treated on‐site in special treatment facilities, while of both field monitoring and laboratory experiments to assess DP
waters from filter backwash should be treated by sedimentation, impacts on the biodiversity in the Persian Gulf; (c) Provide data on
|
10       SHARIFINIA et al.

positive or negative responses of each species to brine discharges Cambridge, M., Zavala‐Perez, A., Cawthray, G., Mondon, J., & Kendrick,
for use in future plan construction efforts; (d) Conduct a compre‐ G. (2017). Effects of high salinity from desalination brine on growth,
photosynthesis, water relations and osmolyte concentrations of
hensive Environmental Impact Assessment before and after each
seagrass Posidonia australis. Marine Pollution Bulletin, 115, 252–260.
desalination project to understand all ecological impacts of DP con‐ https​://doi.org/10.1016/j.marpo​lbul.2016.11.066
struction; (e) Develop collaborative research projects to prevent the Cardoso, P. G., Raffaelli, D., & Pardal, M. A. (2008). The impact of extreme
negative impacts of DPs and other activities on the Persian Gulf bio‐ weather events on the seagrass Zostera noltii and related Hydrobia
ulvae population. Marine Pollution Bulletin, 56, 483–492. https​://doi.
diversity; and (f) Creation of a joint task force on how to protect the
org/10.1016/j.marpo​lbul.2007.11.006
regional environment, or establishing a forum for Persian Gulf coun‐ Chang, J. S. (2015). Understanding the role of ecological indicator use in
tries to reach a consensus. Such a system will allow the development assessing the effects of desalination plants. Desalination, 365, 416–
of reasonable scenarios of future environmental impacts of DPs and 433. https​://doi.org/10.1016/j.desal.2015.03.013
Daliri, M., Kamrani, E., Jentoft, S., & Paighambari, S. Y. (2016). Why is
marine biodiversity.
illegal fishing occurring in the Persian Gulf? A case study from the
Hormozgan province of Iran. Ocean & Coastal Management, 120, 127–
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AC K N OW L E D G E M E N T S
de la Ossa‐Carretero, J. A., del Pilar‐Ruso, Y., Loya‐Fernández, A.,
Ferrero‐Vicente, L. M., Marco‐Méndez, C., Martinez‐Garcia, E.,
This research was supported by a grant from the Iran National
… Sánchez‐Lizaso, J. L. (2016a). Bioindicators as metrics for en‐
Science Foundation (INSF; 97015984) to Dr. Moslem Sharifinia. The
vironmental monitoring of desalination plant discharges. Marine
author is very grateful to the INSF for financial support. We would Pollution Bulletin, 103, 313–318. https​://doi.org/10.1016/j.marpo​
also like to thank all colleagues at Iran Shrimp Research Center lbul.2015.12.023
(ISRC) and Chabahar Oceanographic Research Station for their kind de la Ossa‐Carretero, J. A., del Pilar‐Ruso, Y., Loya‐Fernández, A.,
Ferrero‐Vicente, L. M., Marco‐Méndez, C., Martinez‐Garcia, E., …
assistance and cooperation. Finally, the authors are grateful to the
Sánchez‐Lizaso, J. L. (2016b). Response of amphipod assemblages
reviewers and the editor for the time and effort they put into their to desalination brine discharge: Impact and recovery. Estuarine,
detailed comments that helped improve this paper. Coastal and Shelf Science, 172, 13–23. https​ ://doi.org/10.1016/
j.ecss.2016.01.035
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C O N FL I C T O F I N T E R E S T & Sánchez‐Lizaso, J. L. (2008). Effects of a brine discharge over soft
bottom Polychaeta assemblage. Environmental Pollution, 156, 240–
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Moslem Sharifinia  https://orcid.org/0000-0003-2969-0036 Aquatic Ecosystem Health and Management, 15, 73–83. https​://doi.
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