Walker et al JAE 2014 Atriplex-halimus

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Review

Atriplex halimus L.: Its biology and uses

D.J. Walker a,*, S. Lutts b, M. Sánchez-García c, E. Correal a

a Instituto Murciano de Investigación y Desarrollo Agricola y Alimentario, Calle Mayor s/n, La Alberca, 30150 Murcia, SpainbGroupe de Recherche en Physiologie végétale (GRPV), Earth and Life Institute e Agronomy (ELIA), Université catholique de Louvain, Croix du sud 4-5 bteL7.07.13 à, 1348 Louvain-la-Neuve, BelgiumcCEBAS-CSIC, Campus Universitario de Espinardo, Apartado de Correos 164, 30100 Espinardo, Murcia, Spain

a r t i c l e i n f o

Article history:Received 17 June 2013Received in revised form20 September 2013Accepted 26 September 2013Available online 11 October 2013

Keywords:DroughtFodderHalophytePhytoremediationSalinitySaltbush

a b s t r a c t

Atriplex halimus L. (Amaranthaceae) (Mediterranean saltbush) is a halophytic shrub that is widelydistributed in arid and semi-arid regions around the Mediterranean basin and east to Saudi Arabia, atelevations less than 900 m. It grows on a variety of soils, from fine to coarse texture, with varying degreesof salinity. There are two sub-species of A. halimus: halimus is diploid (2n ¼ 2x ¼ 18) and is found at semi-arid, less-saline sites, while schweinfurthii is tetraploid (2n ¼ 4x ¼ 36) and occupies arid, saline sites.Throughout its distribution, A. halimus is exposed to high light intensity and temperature and varyingdegrees of drought and salinity; it can also withstand sub-zero winter temperatures or soil contami-nation by trace elements. Some of its physiological and biochemical tolerance mechanisms e such asadjustment of plant water relations e are common to all or several of these environmental stresses, butothers are specific to particular stresses. The importance of A. halimus in the functioning of ecosystems isreflected in its promotion of soil biota, while it also acts as a food plant for mammals and arthropods. Itsdeep root system decreases soil erosion in arid zones, due to stabilisation of the soil. The protein-richshoot material of A. halimus makes it an important fodder species for livestock, particularly sheep andgoats. However, its low energy value means that it should be supplemented with carbohydrate-richmaterial, such as cereal straw. Potential new uses of this versatile plant species include the phytor-emediation of soils contaminated by trace elements and the exploitation of its biomass as a source ofrenewable energy. Such applications, together with its continued use in low-intensity farming systems,should ensure that A. halimus remains a vital plant species in low-rainfall regions.

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1. Introduction

Atriplex halimus L. (syn. Atriplex capensis Mog., Chenopodiumhalimus Thunb. and Schizotheca halimus Fourr.) is a perennial,halophytic and nitrophilous shrub. Its variety of common namesreflects its wide geographical distribution: they include Mediter-ranean saltbush (English), salado/a (Spanish), alismo (Italian),arroche halime (French) and salgadeira (Portuguese). It grows un-der semi-arid and arid conditions throughout Eurasia: from theAtlantic coasts, through theMediterranean basin countries and intothe Middle East. On saline and degraded soils, it is often thedominant plant species, forming mono-specific stands. The abilityof A. halimus to thrive under harsh environmental conditions hascontributed to its traditional use as a source of browsing fodder forlivestock in these areas.

The first part of this review describes the geographical distri-bution of A. halimus and the habitats inwhich it occurs, while in thefollowing section we explore its botanical and genetic character-istics. Then, we discuss the morphological, anatomical, biochemicaland physiological factors underlying its adaptation to importantenvironmental stresses: salinity, drought, extreme temperaturesand soil contamination by trace elements. We examine the in-teractions of this species with other biota and the characteristicsthat make its biomass suitable for livestock, as well as the factorsthat may limit its exploitation. Other existing uses of A. halimus arereviewed, as well as its possible utilisation in the emerging tech-nologies of phytoremediation of contaminated soils and energyproduction from plant biomass.

2. Geographical distribution and habitat

A. halimus grows naturally throughout Macronesia, the Medi-terranean basin and beyond into western Asia: including southernPortugal, France, southern and eastern Spain (and the Canary

* Corresponding author. Tel.: þ34 634 883866.E-mail address: [email protected] (D.J. Walker).

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Journal of Arid Environments

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Journal of Arid Environments 100-101 (2014) 111e121


Islands), Italy, Greece, Malta, Turkey, Cyprus, Israel, Syria, Lebanon,Jordan, Tunisia, Morocco, Algeria, Libya, Egypt and Saudi Arabia (Al-Turki et al., 2000; Gu et al., 2011; Le Houérou, 1992; Walker et al.,2005). A few small populations are present in Brittany (France)and on islands such as Belle-Ile, Jersey and Guernsey (Lutts, un-published). Due to its varied uses, particularly as livestock forage, ithas been introduced elsewhere: for example, Oman, Iran, Iraq,Pakistan, South Africa, Chile, Argentina, New Zealand and the U.S.A.In countries closer to the Equator where it has been introduced, likeKenya and Ethiopia, the small photoperiod variation during theyear means that it does not flower.

It grows in areas of low annual rainfall (R) and high potentialevapotranspiration (PET), many of which can be classified as arid(R ¼ 100e400 mm, R:PET ¼ 0.06e0.28) or semi-arid (R ¼ 400e600 mm and R:PET ¼ 0.28e0.45) (Le Houérou, 1992). It exists astwo sub-species (Le Houérou, 1992), which are described in detaillater: subsp. schweinfurthii generally occurs in arid and/or salineareas and subsp. halimus in semi-arid, non-saline zones (in thewestern Mediterranean basin and Macronesia). Although possess-ing moderate cold tolerance (Le Houérou, 1992), it is limited toaltitudes below around 1200 m asl, reflecting the fact thatincreasing altitude reduces the temperature and the abundance of

C4 species. Blasco et al. (2008) found the distribution of A. halimusin eastern Spain to be influenced strongly by the mid-winter(January) temperature and by the altitude (only growing below920 m asl) and showed a negative relationship between annualrainfall and the presence of A. halimus.

It occurs at open, sunny sites, on neutral or alkaline soils (pH7.0e11.0), which are often saline (electrical conductivity, EC, of asaturated soil paste> 4 dS m�1), beingmore vigorous on loams andless so on sandy or clay soils (Le Houérou, 1992). A. halimus is oftenthe dominant species at such sites (Cañadas et al., 2010) due to itsdense foliage, which inhibits growth of herbaceous species. UnderMediterranean climates, A. halimus is often exposed to varying soilconditions, as a result of the drying of the soil in hot summers andits re-wetting in moist winters. For example, Nedjimi (2012) re-ported that for plants growing in an Algerian chott (seasonal salinewetland), soil pH (7.00e8.02) and EC (2.0e4.5 dS m�1) rangedwidely over a 12-month period.

A. halimus generally forms part of the halophilous communitieson saline soils. Tadros (1953) related that an association ofA. halimus and Picris radicata (Forssk.) Less. (the “AtriplicetumHalimi”) was the most highly developed of the halophilous com-munities in the Mediterranean coastal belt of Egypt, and was

Fig. 1. (A) Plants of Atriplex halimus growing in the region of Murcia (Spain): subspp. schweinfurthii (left) and halimus (right). Total height of calibrated pole ¼ 1.10 m. (B) Fruits andseeds of A. halimus subsp. schweinfurthii. Large squares are 10 � 10 mm. (C) Fruits and seeds of A. halimus subsp. halimus. Large squares are 10 � 10 mm. (D) Seed of A. halimus subsp.schweinfurthii. Diameter ¼ 1.2 mm. (E) Leaves of A. halimus subsp. halimus.

D.J. Walker et al. / Journal of Arid Environments 100-101 (2014) 111e121112


dominant on elevated, well-drained, saline soils. Ayyad and El-Ghareeb (1982) found that A. halimus was one of the dominantspecies in the transitional zones between areas of shallow and deepwater tables, in the salt marshes of the western Mediterraneandesert of Egypt, while Shaltout et al. (1995) reported that it wasassociated with Chenopodium murale L. in the man-made terracesof the Egyptian Nile delta. Close to desert oases in southern Israel,A. halimus was one of the dominant species, together with Salsolacyclophylla Baker, Suaeda fructicosa (L.) Forsk. and Alhagi graecorumBoiss. (Gu et al., 2011). On abandoned agricultural land in south-eastern Spain, Cañadas et al. (2010) found that A. halimus was thedominant species on the soils of higher salinity andmoisture, in the“Atriplicetum glauco-halimi” phytosociological association, withspecies such as Lygeum spartum L. and Limonium spp. Khaznadaret al. (2009) reported that A. halimus was one of the dominanthalophytes at the edge of an Algerian chott, together with Atriplexcanescens (Pursh) Nutt., Chenopodium album L. and S. fructicosa. Onthe Greek island of Palea Kaimeni, in the Aegean sea, A. halimus andLycium intricatum Boiss. were the dominant species of the climaxshrub vegetation of the supralittoral zone (Raus,1988). It also growsin urban environments; for example, in Almeria city (Spain) onsaline soils, in communities of nitrophilous shrubs dominated bychamaephytes - such as A. halimus - and nanophanerophytes (Danaet al., 2002).

3. Botany and genetics

3.1. Morphology

A. halimus is an upright perennial shrub, up to 3 m in height,which is branched from the base, the bark being greyewhite incolour, and has leaves which are 10e30 mm long and 5e20 mmwide (Fig. 1A,E). The leaves are highly variable in form, rangingbetween deltoid-orbicular and lanceolate, and are attenuated at thebase with a short petiole. Although A. halimus is evergreen, someleaves are lost during the hot, dry summers typical of its distribu-tion. Franclet and Le Houérou (1971) and Le Houérou (1992)divided A. halimus into two sub-species or varieties: halimus(¼ var. typica Aellen, var. genuinaMaire etWeill.) and schweinfurthii(Boiss.) Le Houérou (¼ var. glaucoidea L. Chevall, var. ramosissima L.Chevall, var. argutidens Bornm). This was based on differences inmorphology (Fig. 1A), with halimus having a more-erect habit, asmaller size (0.5e2.0 m height, compared to 1.0e3.0 m forschweinfurthii) and shorter fruit-bearing branches (0.2e0.5 m,compared to 0.5e1.0 m). For subsp. schweinfurthii, the fruitingbranches are leafless, rigid and often have a reddish hue, while itsleaves are very variable in size, shape and colour, from greenish togreyish, and its fruit valves are reniform and with obscurely-toothed margins (Fig. 1B). Sub-species halimus has upperbranches which are twisted with somewhat scorpioid leafy twigs.Its leaves are more or less hastate, greenish when young andsilvery-grey when old, and its fruit valves are reniform with entiremargins (Fig.1C). However, themorphology of subsp. schweinfurthiiis highly variable and intermediate phenotypes are common.

3.2. Reproductive structures

Although it can propagate vegetatively, via shoot-borne roots(Guerrero-Campo et al., 2006), A. halimus spreads principally viaseeds (which develop from wind-pollinated flowers) transportedby animals, air or water; for instance, Raus (1988) described itscolonisation of a Greek island by means of seeds transported by theAegean sea.

The inflorescence is tapered, compact and paniculiform; thefemale flowers develop mainly towards the base and the male

flowers towards the tip. This gives the stems a pale greenish-browncolour during flowering; between May and December, according tothe site. A. halimus was considered a monoecious species, bearingbractless male flowers (diameter ca. 2 mm) with five yellowishtepals and female flowers (longest axis ca. 10 mm) possessing twobracts. However, Talamali et al. (2001, 2003) described a complexarchitecture of the inflorescences and flowers (for a population ofsubsp. schweinfurthii). In the pentamerous flowers, both sets ofreproductive organs were present initially but suppression of thegynoecium overwhelmingly resulted in male flowers, althoughbisexual and even pistillate flowers also occurred. Also, the brac-teate flowers were occasionally bisexual, bearing stamens as well asthe pistil. The plants studied by Talamali et al. were trimonoeciousand exhibited as many as six floral phenotypes. Talamali et al.(2003) suggested that this labile sex expression is an adaptationto harsh environments; they also demonstrated that short days andlow irradiance gave rise to female, bracteate floral architecture.

Talamali et al. (2007) found heterostyly in a Tunisian populationof A. halimus: female flowers on the same plant could be separatedinto three types according to their style length. Abbad et al. (2003)found an increase in the ratio of male to female flowers under non-irrigated conditions; they proposed that this may have been due tocompetition between vegetative and reproductive growth. Incomparison with 20 other Atriplex spp., Flores Olvera et al. (2006)found the pollen grains of A. halimus to be in the mid-rangeregarding diameter (16e30 mm) and number of pores per grain(54e72) and in the lower part of the range for pore diameter (1.0e1.2 mm).

The fruits bear bracts which are ca. 6 mm in diameter, reniformto sub-orbicular and entire or toothed (Fig. 1B,C). They reachmaturity in autumn-winter and the 100-seed weight is variable:between 1 and 4 g, the seeds being 0.8e1.2 mm in diameter(Fig. 1D). Under the same growth conditions, subsp. schweinfurthiigenerally produces larger fruits and seeds than subsp. halimus(compare Fig. 1B and C) and its seedlings grow more rapidly.However, a lower proportion of the fruits of subsp. schweinfurthiicontain seeds (due to the occurrence of hermaphroditic or sterileflowers, which do not produce viable seeds; Talamali et al., 2001)and their germination is poorer than that of subsp. halimus (Correalet al., 2010). Although seed dimorphism has been observed invarious species belonging to the genus Atriplex (Katembe et al.,1998), this has never been reported for A. halimus. The inhibitionof seed germination by the presence of the fruit bracts was thoughtto arise from their content of saponins (Askham and Cornelius,1971) and perhaps salt. However, Osman and Ghassali (1997) re-ported that bract removal strongly increased germination per-centage in A. halimus but they did not identify any specific water-extractable substance able to inhibit germination and concludedthat the negative influence of bracts on germination is mechanicalrather than chemical.

3.3. Anatomy

A. halimus possesses the C4 photosynthetic pathway (Shomer-Ilan et al., 1981; Zervoudakis et al., 1998), in which CO2 is incor-porated into phosphoenolpyruvate (PEP) to form oxaloacetatethrough the action of PEP carboxylase. Accordingly, its leaves havethe “Kranz” anatomy with a layer of bundle sheath cells sur-rounding each vascular bundle and radially-arranged palisade cells,although the bundle sheath is open (Shomer-Ilan et al., 1981).Whereas the stems of most vascular plant species form only onecylindrical vascular cambium, those of A. halimus undergo increasein girth through the meristematic activity of several successivecambia (Fahn and Zimmermann, 1982). The epidermis is relativelythin and a hypodermis - able to store water - is present beneath it

D.J. Walker et al. / Journal of Arid Environments 100-101 (2014) 111e121 113


(Blumenthal-Goldschmidt and Poljakoff-Mayber, 1968). An impor-tant anatomical feature of A. halimus (and other Atriplex spp.),particularly in relation to stress tolerance, are the vesiculated hairs(Mozafar and Goodin, 1970) or vesicular trichomes (Smaoui et al.,2011) present on the leaf surface. These living cells consist ofballoon-like hairs or bladder cells (Smaoui et al., 2011), 80e200 mmin diameter and with a surface coating of a waxy material, attachedto a stalk that is embedded in an epidermal cell.

3.4. Genetics

Although “traditionally” a member of the Chenopodiaceaefamily, the Angiosperm Phylogeny Group III system relocated it tothe Amaranthaceae (sub-family Chenopodioideae, tribe AtripliceaeC.A. Mey, genus Atriplex L.) based on molecular phylogenies(Kadereit et al., 2010; The Angiosperm Phylogeny Group, 2009).

The base chromosome number (x) in the genus Atriplex is nine(McArthur and Sanderson, 1984). Talamali et al. (2004) and Walkeret al. (2005) determined ploidy levels for 26 populations ofA. halimus from across the Mediterranean Basin and the CanaryIslands. Both studies showed that populations from France andSpain e corresponding to the phenotype of subsp. halimus - werediploid (2n ¼ 2x ¼ 18) whereas those of North Africa, Italy, Egypt,Israel and Syria were tetraploid (2n ¼ 4x ¼ 36) and generally cor-responded to the phenotype of subsp. schweinfurthii. For pop-ulations having morphologies intermediate between thoseconsidered typical of these two sub-species, nuclear DNA contentsshowed them to be tetraploid. Hcini et al. (2006) also found that allseven of the Tunisian populations they analysed were tetraploid.However, diploid populations of A. halimus from Israel have beenreported (Osmond et al., 1980) and Zhu et al. (2001) recorded theexistence of a hexaploid (2n ¼ 6x ¼ 54) population, as well astriploid plants (2n ¼ 3x ¼ 27), from Morocco. The wide geograph-ical distribution of A. halimus suggests that other ploidy levels couldexist; multiple ploidy levels have been found for other Atriplex spp.(Stutz, 1989). Ploidy levels may have a strong impact on sexexpression in Atriplex spp. (Barrow, 1987). In some Atriplex spp., adirect influence of the ploidy level on the plant physiologicalbehaviour has been reported, tetraploid plants having higherRubisco activity in the bundle sheath (Warner and Edwards, 1989)or more-efficient water use (Senock et al., 1991).

With respect to the 2C nuclear DNA content (of a diploid somaticcell),Walker et al. (2005) andHcini et al. (2006) detected two groupsof populations: those of the diploids ranged between 2.40 and2.44 pg while those of the tetraploids were 4.77e5.13 pg. Talamaliet al. (2004) estimated values of 2.29 each for two diploid pop-ulations and of 4.28e4.40 for six tetraploids. The variation in nuclearDNA among the tetraploids may reflect their independent produc-tion from different diploid populations on numerous occasions, viaautopoly- or allopoly-ploidisation (Stutz, 1989). An autopolyploidorigin for subsp. schweinfurthii is suggested by the fact that it ex-hibits lower seed fertility than halimus (Osmond et al., 1980).

Haddioui and Baaziz (2001), analysing isozyme polymorphismin Moroccan populations of A. halimus, found a relatively-high de-gree of genetic diversity, predominantly due to within-populationdiversity, with between-population variation accounting for only8%. These authors attributed this to the highly-outbreeding natureof A. halimus. Ortiz-Dorda et al. (2005), after studying RAPD-PCRproducts of DNA extracted from 51 populations of A. halimus andsequencing of the ITS region of the ribosomal DNA, separated thepopulations into two genetic groups, which, according tomorphological characters, corresponded to subspp. halimus andschweinfurthii. Using phylogenetic analysis and RAPD markers,Bouda et al. (2008) found that A. halimus was more-closely relatedto A. lentiformis S. Wats. than to five other Atriplex spp.

4. Exposure to stresses

4.1. High temperature and light

A. halimus is a species adapted to sites having summers withvery-high light intensity and temperature. Since it possesses the C4carboxylation pathway, the optimum temperature for photosyn-thesis is relatively high, around 35 �C (Le Houérou, 1992; Shomer-Ilan et al., 1981; Zervoudakis et al., 1998). Streb et al. (1997)concluded that A. halimus is able to withstand high light intensity(photosynthetically active radiation > 2000 mmol m�2 s�1) due tomutual shading of leaves and reflection of light by salt crystalsdeposited on the leaf surface by the collapse of vesiculated hairs,which give the leaves a greenish-grey colour (Fig. 1E). Qiu et al.(2003) demonstrated that in Atriplex centralasiatica Iljin resis-tance to high temperatures could be related to high endogenousconcentrations of xanthophylls, which confer photosystem pro-tection. According to Qiu and Lu (2003), external salinity helps theplant to cope with high temperatures.

4.2. Salinity

Le Houérou (1992) classified A. halimus as a “euhalophyte”, ableto withstand soil salinity levels equivalent to saturated paste ECvalues of 25e30 dS m�1. Debez et al. (2001) demonstrated that theseed germination of a coastal population of A. halimus was moresalt-tolerant than that of a population from a non-saline site;complete inhibition occurred at 700 and 350 mM NaCl, respec-tively, which represents very-high tolerance in both cases. Thegermination of A. halimus seems to be more resistant to salinitythan that of A. canescens or Atriplex nummularia Lindl. (Mâalen andRahmoune, 2009). Moderate concentrations of NaCl (<200 mM)enhance growth of A. halimus while higher levels are inhibitory e

populations from coastal (saline) sites generally being moretolerant (Bajji et al., 1998; Ben Ahmed et al., 1996; Ben Hassine andLutts, 2010; Ben Hassine et al., 2009, 2008; Nemat Alla et al., 2011).This superior growth has been attributed to stimulation of photo-synthesis and sugar transport (Khedr et al., 2011; Martínez et al.,2005) and improvements in net CO2 assimilation, stomatalconductance and transpiration (Boughalleb et al., 2009). Sadderet al. (2013) recently listed several genes controlling photosyn-thetic efficiency, chlorophyll, carotenoids and free proline that areregulated specifically by lowNaCl doses. In contrast to NaCl, KCl hasbeen shown to be highly toxic for halophyte plants belonging to thegenus Atriplex (Freitas and Breckle, 1992; Ramos et al., 2004).

Like other halophytes, A. halimus accumulates the maincomponent ions of salinityeNaþ (Martínez et al., 2005; Nemat Allaet al., 2012) and Cl- and other anions (Ben Ahmed et al., 1996; BenHassine et al., 2009) - in its tissues, storing them in the vacuole. Thevesiculated hairs on the leaf surface also act as a sink for salt(Mozafar and Goodin, 1970); according to Osmond et al. (1980),more than 50% of the Naþ and Cl� accumulated is translocated tothe hairs. This active intracellular accumulation of osmolytes or“osmotic adjustment” generates low values of tissue water poten-tial (Jw); simultaneous decreases in osmotic potential (Js) (e.g.,�7.5 MPa; Bajji et al., 1998) maintain tissue turgor. Hence, theplants can maintain water uptake and transport from extremely-saline external media. Together with the accumulation of ionicosmolytes in the vacuole, there is cytoplasmic accumulation of“compatible” organic osmolytes (notably proline and glycinebe-taine) which do not interfere with metabolic processes. Thesemaintain the osmotic balance across the tonoplast and protectmembranes, organelles and proteins; proline also regulates carbonand nitrogen metabolism, acts as an anti-oxidant and promotesrecovery once the stress has eased (Szabados and Savouré, 2009).



Salt resistance may also be related to the efficiency of mechanismsinvolved in mitigating salt-induced damage. Bouchenak et al.(2012) showed that peroxiredoxins and methionine sulphoxidereductases, key enzymes scavenging organic peroxides andrepairing oxidised proteins, respectively, were more-efficientlyinduced in the most-salt-resistant populations of A. halimus.

At very-high external salt concentrations (�300 mM NaCl),damage appears, regarding stomatal conductance (Nemat Allaet al., 2011), the root plasma membrane permeability, root hy-draulic conductivity and chlorophyll content (Nedjimi and Daoud,2009), photosynthesis (Boughalleb et al., 2009; Khedr et al., 2011)and intracellular organelles (Blumenthal-Goldschmidt andPoljakoff-Mayber, 1968; Wong and Jäger, 1978). The tissue levelsof mineral nutrients such as Ca2þ, Mg2þ and inorganic phosphorusalso decline (Bajji et al., 1998).

4.3. Drought

Xerophytic C4 species such as A. halimus are generally efficient intheir water use and hence adapted to dry climates. Le Houérou(1992) labelled A. halimus an “occasional” phreatophyte, some-times obtaining water from below the vadose zone. It produceslong, main roots and secondary roots borne on them that allow theuptake of water from deep soil horizons (down to 5 m), while adense network of fine, shoot-borne roots can access moisture andnutrients following rainfall (Guerrero-Campo et al., 2006).

As when exposed to salinity, water-deprived plants of A. halimuscan generate extremely-low values of Jw and Js (e.g., �4.20 and�6.57 MPa, respectively; Bajji et al., 1998). Differences betweenpopulations of A. halimus, related to the pedo-climatic conditions attheir native sites, exist with respect to their adaptation to externalwater shortage and their tolerance, in terms of growth. Lutts andco-workers (Ben Hassine et al., 2009, 2008; Martínez et al., 2004)concluded that improved water use efficiency contributed to thebetter maintenance of growth under restricted water supply bypopulations frommore-arid sites. Ben Hassine and co-workers (BenHassine and Lutts, 2010; Ben Hassine et al., 2009, 2008) comparedtwoTunisian populations of A. halimus, one from an inland, arid siteand one from a coastal, saline site: the former was more tolerant ofwater deprivation (in terms of growth) and accumulated moreproline, had more-negative values of Jw and Js (and higherturgor), higher CO2 assimilation rate and lower stomatal conduc-tivity (and hence higher water use efficiency). There seems to be aspecific accumulation of Naþ as the cationic osmolyte underdrought (Ben Hassine et al., 2010; Martínez et al., 2005; Nedjimi,2012). According to Freitas and Breckle (1993), tissue accumula-tion of nitrate may be observed, to maintain the electrical balancein the absence of chloride salts in the surrounding environment.

4.4. Stress-specific adaptations to drought and salinity

Ben Hassine and co-workers (Ben Hassine and Lutts, 2010; BenHassine et al., 2009, 2008) compared the responses of individualpopulations of A. halimus to water deprivation and salinity. Theirresults indicate a role for the polyamines spermine and sper-imidine in the response to salinity and perhaps for putrescine indrought tolerance. These compounds are thought to protect bio-membranes and proteins under abiotic stress, but their over-synthesis could also help to reduce synthesis of the senescinghormone ethylene. These authors also proposed that the role ofabscisic acid (ABA) differs between the two stresses: under os-motic stress, it enhances stomatal regulation and water use effi-ciency whereas under external salinity it promotes excretion ofNaþ and Cl- into the vesiculated hairs. Ben Hassine and co-workerssuggested that the slower (chloroplastic) accumulation of

glycinebetaine protects the photosynthetic apparatus againstpermanent soil salinity, while proline (which accumulates morequickly) may protect against oxidative damage and also regulatecarbon and nitrogen metabolism when the plants are faced withshort-term drought.

Khedr et al. (2012) studied the Dehydration Responsive ElementBinding (DREB) transcription factor in A. halimus, which regulatesthe expression of many stress-inducible genes, and showed that itwas up-regulated greatly by both water deprivation and salinity; inthe latter case, it was the osmotic component of the stress that wasresponsible. Nemat Alla et al. (2012) published a metabolomics-based analysis of the changes in A. halimus caused by exposure tosalt (NaCl) or water deprivation (polyethylene glycol). They foundcommon responses to these two stresses (e.g., up-regulation of thetricarboxylic acid cycle and synthesis of b-alanine) and others thatwere specific to salinity (e.g., up-regulation of ABA transport andalkaloid synthesis) or polyethylene glycol (e.g., up-regulation oftryptophane metabolism). In the near future, proteomic ap-proaches could help us to decipher specific pathways involved inionic and water stresses.

4.5. Cold

Within the genus Atriplex, Le Houérou (1992) placed A. halimusin a group of species exhibiting moderate cold tolerance (able towithstand temperatures as low as �10 to �12 �C). Walker et al.(2008) showed that the tolerance of A. halimus to sub-zero tem-peratures in the field (as low as �18 �C) correlated positively withleaf accumulation of Naþ, Kþ, amino acids, quaternary ammoniumcompounds and soluble sugars. In behaviour analogous to that insalinity and drought adaptation, the leaf sap Jw and Js values ofcold-acclimated plants (as low as �2.69 and �6.32 MPa, respec-tively) were lower than in the following spring. This reflects theimportance of osmotic adjustment with regard to minimisingcellular dehydration throughwater loss to extracellular ice (Xin andBrowse, 2000). Quaternary ammonium compounds may assumekey functions in this respect since their over-synthesis is inducedby a wide range of environmental constraints, not only by salt andwater stress (Koheil et al., 1992). In the study ofWalker et al. (2008),diploid populations (subsp. halimus) resulted more tolerant thantetraploid ones (subsp. schweinfurthii), probably due to the less-negative Js values of the latter. Compatible organic osmolytescan maintain membrane and protein structure, hence acting as“osmoprotectants” in the face of freezing temperatures. AlthoughZervoudakis et al. (1998) showed a reduction of 83% in the activityof A. halimus PEP carboxylase at 0 �C, Salahas et al. (2002) foundthat high concentrations of glycinebetaine and proline protectedboth this enzyme and pyruvate orthophosphate dikinase againstcold inactivation.

4.6. Trace elements

The term “trace elements” refers to elements such as arsenic(As), cadmium (Cd), copper (Cu), manganese (Mn), nickel (Ni), lead(Pb) and zinc (Zn), which are important contaminants of soil due toanthropogenic activities such as agriculture, industry and mining.Since A. halimus has colonised trace element-contaminated sites,for example, in southern Spain (Lutts et al., 2004; Márquez-Garcíaet al., 2013) and Algeria (Lotmani et al., 2011), its tolerance mech-anisms have been researched.

The germination of A. halimus seems resistant to elevated levelsof trace elements in soil (Lotmani et al., 2011; Martínez-Fernándezand Walker, 2012). Studies of A. halimus grown in pots of contam-inated soil (Manousaki and Kalogerakis, 2009; Martínez-FernándezandWalker, 2012), in hydroponic culture (Lefèvre et al., 2009; Lutts



et al., 2004) or in Petri dishes (Márquez-García et al., 2013) showthat, in terms of growth, it is tolerant of high concentrations of Cd,Cu, Mn, Ni, Pb and Zn in the growth medium. The Cd tolerancemechanisms may include precipitation with oxalate, in the stem(Lutts et al., 2004), and excretion into vesiculated hairs (Lefèvreet al., 2009). Lefèvre et al. (2009) also found that Cd exposureincreased the accumulation of glycinebetaine, proline and sper-mine and spermidine, as under salinity (Ben Hassine et al., 2009).Lefèvre et al. (2010) showed that a key component of Cd resistanceis the synthesis of the endogenous antioxidants glutathione,ascorbic acid and a-tocopherol and stimulation of glutathionereductase. A. halimus has a high tolerance of elevated tissue Znconcentrations, which may result from co-precipitation with oxa-late (Lutts et al., 2004), while exposure to elevated Cu concentra-tions may trigger mechanisms which reduce Cu translocation fromthe roots to the shoots (Mateos-Naranjo et al., 2013). Lotmani andMesnoua (2011) demonstrated that Cu accumulation may lead tothe appearance of new isoforms of superoxide dismutase andperoxidase.

5. Interactions with other organisms

The beneficial effects of the planting of A. halimus includerecycling of plant mineral nutrients, incorporation of organicmatter (root material and leaf litter) into the soil to improve soilphysical properties (such as water permeability) and provision ofshelter and food for birds and mammals (Henni and Mehdadi,2012; Le Houérou, 1992). The leaching-out of saponins from thebracts of A. halimus by autumn andwinter rain permits germinationto occur in optimal soil conditions e regarding moisture andsalinity e and may have an allelopathic effect, inhibiting thegermination of nearby seeds (Askham and Cornelius, 1971). Theaccumulation of salt in the surface soil below the plants may occur,due to litter fall, but A. halimus has been found to stimulate certainsoil biota. In desert soils, the presence of A. halimus raised the sporedensity of arbuscular mycorrhizal fungi (He et al., 2002), increasedthe organic carbon and microbial biomass at soil depths down to50 cm (Barness et al., 2009) and augmented the numbers of pro-tozoa (Rodriguez Zaragoza et al., 2005) and nematodes (Pen-Mouratov et al., 2003). Mycorrhizae have numerous positivefunctions, mainly in relation to phosphorus nutrition, butmycorrhization has been shown to decline in Atriplex spp. exposedto NaCl stress (Asghari et al., 2005). Simon et al. (1994) found, forA. halimus growing in Israel, that the microbial population of theleaf phylloplane was dominated by a halo-tolerant Pseudomonasspecies, while Zvyagilskaya et al. (2001) identified several aerobicspecies of yeast on the leaf surface that were moderately salt- andalkali-tolerant.

The productivity of A. halimus can be limited (although theplants do not usually die) by the infection of roots by parasites ofthe Orobanchaceae, such as Cistanche phelypaea (L.) Coutinh andCistanche violacea (Desf.) Beck (Le Houérou, 1992; Tadros, 1953).Plantations can also be decimated by the fat sand rat (Psammomysobesus Cretzschmar), a large gerbillid rodent common in theSaharoeArabian deserts, which feeds solely on species such asA. halimus whose tissues are of low calorific value; otherwise itdevelops diabetes (Degen et al., 1988). Hegazi et al. (1980), workingin Egypt, found that arthropods of the orders Hymenoptera andDiptera could impact seed production, through formation of gallsand dwarf leaves, while Wills et al. (1990) reported that leaf-rollercaterpillars harmed young plants in New Zealand. Kravchenko et al.(2006) described the occurrence of Noctuidae spp. larvae onA. halimus in Israel and the plants can also act as a breeding site forleafhoppers that injure crops and act as disease vectors (Klein et al.,1982).

6. Traditional uses

6.1. Livestock feed

Since the 1960s, A. halimus has been planted in the Mediterra-nean arid zone to provide standing feed browse, or silage, for smallruminants (sheep and goats) and also cattle and camels (Correal,1993; Franclet and Le Houérou, 1971; Khattab, 2007; Le Houérou,1992). The planted area is estimated at around 100,000 ha inAlgeria, the Arabian Peninsula, Egypt, Iraq, Israel, Jordan, Libya,Morocco, Spain and Tunisia. This reflects the ability of Atriplex spp.to provide year-round forage and their much-greater salt tolerancerelative to many other pasture species (Azam et al., 2012). Beyondits natural distribution, Wills et al. (1990) found A. halimus to be apromising forage species for Merino sheep on dry, open slopes ofthe South Island of New Zealand, but in California (U.S.A.) it did notthrive (Juhren and Montgomery, 1977) and in the Cape VerdeIslands its palatability to livestock was low (Pasiecznik et al., 1996).

The most-efficient method of establishment is via transplantedseedlings, rather than direct sowing, but this is slow and expensive(Le Houérou, 1992). Around 2000 seedlings per hectare are planted,with a spacing of 1 � 5 m. Direct sowing requires the soaking ofseeds in running water in order to eliminate the salt and saponins.The utilisation of pre-germinated seeds, just after swelling but priorto the emergence of the radicle, is particularly successful inautumn. Plantationsmay be established without removal of naturalvegetation or as high-density stands, but nitrogen fertilisation maybe required to improve seedling growth (Bouzid and Papanastasis,1996). To ensure their long-term productivity, weeds should becontrolled, shrubs should be cut back every 2e3 years and very-infrequent browsing (leading to woody plants) should be avoided.Bouzid and Benabdeli (2011) emphasised the importance of keep-ing the plantations enclosed to protect against over-grazing (whichcan eliminate re-growth). The forage yields are usually 2e5 Mg dry matter ha�1 yr �1, depending on the local conditions andmanagement, and rain-use efficiency is high, compared to nativerangelands (Franclet and Le Houérou, 1971; Le Houérou, 2000).Although Abu-Zanat et al. (2004) found the dry matter productionand rain-use efficiency of A. halimus to be lower than those ofA. nummularia, the latter is less cold-tolerant.

A. halimus shrubs produce a nitrogen-rich fodder (3e4% in thedry matter), but the rumen microflora take time to adjust to thissource of nitrogen (ca. 3 months) since some 40e45% of the ni-trogen is non-proteinic (e.g., proline and glycinebetaine) (Anduezaet al., 2005; Walker et al., 2008). The glycinebetaine content ofA. halimus tissues may have beneficial effects on monogastric ani-mals such as pigs and poultry: it seems to be important in variousmetabolic processes (as a methyl group donor and in protein andenergy metabolism), as an osmoprotectant of intestinal cells andgut microbes and in the improved digestibility of fibre (Ratriyantoet al., 2009). It is rich in protein (14e21% crude protein; Anduezaet al., 2005; Bhattacharya, 1989; El-Shatnawi and Turuk, 2002); infact, since ancient times, it has been consumed by humans in timesof scarcity of other food sources. Bhattacharya (1989) found that thecrude protein content and digestibility and retention of nitrogenwere higher than for other forage species such as alfalfa, while thedigestibilities of the crude protein, organic matter and crude fibrewere similar to or greater than those of the other species. The fibrecontent may be beneficial for the quality of goat-derived dairyproducts (Alvarez et al., 2008). Otal et al. (2010) demonstrated thatthe quality of A. halimus forage was related to the proportion ofleaves and twigs eaten voluntarily by the animals. According toSalem et al. (2012), sun-drying and addition of exogenous dietaryenzymes may be beneficial for both intake of A. halimus forage bysheep and its digestibility.



One drawback of the browse (leaves and young twigs) ofA. halimus is its low content of energy (digestible andmetabolisableenergy values of 8e9 and ca. 7 MJ kg�1 dry matter, respectively)(Alvarez et al., 2008; Mirreh et al., 2000) and its high salt content(e.g., up to 10% Na in dry matter) (Bhattacharya, 1989; El-Shatnawiand Turuk, 2002; Walker et al., 2008), the latter requiring elevatedintake of water by livestock (up to 11 L sheep�1 day�1; Mirreh et al.,2000). However, Ruiz-Mirazo and Robles (2011) demonstrated thatspring grazing increased the shootmoisture content in the summer.Also, when given alone, the phosphorus content can be insufficientfor ewes (El-Shatnawi and Mohawesh, 2000) and the calciumcontent insufficient for lambs (Khattab, 2007), while the levels ofoxalate (up to 10% of dry matter) and certain tannins may reducethe palatability (Abu-Zanat et al., 2003a). Abu-Zanat et al. (2003b)demonstrated that the oxalate content varied drastically accordingto the season and that the mineral composition of A. halimus wasbetter than that of A. nummularia. Due to these factors, the com-bination of A. halimus with a source of high-carbohydrate forage orsupplement is appropriate, particularly when the energy demandsof the livestock are greater (e.g., during pregnancy and lactation).Hence, A. halimus has been evaluated by ICARDA and other researchinstitutions as a potential alley crop with cereals to provide proteinand mineral supplement to cereal straw and stubbles. For example,inter-cropping of A. halimuswithin barley crops provides forage forsheep and goats in south-eastern Spain in the summer and earlyautumn, when alternative sources are very scarce (Sotomayor andCorreal, 2000). The planting of A. halimus in selenium (Se)-richsoils may represent a risk, considering the ability of other Atriplexspp. to accumulate this element which, following the ingestion ofhigh amounts by livestock, could be harmful (Bañuelos et al., 2002).In fact, Alazzeh and Abu-Zanat (2004) reported elevated bloodserum levels of Se in sheep after six weeks of feeding with anA. halimus/A. nummularia mixture.

6.2. Soil remediation

A. halimus represents one of the best options for the reclamationof degraded agricultural land in arid and semi-arid zones. Due to itsextensive, deep root system, it has been used in soil conservationprojects in arid lands in Algeria, Egypt, Libya, Israel, Jordan, NewZealand, Spain, Syria and Tunisia, particularly as a contour hedge tocontrol runoff and erosion in clay and marl soils and shales.

Its planting promotes recycling of nutrients, reduction of windspeed at ground level and decreases in run-off and erosion (LeHouérou, 1992). Chisci et al. (2001) found that A. halimus plantedtogether with Hedysarum coronarium L. on marginal clay soil inItaly improved soil porosity and the formation of soil aggregatesand reduced soil loss through run-off, while Marqués et al. (2005)demonstrated that A. halimus together with a low dose of sewagesludge was optimal for diminishing run-off and sediment loss.Although De Baets et al. (2008) showed A. halimus to have thestrongest roots of 25 Mediterraneanmatorral species tested, Mattiaet al. (2005) calculated that the soil reinforcement of A. halimusroots was inferior to that of L. spartum and Pistacia lentiscus L. Forthe rehabilitation of gypsum quarry spoil in Spain, Castillejo andCastelló (2010) discovered that addition of municipal solid wastecompost stimulated A. halimus germination and growth; however,they cautioned that high rates of nutrient-rich amendments, whileaccelerating initial plant growth, might lead to the exclusion of thenative flora by A. halimus. So, before implementing a site-restoration project, it must be decided whether the aim is therecreation, as near as possible, of the original vegetation (andecosystem) or simply the establishment of a “green cover”. Thephysico-chemical conditions of saline soils can be improved bycultivation of halophytes such as A. halimus (Gharaibeh et al., 2011),

due in part to uptake of salt by the plants but mainly to thedissolution of calcite (CaCO3) in the rhizosphere, which results fromincreased partial pressure of CO2 and proton release by the roots.The solubilised Ca2þ displaces Naþ from cation exchange sites,although irrigation water is required to leach the Naþ below theroot zone (Manousaki and Kalogerakis, 2011).

6.3. Traditional medicine and modern pharmacology

Plants of A. halimus have been used as traditional cures for manyconditions for thousands of years. Although in some cases ineffec-tive, as in the use of a decoction to treat syphilis (Rolleston, 1942),their use persists and in recent years the pharmacological bases forcertain of the activities have been elucidated. The ash from burntplants is used as an alkali to make soap, while the shoots can beburnt to yield an antacid powder (Uphof, 1968). Arabic indigenousherbal practitioners employ the leaves to treat heart diseases anddiabetes (decoction) and rheumatism (an extract prepared withboiling water is added to bath water) (Said et al., 2002). The anti-diabetic effect has been developed further, in a product (“Glucole-vel”) combining leaf extracts of A. halimus, Juglans regia L., Oleaeuropea L. and Urtica dioica L. (Said et al., 2007). Extracts of the aerialparts of A. halimus obtained with methanol or hexane (and con-taining alkaloids, steroids, flavonoids and glycosides) showed anti-bacterial activity against various Gram-positive and negativepathogenic bacteria (Abdel Rahman et al., 2011). Endophytic fungiisolated from A. halimus had antimicrobial effects against species ofbacteria possessing antibiotic resistance (Peláez et al., 1998).

7. Potential new uses

7.1. Phytoremediation of contaminated soils

A possible application of A. halimus, suggested by its ability tostabilise soils physically and its tolerance of elevated concentrationsof trace elements in the growth medium, is in the remediation oftrace element-contaminated soils. Due to mining or industrial ac-tivity, such soils exist in many low-rainfall areas such as the Medi-terranean basin (Clemente et al., 2012; Laffont-Schwob et al., 2011;Lotmani et al., 2011), northern Chile (Vromann et al., 2011) and theU.S.A. (Mendez and Maier, 2008). At such sites, phytoremediationrequires species tolerant not only of poor soil conditions (elevatedtrace element concentrations, poor structure and nutrient avail-ability and often high EC), but also of seasonal drought and hightemperatures. Hence, native halophytes have advantages due totheir stress tolerance and other Atriplex spp. have been investigatedfor this purpose, with promising results (Mendez and Maier, 2008).

To date, there is only one report (Clemente et al., 2012) con-cerning the utilisation of A. halimus in phytoremediation underfield conditions, but it yielded important information regarding theviability of this application. The soil was highly-contaminated (totalconcentrations of As, Cu, Pb and Zn: 664, 193, 10,188 and9686mg kg�1, respectively) and possessed characteristics typical ofsoils affected by mining waste: high EC and very low nutrientavailability. The survival of the transplanted seedlings and theirsubsequent growth were improved greatly by addition of compostor pig slurry to the soil before transplanting, mainly due to theirprovision of nutrients. The results of Clemente et al. (2012)confirmed the ability of A. halimus to restrict shoot accumulationof As and Pb (Manousaki and Kalogerakis, 2009), an importantpoint in the phytostabilisation of contaminated soils, in which theaim is that the contaminants remain in situ in the soil and roots.Extrapolating from pot or nutrient solution studies, previous au-thors suggested that A. halimus could be employed in the phy-toextraction from contaminated soils (their removal in the plant



biomass) of Cd and Zn (Lutts et al., 2004; Tapia et al., 2011). Thelevels of A. halimus foliar Cd and Zn (up to 1253 mg kg�1 for Zn)found by Clemente et al. (2012) show that this is not feasible, a viewshared by Lotmani et al. (2011), but are a concern. Although theingestion of its leaves and stems by herbivorous mammals islimited by their high salt content, A. halimus is colonised by ar-thropods (phytophages and their predators; Hegazi et al., 1980);this, together with leaf litter, is a route by which contaminantscould move through the food chain.

As mentioned earlier, the ability of A. halimus to grow quicklyand form dense stands may exclude other plant species. Notwith-standing, this may be the best option for the establishment of asubstantial vegetation cover at a contaminated site (Mendez andMaier, 2008). Tapia et al. (2013) recently recommendedA. halimus to generate plant cover in As-contaminated soils. Also,Clemente et al. (2012) reported a significant interaction betweenthe addition of organic matter and the presence of A. halimus,regarding stimulation of the soil microbial biomass e a crucialfactor in the remediation of degraded sites. Laffont-Schwob et al.(2011) showed that A. halimus is capable of forming endomycor-rhizae in trace element-contaminated sites; this would increase theavailability of water and nutrients, especially phosphorus, to theplants and may also limit trace element uptake.

7.2. Energy crop

Thewood produced by A. halimus has been used for centuries forheating and cooking, a practice which continues today in ruralareas (Bouzid and Benabdeli, 2011). Abandoned agricultural landsare considered to be the optimal sites for yielding biomass energy,up to 5% of global primary energy consumption, without affectingfood production, since there are no competing uses (Field et al.,2007). Also, the scarce existing vegetation in these areas meansthat little fixed carbon is lost during the installation of biomassplantations, while their subsequent growth should increase soiland vegetation carbon stocks. At abandoned agricultural sites inarid and semi-arid areas, A. halimuswould have an acceptable yieldof leaf and stem dry matter (up to 10 Mg ha�1) in the absence ofinputs. A. halimus is considered as “dry” biomass as its moisturecontent is very low; as such, it is best-suited economically togasification, pyrolysis or combustion (McKendry, 2002). The mainproperties of interest of “dry” biomass as an energy source are itsmoisture content, calorific value, proportions of fixed carbon andvolatiles, ash/residue content and alkali metal content.

We analysed the dry biomass from plants of A. halimus grown ina semi-arid, saline soil in southern Spain, to evaluate its suitabilityas a source of bioenergy (unpublished results). The calorific valuesof A. halimus dry matter (stems: 17.2 kJ g�1; leaves: 12.8 kJ g�1)were similar to those reported for other materials (rice straw: 16.1e16.4 kJ g�1; sugar cane: 17.3; maize: 15.6e18.8; de Ramos e Paulaet al., 2011). However, the ash content (13.7% in this study and29% for leaves and 6e11% for young stems in the work of Anduezaet al., 2005) was well above the recommended level (�1%; deRamos e Paula et al., 2011; McKendry, 2002) and the levels of al-kali metals, which impact adversely on thermal conversion pro-cesses, were very high; this may restrict its use as a bioenergy cropto non-saline sites (Miles, 1994). However, A. halimus could beutilised in another “green” technology: the use of its standingbiomass (both aerial and underground) in carbon sequestration(Field et al., 2007; Glenn et al., 1992).

7.3. Other potential applications

The isolation from A. halimus of the genes controlling the traitswhich confer salt tolerance and their transfer into economically-

important crop species, to extend the range of conditions underwhich they give viable yields, is an emerging technology (Sadderet al., 2011). Its dried biomass could be used for the removal oftrace elements from contaminated water, as demonstrated forA. canescens by Sawalha et al. (2008). This seems to depend on thepresence of functional groups such as carboxyl, hydroxyl and sul-phate on the surface of the biomass. In addition, the accumulationof saponins and glycinebetaine by A. halimus might be exploited:saponins (as biosurfactants) are effective in the removal of traceelements from contaminated soils (Hong et al., 2002), while gly-cinebetaine, added as a feed supplement, can enhance the nutritionand growth of monogastric animals (Ratriyanto et al., 2009). Likemany other species, A. halimus continues to be a source of newphytochemicals: Clauser et al. (2013) recently isolated four newglycosylated flavonoids from its aerial parts.

8. Concluding remarks

Its morphological, anatomical and physiological adaptations toharsh environmental conditions allow A. halimus to growthroughout the arid and semi-arid zones of the Mediterraneanbasin, western Asia and beyond. External salinity, water depriva-tion and sub-zero temperatures (and high concentrations of certaintrace elements) all perturb plant water relations. So, it is not sur-prising that the physiological adaptations of A. halimus to thesestresses e described earlier e have in common certain processes,notably intracellular osmotic adjustment, in addition to stress-specific responses.

A. halimus should continue to be used in soil protection and low-intensity farming systems of semi-arid and arid zones where,together with crop residues and rough grazing, it can form part of abalanced diet for livestock. It could also have a role in the phytor-emediation of moderately-contaminated sites, where it wouldreduce the wind- and water-provoked movement of contaminantsaway from the site (phytostabilisation). Its accumulation of ionicosmotica might restrict its exploitation as a bioenergy crop to non-saline soils. In all cases, A. halimus is attractive as a species becauseit is relatively undemanding in terms of management and is able tothrive on degraded soils.

Acknowledgements

All authors contributed to the writing of the text: DJW proposedthe review and DJW, EC, MSG and SL wrote parts of the original text,provided original data and/or revised the text. All authors approvedthe final version.

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