Incorporating thresholds into understanding salinity tolerance: A study using salt- tolerant plants in salt marshes
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- Rudolf Holt
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1 Reeived: 18 Mrh 217 Revised: 29 My 217 epted: 7 June 217 DOI: 1.2/ee3.329 ORIGINL RESERH Inorporting thresholds into understnding slinity tolerne: study using slt- tolernt plnts in slt mrshes Qing He 1,2 Brin R. Sillimn 2 Boshn ui 1 1 Shool of Environment, Stte Key Lbortory of Wter Environment Simultion, Beijing Norml University, Beijing, hin 2 Division of Mrine Siene nd onservtion, Nihols Shool of the Environment, Duke University, Beufort, N, US orrespondene Boshn ui, Shool of Environment, Stte Key Lbortory of Wter Environment Simultion, Beijing Norml University, Beijing, hin. Emil: uibs@bnu.edu.n Funding informtion Ntionl Key Bsi Reserh Progrm of hin, Grnt/wrd Number: 213B436; Key Projet of Ntionl Nturl Siene Foundtion of hin, Grnt/ wrd Number: ; Ntionl Siene Foundtion for Innovtive Reserh Group, Grnt/wrd Number: 51123; The Edwrd S Stolrz Foundtion bstrt lthough slinity in mny eosystems suh s slt mrshes n be extremely high, n symmetry in slinity rnge between experimentl studies (reltively nrrow) nd field onditions (potentilly brod) hs strongly ffeted urrent understnding of plnt slinity tolerne. To improve understnding, it is thus importnt to exmine plnt tolernes over brod rnge of slinities nd identify potentil tolerne thresholds. We exmine tolernes of two widely distributed mrsh plnts, Sued sls nd Sliorni europe, to slinities rnging from to g/kg, nd determine survivl, bove- nd belowground biomss fter 8 weeks of slinity tretment. Both speies, S. europe in prtiulr, hve muh broder slinity tolernes thn other plnts previously exmined, (2) plnt survivl, bove- nd belowground biomss hve remrkbly different responses to slinity, nd (3) there is nonliner, threshold response of S. sls to slinity, bove whih S. sls survivorship drstilly dereses. These results provide multiple importnt insights. Our study suggests tht the potentil for using these hlophytes to revegette nd restore slt- ffeted lnd my be greter thn previously thought, nd highlights the importne of studying multiple plnt responses. Importntly, our study lls for better integrtion of thresholds into understnding plnt slinity tolernes nd their pplitions. KEYWORDS ostl wetlnds, nonliner eologil proesses, Sliorni europe, slt mrsh, soil slinity, Sued sls 1 INTRODUTION Sliniztion is detrimentl environmentl problem tht thretens mny nturl nd rtifiil eosystems worldwide. Sliniztion ssoited with groundwter nd irrigtion ffets ~16% of the world s griulturl eosystems (Rengsmy, 26); inreses in rodwys nd deier use hve been shown to slinize freshwters ross Europe nd the United Sttes (Kushl et l., 25; Löfgren, 21); limte hnge, drought, dereses in esturine freshwter flow, se- level rise, nd storm surges hve been suggested to inrese the extent nd severity of sliniztion in ostl wetlnds globlly (Herbert et l., 215). Under this trend in sliniztion worldwide, mnging nd prediting the impt of sliniztion on eosystems require better understnding of slinity tolerne in plnts nd other primry produers tht re often the foundtions of eosystems. Plnt slinity tolerne hs been studied intensively for long time. It is well known tht plnts widely differ in slinity tolerne, nd those tht tolerte slt onentrtions (~2 mmol/l Nl or 11.5 g/kg) tht kill 99.8% of other speies re often lled hlophytes (definitions of hlophytes n vry; Flowers & olmer, 215). Hlophytes re equipped with number of strtegies to tolerte slinity, inluding t lest seletive umultion or exlusion of ions, ontrol of ion uptke This is n open ess rtile under the terms of the retive ommons ttribution Liense, whih permits use, distribution nd reprodution in ny medium, provided the originl work is properly ited. 217 The uthors. Eology nd Evolution published by John Wiley & Sons Ltd Eology nd Evolution. 217;7:
2 HE et l nd trnsport, nd omprtmentliztion of ions (Prid & Ds, 25). The effets of inresing slinity on plnt performne, however, vry remrkbly even within hlophytes. Mny hlophytes generlly grow optimlly in freshwter (Flowers & olmer, 28; Munns & Tester, 28), while some ould show optiml growth in low slinities. In either se, it hs been implited tht most hlophytes die or show strongly redued growth in slinities round tht of sewter (Flowers, Gll, & Bromhm, 21; Greenwy & Munns, 19). Slinities in mny eosystems, however, n be substntilly higher thn sewter slinity. In slt mrshes, for exmple, soil pore wter slinity n be severl times tht of sewter (7 15 g/kg), espeilly in regions with dry limte (e.g., liforni, southestern United Sttes, nd temperte hin) or in upper mrsh zones where slt onentrtion by evportion is intense (ui, He, & n, 211; Hoffmn & Dwes, 1997; Hsieh, 24; Pennings & Bertness, 21). Even in New Englnd, slt mrshes with riny, old limte, soil slinity n be up to 5 g/kg (Bertness, Gough, & Shumwy, 1992; Shumwy & Bertness, 1992). lthough hyperslinity stress limits reltively sltsensitive mrsh grsses, some hlophytes suh s Sliorni spp. ould olonize hypersline mrsh res (Bertness et l., 1992; Pennings & llwy, 1992; Shumwy & Bertness, 1992), inditing their gret pity to tolerte hyperslinity stress. Despite the potentil for plnts to tolerte suh high levels of slinity stress, the mjority of pst studies, even those from slt mrshes, exmined reltively smll grdients of slinity, typilly up to ~ g/kg (Bertness et l., 1992; Egn & Ungr, 21; Howrd & Rfferty, 26; Hukle, Potter, & Mrrs, 2; Ktshnig, Broekmn, & Rozem, 213; Kuhn & Zedler, 1997; Phleger, 1971; Redondo- Gómez et l., 27; Ungr, Benner, & MGrw, 1979). Muh fewer studies exmined plnt tolerne to slinities s high s 5 g/kg (Guo & Pennings, 212; He, ui, & n, 211; He, ui, Bertness, & n, 212; Khn, Ungr, & Showlter, 2; Yeo & Flowers, 19). However, in these studies, highly slt- tolernt plnts often survived nd ontinued biomss umultion (lthough t lower rtes), nd their slinity tolerne thresholds re unknown. few studies tht exmined broder slinity grdients up to 7 g/kg suggested, without speifi sttistil tests, tht slinity tolerne thresholds might exist (rin, Sillimn, Bertness, & Bertness, 24; Li, Liu, Khn, & Ymguhi, 25). Suh studies, however, re rre nd hve often foused on single plnt response vrible (e.g., boveground biomss). Other plnt response vribles, espeilly plnt survivl, n gretly differ in response to environmentl stress (He, Bertness, & ltieri, 213). lerly, there is signifint symmetry in slinity rnge between experimentl studies nd doumented field onditions in the literture, nd our urrent understnding of plnt slinity tolerne hs been strongly ffeted nd limited due to this symmetry. To improve urrent understnding, it is thus importnt to exmine plnt tolernes over brod rnge of slinities nd to identify potentil tolerne thresholds bove whih slinity stress will led to drsti deline in plnt survivl/growth. Here, we exmined slinity tolernes of two obligte hlophytes, Sued sls (Linneus) Plls nd Sliorni europe L. (Fig. 1), speies widely distributed in slt mrshes nd sline drylnds. Sued sls hs been found ross northest si, nd S. europe ross si, Europe, North meri, nd fri (He, ltieri, & ui, 215; Musolo, Pnuio, & Piernik, 214). Both S. sls nd S. europe re in the fmily of mrnthee nd re mong the slt- tolernt plnts known in slt mrshes (He et l., 215). lthough slinity tolernes of S. sls nd S. europe hve been exmined in number of studies, s disussed bove, pst studies often exmined reltively smll rnge of slinities, despite the ft tht these speies n potentilly survive muh higher slinities. Furthermore, we know of no study tht hs determined potentil thresholds in the slinity tolerne of these speies long brod rnge of slinity nd ompred their slinity tolerne thresholds. Identifying potentil slinity tolerne thresholds is ruil, s reltively smll hnge round this point n led to drsti deline in plnt performne nd eosystem produtivity (Brook, Ellis, Perring, Mky, & Blomqvist, 213). () (b) FIGURE 1 Photogrphs showing Sued sls () nd Sliorin eutrope (b) in hypersline slt mrsh in the Yellow River Delt, northern hin. Photo redits: QEology.org
3 6328 HE et l. We investigted the responses of S. sls nd S. europe survivl nd growth to brod rnge of soil pore wter slinities ( g/kg) in pot experiment. We imed to exmine whether these plnts n tolerte slinity stresses times tht of sewter nd whether there re thresholds in their slinity tolerne. Speifilly, we hypothesized tht: (1) both speies perform optimlly in low- slinity tretments nd ould well survive muh higher slinity stress thn tht of sewter; (2) S. europe hs greter pity to tolerte slinity stress thn does S. sls; nd (3) there re ritil thresholds in the slinity tolernes of these two speies. 2 MTERILS ND METHODS Experimentl work ws onduted t our field sttion (37 5 N, E) in the Yellow River Delt, northern ostl hin. The Yellow River Delt hs wrm temperte limte, with dry flls, winters nd springs, nd riny summers. The long- term verge nnul preipittion is mm, nd the long- term verge nnul temperture of 12.8 (see He et l., 215 nd referenes therein). Slt mrshes in the Yellow River Delt re primrily dominted by S. sls. Sliorni eutrope ours often s subordinte in S. sls ommunities (He et l., 215). Other plnt speies tht exist in the Yellow River Delt inlude Phrgmites ustrlis, Tmrix hinensis, nd the invsive ordgrss Sprtin lterniflor (ui et l., 211). Slt mrshes re flooded irregulrly by semidiurnl mirotides. The mrsh pltform is often hypersline, nd soil slinities n vry gretly from 3 to 2 g/ kg, with pprent slt umultion on the soil surfe, espeilly in dry, low- rinfll periods (ui et l., 211; He et l., 215). The experiment hd 11 levels of slinity tretment ( g/ kg, with 1 g/kg intervls) replited six times for eh of the two study speies S. europe nd S. sls (n = 132 pots in totl). In erly June 213, we exvted using soil orer soil bloks (7.5 m in dimeter, 1 m in depth) eh ontining >3 S. europe nd S. sls seedlings, respetively, from high mrsh re in the Yellow River Estury (i.e., intertidl popultions; Song, Shi, Go, Fn, & Wng, 211). Eh of these soil bloks ws trnsplnted into plsti pot of 2.5 L. ll pots were pled in ommon grden under nturl light nd temperture onditions, exept tht preipittion ws exluded by rin shelter mde of trnsprent plsti. fter two- week limtiztion period, during whih we wtered the plnts with freshwter, we thinned the plnts in eh pot to 1 individuls of similr size (5 8 m for S. europe, nd 7 1 m for S. sls) nd ssigned them to eh of the 11 slinity tretments. The density of 1 individuls in eh pot ws within their nturl rnge. To ontrol for soil pore wter slinity, we pled pots into shllow lyer (~4 6 m) of stnding wter of different slinities nd llowed the tretment solution to rise to the soil surfe. This wy, soil pore wter ws omposed of the tretment solution, nd soil pore wter slinity would be onsistent with tht of the tretment solution. This is ommon method to ontrol soil pore wter slinity levels in plnt slt tolerne studies nd hs been onsidered to be effetive nd effiient (e.g., o et l., 26; rin et l., 24; English & olmer, 211; He et l., 212; Sorino et l., 214; Youngmn & Hekthorn, 1992). We monitored nd djusted slinities t lest every other dy by dding freshwter or se slt. Slinities were inresed grdully (by 1 2 g/kg every 2 dys) to void shok, nd ll slinity tretments were in fore fter 1 dys. Eight weeks lter, the number of S. europe nd S. sls survivors in eh pot ws ounted, boveground biomss hrvested, oven- dried t for 48 hr nd weighed. Plnt roots were rinsed in tp wter, oven- dried, nd weighed to quntify belowground biomss. We used one- wy NOVs followed by Tukey HSD multiple omprisons to test for the effets of different slinity tretments on popultion- level (bove- nd belowground biomss per pot) nd individul- level (bove- nd belowground biomss per plnt survivor) performnes of S. sls nd S. europe. Dt of S. sls belowground biomss per pot were squre root trnsformed to meet the normlity ssumption of NOV. Sued sls nd S. europe survivorship dt did not meet the normlity ssumption of NOV even fter norml trnsformtions, so Kruskl Wllis tests nd nonprmetri multiple omprisons (Dunn ll Pirs for Joint Rnking) were used insted. NOVs nd Kruskl Wllis tests were onduted using JMP 1 (SS Institute, ry, N). Optiml nd threshold slinity levels were determined using the brekpoints funtion (miniml segment size ws set to be 13; so eh segment would hve t lest dt from three slinity levels) in the struhnge pkge in R (R ore Tem, 215). We preferred to use the brekpoints method insted of the two- piee, threshold slope response funtion or the ompound disount funtion (Steppuhn, Vn Genuhten, & Grieve, 25) to determine optiml nd threshold slinity levels, s the response urves of the hlophytes we exmined here did not lwys follow tht of griulturl rops. 3 RESULTS t the popultion level, slinity tretments of <9 g/kg hd signifint effets on the survivl of neither S. sls nor S. europe (p >.5; Tble 1, Fig. 2). However, the effet of inresing slinities on S. sls survivl hd two brek points 5 nd g/kg, respetively (Tble 2): S. sls survivl slightly deresed with slinity tretments of > g/kg nd showed shrp delines when slinities inresed to 9 nd g/ kg, where ~3 nd 1% of S. sls plnts survived, respetively (Fig. 2). By ontrst, S. europe survivl ws not signifintly redued even in g/kg slinity tretments (Fig. 2), nd no brek point in the effet of inresing slinities on S. europe survivl ws found (Tble 2). For both S. europe nd S. sls, boveground biomss rehed pek (13% nd 12% of tht in g/kg slinity tretments, respetively) t low- slinity tretments (Tble 1, Fig. 3), lthough the optiml slinity ws higher (3 g/kg) for S. europe thn tht for S. sls (2 g/kg). Further higher slinities generlly deresed boveground biomss of both S. europe nd S. sls (Fig. 3). However, there were two brek points for S. sls 5 nd g/kg, respetively (Tble 2). Inresing slinities between 2 nd 5 g/kg nd between nd g/kg led to rpid delines in S. sls boveground biomss, while differenes in S. sls boveground biomss between slinity tretments of 5 nd g/kg were minor (Fig. 3). Sued sls belowground biomss ws grdully redued by inresing slinity, nd
4 HE et l TBLE 1 Summry of test sttistis for the effets of slinity tretments on different performne mesures of Sued sls nd Sliorni europe. ll tests were one- wy NOVs, exept tht Kruskl Wllis tests were used for survivorship of both S. sls nd S. europe nd for S. sls belowground biomss per pot Response vrible Sued sls Sliorni europe df F (χ 2 ) p df F (χ 2 ) p Survivorship < boveground biomss per pot 1, <.1 1, <.1 Belowground biomss per pot <.1 1, <.1 boveground biomss per survivor 1, <.1 1, <.1 Belowground biomss per survivor 1, <.1 1, <.1 Survivorship (%) b Sued Sliorni FIGURE 2 Effets of g/kg slinity tretments on the survivorship of Sued sls nd Sliorni europe. Dt re mens ± SE (n = 6). Within eh speies, dt points shring letter re not signifintly different from one nother (p >.5) Slinity (g/kg) TBLE 2 Brek points (slinity levels in g/kg) in the effet of inresing slinities on the survivorship nd growth of Sued sls nd Sliorni europe. N indites no brek points Response vrible Sued sls Survivorship 5; N boveground biomss per pot 2; 5; 3 Belowground biomss per pot N 3 boveground biomss per survivor N 3 Belowground biomss per survivor 7 3 Sliorni europe boveground biomss per pot Belowground biomss per pot b () B (b) B B B Sued Sliorni 12 B B B B b Slinity (g/kg) FIGURE 3 Effets of g/kg slinity tretments on the boveground () nd belowground (b) biomss of Sued sls nd Sliorni europe per pot. Dt re mens ± SE (n = 6). To filitte omprison between speies, biomss dt re shown s perentges of plnt performne in g/kg slinity tretments. Within eh speies, dt points shring letter re not signifintly different from one nother (p >.5) d B d d DE de E e there were no optiml or threshold responses. By ontrst, S. europe belowground biomss inresed up to 145% of tht in g/kg slinity tretments by inresing slinities up to 3 g/kg, nd generlly deresed with further higher slinities (Fig. 3b). When dt were nlyzed t the individul level for plnt survivors, we found generlly similr effets of slinity tretments (Fig. 4). However, high- slinity tretments between 5 nd g/kg hd generlly minor effets on bove- nd belowground biomss of S. europe nd S. sls plnts tht survived these slinity tretments, with bove- nd belowground biomss s high s 5% % of tht in g/kg slinity tretments. No brek point for S. sls boveground biomss ws deteted (Tble 2), lthough brek point of 7 g/kg ws found for belowground biomss (Tble 2): S. sls belowground biomss generlly deresed with inresing slinity before this slinity level, but slightly inresed fter this slinity level (Fig. 4b). 4 DISUSSION These results support our hypothesis tht both S. sls nd S. europe perform optimlly in low- slinity tretments (2 3 g/kg) nd n survive muh higher slinity stresses thn the highest slinity levels investigted in the mjority of pst plnt slinity tolerne studies (inluding studies on slt mrsh plnts). Our results lso show tht
5 633 HE et l. boveground biomss per survivor Belowground biomss per survivor () B B b (b) B B b B B b b B FIGURE 4 Effets of g/kg slinity tretments on the boveground (), nd belowground (b) biomss of Sued sls nd Sliorni europe per survivor. Dt re mens ± SE. To filitte omprison between speies, biomss dt re shown s perentges of plnt performne in g/kg slinity tretments. Within eh speies, dt points shring letter re not signifintly different from one nother (p >.5) S. europe hs greter pity to tolerte slinity stress thn does S. sls: S. europe n well survive slinities even exeeding g/kg, while S. sls hs slinity tolerne threshold of ~ g/kg, bove whih higher slinities led to shrp deline in survivl nd growth. Our findings from hypersline eosystem hve multiple importnt implitions for understnding plnt slinity tolernes nd their pplitions. 4.1 Slinity tolernes of S. sls nd S. europe Our results demonstrte the brod slinity tolerne of S. sls nd S. europe, showing tht both speies n survive muh higher levels of slinity stress thn previously reported. Pst studies suggested tht S. europe grow best t ~ g/kg slinity tretments (85 3 mmol/l Nl) nd then derese with inresing slinity (Moghieb, Sneok, & Fujit, 24; ghleh, Niknm, Ebrhimzdeh, & Rzvi, 29; Fn et l., 211; see Ktshnig et l., 213 for reent review on the slt tolerne of Sliorni spp.). In our study, however, the optiml slinity for S. europe ws higher t 3 g/kg. In nother study (rin et l., 24), lthough no optiml slinity ws found, S. europe biomss ws onsistently high mong slinity tretments rnging from to 7 g/kg. Egn nd Ungr (21) found B Sued (p <.1) Sliorni (p <.1) B DE Sued (p <.1) Sliorni (p <.1) Slinity (g/kg) E DE E tht S. europe biomss did not differ mong 5, 1, nd 2 g/kg slinity tretments. Gul, nsri, nd Khn (29) reported tht nother speies in the sme genus, Sliorni uthensis, grew best t ~35 g/kg slinity tretments in Pkistn slt desert. Differenes in speies dpttion, lol limte, nd experimentl methodology my ontribute to vrition in the reported optiml slinity. Studies fousing on plnt physiologil responses (e.g., ghleh et l., 29; Fn et l., 211; Moghieb et l., 24) often used Nl nd sterilized snd for slinity tretments nd grew plnts in limte hmbers, while eologil studies suh s ours nd rin et l. (24) often used se slt nd field- olleted soils nd grew plnts in glsshouse or outdoor ommon grden. lthough how slinity tretments were enfored nd mintined were generlly similr between our study nd rin et l. (24), multiple plnt individuls per pot were used in our study in ontrst to one per pot s used in rin et l. (24), nd our study my thus hve llowed individul- level vrition in plnt performne within slinity level to be redued nd therefore verge plnt performne better represented. Sued sls hs been less studied thn S. europe, but multiple pst studies lso reported tht S. sls performed best in low- slinity tretments (~3 12 g/kg) rther thn in g/kg slinity tretments nd then deresed by ~% 5% with inresing slinity up to 35 g/kg (Dun, Li, Liu, Ouyng, & n, 27; Song et l., 29, 211; see Song & Wng, 215 for reent review on the slt tolerne of S. sls), in brod greement with our results. However, the optiml slinity ws found to be higher in our study. s disussed bove, plnt physiologil studies suh s Song et l. (211) nd Dun et l. (27) often used Nl nd sterilized snd for slinity tretments nd grew plnts in limte hmbers, while eologil studies often used se slt nd field- olleted soils nd grew plnts in glsshouses or outdoor ommon grdens. The former hs the dvntge of fully ontrolled indoor experimentl settings, while the ltter hs the dvntge of better simulting nturl onditions. Indeed, our pst experiments under similr onditions (se slt nd field- olleted soil substrtes), but with limited rnge or number of slinity levels (He et l., 212, 215), found no differene in S. sls growth mong slinity tretments rnging from 2 to g/kg, lthough 9 g/kg slinity tretments substntilly redued S. sls growth by 7% 9%, generlly supporting the brod slinity tolerne we found in this experiment. 4.2 Importne of studying multiple plnt responses Our study highlights the importne of studying multiple plnt responses tht inlude survivl nd belowground biomss in understnding plnt slinity tolerne. Mny pst studies on slinity tolerne often exmined plnt growth using boveground biomss. Our results, however, suggest tht the effets of slinity on plnt survivl n remrkbly differ from those on plnt boveground biomss. Sued sls nd S. europe plnts tht survived high slinities were ble to mintin reltively high biomss. t high slinities, popultion- level biomss deline in S. sls ws primrily driven by plnt mortlity, not by redution in the biomss of surviving plnts.
6 HE et l Furthermore, lthough stimultion of boveground biomss by low slinities ws found for both speies, stimultion of belowground biomss ws found only for S. europe, not for S. sls. Stimultion of belowground growth by low slinities hs been previously reported for other slt mrsh plnts (Venbles & Wilkins, 1978). In ft, the effets of slinity on plnt belowground growth n vry s gretly s those on boveground growth (dm, 1993). Our finding of no slinity stimultion of S. sls belowground biomss grees with pst studies (Song et l., 29; Yng, Song, & Wng, 21), lthough ontrry results exist (Dun et l., 27; Liu, Dun, Li, Tdno, & Khn, 28; Song et l., 29). Even in these studies, nevertheless, growth stimultion by slinity ws often weker for belowground thn for boveground. In ontrst to S. sls, stimultion of S. europe belowground growth by low slinities ws more onsistent mong studies (ooper, 1982; Keiffer, Mrthy, & Ungr, 1994; Ungr et l., 1979). Differenes in root tolerne to slinity my be use of the lower slinity tolerne of S. sls survivl reltive to tht of S. europe. Our study foused on the effets of slinity on plnt survivl, bove- nd belowground growth, s the effets of slinity stress on seed germintion of S. sls nd S. europe hve been well studied. It hs been known tht seed germintion my require slinities to be lower. Indeed, while we found both S. sls nd S. europe grow optimlly t low- slinity onditions, seed germintion of both speies is often highest in freshwter rther thn in low- slinity tretments, nd generlly dereses with inresing slinity (Dun et l., 27; Ungr, 1977). For S. europe, it hs been found tht no seeds ould germinte in the 5.% Nl solutions (~5 g/kg) (Ungr, 1977). For S. sls, Dun et l. (27) found tht only ~6.3% of seeds germinted under 35 g/kg slinity tretments in omprison with 63.8% in g/kg slinity tretments. However, muh higher germintion rtes under highslinity tretments hve been reported in other studies. Song et l. (29) found tht S. sls seed germintion remined ~71% 88% in 35 g/kg slinity tretments. Li et l. (25) found tht 1% of S. sls brown seeds (S. sls hs dimorphi seeds brown nd blk; see Wng et l., 215; Song et l., 216; Zhou et l., 216) were still ble to germinte in 7 g/kg slinities, lthough shrp deline in germintion rte ourred between 35 nd 47 g/kg slinity tretments. In either se, high- slinity stress did not ffet the vibility of S. sls seeds, nd nongerminted seeds in high- slinity tretments germinted when slinity stress ws lowered (Dun et l., 27). 4.3 Inorporting thresholds into understnding plnt slinity tolerne Our results suggest tht S. europe nd S. sls hve muh greter pity to tolerte slinity stress thn mny other plnts. Previous omprtive studies lso found S. europe to be the most slt- tolernt mong nine mrsh plnts in southern New Englnd (rin et l., 24) nd 15 mrsh plnts in the Netherlnds (Rozem, Luppes, & Broekmn, 1985). He et l. (212) ompred the stress tolernes of S. sls nd Sued glu nd found S. sls to hve muh higher slinity tolerne. It is not surprising tht slt mrsh plnts, inluding Sprtin lterniflor, Btis mritime, nd Sliorni virgini, n survive slinities s high s ~5 g/kg (Guo & Pennings, 212). Our work on S. europe nd S. sls shows tht these plnt speies hve even higher slinity tolerne limits thn reported in pst studies. The brod slinity tolernes of S. europe nd S. sls hve been ttributed to their high N + nd l umultion pities. Both speies do not hve slt glnds or slt bldders, but hve multiple sodium omprtmentliztion mehnisms nd n umulte onsiderble mounts of N + nd l in their shoots (Lv et l., 212; Ushkov, Kovlev, Gribovsky, Dolgushev, & Tikhomirov, 25; Wng, Lüttge, & Rtjzk, 21). Importntly, lthough for both speies there re often nonliner reltionships between performne nd slinity stress, our study found tht there ws ritil tolerne threshold ( g/kg) for S. sls survivl. The shrp deline in S. sls survivorship under slinities of bove g/kg probbly resulted from root funtionl filures (see bove). lthough our group hs foused on the eology rther thn the physiology of these plnts, we enourge tht future studies investigte the physiologil mehnisms underlying suh thresholds. Similrly, Li et l. (25) lso found drsti deline in the germintion rte of S. sls seeds (brown seeds) under slinities of bove 35 g/kg. While we did not find slinity threshold for S. europe, rin et l. (24) found drsti deline in the growth of S. europe under slinities of bove 7 g/ kg. Thresholds in plnt slinity tolerne hve lso been reported in other studies, often in rops (Mggio, Rimondi, Mrtino, & De Psle, 27; Steppuhn et l., 25). In nturl systems, for exmple, Koyro (26) found slinity threshold of 8.75 g/kg for Plntgo oronopus, nd Koh, Shopmeyer, Kyhn- Hnsen, Mdden, nd Peters (27) found slinity thresholds of ~5 65 g/kg for three tropil segrsses. Threshold responses to slinity nd other stresses re likely ommon in mny eosystems. Given tht nthropogeni ftors inluding limte hnge, drought, nd freshwter resoure deline re inresing slinity stress in mny eosystems, gurding exeedne of slinity tolerne thresholds will be key to helping onserve these eosystems. 5 ONLUSIONS Our study shows tht (1) both S. sls nd S. europe, espeilly S. europe, hve muh broder slinity tolernes thn other plnts previously reported, (2) plnt survivl, bove- nd belowground biomss n hve remrkbly different responses to slinity, nd (3) there is nonliner, threshold response of S. sls to inresing slinity stress. Our findings highlight the gret potentil for these plnts to endure slinity stress, nd hve importnt implitions for understnding plnt slinity tolernes nd their pplitions. Sued sls nd S. europe hve been widely onsidered idel for revegettion nd remedition of slt- ffeted lnd (Rozem & Sht, 213; Song & Wng, 215). Our work suggests tht the potentil for using these speies to revegette nd restore slt- ffeted lnd my be greter thn previously thought. Our results lso emphsize tht suh prties should inorporte slinity tolerne thresholds nd void situtions tht exeed these thresholds vi proper site seletion, slinity redution, nd other mesures, so suess ould be mximized. Understnding slinity tolerne thresholds in plnts is n importnt first step to prtil
7 6332 HE et l. pplitions nd prediting nturl ommunity dynmis tht re lso ontingent on other ftors (e.g., ompetition nd herbivory; He et l., 215) tht ffet plnt performne. KNOWLEDGMENTS We thnk Prof. Junhong Bi for vluble omments. Funding ws provided by Ntionl Key Bsi Reserh Progrm of hin (213B436), Key Projet of Ntionl Nturl Siene Foundtion of hin (516391), nd Ntionl Siene Foundtion for Innovtive Reserh Group (51123). Q.H. ws the Edwrd S Stolrz Postdotorl Fellow nd ws supported by the Edwrd S Stolrz Foundtion. ONFLIT OF INTEREST None delred. REFERENES dm, P. (1993). Sltmrsh eology. mbridge: mbridge University Press. ghleh, M., Niknm, V., Ebrhimzdeh, H., & Rzvi, K. (29). Slt stress effets on growth, pigments, proteins nd lipid peroxidtion in Sliorni persi nd S. europe. Biologi Plntrum, 53(2), Bertness, M. D., Gough, L., & Shumwy, S. W. (1992). Slt tolernes nd the distribution of fugitive slt mrsh plnts. Eology, 73(5), Brook, B. W., Ellis, E.., Perring, M. P., Mky,. W., & Blomqvist, L. (213). Does the terrestril biosphere hve plnetry tipping points? Trends in Eology & Evolution, 28(7), o, W.-H., Liu, J., Zhou, Q.-Y., o, Y.-R., Zheng, S.-F., Du, B.-X., hen, S.- Y. (26). Expression of tobo ethylene reeptor NTHK1 lters plnt responses to slt stress. Plnt, ell & Environment, 29(7), ooper,. (1982). The effets of slinity nd wterlogging on the growth nd tion uptke of slt mrsh plnts. New Phytologist, 9(2), rin,. M., Sillimn, B. R., Bertness, S. L., & Bertness, M. D. (24). Physil nd bioti drivers of plnt distribution ross esturine slinity grdients. Eology, 85(9), ui, B.-S., He, Q., & n, Y. (211). ommunity struture nd bioti determinnts of slt mrsh plnt zontion vry ross topogrphi grdients. Esturies nd osts, 34(3), Dun, D. Y., Li, W. Q., Liu, X. J., Ouyng, H., & n, P. (27). Seed germintion nd seedling growth of Sued sls under slt stress. nnles Botnii Fennii, 44(3), Egn, T. P., & Ungr, I.. (21). ompetition between Sliorni europe nd triplex prostrt (henopodiee) long n experimentl slinity grdient. Wetlnds Eology nd Mngement, 9(6), English, J. P., & olmer, T. D. (211). Slinity nd wterlogging tolernes in three stem- suulent hlophytes (Tetiorni speies) from the mrgins of ephemerl slt lkes. Plnt nd Soil, 348(1 2), Fn, P., Feng, J., Jing, P., hen, X., Bo, H., Nie, L., Li, Y. (211). oordintion of rbon fixtion nd nitrogen metbolism in Sliorni europe under slinity: omprtive proteomi nlysis on hloroplst proteins. Proteomis, 11(22), Flowers, T. J., & olmer, T. D. (28). Slinity tolerne in hlophytes. New Phytologist, 179(4), Flowers, T. J., & olmer, T. D. (215). Plnt slt tolerne: dpttions in hlophytes. nnls of Botny, 115(3), Flowers, T. J., Gll, H. K., & Bromhm, L. (21). Evolution of hlophytes: Multiple origins of slt tolerne in lnd plnts. Funtionl Plnt Biology, 37(7), Greenwy, H., & Munns, R. (19). 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Slt tolerne in the hlophyte Sliorni dolihosthy Moss: Growth, morphology nd physiology. Environmentl nd Experimentl Botny, 92, Kushl, S. S., Groffmn, P. M., Likens, G. E., Belt, K. T., Stk, W. P., Kelly, V. R., Fisher, G. T. (25). Inresed sliniztion of fresh wter in the northestern United Sttes. Proeedings of the Ntionl demy of Sienes of the United Sttes of meri, 12(38), Keiffer,. H., Mrthy, B.., & Ungr, I.. (1994). Effet of slinity nd wterlogging on growth nd survivl of Sliorni europe L., n inlnd hlophyte. Ohio Journl of Siene, 94(3), Khn, M.., Ungr, I.., & Showlter,. M. (2). The effet of slinity on the growth, wter sttus, nd ion ontent of lef suulent perennil hlophyte, Sued frutios (L.) Forssk. Journl of rid Environments, 45(1), Koh, M., Shopmeyer, S., Kyhn-Hnsen,., Mdden,., & Peters, J. (27). Tropil segrss speies tolerne to hyperslinity stress. quti Botny, 86(1), Koyro, H.-W. (26). 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8 HE et l Liu, X., Dun, D., Li, W., Tdno, T., & Khn, M.. (28). omprtive study on responses of growth nd solute omposition in hlophytes Sued sls nd Limonium biolor to slinity. In M.. Khn, & D. J. Weber (Eds.), Eophysiology of high slinity tolernt plnts (pp ). Dordreht: Springer. Löfgren, S. (21). The hemil effets of deiing slt on soil nd strem wter of five thments in southest Sweden. Wter, ir, nd Soil Pollution, 13(1 4), Lv, S., Jing, P., hen, X., Fn, P., Wng, X., & Li, Y. (212). Multiple omprtmentliztion of sodium onferred slt tolerne in Sliorni europe. Plnt Physiology nd Biohemistry, 51, Mggio,., Rimondi, G., Mrtino,., & De Psle, S. (27). Slt stress response in tomto beyond the slinity tolerne threshold. Environmentl nd Experimentl Botny, 59(3), Moghieb, R. E., Sneok, H., & Fujit, K. (24). Effet of slinity on osmoti djustment, glyinebetine umultion nd the betine ldehyde dehydrogense gene expression in two hlophyti plnts, Sliorni europe nd Sued mritim. Plnt Siene, 166(5), Munns, R., & Tester, M. (28). Mehnisms of slinity tolerne. nnul Review of Plnt Biology, 59, Musolo,., Pnuio, M., & Piernik,. (214). Eology, distribution nd eophysiology of Sliorni europe L. In M.. Khn, B. Böer, M. Öztürk, T. Z. l bdesslm, M. lüsener-godt, & B. Gul (Eds.), Sbkh eosystems: Volume IV: sh rop hlophyte nd biodiversity onservtion (pp ). Dordreht: Springer. Prid,. K., & Ds,. B. (25). Slt tolerne nd slinity effets on plnts: review. Eotoxiology nd Environmentl Sfety, (3), Pennings, S.., & Bertness, M. D. (21). Slt mrsh ommunities. In M. D. Bertness, S. Gines, & M. Hy (Eds.), Mrine ommunity eology (pp ). Sunderlnd, M: Sinuer ssoites. Pennings, S.., & llwy, R. M. (1992). Slt mrsh plnt zontion: The reltive importne of ompetition nd physil ftors. Eology, 73(2), Phleger,. F. (1971). Effet of slinity on growth of slt mrsh grss. Eology, 52(5), R ore Tem (215). R: lnguge for sttistil omputing. Vienn, ustri: R Foundtion for Sttistil omputing. Redondo-Gómez, S., Mteos-Nrnjo, E., Dvy,. J., Fernández-Muñoz, F., stellnos, E. M., Luque, T., & Figuero, M. E. (27). Growth nd photosyntheti responses to slinity of the slt- mrsh shrub triplex portuloides. nnls of Botny, (3), Rengsmy, P. (26). World sliniztion with emphsis on ustrli. Journl of Experimentl Botny, 57(5), Rozem, J., Luppes, E., & Broekmn, R. (1985). Differentil response of sltmrsh speies to vrition of iron nd mngnese. Vegettio, 62(1 3), Rozem, J., & Sht, H. (213). Slt tolerne of hlophytes, reserh questions reviewed in the perspetive of sline griulture. Environmentl nd Experimentl Botny, 92, Shumwy, S. W., & Bertness, M. D. (1992). Slt stress limittion of seedling reruitment in slt mrsh plnt ommunity. Oeologi, 92(4), Song, J., hen, M., Feng, G., Ji, Y., Wng, B., & Zhng, F. (29). Effet of slinity on growth, ion umultion nd the roles of ions in osmoti djustment of two popultions of Sued sls. Plnt nd Soil, 314(1 2), Song, J., Shi, G., Go, B., Fn, H., & Wng, B. (211). 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Orgn speifi responses of vuolr H + - TPse in the shoots nd roots of 3 hlophyte Sued sls to Nl. Journl of Integrtive Plnt Biology, 52(3), Yeo,., & Flowers, T. (19). Slt tolerne in the hlophyte Sued mritim L. Dum.: Evlution of the effet of slinity upon growth. Journl of Experimentl Botny, 31(4), Youngmn,. L., & Hekthorn, S.. (1992). Effet of slinity on wter reltions of two growth forms of Sued leoliformis. Funtionl Eology, 6(6), Zhou, J.., Fu, T. T., Sui, N., Guo, J. R., Feng, G., Fn, J. L., & Song, J. (216). The role of slinity in seed mturtion of the euhlophyte Sued sls. Plnt Biosystems, 15(1), How to ite this rtile: He Q, Sillimn BR, ui B. Inorporting thresholds into understnding slinity tolerne: study using slt- tolernt plnts in slt mrshes. Eol Evol. 217;7:
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