M any species are changing their distributions in response to climate change, such as elevational upper

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1 OPEN SUBJECT AREAS: COMMUNITY ECOLOGY ENVIRONMENTAL SCIENCES Received 17 Novemer 14 Accepted 28 Jnury 15 Pulished 27 Ferury 15 Correspondence nd requests for mterils should e ddressed to B.S.C. (cuis@nu. edu.cn) * Current ddress: Division of Mrine Science nd Conservtion, Nichols School of the Environment, Duke University, 135 Duke Mrine L Rod, Beufort 28516, North Crolin, USA. Multiple mechnisms sustin plnt-niml fcilittion on costl ecotone Qing He* & Boshn Cui School of Environment, Stte Key Lortory of Wter Environment Simultion, Beijing Norml University, Beijing 1875, Chin. Theory suggests tht species distriutions re expnded y positive species interctions, ut the importnce of fcilittion in expnding species distriutions t physiologicl rnge limits hs not een widely recognized. We investigted the effects of the nurse shru Tmrix chinensis on the cr Helice tientsinensis on the terrestril orders of slt mrshes, typicl costl ecotone, where Tmrix nd Helice were on their lower nd upper elevtionl distriution edges, respectively. Cr urrows were undnt under Tmrix, ut were sent in open res etween Tmrix. Removing Tmrix decresed ssocited cr urrows with time, while simulting Tmrix in open res y shding, excluding predtors, nd dding Tmrix rnches s cr food, incresed cr urrows. Mesurements of soil nd microclimte fctors showed tht removing Tmrix incresed iotic stress, while simulting Tmrix y shding decresed iotic stress. Survivl of tethered crs ws high only when protected from desicction nd predtion. Thus, y lleviting iotic nd iotic stresses, s well s y food provision, Tmrix expnded the upper intertidl distriution of Helice. Our study provides cler evidence for the importnce of fcilittion in expnding species distriutions t their rnge limits, nd suggests tht fcilittion is crucil iologicl force mintining the ecotones etween ecosystems. M ny species re chnging their distriutions in response to climte chnge, such s elevtionl upper limits of lpine 1 nd intertidl species 2. Predicting species distriution chnges, however, needs to incorporte species interctions tht cn lter species individulistic responses to environmentl chnge 3,4. Negtive nd positive species interctions oth ffect community dynmics, nd their reltive importnce chnges with environmentl stress, with fcilittion more prevlent in stressful thn in enign environments 5,6. Although fcilittion is suggested to expnd the distriutions nd relized niche of species 7,8, the importnce of fcilittion in expnding species distriutions t their physiologicl rnge limits remins not widely recognized or tested in the field. An idel hitt to exmine this role of fcilittion is ecotone, which is the trnsitionl re etween different ecosystems. Ecotones, such s terrestril orders of slt mrshes in the intertidl 9 11 nd lpine treelines 12,13, re species distriution edges where species dpted to their ntive ecosystems fce environmentl stress of their tolernce limits. Here, we exmine fcilittion y nurse plnt on distriution expnsion of cr on the terrestril orders of slt mrshes. Although fcilittion theory pplies to oth plnts nd nimls, it hs only een extensively investigted in plnt communities 6. Plnt-plnt fcilittion is widely known to e owing to llevition of oth iotic (e.g. wter, slinity) nd iotic (e.g. herivory) stresses, while plnt-niml fcilittion is often ttriuted to llevition of iotic stress, prticulrly in physiclly stressful intertidl ecosystems where consumer pressure is trditionlly thought to e low 14. For exmple, plnt-niml fcilittions on high rocky intertidl shores re often ttriuted to llevition of desicction stress 15, rther thn ssocitionl defense, ecuse on rocky shores predtion is often high only in the low intertidl. Similrly, plnt-niml fcilittions in slt mrshes were lso ttriuted to the llevition of iotic stress This is contrry to studies of sutidl ecosystems, such s segrss eds, kelp forests, nd corl reefs, where predtion hs long een known to drive plnt-niml fcilittions 18. Although predtion in intertidl hitts cn e high, prticulrly y moile species such s vin predtors 17,21,itis generlly ignored in plnt-niml fcilittion investigtions. Furthermore, previous studies often ttriute plnt-niml fcilittion to llevition of either iotic (e.g. wter, slinity) or iotic (e.g. herivory) stresses, which re not mutully exclusive. Field investigtions of whether these two mechnisms of fcilittion cn coexist remin very few (ut see Refs. 22, 23), however. Additionlly, lthough plnts my e food resource for SCIENTIFIC REPORTS 5 : 8612 DOI: 1.138/srep8612 1

2 their intercting nimls, few studies hve disentngled the roles of food provision vs. non-trophic fcilittion y plnts on nimls 24. We report two-yer field experiments exmining the interctions etween the shru Tmrix chinensis nd the cr Helice tientsinensis on the terrestril orders of two northern Chinese slt mrshes (see Methods). These orders re typicl costl ecotone 1, which is flooded only during spring nd storm tides, nd re dry nd hypersline, leding to extreme therml nd desicction stress for mrine nimls 9,16,17. Tmrix is nurse shru distriuted in costl uplnds without tides. Although Tmrix persists on the terrestril orders, it is sent from lower mrshes 9. In contrst, Helice is cr found minly in intertidl mrsh hitts, nd is sent from costl uplnds 25,26. On the terrestril orders, oth Tmrix nd Helice re on their hitt edges. Helice urrows re undnt under Tmrix, ut sent in open res etween Tmrix. We conducted Tmrix removl, Tmrix simultion nd cr tethering experiments to test the following hypotheses: (1) Tmrix is criticl fctor in expnding Helice distriutions on the physiologicl rnge limits, nd (2) the fcilittive effects of Tmrix on Helice re due to llevition of oth iotic nd iotic stresses (i.e. ssocitionl defense ginst predtion). Results At oth sites, cr urrows were generlly sent in open res, ut were dense under Tmrix (Fig. 1). At the eginning of the Tmrix removl experiment, there ws no significnt difference in urrow density etween Tmrix nd Tmrix removl plots (P..5; Fig. 1). Removing Tmrix led to grdul decreses in cr urrows, nd decresed y.5% fter two yers (Fig. 1). Tmrix removl significntly elevted solr rdition, soil temperture, nd ir temperture nd humidity to levels similr to open plots ut significntly different from Tmrix plots (Fig. 2). Soil slinity ws significntly higher in open thn in Tmrix plots in Septemer, ut not in My (Fig. 3). In contrst, soil moisture ws significntly lower in open thn in Tmrix plots in Septemer, ut not in My (Fig. 3). At the eginning of the experiment, there ws no difference in soil slinity nd moisture etween in Tmrix nd removl plots (Fig. 3). Removing Tmrix incresed soil slinity nd decresed soil moisture to levels similr to open plots ut signficntly different from Tmrix plots (Fig. 3). Simultion of Tmrix s shding nd predtion-protection using shde houses significntly incresed cr urrows in open res (Fig. 4; F 1, 5 9.8, P,.1). Addition of Tmrix s cr food lso significntly incresed cr urrows in open res (Fig. 4; F 1, 5 7.2, P 5.15). There were no significnt interctive effects of shde house nd food ddition on cr urrows (Fig. 4; F 1, 5.4, P 5.84). Differences were lso not found in the numer of cr urrows etween procedurl control nd control tretments (df 5 1, x , P 5.59). Shding open res with shde houses significntly decresed solr rdition, soil nd ir temperture, ir humidity nd soil slinity, nd incresed soil moisture, ll of which ecme similr to Tmrix plots ut different from open plots (P,.5, Supplementry Fig. S1; lso see Figs. 2 nd 3). Survivorship of crs tethered in Tmrix plots ws 6% (Fig. 5), significntly higher thn in open plots (P 5.46) nd cge plots (P 5.46), ut not significntly different from shde-house plots (P Density of cr urrows (ind./2.25m 2 ) Density of cr urrows (ind./2.25m 2 ) A Hunghekou B Yiqin er c c c c Smpling time Tmrix plot Tmrix removl plot c 12/5 12/9 13/5 13/8 13/9 PAR (1 μmol/m 2 s) Air temperture ( C) A C Tmrix plot Tmrix removl plot Soil temperture ( C) Air humidity (%) Tmrix plot Smpling re B D c Tmrix removl plot Figure 1 Tmrix removl experiment: density of cr urrows in ech tretment t Hunghekou (A) nd Yiqin er (B). Dt re mens 6 SE (n 5 1). Within ech smpling time, rs shring letter re not significntly different from one nother (P..5; Tukey HSD multiple comprisons). Figure 2 Tmrix removl experiment: microclimte fctors in ech tretment t Hunghekou. (A), Photosyntheticlly ctive rdition (PAR); (B), soil temperture; (C), ir temperture; nd (D), ir humidity. Dt re mens 1 SE (n 5 1). Brs shring letter re not significntly different from one nother (P..5). SCIENTIFIC REPORTS 5 : 8612 DOI: 1.138/srep8612 2

3 Soil slinity (PSU) 3 1 A Hunghekou c Tmrix plot Tmrix removl plot C Yiqin er c Soil moisture (%) B D 16 12/5 12/9 13/5 13/9 12/5 12/9 13/5 13/9 Smpling time Smpling time Figure 3 Tmrix removl experiment: soil condition in ech tretment t Hunghekou nd Yiqin er. (A) nd (C), Soil slinity; (B) nd (D), soil moisture. Dt re mens 6 SE (n 5 1). Within ech smpling time, rs shring letter re not significntly different from one nother (P..5). 5.67). All crs in open nd cge plots were ded. All ded crs in cge plots (s well s in Tmrix nd shde-house plots) were intct, indicting tht the deth ws minly cused y iotic stress. In contrst, ll ded crs in open plots hd missing ody prts nd crushed crpces, which, long with the presence of ird feces nd footprints, indictes tht predtion cused the deth. Discussion Our results revel tht Helice is dependent on Tmrix on the terrestril orders of slt mrshes, nd tht this dependence is not only ecuse Tmrix is food resource for Helice, ut lso strongly due to non-trophic fcilittion. Thus, in the costl ecotone, fcilittion expnds the lndwrd distriution of mrsh crs. Our work provides n unmiguous demonstrtion for the criticl role of fcilittion in mediting species distriutions in nturl communities, nd in mintining ecotones. Fcilittion nd species rnge expnsion t physiologicl rnge limits. Our results show tht therml nd desicction stresses on the terrestril orders of slt mrshes re extreme nd lethl to Helice (tethered Helice without shding ll died, nd Helice urrows re sent in open res). Where Tmrix occurs, shding y its cnopy retins soil moisture nd decreses therml nd desicction stress, creting microhitts tht re physiclly suitle to Helice. Therml nd desicction stresses re the mjor iotic fctors limiting the distriution of mrine nimls in the upper intertidl, nd llevition of these stresses y shding hs commonly een found Density of cr urrows (ind./m 2 ) No food Addition of food Percentge Ded - Predtion Ded - Dessiction Alive Prd. control Control Shde house Tretments Figure 4 Tmrix simultion experiment: density of cr urrows in ech tretment. Dt re mens 1 SE (n 5 6). Prd. control indictes procedurl control. Open Cge Shde house Tmrix Tretments Figure 5 Cr tethering experiment: proportion of ded (y desicction or predtion) nd live crs in ech tretment. SCIENTIFIC REPORTS 5 : 8612 DOI: 1.138/srep8612 3

4 to drive their fcilittive interctions 15,16. Although it hs een rgued tht fcilittion should collpse with extreme stress due to diminished effects of neighors, or switch to competition for limiting resources (reviewed in Ref. 8), our results provide no support for these rguments (lso see Ref. 27). The two species studied in our work re on different trophic levels nd do not compete for limiting resources nywy. Although dult Tmrix persist on the terrestril orders of slt mrshes, iotic stress such s slinity strictly limits its growth nd regenertion 9. This suggests tht even in hitts where enefctor species themselves re severely limited 28, fcilittion cn still function s structuring force of communities. Our work provides strightforwrd exmple of how fcilittion expnds species relized niche t their verticl distriution limits. Fcilittion y Tmrix drives the expnsion of the distriution of Helice from mrshes t low elevtions to the upper terrestril order. Without Tmrix, the distriution of Helice would retrct to lower elevtions tht re more frequently flooded. Fcilittion hs lso een shown to expnd the high intertidl orders of lge nd invertertes 15, the low intertidl limits of mrsh plnts 9,29, the rid orders of plnts in dry hitts 8,3, nd the lndwrd expnsion of mngroves 31. Our work, together with these studies, support the hypothesis tht including fcilittion in niche theory leds to species relized niches eing lrger thn their fundmentl niches 7,8. Biotic drivers of plnt-niml fcilittion in physiclly stressful hitts. Our results lso show tht in ddition to llevition of iotic stress, Tmrix s ssocitionl defense ginst predtion is mechnism of fcilittion of Helice. Mny seirds such s terns re undnt t our study sites nd feed on Helice. It is lso known tht some seirds prefer to feed in unvegetted hitts, possily due to the ese of wlking nd ttcking without vegettion (see Ref. 17). The existence of Tmrix on the lrgely re terrestril orders thus reduces Helice s risk of predtion. A previous study lso suggested tht the fcilittion effects of vegettion on fiddler crs in hypersline mrshes in Georgi (USA) is likely to due to ssocition defense ginst vin predtors 17, ut hd no experimentl tests. Bortolus, et l. 16 lso conducted cr tethering experiment in n Argentinen high mrsh, ut found no evidence for plnt ssocitionl defense s mechnism of plnt fcilittion on crs. This my hve een due to the fct tht their tethering experiments lsted only few hours nd this my not hve een long enough to detect predtion. Avin predtors, even those resident in n re, re often not continuously present nd my move round quite it. Since predtion is potentilly high in mny physiclly stressful hitts including the high intertidl 21,32, our work emphsizes the overlooked importnce of ssocitionl defense in plnt-niml fcilittions in these hitts. Highlighting the importnce of fcilittion in ecotones. The importnce of fcilittion in the costl ecotone demonstrted in our study is consistent with other studies on other types of ecotones, such s steppe-woodlnd 33,34, lpine treeline 12,13, nd open wter-lke shore ecotones 35. Ecotones re often ioticlly extreme to species originted from t lest one of the djcent ecosystems 12 or oth (our study). These species re le to persist on ecotones where neighors meliorte iotic stress to their physiologicl tolernce rnge, while eyond the ecotones they re limited y iotic stress. Associtionl defenses cn lso e mechnism driving fcilittion on ecotones. For exmple, ecotones etween open wter nd lke shores provide refugi for fish tht would e t risk of predtion in open wters or desicction stress on lke shores 35. Other mechnisms lso likely occur, such s entrpment of propgules 31. Ecotones hve een long known s iodiversity hotspots, nd our study together with these previous studies suggest tht fcilittion is likely one of the key iologicl forces enhncing diversity in ecotones 36. Ecotones re often species oundries sensitive to environmentl chnge, nd hve een widely used for monitoring the effects of climte chnge 1. Future reserch on fcilittion nd community orgniztion on species distriution orders or ecotones will e criticl to understnding how environmentl chnge ffects nturl communities. Methods Study sites. Field work ws conducted on the terrestril orders of two slt mrshes in the Yellow River Delt, northern Chin: Hunghekou (37u439 N, 119u149 E) nd Yiqin er (38u59 N, 118u429 E). The climte is temperte monsoonl, with cool, dry springs nd hot, riny summers. The long-term nnul precipittion is mm, nd the verge temperture is 12.8uC 37. The terrestril orders t oth sites were re flts, with scttered Tmrix trees nd Sued sls (Linneus) Plls, n nnul succulent. These orders re typiclly dry nd extremely sline (slinities. 1 PSU), hving lyer of slt on the soil surfce. Tmrix is shruy recretohlophyte tht inhits costl nd riprin zones in Est Asi (ntive) nd North Americ (invsive 38 ). In the Yellow River Delt, Tmrix is sent from flooded mrsh hitts t lower elevtions, ut is undnt on the orders etween mrshes nd terrestril uplnds t upper elevtions 9,39. Tmrix lso occurs in terrestril uplnds, ut is limited y competition from perennil grsses 9. Helice is grpsoid cr common in Est Asi, nd is primrily herivorous 26,. The distriution of Helice long intertidl grdients in the Yellow River Delt hs een previously quntified 41,42. Helice occurs in low undnces in flooded mudflts nd low mrshes t low elevtions where other crs (e.g., Mcrophthlmus jponics) re dominnt. At higher mrshes, Helice ecomes undnt, eing the only common cr species there. On the terrestril orders t upper elevtions, Helice occurs only under the cnopies of Tmrix trees. Helice is completely sent from terrestril uplnds eyond tidl influence. Common vin predtors include Lrus spp., Stern spp. nd Arde spp. 43, which forge on the terrestril orders of slt mrshes nd nery wter odies (Qing He, personl oservtion). Tmrix removl experiment. To test the hypothesis tht removing Tmrix would reduce the density of cr urrows, we performed removl experiment in My 12. We mrked 1 locks on the terrestril order t ech site. Within ech lock, we rndomly selected two Tmrix trees with m 2 cnopies (.3 5 m etween trees), nd cut down one of the two trees t the soil surfce. We estlished permnent m plot centered t the se of ech Tmrix tree, nd m plot in open res etween trees within ech lock. Removl tretments were mintined monthly s necessry. We counted numer of cr urrows in ech plot in My, Septemer 12 nd Septemer 13 t oth sites, nd lso in My nd August 13 t Hunghekou. We estimted cr undnce y quntifying the density of cr urrows, which followed previous studies from similr hitts 16,17,25,44. We exmined differences in cr urrow density mong tretments t ech site nd smpling dte with rndomized-locked ANOVAs followed y Tukey HSD multiple comprisons t the significnce level P,.5. All sttisticl nlysis ws done with JMP 1 (SAS Institute, NC, USA). Edphic nd microclimte conditions were quntified following Tmrix removl. Soil cores (5.5 cm dimeter 3 5 cm depth) were collected in ech plot in My nd Septemer 12 nd 13. To determine soil moisture, soil cores were weighed, ovendried t 6uC for 48 hours, nd reweighed. Soil slinity ws determined using the initil soil moisture content nd the slinity of the wter extrct from the soil cores (determined using conductivity meter; model JENCO 31, Shnghi, Chin) 45. Photosyntheticlly ctive rdition (PAR), ir temperture, ir humidity, nd soil temperture were quntified t 11: 13: on cloudless dy in erly Septemer 12. PAR, ir temperture, nd ir humidity were quntified cm ove the soil surfce with quntum light meters (model 3415, Spectrum Technologies, Auror, IL, USA) nd temperture/reltive humidity pens (Spectrum Technologies), nd soil temperture 5 cm elow the soil surfce with soil thermometer (model 631, Spectrum Technologies) 46. Differences in edphic/microclimte fctors etween tretments on ech dte were nlyzed with rndomized-locked ANOVAs followed y Tukey HSD multiple comprisons. Soil slinity nd moisture dt were log 1 (x)- nd (x) 3 -trnsformed, respectively, to increse normlity when necessry. Tmrix simultion experiment. To test the hypothesis tht the dependence of Helice on Tmrix is due to fcilittion y shding nd predtion-protecting, s well s due to food provision, we conducted shru simultion experiment crossing shde house nd food ddition tretments. In My 12, we locted plots in open res t Hunghekou, nd rndomly ssigned 6 to ech of the five tretments: shde house, food ddition, shde house plus food ddition, control, nd procedurl control. Plots ssigned to shde house tretments were covered y shde cloth ( m, l 3 w 3 h) on ll sides. PAR in the shde houses rnged from 1 to 3 mmol/m 2?s, which ws comprle to those under the trees (3 2 mmol/m 2?s). Shde house tretments lso excluded ird ccess, nd no ird footprints/feces were oserved within these plots. To llow cr ccess, shde cloth ws 1 15 cm ove the soil surfce. Procedurl controls hd shde cloth only on two sides. For food ddition tretments, five live 3 cm long Tmrix rnches were cut, tied t one end, nd plced in the center of the plot, nd were replced t lest weekly throughout the experiment. We counted the numer of cr urrows in ech plot in mid-septemer. The experiment ws discontinued in the following yer, due to potentil winter ice nd humn dmge. We exmined the seprte nd interctive effects of shde house nd food ddition on numer of cr urrows (sqrt-trnsformed) with two-wy SCIENTIFIC REPORTS 5 : 8612 DOI: 1.138/srep8612 4

5 ANOVA, nd differences etween control nd procedurl control tretments with Wilcoxon test. To quntify the effects of shde tretments on edphic nd microclimte conditions, we determined soil slinity, soil moisture, PAR, ir temperture, ir humidity, nd soil temperture in ech plot in Septemer, using the sme methods s descried ove. We exmined differences in ech fctor etween tretments using nonprmetric multiple comprisons for ir temperture dt (Dunn method for joint rnks; the ir temperture dt did not meet the normlity ssumptions of prmetric tests) nd Tukey HSD multiple comprisons for ll others. Cr tethering experiment. To test the hypothesis tht Tmrix s llevition of oth iotic stress nd predtion is criticl to the fte of Helice on the terrestril orders of slt mrshes, we conducted cr tethering experiment. In August 12, we tethered Helice (crpce width mm; hnd collected in the field) on the terrestril order t Hunghekou. We plced tethered cr in the center of ech of 24 open re plots, 12 Tmrix plots nd the 12 shded plots used in the shru simultion experiments. Crs in hlf of the open re plots were protected from predtion with cges ( cm) of glvnized-steel hrdwre cloth (7 mm mesh size). Tethers were constructed of 15 cm long fishing line, tied round the crpce of crs, secured to the crpce with cynocrylic glue, nd held y steel stkes pushed flush with the soil surfce 16. We deployed Helice t dusk, nd exmined their survivorship fter 24 hours. Crs tht died from either desicction stress (with intct ody) or predtion (with dismemered ody nd presence of ird footprints) were counted. Tretment differences in survivorship were nlyzed with chi-squre tests (Fisher s exct test). 1. Lenoir, J., Gegout, J., Mrquet, P., De Ruffry, P. & Brisse, H. A significnt upwrd shift in plnt species optimum elevtion during the th century. Science 3, (8). 2. Hrley, C. D. G. Climte chnge, keystone predtion, nd iodiversity loss. Science 334, (11). 3. Suttle, K. B., Thomsen, M. A. & Power, M. E. Species interctions reverse grsslnd responses to chnging climte. Science 315, (7). 4. Brooker, R. W., Trvis, J. M., Clrk, E. J. & Dythm, C. Modelling species rnge shifts in chnging climte: the impcts of iotic interctions, dispersl distnce nd the rte of climte chnge. J. Theor. Biol. 245, (7). 5. Bertness, M. D. & Cllwy, R. Positive interctions in communities. Trends Ecol. Evol. 9, (1994). 6. He, Q., Bertness, M. D. & Altieri, A. H. Glol shifts towrds positive species interctions with incresing environmentl stress. Ecol. Lett. 16, (13). 7. Bruno, J. F., Stchowicz, J. J. & Bertness, M. D. Inclusion of fcilittion into ecologicl theory. Trends Ecol. Evol. 18, (3). 8. He, Q. & Bertness, M. D. Extreme stresses, niches, nd positive species interctions long stress grdients. Ecology 95, (14). 9. He, Q., Cui, B. & An, Y. The importnce of fcilittion in the zontion of shrus long costl slinity grdient. J. Veg. Sci. 22, (11). 1. Wsson, K., Woolfolk, A. & Fresquez, C. Ecotones s indictors of chnging environmentl conditions: rpid migrtion of slt mrsh uplnd oundries. Estur. Cost 36, (13). 11. Trut, B. H. The role of costl ecotones: cse study of the slt mrsh/uplnd trnsition zone in Cliforni. J. Ecol. 93, (5). 12. Btllori, E., Cmrero, J. J., Ninot, J. M. & Gutiérrez, E. Seedling recruitment, survivl nd fcilittion in lpine Pinus uncint tree line ecotones. Implictions nd potentil responses to climte wrming. Glol Ecol. Biogeogr. 18, (9). 13. Smith, W. K., Germino, M. J., Hncock, T. E. & Johnson, D. M. Another perspective on ltitudinl limits of lpine timerlines. Tree Physiol. 23, (3). 14. Menge, B. A. & Sutherlnd, J. P. Community regultion: vrition in disturnce, competition, nd predtion in reltion to environmentl stress nd recruitment. Am. Nt. 13, (1987). 15. Bertness, M. D., Leonrd, G. H., Levine, J. M., Schmidt, P. R. & Ingrhm, A. O. Testing the reltive contriution of positive nd negtive interctions in rocky intertidl communities. Ecology 8, (1999). 16. Bortolus, A., Schwindt, E. & Irirne, O. Positive plnt-niml interctions in the high mrsh of n Argentinen costl lgoon. Ecology 83, (2). 17. Nomnn, B. E. & Pennings, S. C. Fiddler cr vegettion interctions in hypersline hitts. J. Exp. Mr. Biol. Ecol. 225, (1998). 18. Peterson, C. H. Clm predtion y whelks (Busycon spp.): experimentl tests of the importnce of prey size, prey density, nd segrss cover. Mr. Biol. 66, (1982). 19. Witmn, J. D. Sutidl coexistence: storms, grzing, mutulism, nd the zontion of kelps nd mussels. Ecol. Monogr. 57, (1987).. Stchowicz, J. J. & Hy, M. E. Mutulism nd corl persistence: the role of herivore resistnce to lgl chemicl defense. Ecology 8, (1999). 21. Ellis, J. C., Shulmn, M. J., Wood, M., Witmn, J. D. & Lozynik, S. Regultion of intertidl food wes y vin predtors on New Englnd rocky shores. Ecology 88, (7). 22. Angelini, C. & Sillimn, B. R. Secondry foundtion species s drivers of trophic nd functionl diversity: evidence from tree epiphyte system. Ecology 95, (14). 23. Dijkstr, J. A., Boudreu, J. & Dionne, M. Species-specific medition of temperture nd community interctions y multiple foundtion species. Oikos 121, (12). 24. Wright, J. T., Byers, J. E., DeVore, J. L. & Sotk, E. E. Engineering or food? Mechnisms of fcilittion y hitt-forming invsive seweed. Ecology 95, (14). 25. He, Q., Altieri, A. H. & Cui, B. Herivory drives zontion of stress-tolernt mrsh plnts. Ecology, doi:1.189/ (15). 26. Liu, W. L. & He, W. S. The Benthic Mcro-invertertes in the Yngtze Estury (Shnghi Science nd Technology Press, 7). 27. Pugnire, F. I., Zhng, L., Li, R. & Luo, T. No evidence of fcilittion collpse in the Tietn plteu. J. Veg. Sci. doi:1.1111/jvs (15). 28. Brooker, R. W. et l. Fcilittion in plnt communities: the pst, the present, nd the future. J. Ecol. 96, (8). 29. Hcker, S. D. & Bertness, M. D. Morphologicl nd physiologicl consequences of positive plnt interction. Ecology 76, (1995). 3. Arms, C., Rodríguez-Echeverrí, S. & Pugnire, F. I. A field test of the stressgrdient hypothesis long n ridity grdient. J. Veg. Sci. 22, (11). 31. Peterson, J. M. & Bell, S. S. Tidl events nd slt-mrsh structure influence lck mngrove (Avicenni germinns) recruitment cross n ecotone. Ecology 93, (12). 32. Frix, M. S., Hostetler, M. E. & Bildstein, K. L. Intr- nd interspecies differences in responses of Atlntic snd (Uc pugiltor) nd Atlntic mrsh (U. pugnx) fiddler crs to simulted vin predtors. J. Crustcen Biol. 11, (1991). 33. Kitzerger, T., Steinker, D. F. & Velen, T. T. Effects of climtic vriility on fcilittion of tree estlishment in northern Ptgoni. Ecology 81, (). 34. Dios, V. R., Weltzin, J. F., Sun, W., Huxmn, T. E. & Willims, D. G. Trnsitions from grsslnd to svnn under drought through pssive fcilittion y grsses. J. Veg. Sci. 25, (14). 35. Chpmn, L. J., Chpmn, C. A. & Chndler, M. Wetlnd ecotones s refugi for endngered fishes. Biol. Conser. 78, (1996). 36. Hcker, S. D. & Bertness, M. D. Experimentl evidence for fctors mintining plnt species diversity in New Englnd slt mrsh. Ecology 8, (1999). 37. He, Q., Xu, J. & Zhng, B. Geologicl Environment nd Sustinle Development of the Yellow River Delt (Geologicl Pulishing House, 6). 38. Stromerg, J. C. et l. Altered strem-flow regimes nd invsive plnt species: the Tmrix cse. Glol Ecol. Biogeogr. 16, (7). 39. Cui, B.-S., He, Q. & An, Y. Community structure nd iotic determinnts of slt mrsh plnt zontion vry cross topogrphic grdients. Estur. Cost. 34, (11).. Qin, H. M. et l. Effects of invsive cordgrss on cr distriutions nd diets in Chinese slt mrsh. Mr. Ecol. Progr. Ser. 415, (1). 41. Wng, X.-C. et l. Mcroenthic ecology of the intertidl zones of Chjindo, Dkouhedo nd Wngzido of Yellow River Estury in utumn. Chinese Journl of Zoology 43, (8). 42. Leng, Y. et l. Community structure nd diversity of mcroenthos in southern intertidl zone of Yellow River Delt, Chin. Chinese Journl of Ecology 32, (13). 43. Liu, Y. L. Birds of the Yellow River Delt. (Chin Forestry Pulishing House, 13). 44. Bertness, M. D., Holdredge, C. & Altieri, A. H. Sustrte medites consumer control of slt mrsh cordgrss on Cpe Cod, New Englnd. Ecology 9, (9). 45. He, Q. et l. Wht confines n nnul plnt to two seprte zones long costl topogrphic grdients? Hydroiologi 63, (9). 46. He, Q., Cui, B., Bertness, M. D. & An, Y. Testing the importnce of plnt strtegies on fcilittion using congeners in costl community. Ecology 93, (12). Acknowledgments We thnk M. D. Bertness nd S. C. Pennings for comments nd edits. This study ws funded y Ntionl Key Bsic Reserch Progrm of Chin (13CB436), Chin Ntionl Funds for Distinguished Young Scientists ( ), nd Ntionl Science Foundtion for Innovtive Reserch Group (511213). Author contriutions Q.H. nd B.C. designed the study, Q.H. performed the experiments nd nlyzed the dt, nd Q.H. nd B.C. wrote the pper. Additionl informtion Supplementry informtion ccompnies this pper t scientificreports Competing finncil interests: The uthors declre no competing finncil interests. How to cite this rticle: He, Q. & Cui, B. Multiple mechnisms sustin plnt-niml fcilittion on costl ecotone. Sci. Rep. 5, 8612; DOI:1.138/srep8612 (15). SCIENTIFIC REPORTS 5 : 8612 DOI: 1.138/srep8612 5

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