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sustainability
Review
Sustainable Agriculture in the Arabian/Persian Gulf
Region Utilizing Marginal Water Resources: Making
the Best of a Bad Situation
J. Jed Brown, Probir Das and Mohammad Al-Saidi * ID
Center for Sustainable Development, College of Arts and Sciences, Qatar University, P.O. Box 2713, Doha 2713,
Qatar; jedb00@gmail.com (J.J.B.); probir.das@qu.edu.qa (P.D.)
*Correspondence: malsaidi@qu.edu.qa
Received: 12 March 2018; Accepted: 24 April 2018; Published: 27 April 2018
Abstract:
One way to encourage agricultural self-sufficiency in arid regions is to increase the
productivity of conventional freshwater agriculture. Another way is to develop and implement
novel strategies and technologies that do not deplete scarce freshwater. Here we describe several
options for countries in the Gulf region to increase their agricultural production by taking advantage
of a lesser used resource—marginal water. Marginal water can be treated sewage effluent, produced
oilfield water, brackish groundwater or seawater. We describe how this resource can be used to grow
salt-tolerant forage crops, microalgae and aquaculture crops. Policies needed to implement and/or
scale-up such practices are also outlined.
Keywords:
Arabian Gulf; Persian Gulf; GCC; microalgae; saline agriculture; halophytes; aquaculture;
treated sewage effluent; produced water; aquafeeds
1. Introduction
As a result of the arid/hyper-arid climatic conditions, the majority of the area of the Gulf
Cooperation Council Countries (GCC—Bahrain, Kuwait, Oman, Qatar, Saudi Arabia and UAE) is beset
by a lack of freshwater resources. This lack of freshwater is an obvious constraint to development of
conventional agriculture in this region. Arable land is quite limited, averaging around 4.25% of the
total land area in the GCC region [
1
]. At the same time, water use for irrigation and livestock represent
the biggest share of total water use, 45% in Bahrain, 54% in Kuwait, 88% in Saudi Arabia, 89% in Oman,
59% in Qatar and 83% in the UAE (FAO Aquastat for the year 2014). Local agriculture largely depends
on the use of non-renewable groundwater supplies and suffers from poor practices such as low
irrigation efficiency, leakages due to poor agricultural water networks and water-intensive cropping
patterns [
2
]. Altogether, freshwater resources in the region are becoming threatened by agricultural
water overuse and mismanagement. There are, however, opportunities for food production and/or
landscape that do not entail the utilization of large quantities of freshwater.
One way forward would be to concentrate on conducting conventional agriculture more
sustainably. There have been many attempts in the region to improve local agricultural production
through the development of soil surveys and measures to improve productivity [
3
]. However, in
reality, since the rate of groundwater recharge is so slow in this region, one could argue that any use
of this fossil groundwater resource is not sustainable, as this is essentially a non-renewable resource.
Similarly, use of desalinized water for agriculture will not be sustainable due to the high energy costs
associated with the desalination process in the GCC region, namely between $0.45 (subsidized) and $1
per cubic meter [4].
Sustainability 2018,10, 1364; doi:10.3390/su10051364 www.mdpi.com/journal/sustainability
Sustainability 2018,10, 1364 2 of 16
Therefore, food imports are expected to increase in the region in order to meet the region’s
growing population. Sustainable local agriculture of some type needs to be developed or enhanced in
order to provide some level of self-sufficiency using crops suitable for the desert climate [5].
Another way forward would be to try to make use of marginal or underutilized water sources.
For example, the region does have access to seawater in the Arabian (Persian) Gulf. Additionally, there
is also a large volume of brackish water that is too saline for conventional agriculture, which underlies
much of the region. This brackish water is present naturally, and/or has increased due to the increased
freshwater abstraction followed by seawater intrusion. For example, in Qatar in 2009, only 2% of the
land area was underlain by high quality freshwater that is less than 1 part per thousand (ppt) salt and
only 8% of the land was underlain by water less than 2 ppt salt [
6
]. In other words, over 90% of the
land area is underlain by groundwater that is far too saline for any type of conventional agriculture;
therefore, there is huge unutilized resource in Qatar and other Gulf countries that could be used for
non-traditional agriculture.
Additionally, large quantities of treated sewage effluent are underutilized. And finally, there are
large volumes of produced water available in the Gulf, that is, water that is produced in the process of
oil and gas extraction, which could be used for agriculture. The potential to use such marginal water
sources for food and landscape production will be explored here. In particular, we explore the use of
marginal water to produce salt-tolerant plants (halophytes), micro-algae and mariculture products.
To meet the food demand of the world’s growing population, it is critical to develop novel agricultural
systems that can take advantage of vast non-arable arid land areas and brackish water. Further, the
challenges facing large-scale adoption of the highlighted alternatives for enhancing local agriculture
will be discussed. Here we deem seawater as a marginal water source in the sense that it cannot be
used for conventional agriculture, not meaning to imply that it is of poor quality.
2. Treated Sewage Effluent (TSE)
The use of treated domesticated wastewater or treated sewage effluent (TSE) for irrigating
agricultural crops and landscapes is a widely used method to conserve and re-use water. TSE is
widely used for these purposes in Gulf countries and other arid countries [
7
]. However, this TSE
resource is underutilized. Currently, the wastewater treatment average in the GCC is around 56%,
while only 43% of the treated wastewater in the region is being recycled, contributing to only 1.8%
of total water supply [
8
]. One of the chief reasons for this wastage is due to poorly organized or
fragmented distribution networks, which makes dispersal of this resource difficult or problematic.
In Qatar, currently, a large percentage of the TSE that is utilized for agriculture is used to grow forage
grasses (mostly Rhodes grass) to feed livestock (M. Atta, Qatar Ministry of Environment, personal
communication). However, much of this grass-growing takes place adjacent to the sewage treatment
plants. This is fine if your farming land is next to the sewage treatment plant. However, if your farm is
distant from the sewage plant, (e.g., northern Qatar), then it is obviously difficult to gain access to this
water. Wastage of the TSE is not only an environmental sustainability issue but also an economic one.
So from a longer term perspective, it makes sense to develop more integrated wastewater distribution
networks. The State of Qatar plans to more than double the allocation of TSE to agriculture/fodder
production by 2020 and estimates that this will result in a three-fold increase in domestic livestock
herd size.
Similarly, TSE can be wasted if it used to irrigate plants that require a great deal of water or
very frequent irrigation. Use of drought tolerant plants (xerophytes), particularly native species,
for landscaping can further reduce the demand on TSE. Although TSE is certainly an option for
agriculture, many concerns exist as to its safety and social acceptability, particularly the accumulation
of heavy metals that are toxic to humans and animals, as well as the potential to transmit pathogenic
micro-organisms [
9
–
12
]. TSE typically has higher salt (200–3000 mg/L TDS), nutrient, solids and
frequently metal content than conventional irrigation water [
13
–
16
] and it has been observed that these
metals can accumulate in food crops. For example, a recent study in which TSE was used to grow okra
Sustainability 2018,10, 1364 3 of 16
in Saudi Arabia found that the okra frequently accumulated Ni, Pb, Cd and Cr above safe limits and
the authors concluded that the vegetable was not safe for direct consumption by human beings [
17
].
But other reviews have noted that high metal content in TSE is not a universal fact and can vary among
localities [18].
Solids and nutrients such as nitrogen and phosphorus can improve the water holding capacity
and the fertility of the soils, respectively [
18
], which can be particularly beneficial for arid land soils.
The increased salt content of the TSE can increase salinity/sodicity of the soil especially in arid areas
and this may or may not affect crop yields; basically higher salinity water will decrease yields [
19
],
whereas lower salinity may not (e.g., [
20
]). Irrigation strategies such as using a high leaching fraction
can be employed to decrease soil salinity and flush salts below the root zone [
19
]. In summary, TSE
represents a useful water resource but systems need to be monitored to ensure that concentrations of
heavy metals and salts are not becoming a problem.
3. Produced Water
Produced water, which is generated during the extraction of oil and gas from the ground, may
also be a potential source for irrigation water, especially given the huge petroleum industry in the Gulf.
Produced water is a combination of formation water that is trapped with oil and gas and the injection
water that is used to enhance recovery rates of the oil and gas [
21
]. Produced water contains organic
and inorganic chemicals where the salinity can range from close to freshwater to concentrated saline
brine; aromatic hydrocarbons, some alkylphenols and a few metals from produced water are potential
environmental concerns [
21
]. A wide variety of methods are available to treat produced water [
22
].
Currently most produced water in the Gulf is re-injected into the reservoir to maintain pressure, or
injected into a disposal well.
Produced water from the Gulf tends to be saline—one study found 5 g/L TDS in produced water
from a Qatar gas field [
23
] and much higher in Kuwait ~100 g/L [
24
]. Produced water from oilfields
has been used to irrigate crops in California for over 30 years [
25
]. Perhaps produced water could
also be used in the Gulf for irrigation or algae cultivation. If salt-tolerant crops or algae are grown,
then depending on its salinity, perhaps the produced water would only need to be treated to remove
hydrocarbons and would not need to be desalinated, thereby reducing costs.
4. Use of Saline Water for Terrestrial Agriculture
Most conventional crops are sensitive to salt in the irrigation water and depending on the crop,
yields will generally begin to decrease with irrigation water conductivities of 1–3 ds/m [
26
]. There
are, however, salt-tolerant plants, called halophytes that can grow and complete their life cycles in
saline water. Halophyte species have been identified to produce a variety of useful products, including
firewood or timber from mangroves for example [
27
]; fresh vegetables [
28
,
29
]; oilseeds
[30–32]
;
grains [
31
]; medicine [
33
,
34
]; forages for livestock [
35
–
37
]; for phytoremediation [
38
,
39
]; biofuel [
40
–
43
];
as biofilters for saline aquaculture effluent [
44
,
45
] and ornamentals [
46
]. There have been efforts to
grow some of these species in agricultural settings using seawater [
30
,
31
]. There are many halophyte
species native to the Gulf that could be considered for potential crops for saline-water irrigation [47].
Perhaps the most promising use of halophytes in the GCC region might be for use as forage.
Livestock, especially sheep, are widely grown for meat production in the Gulf. Large quantities of
water are used to irrigate to grow these forages, such as Rhodes grass, for livestock. Many countries
subsidize or recently ended subsidies for forage production. These subsidies led to increased use
of fresh water for agricultural irrigation. For example, in the Emirate of Abu Dhabi, which ended
subsidies to farmers for producing Rhodes grass in 2010, up to 59% of the total irrigation water volume
was to grow Rhodes grass [
48
]. Not only is Rhodes grass subsidized but other feed ingredients such as
wheat bran and barley are also subsidized. Developing locally-produced feed ingredients will not only
increase food independence but will also be an incentive for the government to remove subsidies for
feed ingredients and thereby reduce spending.
Sustainability 2018,10, 1364 4 of 16
Halophytes can comprise a portion of livestock feed and in particular, sheep feed. It has been
observed that in circumstances where sheep have access to halophytes and other low quality forage
supplements, the animals remained healthy and could gain weight [
49
]. Similarly, when sheep in pens
were fed halophytes mixed with grain, animals had modest weight gains and produced high lean
meat [
49
]. Meat from sheep fed halophyte-based diets has been found to have high eating quality [
49
]
and the high vitamin E levels in the halophytes improved the shelf life of meat and can potentially
benefit human health [50].
The potential forage plants fall into two categories. Firstly, the grasses, which tend to exclude
salts from their tissues, grow at low-moderate salinity and under irrigation they have been reported
to produce up to 40 t DM/year [
51
–
55
]. Biomass yields of about 60 t/ha/year (fresh weight) for
Panicum antidotale were reported when grown in saline soil (EC 10–15 mS cm
−1
) and irrigated with
brackish water (EC 10–12 ms cm
−1
) [
52
]. The plant was subjected to analysis for both nutrient and
anti-nutrient factors and cattle fed a P. antidotale diet achieved growth and meat production equivalent
to those fed a conventional maize-based diet.
Other grasses have also been successfully used to replace ingredients such as maize forage in
ruminant diets [
56
–
58
]. They produced similar biomass to conventional pasture plants and did not
accumulate salt. However, the grasses tend to be low in nutritive value (metabolizable energy and
crude protein), indicating that high quality supplements must also be added to ensure that the animals
can grow quickly. Variation in nutritive value between plant species allows for the potential to select
plants that can support higher levels of livestock production [59].
The second category are dicot plants that grow well under highly saline conditions, such as
seawater. The dicot halophytes accumulate salt in their tissues, are succulent and tend to have high
nitrogen content. These plants often have low biomass production when grown under extensive arid
conditions [
60
] but this has been reported to increase to 20 t DM/ha under seawater irrigation for the
oilseed halophyte Salicornia bigelovii [
31
]. Ruminants are moderately tolerant of salt and can grow
well with a salt intake of up to 5% of the diet [
61
]. The high nitrogen levels in halophytes may be
beneficial as ruminants fed adequate energy can convert plant nitrogen into protein. Therefore, these
dicots can be included as a significant component of a total mixed ration to provide energy and a
nitrogen source for protein production. It has recently been shown that halophytes can be included as
a significant component of a feedlot diet in a series of experiments investigating how consumption
of halophytes influences meat eating quality [
49
,
50
,
62
,
63
]. Sheep that were fed diets that contained a
high proportion of halophytes exhibited moderate weight gain and produced meat with a high eating
quality (determined by a taste panel) and the meat also had extended shelf life. Similar to the grasses,
there is variation in nutritive value across these plants and their value as a feed component can be
improved through management and selection [64,65].
5. Marginal Water to Cultivate Microalgae for Use as Feed
Although the production of algae for biofuel may not be economically feasible currently, there
may be some value to grow algae for its protein content to be used as component of aquafeeds for
aquaculture. Fish constitute a major source of animal protein in human diets. In addition to protein,
fish also provide various polyunsaturated fatty acids (PUFA) which are very useful for human health.
Capturing fish from the wild may not be sustainable in certain fisheries due to over-fishing. To meet
the deficit in supply, fish farming is being developed in almost all parts of the world. The existing
practice of farming fish, livestock and poultry mostly rely on terrestrial plants crops for the formulation
of the feed; most of these plants require both arable land and freshwater. Therefore, expansion
of fish farming will likely result in an increase in terrestrial feed production. The increase in feed
production, would likely require energy and water-intensive irrigation systems. Furthermore, limited
land and freshwater availability and widespread pollution are already creating pressure on the existing
agricultural systems.
Sustainability 2018,10, 1364 5 of 16
Microalgae and cyanobacteria (hereafter collectively referred to as microalgae) are photosynthetic
microorganisms which are found virtually world-wide. Some species can double their biomass
multiple times in a single day, under favorable growth conditions. The potential biomass production of
selected microalgae strains can be an order magnitude higher than any other terrestrial plants (Table 1).
Table 1.
Comparison of aerial biomass productivity of conventional feed sources with a few marine
microalgae with commercial potential.
Feedstock Yield (t/hectare) Reference
Corn 9.4 [66]
Soybean 2.7 [67]
Wheat 5.7 [68]
Nannochloropsis sp. φ80.3 [69]
Nitzschia sp. φ78.8 [70]
Isochrysis galbana φ86.1 [71]
Phaeodactylum tricornutm φ63.7 [72]
φRepresent microalgae.
While seawater and saline groundwater are ideal water sources to grow microalgae, TSE could be
another source of water for growing microalgae biomass. TSE could also be used as a makeup water to
balance the daily evaporation loss. The availability of organic and inorganic compounds in the TSE
could be beneficial for microalgal growth; however, certain toxic compounds and heavy metals, if
present in high concentrations, could be absorbed into the microalgae biomass [
73
,
74
]. To eliminate or
minimize the pathogens and other micro-organisms in the microalgae culture, a disinfection method
should be applied to the TSE; some of the advanced wastewater treatment plants s are applying
chlorination before reusing the TSE. In case, if the concentration of heavy metals in the TSE is high, the
TSE could be diluted with seawater or the brackish water [75].
Microalgae are composed of carbohydrate, protein, and lipids, as well as other secondary
metabolites (e.g., pigments, vitamins, and minerals). The concentration of these metabolites can
vary among strains and growth conditions. Protein content in certain microalgae and especially in
cyanobacteria can exceed 50% of the dry weight (see Table 2). Furthermore, some of these strains have
all the essential amino acids in the desired ratio, unlike conventional protein sources (e.g., cornmeal,
wheat gluten meal and soy meal.) for proper protein synthesis (see Table 3). A few of the strains can
produce copious amount of omega-3 polyunsaturated fatty acid (e.g., EPA and DHA) which terrestrial
plants cannot synthesize. These fatty acids are beneficial for human health. Human dietary intake of
these fatty acids is mainly derived from consuming wild and farmed fishes. However, the primary
source of these fatty acids are the aquatic photosynthetic microbes. It was further reported that as per
their nutritional value and digestibility, algae were on par or even exceeded many other sources of
feed [
76
]. Taking advantage of their prolific growth rate and high protein content, researchers explored
the commercial exploitation of these strains as single cell proteins beginning in 1960 [
77
]. However,
large-scale deployment of this technology was not practiced because of higher production costs at
that time and the algae odor (fish-like) proved problematic for direct human consumption. With the
dwindling supply and increased price of fishmeal in recent times [
78
], it is becoming crucial to develop
cost and energy effective techniques for microalgal biomass production.
Sustainability 2018,10, 1364 6 of 16
Table 2. Metabolites composition of some of the microalgae and cyanobacteria.
Strains Name Protein (%) Carbohydrate (%) Lipid (%) Ref.
Chaetoceros sp. 33 12 20.9 [79]
Dunaliella sp. 25.7 40.2 18 [80]
Isochrysis sp. 47.9 26.8 14.5 [81]
Nannochloropsis sp. 30.3 9.6 21.8 [82]
Phaeodactylum sp. 49.5 45.5 5.5 [83]
Synechococcus sp. 63 15 11 [84]
Tetraselmis sp. 30.7 33.6 17.6 [85]
Chroococcidiopsis sp.
60.3 22.2 3.8 [86]
Table 3.
The composition of essential amino acids (g/100 g protein) in different feed ingredients and
microalga Nannochloropsis sp. and cyanobacterium Chroococcidiopsis sp.
EAA Fish Meal
(Herring) Soybean Meal Corn Meal Nannochloropsis sp. Chroococcidiopsis sp.
Histidine 2.4 1.442 0.91 1.5 0.8
Isoleucine 4.5 3.17 2.37 3.5 2.6
Leucine 7.5 5.53 10.26 6.7 7
Lysine 7.7 3.84 0.91 4.8 3.8
Methionine 2.9 0.81 1.09 1.8 0.4
Phenylalanine 3.9 2.76 2.79 3.9 6.3
Threonine 4.3 3.03 2.06 3.6 6.1
Tryptophan 1.2 0.57 1.3 1.7 -
Valine 5.4 5.59 2.85 4.6 7.8
Reference [87] [88] [89] [90] [86]
6. Challenges in Large-Scale Cultivation of Microalgae
Current annual global production of microalgae biomass was estimated as 15,000 t [
91
]; every
year, almost 1000 t of produced biomass is being used to grow mollusks, shrimp and other fishes [
92
].
Live microalgae feed is preferable for certain types of fishes and aquatic invertebrates. Whole
microalgae biomass or even metabolites extracted from microalgal are being successfully studied
as feed ingredients for fish, cattle, and poultry. The major challenge in the production of large-scale
microalgal biomass as feed is the production cost. Microalgae can be grown in photobioreactors (PBR)
or open raceway ponds (ORP). Although PBRs have more control in the cultivation of the strains,
preventing contamination and evaporative water loss, construction, operation and maintenance of
the PBRs can be very energy and cost intensive [
91
], especially for bulk feed. On the other hand,
biological contamination, evaporative water loss, relatively lower biomass density are some of the
major challenges for operating ORPs. Fast growing and halophilic microalgae are ideal ORP candidates
to minimize the effect of contamination and evaporation. For a few strains, the growth conditions are
so extreme (low pH, high pH, hypersaline) that other strains cannot contaminate them in large-scale
operations. In order to grow other useful strains, appropriate growth conditions should be developed
that can prevent or minimize contamination from unwanted microalgae and predators.
Only a few microalgal strains have been extensively characterized for their nutritional properties;
however, these strains might require very specific climate conditions. Therefore, more strains need to
be isolated and characterized, especially from the area where microalgal cultivation would take
place. For example, the very high light intensity and extreme temperature in the GCC region
require strains which can flourish in such environments. Researchers have studied the biomass
and lipid productivities of Nannochloris sp., Picochlorum sp., Desmochloris sp., isolated from Red sea,
as feedstock for biofuel [
93
]. Similarly, in Kuwait, there were a few small-scale indoor studies of
Nannochloropsis sp. and Chlorella sp. [
94
,
95
]. Several Dunaliella species can grow in hypersaline
water (as high as 25% salt content) and produce 2–10% of the cell weight as
β
-carotene; several
groups in the region explored the potential of growing Dunaliella strains [
96
,
97
]. Although there
Sustainability 2018,10, 1364 7 of 16
are multiple groups and companies conducting research on microalgae in the GCC region, only a
few groups have demonstrated large-scale outdoor cultivation of selected strains. In Abu Dhabi,
a larger, commercial-scale operation was initiated on a coastal island [
96
] but it has since ceased
operating (Brown, personal observation). The Algal Technology Program (ATP) of Qatar University
has a small-scale (1 hectare in size) research demonstration farm. ATP has isolated and preserved
over 200 strains and microalgae and cyanobacteria from the surrounding environment [
98
]. Eleven
marine cyanobacterial strains from the ATP strain bank were analyzed for paralytic shellfish toxins,
microcystins, nodularins, anatoxins and cylindrospermopsins; none of the cyanobacteria had any of
these toxins (data not published). On the contrary, some of these strains (Synechococcus sp., Leptolyngbya
sp., Chroococcidiopsis sp.) produce high-value pigments like phycobiliproteins and carotenes that
could improve feed quality. Some of the promising strains (e.g., Nannochloropsis sp., Tetraselmis sp.,
Chroococcidiopsis sp., Synechococcus sp., Chlorella sp., Scenedesmus sp.) were successfully grown in the
desert at a scale 200 L–100,000 L [85,86,99,100].
Typical depth of microalgae culture in ORP’s can be in the range of 20–30 cm; the daily evaporative
water loss can be 0.1–2.0 cm, depending on the climate condition. To maintain the culture volume
and water salinity, addition of freshwater was practiced for outdoor cultivation of most of the
marine microalgae—however, TSE or other brackish water can be added to ensure sustainability
in freshwater-scarce regions. Some potential halophilic microalgae (e.g., Tetraselmis sp., Dunaliella sp.)
have the ability to adapt to incremental salinity in culture and therefore the evaporative water loss
can be balanced by adding seawater [
85
,
101
,
102
]. Coastal areas are an ideal place for the cultivation of
microalgae as the collection and pumping of seawater would require minimal energy. In the case of
using brackish groundwater, the cultivation site should be selected such that the elevation difference
between the water source and the ORP is minimized.
About half of the microalgae biomass is comprised of carbon and it was estimated that 1.73 kg of
carbon dioxide is required to produce 1 kg of biomass [
103
]. The solubility of atmospheric CO
2
in water
is very low, which is inefficient to produce sufficient dense culture. Hence, an adequate amount of CO
2
must be supplied to the culture; the rate of CO
2
supply should match the growth rate of the biomass.
CO
2
uptake rate will vary among microalgae strains; however, to reduce the cost of CO
2
utilization,
efficiency should be increased. Although purified bottled CO
2
is commonly used in research and
commercial microalgae production, to reduce the production cost, flue gas from the power plants
could be utilized. Therefore, large-scale microalgal cultivation sites could be co-located with a power
plant or any other industry that generates an adequate amount of flue gas. In addition to carbon,
nitrogen needs to be supplied in a useful form. Urea and other ammonium salts are commonly used
as sources of nitrogen fertilizer. However, the waste from livestock, poultry and fishery processing
industries can be processed and recycled as sources of nitrogen.
The cell size (2–20
µ
m) and dilute concentration of microalgae in the culture (0.5 g/L), makes
biomass harvesting an energy-intensive process, which could contribute to as much as 40% of the
biomass production costs. Sedimentation, filtration, and centrifugation are some of the conventional
microalgal harvesting techniques. Coagulation-flocculation could also be used to harvest some
microalgae. Bio-based coagulants (e.g., chitosan, poly
γ
-glutamic acid and rice starch) have been found
effective in harvesting freshwater microalgae [
104
–
106
]. Since the marine microalgae cultures usually
have much higher ionic strength compared to that of freshwater cultures, these organic coagulants are
often less effective for harvesting marine microalgae; polyvalent metal coagulants (e.g., alum, ferric
chloride) are often used to harvest marine microalgae. Presence of higher concentration of metals in the
harvested biomass is not desirable [
107
,
108
]; very recently, it was shown that dilute acidic water could
be used to recover the iron from the ferric-chloride coagulated harvested Chlorella sp. biomass [
100
].
There were a few attempts to bioflocculate the desired microalgae with other microalgae [
109
] and
yeast [
110
] in small-scale studies; despite the efficient harvesting, this method requires a large amount
of bioflocculating microorganisms that could affect the harvested biomass quality. Whereas the
sedimentation process requires less energy, the centrifugation process consumes the most energy.
Sustainability 2018,10, 1364 8 of 16
However, only a few large cell size and colony forming microalgae undergo gravity sedimentation [
86
].
Microalgae are efficient in terms of nutrient utilization. However, after removal of the biomass, the
harvested water often contains residual nutrients, which need to be recycled to improve the process
economics and to prevent pollution. Usually, for large-scale biomass harvesting, two different methods
are combined. In the first set, the biomass is separated from the bulk of the water using an appropriate
method—the solid content in the harvested biomass slurry can be in the range of 1–2%. Next, the
biomass slurry is further dewatered to 10–30% solid content by adopting different techniques, based
on the final use. Since the biomass still has a great deal of water, it is important to preserve the biomass
soon after the harvesting process. Spray drying, although very energy intensive, is commonly used to
dry the biomass.
7. Marine Aquaculture
In addition to microalgae production, an obvious use of the seawater resource is to use it produce
high value products such as finfish, shellfish or crustaceans such as shrimp. As many scientists have
noted, overfishing of wild fish stocks is not sustainable and leads to ecological collapse (e.g., [
111
]).
Marine aquaculture, if conducted in a sustainable fashion, offers a path for food production in the Gulf
that can potentially ameliorate overfishing of wild stocks.
Given that revenues from petroleum resources are declining, combined with the reduced harvest
of wild fish, many of the Gulf countries have invested or are planning to invest in aquaculture. Oman
is currently considering investing in 24 aquaculture projects with a value of over 2 billion USD ([
112
].
Similarly, Saudi Arabia has developed many hectares of aquaculture ponds on its Red Sea coast and
Qatar has requested tenders for companies to operate aquaculture facilities [113].
In addition to fish and shrimp, consideration could also be given to lower value species such
as seaweeds (macroalgae). Seaweeds can be used for human food and also for industrial purposes
such as for the production of hydrocolloids such as carrageenans, agar and alginates. Plus they have
they the added value of being able to uptake large amounts of nutrients, thus, cleaning the water and
reducing eutrophication [114].
There are many challenges for the aquaculture industry in the Gulf. Firstly, if there is a desire to
develop local capacity and expertise (as opposed to using skilled expatriate labor), then there will be a
need to develop specially trained technical staff, with specialized knowledge across many disciplines.
It has been observed that a successful aquaculture team should have mechanical and electronic skills,
a strong working knowledge of water chemistry, fish nutrition and health management and that one
of the most critical components of establishing a successful aquaculture operation is building a team
capable of managing across this wide range of disciplines [
115
]. Additionally, to increase sustainability,
the industry should strive to develop local fish feeds that utilize local ingredients where practicable.
Care should also to taken to avoid overcapitalization/overdevelopment of the sector. Diseases are
always a challenge for aquaculture operations.
The high temperatures and salinity of the Gulf can make it challenging to grow many species—the
growth rates of most species will suffer in the hot summer temperatures. Selecting and improving
locally-adapted species to culture will likely be more prudent than importing and growing non-native
species. Lastly, over time, as the Gulf gradually becomes hotter and more saline due to climate change
and due to the increase in desalination operations, it may ultimately not be feasible to raise fish in the
Gulf in the more distant future.
8. Integrated Seawater Agriculture
Another potential way forward is to combine or integrate the terrestrial high salinity agriculture
with an aquaculture operation for fish or shrimp and even microalgae. In such a system, seawater
(saline groundwater could also be used) can be pumped to ponds on land where fish and/shrimp can
be grown. The wastewater which leaves the ponds, which is enriched in nutrients such as nitrogen and
phosphorus, can be used to irrigate terrestrial halophytes. Water that then drains from the halophytes
Sustainability 2018,10, 1364 9 of 16
fields can then be polished by mangroves in a mangrove wetland or excess water could drain into a
pond for microalgae production. Salinity of the water will increase as it moves through the system due
to evaporation and transpiration from the plants. Typically, the halophytes will need to be irrigated in
excess of their evapotranspiration requirements to provide a leaching fraction to leach salts below the
plant root zone. A study of seawater irrigation of Salicornia bigelovii in a coastal desert found that the
leaching fraction was 0.35, or about 35% of the total seawater applied at the surface leached below the
plant root zone. The salinity of the leachate water increased to over 100 g/L by the end of the growing
season, indicating that additional seawater or other water, e.g. TSE, might need to be added to the
water draining from the halophytes if it was to be used subsequently for microalgae production or if it
was to be recirculated.
The advantages of such a system is that the water only needs to be pumped once from the sea and
the aquaculture wastewater is utilized as a fertilizer for the halophytes or microalgae. The aquaculture
products would provide most of the income from such a farm and the halophyte biomass could
be used as a biofuel feedstock. A recent study showed that for a theoretical integrated seawater
agriculture system located in the Gulf, where the halophyte biomass was used to produce aviation
biofuel, that such a system would generate 38 to 68% less greenhouse gases than conventional fossil jet
fuel production and would yield an overall positive net energy balance [116].
Several such systems have been built, most notably in Eritrea and in Mexico. Although these
systems may have functioned from a technical perspective, they were not successful business efforts.
A comprehensive study of these efforts noted that these projects failed due to “political instability,
mismanagement and community opposition” [117]. Developers of future projects in this area should
therefore pay greater attention to the socio-economic aspects of such projects at the planning stages.
9. Discussion of Challenges with Scaling up
The willingness to accept the use of marginal water for food production on a wide scale depends on
the maturity of technologies to deliver suitable, high quality crops. At the same time, the presented food
production alternatives are at different levels of development and commercial readiness. The use of TSE
for conventional crops is the most advanced and viable option in the short run. (Although mariculture
is also an advanced food production technology in many regions, it can also entail significant economic
investment and is frequently fraught with significant financial risk). The wastewater treatment rate
in the GCC varies across countries from 41% in Oman to 75% in Kuwait, while the mean reuse rate
does not exceed 30% due to fluctuations in water quality and the lack of distribution networks [
8
].
Expanding TSE reuse across the GCC is expected to increase and thus contribute to decreasing the
reliance of groundwater use for agriculture. TSE can supply up to 10% of water demands in the
region by the year 2020, if the current plans are realized and obstacles such as farmers’ acceptance and
adequate distribution networks are solved [118].
Similarly, using saline water for agriculture is an untapped resource that can help save vulnerable
freshwater resources. This option is still not explored on a large scale in the region. Instead, the use
of saline water for irrigation is sometimes seen as unsustainable as policymakers believe that it will
salinize soils or aquifers. However, the suggestion here is to conduct saline agriculture only in areas
with existing saline soils or aquifers, not in areas with high quality arable land. Nevertheless, the
salinity of water and soil should be monitored in all areas to ensure productivity of agricultural lands
in the future [
3
,
119
]. Therefore, for policymakers in the region, saline agriculture is yet to become
accepted as a viable opportunity to produce animal feed or other crops.
As for microalgae, it might require special funds to move to advance its commercialization. Over
the last few years, the cultivation of microalgae has been going through the transition from research and
pilot-scale demonstration to full-scale commercial deployment. The fundamental aspects of large-scale
microalgae cultivation are very similar to that of existing aquaculture and even agriculture. However,
until now, microalgal cultivation neither falls under agriculture nor receives any benefits which are
often given in agriculture. Consideration might be given to providing support to the microalgae
Sustainability 2018,10, 1364 10 of 16
industry from either government or the private sector for continued research and development and
subsequent commercialization.
There are key socio-economic challenges that can hinder the use of marginal water on a wide
scale. First, the awareness and the availability of agricultural services trained on alternative production
systems are necessary to promote marginal water use. Second, setting the right water pricing policies is
crucial to encourage the use of marginal water. In fact, the overconsumption of water and the overuse
of non-renewable freshwater resources in the region is associated with the high subsidies for water
and energy services. Water and energy production systems are highly interlinked in the GCC. High
amounts of cheap energy are used to desalinate water, which is then provided at subsidized prices and
in some countries free of charge for national residents and also used in agriculture [
120
,
121
] Although
GCC countries have moved to gradually reduce subsidies, the lack of universal tariffs on water use
and wastewater treatment is one of the key constrains to water reuse policies [
8
]. At the same time,
energy subsidies account for over 8.5% of the GDP and 22% of public spending in the GCC region [
122
].
Reducing these subsidies can free up resources that can be invested in promoting alternative food
production systems such as saline agriculture or the cultivation of microalgae.
Third, alternative production systems using marginal water need to be incorporated in clear
national strategies for enhancing food and water security. Until now, the majority of options
to reduce freshwater use in food production do not focus on marginal water. These options
include improving irrigation technologies, increased land investments abroad, improving agricultural
productivity, reducing food waste and exploring alternative food production systems such as vertical
farming [
123
]. Moreover, desalinated water is used for irrigation in many GCC countries and this
option might increase if renewable energies contribute to reducing the high energy costs associated
with desalination [124].
Concerning national food strategies and policies, the majority of the GCC countries lack
comprehensive food security strategies with high-level endorsement and commitment. In 2008,
Qatar initiated a National Food Security Program (QNFSP), which established a master plan to
diversify food imports, increase aquaculture and develop integrated systems at the farm level with
water reuse schemes. Although this policy represents the most comprehensive set of soft (awareness,
education, research) and hard (infrastructure and investments) measures, there is no evidence that its
implementation was endorsed by all stakeholders and it is not clear whether it was put into action.
In 2015, the UAE, in cooperation with the Food and Agriculture Organization (FAO) developed a
National Policy for Food and Agriculture, which was endorsed in 2016 by the Climate Change and
Environment Ministry. This policy foresees, among others, market-driven reforms and investments in
marine aquaculture. Aquaculture is also being promoted in other GCC countries such as Saudi Arabia,
which regards this sector as one of the most promising options for food production under the Saudi
Vision 2030.
10. Conclusions
Here we show that marginal water sources such as TSE, produced water, saline ground water
and seawater can be used to produce a variety of useful crops. Utilization of such marginal water
sources can potentially spare scarce freshwater resources. There is a significant potential for utilizing
such marginal water in the GCC region. This potential is currently not fully exploited despite
important advancements in research on use requirements and sectors. Further research should
focus on the economic feasibility of some of these technologies in the GCC. If the economics are
favorable, then these technologies should be able to provide economic diversification in the GCC
countries, which are trying to increase economic activity in the non-petroleum sectors. The adequate
commercial scale of technologies using marginal water needs further research. Moreover, reforming the
subsidization of freshwater, especially for agriculture uses, can encourage the utilization of marginal
water. Additionally, these technologies could aid in increasing domestic food production, which is
a stated strategic goal of many of the GCC nations. In fact, the GCC region is highly dependent on
Sustainability 2018,10, 1364 11 of 16
global food markets despite many GCC countries using more than the global average of water for
domestic agriculture. Advanced marginal water technologies can help reduce both freshwater use
for agriculture and the dependence on food imports. For this, they need to be integrated in national
strategic plans for food security. Such plans can develop clear targets and use incentives and public
investments in order to promote the use of such technologies based on the individual commercial
readiness of each of the technologies.
Author Contributions: J.J.B., P.D. and M.A.-S. wrote the article and contributed equally.
Conflicts of Interest: The authors declare no conflict of interest.
References
1.
Kotilaine, J.T. GCC Agriculture. Available online: https://www.gulfbase.com/ScheduleReports/GCC_
Agriculture_Sector_March2010.pdf (accessed on 17 April 2018).
2.
Saif, O.; Mezher, T.; Arafat, H.A. Water security in the GCC countries: Challenges and opportunities.
J. Environ. Stud. Sci. 2014,4, 329–346. [CrossRef]
3.
Shahid, S.A.; Ahmed, M. Changing face of agriculture in the Gulf Cooperation Council countries.
In Environmental Cost and Face of Agriculture in the Gulf Cooperation Council Countries—Fostering Agriculture in
the Context of Climate Change; Shahid, S.A., Ahmed, M., Eds.; Springer: Berlin, Germany, 2014; pp. 1–25.
4.
Alnaser, W.E.; Alnaser, N.W. The status of renewable energy in the GCC countries. Renew. Sustain. Energy Rev.
2011,15, 3074–3098. [CrossRef]
5.
Pirani, S.I.; Arafat, H.A. Interplay of food security, agriculture and tourism within GCC countries. Glob. Food Secur.
2016,9, 1–9. [CrossRef]
6.
Schlumberger Water Services. Study and Developing the Natural and Artificial Recharge of Groundwater Aquifer
in the State of Qatar; Qatar Ministry of Environment: Doha, Qatar, 2009.
7.
Bank, T.W. Improving Wastewater Use in Agriculture: An Emerging Priority; The World Bank: Washington, DC,
USA, 2010; p. 190.
8.
Aleisa, E.; Al-Zubari, W. Wastewater reuse in the countries of the Gulf Cooperation Council (GCC): The lost
opportunity. Environ. Monit. Assess. 2017,189, 553. [CrossRef] [PubMed]
9.
Darwish, M.; Abdulrahim, H.; Mabrouk, A.N.; Hassan, A.; Shomar, B. Reclaimed wastewater for agriculture
irrigation in Qatar. Glob. J. Agric. Res. Rev. 2014,31, 106–120.
10.
Jasim, S.Y.; Saththasivam, J.; Loganathan, K.; Ogunbiyi, O.O.; Sarp, S. Reuse of Treated Sewage Effluent (TSE)
in Qatar. J. Water Process Eng. 2016,11, 174–182. [CrossRef]
11.
Hong, P.-Y.; Al-Jassim, N.; Ansari, M.I.; Mackie, R.I. Environmental and Public Health Implications of Water
Reuse: Antibiotics, Antibiotic Resistant Bacteria, and Antibiotic Resistance Genes. Antibiotics
2013
,2, 367–399.
[CrossRef] [PubMed]
12.
Ouda, O.K.M. Treated wastewater use in Saudi Arabia: Challenges and initiatives. Int. J. Water Resour. Dev.
2016,32, 799–809. [CrossRef]
13.
Elgallal, M.; Fletcher, L.; Evans, B. Assessment of potential risks associated with chemicals in wastewater
used for irrigation in arid and semiarid zones: A review. Agric. Water Manag.
2016
,177, 419–431. [CrossRef]
14.
Mohammad Rusan, M.J.; Hinnawi, S.; Rousan, L. Long term effect of wastewater irrigation of forage crops
on soil and plant quality parameters. Desalination 2007,215, 143–152. [CrossRef]
15.
Da Fonseca, A.F.; Herpin, U.; de Paula, A.M.; Victória, R.L.; Melfi, A.J. Agricultural use of treated sewage
effluents: Agronomic and environmental implications and perspectives for Brazil. Sci. Agricola
2007
,64,
194–209. [CrossRef]
16.
Al Omron, A.M.; El-Maghraby, S.E.; Nadeem, M.E.A.; El-Eter, A.M.; Al-Mohani, H. Long term effect of
irrigation with the treated sewage effluent on some soil properties of Al-Hassa Governorate, Saudi Arabia.
J. Saudi Soc. Agric. Sci. 2012,11, 15–18. [CrossRef]
17.
Balkhair, K.S.; Ashraf, M.A. Field accumulation risks of heavy metals in soil and vegetable crop irrigated
with sewage water in western region of Saudi Arabia. Saudi J. Biol. Sci.
2016
,23, S32–S44. [CrossRef]
[PubMed]
Sustainability 2018,10, 1364 12 of 16
18.
El-Zohri, M.; Hifney, A.; Ramadan, T.; Abdel-Basset, R. Use of Sewage in Agriculture and Related Activities.
In Handbook of Plant and Crop Physiology, 3rd ed.; CRC Press: Boca Raton, FL, USA, 2014; pp. 931–966,
ISBN 978-1-4665-5328-6.
19.
Hussain, G.; Al-Saati, A.J. Wastewater quality and its reuse in agriculture in Saudi Arabia. Desalination
1999
,
123, 241–251. [CrossRef]
20.
Dorta-Santos, M.; Tejedor, M.; Jiménez, C.; Hernández-Moreno, J.M.; Díaz, F.J. “Using marginal quality water
for an energy crop in arid regions: Effect of salinity and boron distribution patterns”. Agric. Water Manag.
2016,171, 142–152. [CrossRef]
21.
Neff, J.; Lee, K.; DeBlois, E.M. Produced Water: Overview of Composition, Fates, and Effects. In Produced
Water; Springer: New York, NY, US, 2011; pp. 3–54, ISBN 9781461400455.
22.
Duraisamy, R.T.; Beni, A.H.; Henni, A. State of the Art Treatment of Produced Water. In Water Treatment;
Elshorbagy, W., Chowdhury, R.K., Eds.; InTech: Rijeka, Croatia, 2013.
23.
Janson, A.; Katebah, M.; Santos, A.; Minier-Matar, J.; Hussain, A.; Adham, S.; Judd, S. Assessing the
biotreatability of produced water from a Qatari gas field. SPE J. 2015,20, 1113–1119. [CrossRef]
24.
Alfarhan, A.A.; Duane, M.J. Geochemistry and modification of oilfield brines in surface pits in Northern
Kuwait. Arab. J. Geosci. 2012,5, 1055–1068. [CrossRef]
25.
Frequently Asked Question about Recycled Oilfield Water for Crop Irrigation. Available
online: https://www.waterboards.ca.gov/publications_forms/publications/factsheets/docs/prod_water_
for_crop_irrigation.pdf (accessed on 17 April 2018).
26. Shannon, M.C.; Grieve, C.M. Tolerance of vegetable crops to salinity. Sci. Hortic. 1998,78, 5–38. [CrossRef]
27.
Bandaranayake, W.M. Traditional and medicinal uses of mangroves. Mangroves Salt Marshes
1998
,2, 133–148.
[CrossRef]
28.
Ventura, Y.; Sagi, M. Halophyte crop cultivation: The case for salicornia and sarcocornia. Environ. Exp. Bot.
2013,92, 144–153. [CrossRef]
29.
Ventura, Y.; Myrzabayeva, M.; Alikulov, Z.; Cohen, S.; Shemer, Z.; Sagi, M. The importance of iron supply
during repetitive harvesting of Aster tripolium. Funct. Plant Biol. 2013,40, 968–976. [CrossRef]
30.
Glenn, E.P.; O’Leary, J.W.; Watson, M.C.; Thompson, T.L.; Kuehl, R.O. Salicornia bigelovii Torr.: An Oilseed
Halophyte for Seawater Irrigation. Science 1991,251, 1065–1067. [CrossRef] [PubMed]
31.
Glenn, E.P.; Anday, T.; Chaturvedi, R.; Martinez-Garcia, R.; Pearlstein, S.; Soliz, D.; Nelson, S.G.; Felger, R.S.
Three halophytes for saline-water agriculture: An oilseed, a forage and a grain crop. Environ. Exp. Bot.
2013
,
92, 110–121. [CrossRef]
32.
Weber, D.J.; Ansari, R.; Gul, B.; Ajmal Khan, M. Potential of halophytes as source of edible oil. J. Arid Environ.
2007,68, 315–321. [CrossRef]
33.
Xi, J.; Zhang, F.; Mao, D.; Yan, P. The utilization of halophytes for traditional medicine in Xin jiango Title.
Rev. China Agric. Sci. Technol. 2003,5, 43–48.
34.
Qasim, M.; Gulzar, S.; Shinwari, Z.K.; Aziz, I.; Ajmal Khan, M. Traditional ethnobotanical uses of halophytes
from Hub, Balochistan. Pak. J. Bot. 2010,42, 1543–1551.
35.
Swingle, R.S.; Glenn, E.P.; Squires, V. Growth performance of lambs fed mixed diets containing halophyte
ingredients. Anim. Feed Sci. Technol. 1996,63, 137–148. [CrossRef]
36.
Masters, D.G.; Benes, S.E.; Norman, H.C. Biosaline agriculture for forage and livestock production.
Agric. Ecosyst. Environ. 2007,119, 234–248. [CrossRef]
37.
El Shaer, H.M. Halophytes and salt-tolerant plants as potential forage for ruminants in the Near East region.
Small Rumin. Res. 2010,91, 3–12. [CrossRef]
38.
Manousaki, E.; Kalogerakis, N. Halophytes present new opportunities in phytoremediation of heavy metals
and saline soils. Ind. Eng. Chem. Res. 2011,50, 656–660. [CrossRef]
39.
Rabhi, M.; Ferchichi, S.; Jouini, J.; Hamrouni, M.H.; Koyro, H.W.; Ranieri, A.; Abdelly, C.; Smaoui, A.
Phytodesalination of a salt-affected soil with the halophyte Sesuvium portulacastrum L. to arrange in advance
the requirements for the successful growth of a glycophytic crop. Bioresour. Technol.
2010
,101, 6822–6828.
[CrossRef] [PubMed]
40.
Abideen, Z.; Ansari, R.; Khan, M.A. Halophytes: Potential source of ligno-cellulosic biomass for ethanol
production. Biomass Bioenergy 2011,35, 1818–1822. [CrossRef]
41.
Moser, B.R.; Dien, B.S.; Seliskar, D.M.; Gallagher, J.L. Seashore mallow (Kosteletzkya pentacarpos) as a
salt-tolerant feedstock for production of biodiesel and ethanol. Renew. Energy
2013
,50, 833–839. [CrossRef]
Sustainability 2018,10, 1364 13 of 16
42.
Debez, A.; Belghith, I.; Friesen, J.; Montzka, C.; Elleuche, S. Facing the challenge of sustainable bioenergy
production: Could halophytes be part of the solution? J. Biol. Eng. 2017,11, 27. [CrossRef] [PubMed]
43.
Bañuelos, J.A.; Velázquez-Hernández, I.; Guerra-Balcázar, M.; Arjona, N. Production, characterization and
evaluation of the energetic capability of bioethanol from Salicornia Bigelovii as a renewable energy source.
Renew. Energy 2018,123, 125–134. [CrossRef]
44.
Brown, J.J.; Glenn, E.P. Reuse of highly saline aquaculture effluent to irrigate a potential forage halophyte,
Suaeda esteroa. Aquac. Eng. 1999,20, 91–111. [CrossRef]
45.
Shpigel, M.; Ben-Ezra, D.; Shauli, L.; Sagi, M.; Ventura, Y.; Samocha, T.; Lee, J.J. Constructed wetland with
Salicornia as a biofilter for mariculture effluents. Aquaculture 2013,412–413, 52–63. [CrossRef]
46.
Ali, A.; Iqbal, N.; Ali, F.; Afzal, B. Alternanthera bettzickiana (Regel) G. Nicholson, a potential halophytic
ornamental plant: Growth and physiological adaptations. Flora Morphol. Distrib. Funct. Ecol. Plants
2012
,
207, 318–321. [CrossRef]
47.
Cybulska, I.; Brudecki, G.; Alassali, A.; Thomsen, M.; Jed Brown, J. Phytochemical composition of some
common coastal halophytes of the United Arab Emirates. Emir. J. Food Agric.
2014
,26, 1046–1056. [CrossRef]
48.
Farms Stop Cultivating Rhodes Grass. Gulf News, 23 March 2012. Available online: https://gulfnews.com/
news/uae/environment/farms-stop-cultivating-rhodes-grass-1.998624 (accessed on 24 April 2018).
49.
Pearce, K.L.; Norman, H.C.; Wilmot, M.; Rintoul, A.; Pethick, D.W.; Masters, D.G. The effect of grazing
saltbush with a barley supplement on the carcass and eating quality of sheepmeat. Meat Sci.
2008
,79,
344–354. [CrossRef] [PubMed]
50.
Pearce, K.L.; Masters, D.G.; Smith, G.M.; Jacob, R.H.; Pethick, D.W. Plasma and tissue
α
-tocopherol
concentrations and meat colour stability in sheep grazing saltbush (Atriplex spp.). Aust. J. Agric. Res.
2005,56, 663–672. [CrossRef]
51.
Pasternak, D.; Nerd, A.; De Malach, Y. Irrigation with brackish water under desert conditions IX. The salt
tolerance of six forage crops. Agric. Water Manag. 1993,24, 321–334. [CrossRef]
52.
Khan, M.A.; Ansari, R.; Ali, H.; Gul, B.; Nielsen, B.L. Panicum turgidum, a potentially sustainable cattle feed
alternative to maize for saline areas. Agric. Ecosyst. Environ. 2009,129, 542–546. [CrossRef]
53.
Al-Dakheel, A.; Al-Hadrami, G.; Al-Shorabi, S.; AbuRumman, G. Optimizing management practices
for maximum production for two salt-tolerant grasses: Sporobolus virginicus and Distichlis spicata.
In Proceedings of the 7th Annual UAE University Research Conference, Dubai, UAE, 22–24 April 2006.
54.
Al-Dakheel, A.; Al-Hadrami, G.; Saleh Al-Shoraby, G.S.; Shabbir, G. The potential of salt-tolerant plants and
marginal resources in developing an integrated forage-livestock production system. In Salinity, Water and
Society—Global Issues, Local Action, Proceedings of the 2nd International Salinity Forum, Adelaide, Australia, 31
March–3 April 2008; Libraries Australia: Canberra, Australia, 2008; Volume 31, p. 192.
55.
Suyama, H.; Benes, S.E.; Robinson, P.H.; Getachew, G.; Grattan, S.R.; Grieve, C.M. Biomass yield and
nutritional quality of forage species under long-term irrigation with saline-sodic drainage water: Field
evaluation. Anim. Feed Sci. Technol. 2007,135, 329–345. [CrossRef]
56.
Al-Shorepy, S.; Alhadrami, G.; Ayoub, M.; Dakheel, A. Growth performance and body composition of
indigenous goats fed Distichlis hay. In Proceedings of the 5th Annual UAE University Research Conference,
Al-Ain, UAE, 25–27 April 2004.
57.
Al-Shorepy, S.; Alhadrami, G.; Dakheel, A. Effect of feeding Sporobolus grass hay on growth performance
and slaughtering characteristics of fattening indigenous lambs. In Proceedings of the 6th Annual UAE
University Research Conference, Al-Ain, UAE, 24–26 April 2005.
58.
Alhadrami, G.; Al-Shorepy, S.; Dakheel, A. Effect of feeding long term Sporobolus grass hay on growth
performance of Awassi sheep. In Proceedings of the 6th Annual UAE University Research Conference,
Al-Ain, UAE, 24–26 April 2005.
59.
Sarwar, M.; Mahr-un-Nisa; Ajmal Khan, M.; Mushtaque, M. Chemical composition, herbage yield and
nutritive value of Panicum antidotale and Pennisetum orientale for Nili buffaloes at different clipping
intervals. Asian-Australas. J. Anim. Sci. 2006,19, 176–180. [CrossRef]
60.
Norman, H.C.; Masters, D.G.; Wilmot, M.G.; Rintoul, A.J. Effect of supplementation with grain, hay or straw
on the performance of weaner Merino sheep grazing old man (Atriplex nummularia) or river (Atriplex amnicola)
saltbush. Grass Forage Sci. 2008,63, 179–192. [CrossRef]
61.
Masters, D.G.; Rintoul, A.J.; Dynes, R.A.; Pearce, K.L.; Norman, H.C. Feed intake and production in sheep
fed diets high in sodium and potassium. Aust. J. Agric. Res. 2005,56, 427–434. [CrossRef]
Sustainability 2018,10, 1364 14 of 16
62.
Pearce, K.L.; Masters, D.G.; Jacob, R.H.; Hopkins, D.L.; Pethick, D.W. Effects of sodium chloride and betaine
on hydration status of lambs at slaughter. Aust. J. Exp. Agric. 2008,48, 1194–1200. [CrossRef]
63.
Pearce, K.L.; Pethick, D.W.; Masters, D.G. The effect of ingesting a saltbush and barley ration on the carcass
and eating quality of sheepmeat. Animal 2008,2, 479–490. [CrossRef] [PubMed]
64.
Masters, D.; Tiong, M.; Vercoe, P.; Norman, H. The nutritive value of river saltbush (Atriplex amnicola) when
grown in different concentrations of sodium chloride irrigation solution. Small Rumin. Res.
2010
,91, 56–62.
[CrossRef]
65.
Masters, D.G.; Norman, H.C. 15—Genetic and Environmental Management of Halophytes for Improved
Livestock Production. In Halophytes for Food Security in Dry Lands; Khan, M.A., Ozturk, M., Gul, B.,
Ahmed, M.Z., Eds.; Academic Press: San Diego, CA, USA, 2016; pp. 243–257, ISBN 978-0-12-801854-5.
66.
Edgerton, M.D. Increasing Crop Productivity to Meet Global Needs for Feed, Food, and Fuel. Plant Physiol.
2009,149, 7–13. [CrossRef] [PubMed]
67.
Masuda, T.; Goldsmith, P.D. World soybean production: Area harvested, yield, and long-term projections.
Int. Food Agribus. Manag. Rev. 2009,12, 143–162. [CrossRef]
68.
Enghiad, A.; Ufer, D.; Countryman, A.M.; Thilmany, D.D. An Overview of Global Wheat Market
Fundamentals in an Era of Climate Concerns. Int. J. Agron. 2017,2017, 1–15. [CrossRef]
69.
Sukenik, A. Production of eicosapentaenoic acid by the marine eustigmatophyte Nannochloropsis.
In Chemicals from Microalgae; Taylor & Francis: London, UK, 1999; pp. 41–56, ISBN 0748405151.
70.
Corder, R.E.; Hill, A.M.; Lindsey, H.; Lowenstein, M.; McIntosh, R.P. SERI Biomass Program FY, 1983 Annual
Report; Solar Energy Research Institute: Golden, CO, USA, 1984.
71. Arad, A. A Development of Outdoor Raceway Capable of Yielding Oil-Rich Halotolerant Microalgae; Solar Energy
Research Institute: Golden, CO, USA, 1984.
72.
Slegers, P.M.; Lösing, M.B.; Wijffels, R.H.; van Straten, G.; van Boxtel, A.J.B. Scenario evaluation of open
pond microalgae production. Algal Res. 2013,2, 358–368. [CrossRef]
73.
Volesky, B.; Holan, Z.R. Biosorption of heavy metals. Biotechnol. Prog.
1995
,11, 235–250. [CrossRef] [PubMed]
74.
Mehta, S.K.; Gaur, J.P. Use of Algae for Removing Heavy Metal Ions From Wastewater: Progress and
Prospects. Crit. Rev. Biotechnol. 2005,25, 113–152. [CrossRef] [PubMed]
75.
Dunstan, W.M.; Menzel, D.W. Continuous Cultures of Natural Populations of Phytoplankton in Dilute,
Treated Sewage Effluent1. Limnol. Oceanogr. 1971,16, 623–632. [CrossRef]
76.
Becker, W. Microalgae in Human and Animal Nutrition. In Handbook of Microalgae Culture; Blackwell Science:
Oxford, UK, 2004; pp. 312–351.
77. Goldberg, I. Single Cell Protein; Springer: Berlin, Germany, 1985.
78.
Naylor, R.L.; Hardy, R.W.; Bureau, D.P.; Chiu, A.; Elliott, M.; Farrell, A.P.; Forster, I.; Gatlin, D.M.; Goldburg, R.J.;
Hua, K.; et al. Feeding aquaculture in an era of finite resources. Proc. Natl. Acad. Sci. USA
2009
,106, 15103–15110.
[CrossRef] [PubMed]
79.
Saavedra, M.; Voltolina, D. The chemical composition of Chaetoceros sp. (Bacillariophyceae) under different
light conditions. Comp. Biochem. Physiol. Part B Comp. Biochem. 1994,107, 39–44. [CrossRef]
80.
Muhaemin, M.; Kaswadji, R.F. Biomass Nutrient Profiles of Marine Microalgae Dunaliella salina.
J. Penelit. Sains 2009,13, 64–67.
81.
Pav, M.; Garc, J.; Martorell, C.; Aroca, S. Direct spectrophotometric method to determine cell density of
Isochrysis galbana in serial batch cultures from a larger scale fed-batch culture in exponential phase. NEREIS
2015,8, 35–43.
82.
Kent, M.; Welladsen, H.M.; Mangott, A.; Li, Y. Nutritional evaluation of Australian microalgae as potential
human health supplements. PLoS ONE 2015,10, e0118985. [CrossRef] [PubMed]
83.
Buono, S.; Colucci, A.; Angelini, A.; Langellotti, A.L.; Massa, M.; Martello, A.; Fogliano, V.; Dibenedetto, A.
Productivity and biochemical composition of Tetradesmus obliquus and Phaeodactylum tricornutum: Effects
of different cultivation approaches. J. Appl. Phycol. 2016,28, 3179–3192. [CrossRef]
84. Becker, E.W. Micro algae as a source of protein. Biotechnol. Adv. 2007,25, 207–210. [CrossRef] [PubMed]
85.
Das, P.; Thaher, M.I.; Hakim, M.A.; Al-Jabri, H.M.; Alghasal, G.S. A comparative study of the growth of
Tetraselmis sp. in large scale fixed depth and decreasing depth raceway ponds. Bioresour. Technol.
2016
,216,
114–120. [CrossRef] [PubMed]
Sustainability 2018,10, 1364 15 of 16
86.
Das, P.; Quadir, M.A.; Chaudhary, A.K.; Thaher, M.I.; Khan, S.; Alghazal, G.; Al-Jabri, H. Outdoor continuous
cultivation of self-settling marine cyanobacterium Chroococcidiopsis sp. Ind. Biotechnol.
2018
,14, 45–53.
[CrossRef]
87.
FAO. Available online: http://www.fao.org/wairdocs/tan/x5926e/x5926e01.htm (accessed on 24 April 2018).
88.
Grieshop, C.M.; Fahey, G.C. Comparison of quality characteristics of soybeans from Brazil, China, and the
United States. J. Agric. Food Chem. 2001,49, 2669–2673. [CrossRef] [PubMed]
89.
Portz, L.; Cyrino, J.E.P. Digestibility of nutrients and amino acids of different protein sources in practical
diets by largemouth bass Micropterus salmoides (Lacepede, 1802). Aquac. Res. 2004,35, 312–320. [CrossRef]
90.
Tibbetts, S.M.; Bjornsson, W.J.; McGinn, P.J. Biochemical composition and amino acid profiles of
Nannochloropsis granulata algal biomass before and after supercritical fluid CO
2
extraction at two processing
temperatures. Anim. Feed Sci. Technol. 2015,204, 62–71. [CrossRef]
91. Benemann, J. Microalgae for Biofuels and Animal Feeds. Energies 2013,6, 5869–5886. [CrossRef]
92.
Hemaiswarya, S.; Raja, R.; Kumar, R.R.; Ganesan, V.; Anbazhagan, C. Microalgae: A sustainable feed source
for aquaculture. World J. Microbiol. Biotechnol. 2011,27, 1737–1746. [CrossRef]
93.
Pereira, H.; Barreira, L.; Custódio, L.; Alrokayan, S.; Mouffouk, F.; Varela, J.; Abu-Salah, K.M.;
Ben-Hamadou, R. Isolation and fatty acid profile of selected microalgae strains from the red sea for biofuel
production. Energies 2013,6, 2773–2783. [CrossRef]
94.
James, C.M.; Al-Khars, A.M. An intensive continuous culture system using tubular photobioreactors for
producing microalgae. Aquaculture 1990,87, 381–393. [CrossRef]
95.
James, C.M.; Al-Hinty, S.; Salman, A.E. Growth and
ω
3 fatty acid and amino acid composition of microalgae
under different temperature regimes. Aquaculture 1989,77, 337–351. [CrossRef]
96.
Abu-rezq, T.S.; Al-hooti, S.; Jacob, D.A. Optimum culture conditions required for the locally isolated
Dunaliella salina.J. Algal Biomass Util. 2010,1, 12–19.
97.
Kitto, M.R.; Reginald, M. Effect of summer/winter light intensity and salt on growth kinetics and beta
carotene accumulation by Dunaliella in open outdoor earthern ponds in a desert island, off UAE coast.
J. Algal Biomass Util. 2011,2, 14–21.
98.
Saadaoui, I.; Al Ghazal, G.; Bounnit, T.; Al Khulaifi, F.; Al Jabri, H.; Potts, M. Evidence of thermo
and halotolerant Nannochloris isolate suitable for biodiesel production in Qatar Culture Collection of
Cyanobacteria and Microalgae. Algal Res. 2016,14, 39–47. [CrossRef]
99.
Das, P.; Thaher, M.I.; Hakim, M.A.; Al-Jabri, H.M. Sustainable production of toxin free marine microalgae
biomass as fish feed in large scale open system in the Qatari desert. Bioresour. Technol.
2015
,192, 97–104.
[CrossRef] [PubMed]
100.
Das, P.; Thaher, M.I.; Abdul Hakim, M.A.; Al-Jabri, H.M.; Alghasal, G.S. Microalgae harvesting by pH
adjusted coagulation-flocculation, recycling of the coagulant and the growth media. Bioresour. Technol.
2016
,
216, 824–829. [CrossRef] [PubMed]
101.
Fon Sing, S.; Isdepsky, A.; Borowitzka, M.A.; Lewis, D.M. Pilot-scale continuous recycling of growth medium
for the mass culture of a halotolerant Tetraselmis sp. in raceway ponds under increasing salinity: A novel
protocol for commercial microalgal biomass production. Bioresour. Technol.
2014
,161, 47–54. [CrossRef]
[PubMed]
102.
Horiuchi, J.; Ohba, I.; Tada, K.; Kobayashi, M.; Kanno, T.; Kishimoto, M. Effective Cell Harvesting of the
Halotolerant Microalga Dunaliella tertiolecta with pH Control. J. Biosci. Bioeng.
2003
,95, 412–415. [CrossRef]
103.
Rogers, J.N.; Rosenberg, J.N.; Guzman, B.J.; Oh, V.H.; Mimbela, L.E.; Ghassemi, A.; Betenbaugh, M.J.;
Oyler, G.A.; Donohue, M.D. A critical analysis of paddlewheel-driven raceway ponds for algal biofuel
production at commercial scales. Algal Res. 2014,4, 76–88. [CrossRef]
104.
Rashid, N.; Rehman, S.U.; Han, J.-I. Rapid harvesting of freshwater microalgae using chitosan.
Process Biochem. 2013,48, 1107–1110. [CrossRef]
105.
Ndikubwimana, T.; Zeng, X.; He, N.; Xiao, Z.; Xie, Y.; Chang, J.S.; Lin, L.; Lu, Y. Microalgae biomass
harvesting by bioflocculation-interpretation by classical DLVO theory. Biochem. Eng. J.
2015
,101, 160–167.
[CrossRef]
106.
Choy, S.Y.; Prasad, K.M.N.; Wu, T.Y.; Raghunandan, M.E.; Phang, S.-M.; Juan, J.C.; Ramanan, R.N. Separation
of Chlorella biomass from culture medium by flocculation with rice starch. Algal Res.
2018
,30, 162–172.
[CrossRef]
Sustainability 2018,10, 1364 16 of 16
107.
Knuckey, R.M.; Brown, M.R.; Robert, R.; Frampton, D.M.F. Production of microalgal concentrates by
flocculation and their assessment as aquaculture feeds. Aquac. Eng. 2006,35, 300–313. [CrossRef]
108.
Rwehumbiza, V.M.; Harrison, R.; Thomsen, L. Alum-induced flocculation of preconcentrated
Nannochloropsis salina: Residual aluminium in the biomass, FAMEs and its effects on microalgae growth
upon media recycling. Chem. Eng. J. 2012,200–202, 168–175. [CrossRef]
109.
Salim, S.; Bosma, R.; Vermuë, M.H.; Wijffels, R.H. Harvesting of microalgae by bio-flocculation.
J. Appl. Phycol.
2010,23, 849–855. [CrossRef] [PubMed]
110.
Talukder, M.M.R.; Das, P.; Wu, J.C. Immobilization of microalgae on exogenous fungal mycelium:
A promising separation method to harvest both marine and freshwater microalgae. Biochem. Eng. J.
2014,91, 53–57. [CrossRef]
111.
Worm, B.; Barbier, E.B.; Beaumont, N.; Duffy, J.E.; Folke, C.; Halpern, B.S.; Jackson, J.B.C.; Lotze, H.K.;
Micheli, F.; Palumbi, S.R.; et al. Impacts of biodiversity loss on ocean ecosystem services. Science
2006
,314,
787–790. [CrossRef] [PubMed]
112.
MOAF Considering 24 Aquaculture Projects Worth RO 853 Million. 20 May 2017. Available
online: http://www.muscatdaily.com/Archive/Oman/MoAF-considering-24-aquaculture-projects-worth-
RO853mn-50x1 (accessed on 24 April 2018).
113.
Ataullah, S. Plan to Set up Floating Fish Farms in Sea. The Penninsula, 13 February 2017. Available
online: https://www.thepeninsulaqatar.com/article/13/02/2017/Plan-to-set-up-floating-fish- farms-in-sea
(accessed on 24 April 2018).
114.
Xiao, X.; Agusti, S.; Lin, F.; Li, K.; Pan, Y.; Yu, Y.; Zheng, Y.; Wu, J.; Duarte, C.M. Nutrient removal from
Chinese coastal waters by large-scale seaweed aquaculture. Sci. Rep. 2017,7, 46613. [CrossRef] [PubMed]
115.
Goldman, J. So You Want to Be a Fish Farmer. Available online: https://umaine.edu/cooperative-
aquaculture/wp-content/uploads/sites/75/2015/11/So-You-Want-to-be-a-Fish-Farmer-by-Josh-
Goldman.pdf (accessed on 17 April 2018).
116.
Warshay, B.; Brown, J.J.; Sgouridis, S. Erratum to: Life cycle assessment of integrated seawater agriculture in
the Arabian (Persian) Gulf as a potential food and aviation biofuel resource. Int. J. Life Cycle Assess.
2017
,22,
1033. [CrossRef]
117.
Bailis, R.; Yu, E. Environmental and social implications of integrated seawater agriculture systems producing
Salicornia bigelovii for biofuel. Biofuels 2012,3, 555–574. [CrossRef]
118.
Alkhamisi, S.A.; Ahmed, M. Opportunities and Challenges of Using Treated Wastewater in Agriculture.
In Environmental Cost and Face of Agriculture in the Gulf Cooperation Council Countries: Fostering Agriculture
in the Context of Climate Change; Shahid, S.A., Ahmed, M., Eds.; Springer International Publishing: Cham,
Switzerland, 2014; pp. 109–123, ISBN 978-3-319-05768-2.
119.
Shahid, S.A.; Al-Shankiti, A. Sustainable food production in marginal lands—Case of GDLA member
countries. Int. Soil Water Conserv. Res. 2013,1, 24–38. [CrossRef]
120.
Siddiqi, A.; Anadon, L.D. The water-energy nexus in Middle East and North Africa. Energy Policy
2011
,39,
4529–4540. [CrossRef]
121.
Al Iriani, M.A.; Trabelsi, M. The economic impact of phasing out energy consumption subsidies in GCC
countries. J. Econ. Bus. 2016,87, 35–49. [CrossRef]
122.
Meltzer, J.; Hultman, N.E.; Langley, C. Low-carbon energy transitions in Qatar and the Gulf cooperation
council region. In Brookings Pap. Econ. Act.; Brookings Institution: Washington, DC, USA, 2014.
123.
Elmi, A.A. Food Security in the Arab Gulf Cooperation Council States. In Sustainable Agriculture
Reviews; Lichtfouse, E., Ed.; Springer International Publishing: Cham, Switzerland, 2017; pp. 89–114,
ISBN 978-3-319-58679-3.
124.
Sewilam, H.; Nasr, P. Desalinated Water for Food Production in the Arab Region. In The Water, Energy, and
Food Security Nexus in the Arab Region; Amer, K., Adeel, Z., Böer, B., Saleh, W., Eds.; Springer International
Publishing: Cham, Switzerland, 2017; pp. 59–81, ISBN 978-3-319-48408-2.
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