Journl of Ecology 2017, 105, 176 187 doi: 10.1111/1365-2745.12649 Experience of inundtion or drought lters the responses of plnts to susequent wter conditions Shu Wng 1,2, Rgn M. Cllwy 2, Do-Wei Zhou 3 nd Jco Weiner 4 * 1 Institute of Grsslnd Science, nd Key Lortory of Vegettion Ecology, Ministry of Eduction, Northest Norml University, Chngchun 130024, Chin; 2 Division of iologicl Sciences nd the Institute on Ecosystems, The University of Montn, Missoul, MT 59812, US; 3 Northest Institute of Geology nd groecology, Chinese cdemy of Sciences, Chngchun 130012, Chin; nd 4 Deprtment of Plnt nd Environmentl Sciences, University of Copenhgen, 1871 Frederikserg, Denmrk Summry 1. The vilility of wter is often highly vrile over the life of plnt in nture, nd most plnts experience episodic extremes in wter scrcity nd undnce. The importnce of plnt plsticity in coping with such experiences is widely recognized, ut little is known out how plstic responses to current conditions re ffected y prior environmentl experiences. 2. Our ojectives were to investigte the effects of erly inundtion or drought on the susequent responses of plnt species to the sme, opposite or more fvourle conditions. 3. To ddress these questions, we sujected four invsive nd four ntive herceous perennil species from different hitts (xeric, mesic, hydric) to two rounds of hydrologicl tretments (drought, moderte wter, inundtion) nd nlysed the effects of the erly tretments on survivl nd performnce (totl iomss nd reltive growth) of individuls in the lter tretments. 4. In generl, (i) erly drought reduced the performnce of more species thn did erly inundtion, nd decresed the finl totl mss of ll species; (ii) erly inundtion nd erly drought did not led to lower survivl immeditely or lter, ut improved the reltive growth of survivors cross ll lte conditions; (iii) lte drought resulted in the highest mortlity nd lowest performnce fter ny erly tretment. 5. With respect to hitt of origin: (i) erly inundtion ws more eneficil for species from wet hitts thn for other species; (ii) species from xeric hitts hd the strongest drought tolernce fter erly drought; (iii) mesic species were more likely to suffer reduced lter growth fter either inundtion or drought experience. Invsive species enefitted more from erly inundtion thn did ntive species, ut ntive species grew etter fter experiencing erly drought. 6. Results indicte tht erly exposure to inundtion or drought conditions lters how plnts respond to lter conditions nd suggest tht exposure to extreme events cn induce physiologicl or morphologicl chnges tht improve tolernce for either extreme conditions lter. This incresed tolernce cn e t the cost of poorer performnce under more enign conditions. 7. Synthesis. Erly inundtion or drought experience my e hrmful immeditely, ut cn e eneficil for the lter growth of plnts. The ility of species to utilize erly hydrologicl experiences ws ssocited with the wter rnge of their hitts nd whether the species is invsive or ntive. The ility to modulte future plstic responses my e s importnt s short-term plsticity in dpting to temporl environmentl heterogeneity. Such metplsticity cn optimize current performnce, while voiding the potentil costs of mintining high degree of plsticity throughout life. Key-words: drought, hitt rnge, inundtion, invsiveness, metplsticity, plsticity, priming effect, stress memory, stress tolernce, temporl heterogeneity *Correspondence uthor. E-mil: jw@plen.ku.dk 2016 The uthors. Journl of Ecology 2016 ritish Ecologicl Society
Erly experience lters lter responses 177 Introduction In nture, plnts experience lrge vrition in environmentl conditions over the course of their lives. Plnts del with such environmentl heterogeneity vi phenotypic plsticity: the ility to produce different phenotypes in different environments (Pigliucci 2005). The ility of plnt to generte plstic responses is not independent of its pst experiences. Extreme events tht occur t n erly stge of growth not only ffect the survivl nd performnce of plnts t the time they occur, ut lso cn hve profound influences on n individul s growth potentil nd responses to future environmentl conditions (Huer et l. 2012; Niu et l. 2014). Experiencing iotic stress such s herivory or iotic stress such s drought, inundtion, frost or het cn lter the response of n individul plnt to susequent stresses (Thkokorpi et l. 2007; Onte, lnc & Munne-osch 2011), phenomenon referred to s the priming effect (Tnou, Fotopoulos & Molssiotis 2012) or stress memory (Wlter et l. 2013). For exmple, Urtic dioic sujected to comined drought nd nutrient deficiency in the juvenile phse showed improved drought tolernce in their mture leves (Onte, lnc & Munne-osch 2011). Similrly, pretretment of whet seedlings with sumergence during vegettive growth improved tolernce to sumergence fter nthesis (Li et l. 2011). Such responses to previous conditions re thought to involve series of mechnisms including epigenetic modifictions (Roertson & Wolf 2012; Scholes & Pige 2015), s well s metolic, physiologicl nd morphologicl chnges (ruce et l. 2007; Wlter et l. 2013). Experiencing extreme conditions not only lters plnt s susequent performnce in single environment ut cn lso ffect the ility of plnts to respond to different environmentl conditions in the future. This hs een clled plsticity in plsticity (Schmid & Weiner 1993) or metplsticity (Novoplnsky 2009). When plnt is exposed to different extreme environments t different stges of their growth, the effects of temporl heterogeneity my e similr to those of multiple stressors. The cumultive effect of multiple stressors cn e either greter (synergistic) or less (ntgonistic) thn the dditive sum of effects of isolted stressors (Hy 1996; Piggott, Townsend & Mtthei 2015). The effects of individul stresses re reltively well studied, ut few studies hve focused on the effect of multiple stresses (Drling & C^ote 2008), even fewer in the context of temporl heterogeneity. Wter vilility is crucil for plnts, nd vrition in wter vilility over time cn hve profound effects on plnt survivl nd growth (Niu et l. 2014). In mny environments, plnts re exposed to lternting drought nd inundtion t different life stges (Prolin et l. 2010), nd they re le to cope with such heterogeneity through rpid plstic responses (Lnde 2009). Even though inundtion nd drought re t opposite ends of n environmentl continuum, they my elicit similr physiologicl responses from plnts, suggesting tht exposure to one condition might prepre plnt for exposure to the other. To cope with re-oxygention nd susequent wter deficit, species tht disply quiescence during complete sumergence my e etter dpted to dehydrtion fter sumergence (Fuko, Yeung & iley- Serres 2011), nd some drought-tolernt species my lso e flood tolernt (Gomes & Kozlowski 1980). trnscription fctor tht increses during oth sumergence nd drought (Fuko, Yeung & iley-serres 2011) lso suggests common mechnism. On the other hnd, some studies hve reported trde-off etween tolernce to drought nd to inundtion in wetlnd species (Luo, Song & Xie 2008). Different sequences of inundtion nd drought cn ffect plnt survivl nd growth differently (Mio, Zou & reshers 2009). These imply tht erly inundtion nd erly drought hve different effects on lter plnt responses to either stress. Studies tht investigted the comined effects of inundtion nd drought hve produced inconsistent results, nd we hve no informtion on how erly exposure to either of the extremes ffects plnt performnce under fvourle conditions lter. Plnt plsticity in response to wter stress hs een studied extensively (Willims & lck 1994; Pezeshki 2001; Csper, Forseth & Wit 2006; rloto et l. 2007), ut little ttention hs een pid to how prior occurrence of wter extremes ffects responses to susequent wter conditions. Species from different hitts my hve evolved different ilities to djust their plstic responses to the sme environmentl experience. For exmple, species from flooded forests hve greter ility to tolerte inundtion, ut lower tolernce for drought stress, thn congeners from drier hitts (rloto et l. 2007). It is unknown whether species from hydric hitts hve incresed or decresed responses to inundtion or drought lter in their lives thn do other species. lso, invsive species hve een hypothesized to show greter phenotypic plsticity thn ntive species (Richrds et l. 2006), ut this hs not een supported in severl studies (Funk 2008; Hulme 2008; Plcio-Lopez & Ginoli 2011). This could e ddressed y investigting plsticity to n environmentl fctor more closely linked to the context of the specific environmentl hitts occupied y invsive nd ntive species. For exmple, Willims & lck (1994) found tht exotic species from rid regions were more plstic in trits relted to drought tolernce thn their ntive counterprts. s fr s we know, vrition in plsticity in response to erlier hydrologicl experience hs not een investigted. To ddress this, we performed n experiment with eight species, four ntive nd four invsive, from three hydrologicl hitts (wet, mesic nd xeric), sking the following questions: (i) Does erly exposure to inundtion or drought influence lter performnce under inundtion, drought or moderte conditions? (ii) re such effects on lter responses different () for erly inundtion vs. erly drought? () for different lte conditions? (c) for species from different hydrologicl hitts? or (d) for ntive vs. invsive species? 2016 The uthors. Journl of Ecology 2016 ritish Ecologicl Society, Journl of Ecology, 105, 176 187
178 S. Wng et l. Mterils nd methods STUDY SPECIES We chose eight species, including four invsive species: Leucnthemum vulgre Lm. (oxeye disy), Centure stoee L. ssp. micrnthos (Gugler) Hyek (spotted knpweed; nee C. stoee L.), Leonurus crdic L. (common motherwort) nd Potentill rect L. (sulphur cinquefoil), nd four ntive species: Heterothec villos (Pursh) Shinners (hiry flse golden ster), Gillrdi ristt Pursh (common gillrdi), gstche urticifoli (enth.) Kuntze (nettlelef gint hyssop) nd Potentill rgut Pursh (tll cinquefoil). ll seeds were collected from nturl grsslnds in western Montn. The distriutions of these species cn overlp, ut we selected pirs of trget species tht generlly occur in hitts tht differ in soil moisture: C. stoee nd H. villos occur primrily in more xeric hitts, L. vulgre, P. rect, G. ristt nd P. rgut primrily in mesic hitts, nd L. crdic nd. urticifoli generlly in very wet hitts (Tle 1). EXPERIMENTL DESIGN The experiment ws conducted in glsshouse on the cmpus of the University of Montn, Missoul, Montn. Glsshouse tempertures were mintined t 15 30 C, corresponding roughly to nturl summer tempertures in the region. Nturl light ws supplemented y metl hlide uls nd mximum totl photosyntheticlly ctive rdition during the dy reched 1200 lmol m 2 s 1. Seeds of ll species were sown in plstic trys (54.2 9 27.3 cm in width nd 6.5 cm in height) in Jnury 2010. One week fter seedling emergence, individul seedlings were trnsplnted into pots (7 9 7 cm in width nd 20.6 cm in height) filled with 1:1 mixture of top grden soil nd sterile silic snd. Forty dys fter trnsplnting, efore the first round of tretments were pplied, the longest lef of ech plnt ws mesured s n estimte of the initil size of ech individul. split plot design ws implemented with the first round of tretments s min fctor, nd the second round of tretments nd species s sufctors. For oth the first nd second rounds, there were three tretments: inundtion, moderte wtering nd drought. t the end of the first round, sugroup of plnts from ech of the erly tretments ws hrvested to otin informtion on their initil responses to the three wter tretments [erly responses (ER)] nd s reference for clculting their reltive growth fter susequent tretment. The remining plnts from ech of the three erly-tretment groups [erly inundtion (EI), erly moderte wtering (EM) nd erly drought (ED)] were divided into three sugroups, ech of which ws lter exposed to one of the sme three tretments [lte inundtion (LI), lte moderte wtering (LM) nd lte drought (LD)] in the second round (Fig. 1). For ech tretment comintion, ten individuls of ech species were used, with one individul per pot, giving 10 individuls 9 8 species 9 3 erly tretments 9 3 lte tretments + 10 9 8 9 3 (individuls with erly tretments only) = 960 pots in totl. Six identicl tnks were used to crete inundtion, drought nd moderte wter conditions, with two tnks ssigned to ech tretment. Tnks were 161 9 91.3 cm in width nd 8.5 cm in height, lined with hevy plstic nd fit with drins to regulte the mximum wter depth. For the inundtion tretment, the wter level ws mintined t 7 cm depth ove the ottom of the tnk, nd pproximtely 10 cm elow the surfce of the soil in the pots. These pots were wtered to sturtion from the top every dy. There ws no stnding wter in the moderte nd drought tretment tnks. In the moderte tretment, pots Tle 1. Summry of the ttriutes of the eight species studied nd revitions for their nmes Ltin nme rev. English nme Fmily Moisture rnge of hitts Invsiveness Centure stoee L. ssp. micrnthos C Spotted knpweed Composite Mesic~xeric Invsive (Gugler) Hyek Heterothec villos (Pursh) Shinners H Hiry flse golden ster Composite Mesic~xeric Ntive Leucnthemum vulgre Lm. Lv Oxeye disy Composite Hydric~mesic Invsive Potentill rect L. Pr Sulphur cinquefoil Roscee Hydric~mesic Invsive Gillrdi ristt Pursh G Common gillrdi Composite Hydric~mesic Ntive Potentill rgut Pursh P Tll cinquefoil Roscee Hydric~mesic Ntive Leonurus crdic L. Lc Common motherwort Lmicee Hydric Invsive gstche urticifoli (enth.) Kuntze Nettlelef gint hyssop Lmicee Hydric Ntive 1 ST -ROUND TRETMENTS I M D 2 ND -ROUND TRETMENTS I M D I M D I M D Ini l Lte Secondry pls city pls city pls city Fig. 1. Experimentl design showing the two rounds of inundtion (I), moderte (M) nd drought (D) tretments used in this study. suset of plnts ws hrvested nd mesured fter first-round tretments. [Colour figure cn e viewed t wileyonlinelirry.com] 2016 The uthors. Journl of Ecology 2016 ritish Ecologicl Society, Journl of Ecology, 105, 176 187
Erly experience lters lter responses 179 Mesurement of initil size Mesurements Mesurements Pre-tretments & erly tretment Lte tretment 0 40 110 180 Dys Fig. 2. The timing of the two rounds of tretments. Seedlings estlished Strt of 1 st round End of 1 st round Strt of 2 nd round End of 2 nd round were wtered to sturtion every other dy, while those in the drought tretment were wtered to sturtion once or twice per week in n effort to crete very dry conditions, ut prevent high mortlity rtes. The first round of tretments lsted for 70 dys efore plnts in ech tretment were divided nd ssigned to one of the three different conditions in the second round or hrvested nd mesured to evlute their erly responses (Fig. 2). The durtion of the second round of tretments ws nother 70 dys, nd glsshouse nd hydrologicl conditions were s similr s possile to the first round. Thus, plnts receiving oth rounds of tretments were hrvested nd mesured 140 dys fter the eginning of the first round. Height nd lef numer were mesured nd then seprted into roots nd shoots t hrvest, dried t 60 C for 2 dys nd weighed. DT COLLECTION ND STTISTICL NLYSES We clculted mortlity rtes for ll tretment comintions. totl of 728 individuls survived to the end of the experiment nd these were used for further nlyses. ll five trits: totl plnt iomss (TM), height (HE), lef numer (LN), shoot mss (SM) nd root mss (RM), were used to ssess the performnce of species in ech tretment. For ech of the five trits of ech species, reltive growth (RG) for ll erly lte tretment comintions ws clculted ccording to the formul: RG ¼ Y X X ; where X is the men trit vlue of 10 individuls of the erly response group, nd Y is the men trit vlue in the lte tretment of 10 individuls tht hd the sme erly tretment s the erly response group. For exmple, to clculte the RG of totl iomss in lte drought for species with erly inundtion tretment, X is the men totl mss of individuls hrvested fter erly inundtion nd Y is the men vlue of individuls in the lte drought fter erly inundtion. For ech species in ech tretment comintion, RGs of the four trits: height, lef numer, shoot mss nd root mss, were comined into single composite mesure of reltive growth (RG C ) y verging the RGs of the four trits. Thus, we used four response vriles in evluting the performnce of ech species: mortlity rte, totl iomss, reltive growth in iomss (RG M ) nd composite reltive growth (RG C ). For ny individul or group of species, erly inundtion nd drought tretments cn ffect their susequent responses in different wys nd/or to different extents. To ddress this for given trit, we defined difference vriles ( Diff- ), s the difference in the men trit vlue from the control (moderte erly tretment) due to n erly inundtion or drought tretment: Diff-Y ¼ Y 2 Y 1 ; where Diff-Y ws the difference in lte performnce etween individuls with erly inundtion or drought nd those with erly moderte tretment for trit of species, Y 1 ws the men vlue of the trit for the species in lte condition fter erly moderte tretment (control) nd Y 2 ws its men trit vlue in the sme lte condition fter erly inundtion or drought. For exmple, to clculte the Diff-TM due to erly inundtion (EI) for species in lte drought, Y 1 is the men totl iomss of individuls in lte drought fter the erly moderte tretment, nd Y 2 is the men totl iomss of individuls in lte drought fter erly inundtion. Men vlues of height, lef numer, shoot mss, root mss nd totl plnt iomss were log-trnsformed to minimize vrince heterogeneity. The r 2 from models for NOV or NCOV on mortlity, the five mesured trits, reltive growth in iomss nd composite reltive growth were higher with species s vrile thn models with hitt type nd exotic sttus s vriles. Therefore, the results of three-wy NOV or NCOV for effects of the first round of tretments, the second round of tretments, species nd their interctions for ll trits were used for nlyses of men vlues. The five mesured trits were nlysed with three-wy NCOV with the initil size of individuls nested within species s covrite, nd mortlity nd two mesures of reltive growth were nlysed with three-wy NOV. ll dependent vriles were then nlysed with one-wy NOV or NCOV to evlute the effects of the erly tretments for ech species within ech of three lte tretments, nd differences mong the lte tretments nd mong different species (for the two mesures of reltive growth) within ech erly tretment. Since there were not sufficient degrees of freedom to nlyse the effects of individul species on these vriles, we compred the degree of effects of erly experiences, differences in mortlity, totl iomss, reltive growth in iomss nd composite reltive growth (Diff-MR, Diff-TM, Diff-RG M nd Diff-RG C, respectively) due to erly tretments with four-wy NOV, with the first nd second rounds, hitt type, exotic sttus nd their interctions s effects. The LSD method ws used for multiple comprisons on men vlues for mortlity, totl iomss, reltive growth in mss nd composite reltive growth nd the four Diff- vriles mong first-round tretments, mong second-round tretments nd mong species (or mong different hitt types nd etween invsive nd ntive species for differences of vriles), cross ll nd within ech of the other tretments. Results MORTLITY cross ll species nd tretments, men mortlity rte in the first round ws 8.6%, significntly lower thn 20.7%, which occurred in the second round (P = 0.007; Tles 2 nd 3; Fig. 3). The overll mortlity during lte drought ws 36.3%, nerly two times higher thn in the lte inundtion nd moderte tretments (P < 0.001; Fig. 3, Tle 3). Two rounds of drought incresed the overll mortlity of ll species to 2016 The uthors. Journl of Ecology 2016 ritish Ecologicl Society, Journl of Ecology, 105, 176 187
180 S. Wng et l. 47.5%, compred with 28.8% in lte drought fter erly moderte conditions (P = 0.029), while no effects of erly inundtion on lter mortlity were found. Species from xeric hitts showed decrese in mortlity in lte inundtion (P < 0.001) nd n increse in mortlity in lte moderte conditions fter erly drought (P < 0.05), compred with tht fter erly moderte conditions (Fig. 3). Species from hydric hitts hd higher mortlity thn other species under lte moderte conditions fter moderte experience (P < 0.01). Tle 2. Three-wy NOV or NCOV for the effects of species (SP), the 1st nd 2nd rounds of tretments (1st nd 2nd) nd their interctions on mortlity rte (MR), log 10 (Totl mss (TM)), reltive growth of TM (RG M ) nd composite reltive growth (RG C, men RG of four trits including height, lef numer, shoot mss nd root mss), for plnts tht hd een sujected to two rounds of tretments. Log 10 [Initil size (IS)] ws used s covrite in the NCOV on log 10 (TM) nd ws nested in the species effect NOV on MR NOV on RG M Source d.f. F P F P SP 7 2.58 0.022 10.33 <0.001 1st 2 0.63 0.537 1.75 0.184 2nd 2 15.53 <0.001 8.07 <0.001 1st 9 2nd 4 1.61 0.185 1.10 0.366 NCOV on Log 10 (TM) NOV on RG C Source d.f. F P F P Log 10 (IS) 8 29.74 <0.001 SP 7 50.07 <0.001 17.80 <0.001 1st 2 51.52 <0.001 4.49 0.012 2nd 2 22.00 <0.001 18.53 <0.001 SP 9 1st 14 2.18 0.008 3.48 <0.001 SP 9 2nd 14 2.72 <0.001 1.54 0.098 1st 9 2nd 4 0.86 0.081 1.24 0.293 SP 9 1st 9 2nd 28 1.22 0.203 0.84 0.698 TOTL IOMSS For plnts hrvested fter the first round, the men totl iomss of ll species ws significntly lower under drought thn under moderte nd inundtion conditions (P < 0.001; Fig. 4). Compred with moderte conditions, drought reduced the iomss of five of the eight species (the exceptions were G. ristt, P. rgut nd L. crdic; P < 0.05), wheres inundtion only reduced the iomss of. urticifoli (P = 0.02), indicting the tretment of inundtion ws much less stressful thn drought t the erly stge. For plnts tht received oth rounds of tretments, there were highly significnt effects of oth the first- nd secondround tretments on ll mesured vriles, with strong interctions of species with the first- nd second-round tretments (Tle 2 nd Tle S1 in Supporting Informtion). However, there were few significnt interctions etween the first- nd second-round tretments. cross ll species nd ll lte tretments, the men iomss fter erly drought ws 0.31 g, 43.5% lower thn fter erly moderte conditions (0.54 g, P < 0.001), ut there ws no effect of erly inundtion (P = 0.221; Tle 3 nd Fig. 4). For individul species, erly drought decresed finl iomss in mny more cses thn did erly inundtion (Fig. 4). The effects of lte tretments on iomss were more species specific thn those of erly tretments, s indicted y greter significnce of second-round 9 species interctions thn first-round 9 species interctions (Tle 2). Overll, the men iomss fter lte drought ws significntly lower thn fter lte inundtion nd moderte conditions (P < 0.05, Tle 3). iomss ws gretest under continuous (oth rounds of) moderte conditions (F = 6.20; d.f. = 2, 172; P = 0.003; Tle 3), especilly for P. rect nd C. stoee (Fig. 4). fter erly inundtion, negtive responses of iomss to lte drought were found for more species thn fter ny other erly tretment (P < 0.05), wheres erly moderte or drought tretments resulted in negtive response to lte inundtion for only C. stoee (P < 0.01 nd P = 0.01 for erly moderte nd drought experience, respectively). Tle 3. Overll effects of the 1st nd 2nd rounds of tretments on second-round mortlity rte (MR), Log (totl mss) [log (TM)], reltive growth of totl mss (RG M ) nd composite reltive growth (RG C ), for plnts with oth rounds of tretments Tretment MR Log 10 (TM) RG M RG C The 1st round Overll EI = EM > ED ED = EI > EM LI EI = EM > ED ED > EM ED = EI > EM LM EM = EI > ED LD EM < ED EI = EM > ED The 2nd round Overll LI = LM < LD LI = LM > LD LI = LM > LD LI > LM > LD EI LI < LD LI > LD LI > LM = LD EM LM < LD LM = LI > LD LM > LD LI = LM > LD ED LI = LM < LD LI > LD LI = LM > LD LI = LM > LD EI, erly inundtion; EM, erly moderte condition; ED, erly drought; LI, lte inundtion; LM, lte moderte condition; LD, lte drought. Significnce levels for > or < re t P 0.05, nd = indictes no differences etween two tretments (P > 0.05). 2016 The uthors. Journl of Ecology 2016 ritish Ecologicl Society, Journl of Ecology, 105, 176 187
Erly experience lters lter responses 181 Erly response (1 st round) Erly response (1 st round) 0.20 0.15 0.10 0.05 0.00 0.8 0.6 Lte repsonse (2 nd round) Erly inundtion 3.0 2.0 Lte response (2 nd round) Erly inundtion Mortlity 0.4 0.2 0.0 0.8 0.6 0.4 0.2 0.0 0.8 0.6 0.4 0.2 0.0 c c Erly moderte Erly drought Xeric Mesic Hydric Hitt rnge of species c Totl mss (g) 1.0 0.0 3.0 2.0 1.0 0.0 1.0 0.8 0.6 0.4 0.2 0.0 Erly moderte Erly drought C C H Lv Pr G P Lc Xeric Mesic Hydric Species within hitt rnge Fig. 3. Men mortlity rte in inundtion (&), moderte ( ) nd drought (h) tretments in the 1st round (erly response, ER), nd in the 2nd round (lte response, LR) for erly inundtion (EI), moderte (EM) nd drought (ED) tretments (1st round) for species grouped ccording to the hydrology of their hitts. Different lower-cse letters signify differences mong the 2nd round or mong the groups of species, nd different upper-cse letters signify differences mong first-round tretments nd etween those in erly response nd in lte response (P < 0.05). Fig. 4. Men totl mss of individul species in inundtion (&), moderte ( ) nd drought (h) tretments for erly responses (1st round), nd for lte response (2nd round) fter the erly tretments (1st round). Species re grouped ccording to the hydrology of their hitts. revitions for ll species re in Tle 1. For erly responses, different lower-cse letters signify differences mong tretments; for lte responses, different lower-cse letters signify differences due to first-round tretments; different upper-cse letters signify differences due to first-round tretments (P < 0.05). RELTIVE GROWTH For oth reltive growth in iomss (RG M ) nd the composite mesure of reltive growth (RG C, men reltive growth of ll the other four trits), nd cross ll species, the effects of the second round of tretments were much stronger thn the first round (Tle 2). oth mesures of reltive growth, RG M nd RG C, were significntly lower under lte drought thn in more fvourle lte conditions (P < 0.01; Tle 3 nd Figs S2 nd 5). For the effects of the first-round tretments, erly drought improved reltive iomss growth in lte inundtion 2016 The uthors. Journl of Ecology 2016 ritish Ecologicl Society, Journl of Ecology, 105, 176 187
182 S. Wng et l. only when compred to the erly moderte tretment (+99.7% vs. +42.4%, P = 0.037; Tle 3 nd Fig. S2). cross ll lte conditions, oth erly inundtion nd drought incresed the men composite mesure of growth, RG C, y 29.7% nd 32.4%, respectively, reltive to +11.3% of the control (P = 0.017 nd P = 0.006; Tle 3). Significnt differences in growth mong species were found etween the two fstest growing species (P. rgut nd H. villos) nd the other species (Figs S2 nd 5). There were lso differences in growth etween L. vulgre nd P. rect versus the remining species for composite reltive growth (Fig. 5). For individul species, differences in reltive growth mong the first round tretments were found only for species from hydric nd xeric hitts (Fig. S2c; P < 0.05), nd there ws little difference mong the second-round tretments (Fig. S2d). For the composite mesure of reltive growth, interctions etween species nd tretment were much stronger for the first thn for the second round (Tle 2). Species from wet nd xeric hitts were more likely to show improved RG C thn species from mesic hitts (Fig. 5). fter erly inundtion, C. stoee s RG C in lte inundtion nd drought ws +15.9% nd +20.1%, higher thn the control [ 26.9% (P = 0.065) nd 38.9% (P = 0.006), respectively]. RG C s of L. crdic nd. urticifoli were +47.0% nd 4.1%, respectively, cross ll lte tretments, 217.5% nd 91.8% higher thn controls ( 40.0% nd 49.7%, P < 0.05). Erly inundtion reduced the composite reltive growth of P. rect in the lte moderte tretment (P = 0.032). Similrly, effects of erly drought were positive for. urticifoli in ll lte tretments, s it incresed the verge RG C from 49.7% Reltive growth (RG) 10 8 6 4 2 0 2 4 10 8 6 4 2 0 2 4 10 8 6 4 2 0 2 4 2 nd round Inundtion Inundtion Moderte Moderte Drought Col 76 Col 77 Col 78 C C C C C C C C Col 79 C C Drought CD C CD C 1 st round D D C C C C C C C C C C H Lv Pr G P Lc C H Lv Pr G P Lc C H Lv Pr G P Lc Xeric Mesic Hydric Xeric Mesic Hydric Xeric Mesic Hydric Species within hitt rnge Fig. 5. Reltive growth (RG) in the trits: height (&), lef numer ( ), shoot mss ( ) nd root mss (h) during the second-round tretments for eight species fter the first-round tretments. Species re grouped ccording to the hydrology of their hitts. For single species, different letters in lower cse ove the columns indicte significnt differences in men RG of the four trits or the composite reltive growth (RG C ) mong the fistround tretments for ech second-round tretment; different letters in upper cse ove the columns represent significnt differences mong the second-round tretments within the sme first-round tretment (P < 0.05). Different letters in upper cse elow the columns denote significnt difference mong species (P < 0.05). Red circles represent significnt increse nd lue circles significnt decrese (P 0.05), due to first-round inundtion or drought, compred with the control (fter first-round moderte wtering); red nd lue dshed circles represent mrginlly significnt increse or decrese (0.05 < P < 0.10). revitions for ll species re in Tle 1. [Colour figure cn e viewed t wileyonlinelirry.com] 2016 The uthors. Journl of Ecology 2016 ritish Ecologicl Society, Journl of Ecology, 105, 176 187
Erly experience lters lter responses 183 to 8.6% (P < 0.05). However, erly drought lso hd some dverse effects: it decresed RG C of P. rect in lte drought y 257.8% (from 11.90% to 42.60%; P = 0.043). CHNGES DUE TO ERLY TRETMENTS Significnt effects of erly, lte tretments nd hitt type were found for ll Diff- vlues except mortlity (Tles 4, S3 nd Fig. S3). There were significnt interctions etween lte tretments nd invsiveness for oth Diff-RG M nd Diff-RG C (Tles 4 nd S3). For composite reltive growth, there were significnt interctions etween erly tretment nd hitt type, lte tretments nd hitt type, nd erly tretments nd invsiveness. mong the erly tretments, we found significnt difference etween effects of inundtion nd drought only for Diff-TM. Erly inundtion resulted in n verge increse in iomss (Diff-TM = 0.06) cross ll species nd ll lte tretments, significntly higher thn the verge decrese in iomss due to erly drought (Diff-TM =ucodep> 0.24, P = 0.031). Compring species from different hitts in the lte tretments, hydric species showed n increse in reltive growth fter erly inundtion reltive to the control, with Diff- RG M = 1.02 nd Diff-RG C = 0.66 for L. crdic nd. urticifoli, respectively, which ws higher thn those of xeric nd mesic species [verged Diff-RG M = 0.06 (P < 0.05) nd Diff-RG C = 0.01 (P < 0.001); Tle S3]. Xeric species demonstrted greter increse in composite reltive growth fter the erly drought tretment (verge of 0.32) thn fter erly inundtion (verge of 0.02) cross ll lte tretments (P = 0.030). For species from mesic hitts, differences in composite growth due to erly inundtion were higher for lte Tle 4. F-vlues from four-wy NOV on the differences due to effects of erly experience (Diff-, etween fter inundtion or drought experience nd fter moderte experience) for mortlity rte (MR), totl mss (TM), reltive growth in mss (RG M ) nd composite reltive growth (RG C ), for the effects of the 1st nd 2nd rounds of tretments (1st nd 2nd), hitt (H), invsiveness (IN) nd their interctions Source of vrition d.f. Diff-MR Diff-TM Diff-RG M Diff-RG C 1st 1 0.11 7.87* 0.01 0.16 2nd 2 1.73 0.62 1.83 4.81** H 2 1.20 0.33 4.36* 14.19*** IN 1 0.58 0.74 0.01 0.00 1st 9 2nd 2 0.70 0.08 0.56 1.52 1st 9 H 2 0.11 0.29 0.87 5.37** 1st 9 IN 1 0.19 1.47 4.62* 21.20*** 2nd 9 H 4 1.09 0.46 0.83 2.78* 2nd 9 IN 2 2.61 0.47 0.37 0.23 1st 9 H 9 IN 4 1.17 0.22 0.75 2.11 2nd 9 H 9 IN 4 1.48 0.51 0.60 2.10 1st 9 2nd 9 H 4 0.43 0.01 0.46 1.10 1st 9 2nd 9 IN 2 0.00 0.17 0.44 2.14 1st 9 2nd 9 H 9 IN 4 0.44 0.17 0.23 0.53 Significnce levels: *P < 0.05, **P < 0.01, ***P < 0.001. Significnt vlues re in old font. inundtion nd drought tretments thn for lte moderte conditions (0.13 nd 0.29 vs. 0.35, P < 0.001 in oth cses). For invsive versus ntive species cross ll lte tretments, the eneficil effect of erly inundtion on composite growth ws greter for invders thn for ntives (0.44 vs. 0.04, P < 0.001), ut the eneficil effect of erly drought ws greter for ntives (0.41 vs. 0.10, P = 0.003). Discussion EFFECTS OF ERLY TRETMENTS ON LTER PERFORMNCE Improved tolernce for environmentl stress fter previous exposure to stress hs een clled the priming effect (Tnou, Fotopoulos & Molssiotis 2012) or stress memory (Wlter et l. 2013) nd hs een documented for drought nd inundtion in previous studies (Li et l. 2011; Onte, lnc & Munne-osch 2011). ut there hs een little discussion of how the occurrence of these two stresses t different points in time during plnt growth might influence performnce (Mio, Zou & reshers 2009). Our results re the first experimentl evidence tht either kind of experience erly in the life cn improve plnt s performnce to oth forms of stress t lter stge. This is consistent with the theoreticl nd empiricl studies on synergetic effect of multiple stressors (Folt et l. 1999; Coors & Meester 2008; Crin, Kroeker & Hlpern 2008; Piggott, Townsend & Mtthei 2015). Thus, s philosopher Fredrick Nietzsche sid, tht which does not kill us, mkes us stronger my pply to plnts. Prt of the explntion for improved performnce under second-round inundtion or drought fter either erly inundtion or drought my e tht some of the mechnisms for tolernce to drought nd inundtion re similr (Lopez & Kursr 2003). For exmple, n ethylene-response-fctor-like gene Su1 tht confers sumergence tolernce to rice (Xu et l. 2006) lso improves survivl when rice is exposed to rpid dehydrtion (Fuko, Yeung & iley-serres 2011). The sumergence-inducile gene Su1 my endow plnts with the ility to overcome prolonged sumergence, oxidtive dmge nd rpid dehydrtion tht often occur during recovering from sumergence, s well s wter deficit cused y drought (Fuko, Yeung & iley-serres 2011)., the effects of which cn e ugmented y Su1, is key signlling molecule tht coordintes wter lnce, expression of stress-inducile genes nd metolic djustment under wter-deficient conditions (Zhu 2002; Seki et l. 2007). Dehydrtion is lso component of trnsient sumergence event (Setter, heksut & Greenwy 2010), nd exogenous increses survivl of oxygen deprivtion in plnts (Hwng & Vntoi 1991; Ellis, Dennis & Pecock 1999). Therefore, the levels of my lso ct s positive regultor for sumergence tolernce s well s for drought tolernce. The shred mechnisms for tolernce to inundtion nd drought stress lso oserved in physiologicl nd ntomicl trits (Prolin et l. 2010). For exmple, oth inundtion nd drought cn induce stomtl closure (Prolin 2001; Elcn & Pezeshki 2002), 2016 The uthors. Journl of Ecology 2016 ritish Ecologicl Society, Journl of Ecology, 105, 176 187
184 S. Wng et l. reduce lef gs exchnge nd decrese lef trnspirtion nd cron ssimiltion (Prolin 2001; rloto et l. 2007). dventitious roots, erenchym nd lethery xeromorphic leves of trees in mzonin floodplins re commonly recognized s dpttion to inundtion (Prolin 2001), ut they my lso llevite the effects of drought. Plnts my hve the ility to compenste for hrsh conditions erly in their lives through incresed growth lter, just s plnts cn compenste for herivory, sometimes performing s well s or etter thn plnts tht were not grzed (McNughton 1979; Pige & Whithm 1987; grwl 2000). Dmge results in lower immedite growth, ut sometimes promotes fster growth fterwrds, enling dmged plnts to ctch up. n increse in reltive growth rte fter dmge or prior extreme experience cn lso e n llometric effect: the reltive growth rte of plnt decreses s it grows. n event tht mkes or keeps plnts smller cn therefore increse plnt s reltive growth rtes fterwrds. METPLSTICITY SSOCITED WITH SPECIES HITTS Our species from hydric, mesic or xeric hitts responded to the experience of erly inundtion or drought in wys tht were generlly consistent with the hydrology of the hitts in which they occur. For exmple, gs exchnge rtes in flood-tolernt species usully recover rpidly following inundtion event (Kozlowski 1982; Elcn & Pezeshki 2002). Here, species from hydric hitts hd the gretest increse in reltive growth fter erly experience with inundtion, lthough erly drought ws not worse for them thn for other species. Similrly, species from xeric hitts showed greter tolernce for drought fter exposure to erly drought thn did other species, consistent with other studies of drought priming (Onte, lnc & Munne-osch 2011; Wlter et l. 2011; Wng et l. 2014). Enhnced performnce y species from oth more extreme hitts lter under the sme or different stressful conditions, reltive to species from more moderte hitts, suggests the hypothesis tht plnts my evolve generl tolernce for vrious forms of stress. Repeted exposure cn led to the evolution of more stress-tolernt genotype (Chpin, utumn & Pugnire 1993), which my show reduced performnce under more fvourle conditions. We did not find significnt decrese in reltive growth under lter moderte conditions for species from hydric or xeric hitts fter erly drought or inundtion. Evidence for such cost ws only found in one species from mesic environment (P. rect) fter exposure to inundtion. This could e ecuse (i) cost of cclimtion to erly stress my e more likely to occur in species without history of dpttion to extreme environments; or (ii) tht the cost of responses to erly stress my e smll nd difficult to detect (Sultn & Spencer 2002; Weijschede et l. 2006; uld, grwl & Relye 2010); or (iii) the decresed reltive growth of P. rect in lte drought fter erly drought my simply e due to dmge from longer period of continuous drought, which hd more dverse effects thn inundtion. Long-term dpttion to enign hitts my led to the evolution of genotypes with reduced ility to tolerte extreme events. ccording to this hypothesis, species from mesic hitts, especilly P. rect, re less le to cope with more extreme environmentl events. The ility of species to develop metplsticity in response to prior extreme experience my e closely linked to its tolernce for such experience. It is to e expected tht the hitt in which species occurs plys n importnt role in determining metplsticity in response to erly experience. This could e useful focus for future studies on vrition in plsticity nd metplsticity. The wys y which different species djust their lter plsticity in response to prior experience my ply n importnt role in ecotypic differentition (rdshw & Hrdwick 1989; Plcio-Lopez & Ginoli 2011). Metplsticity my e s importnt s genetic differentition for the expnsion of species (Willims & lck 1993; Prker, Rodriguez & Loik 2003) nd llow species to respond to wide rnge of environments nd tolerte novel stresses during invsion. fter expnsion, the mintennce of high degree of plsticity throughout plnt s lifetime my e very costly. ssuming tht the costs of plsticity increse with the degree of plsticity (DeWitt, Sih & Wilson 1998; Givnish 2002; uld, grwl & Relye 2010), nturl selection in response to environmentl heterogeneity my fvour greter vriility in the plsticity of specific trit (ut see (Pigliucci, Murren & Schlichting 2006; Crispo 2007). The complexity nd high opertionl costs of plsticity suggest the involvement of higher-order control nd coordintion (Novoplnsky 2009). Such flexiility in plsticity my llow plnts to produce dptive plstic responses rpidly when needed, while minimizing costs of mintining rod plsticity to the degree possile. Flexiility in plsticity my therefore e s importnt for species cclimtion to temporl heterogeneity in environmentl conditions s the degree of plsticity t one point in time. METPLSTICITY OF INVSIVE VERSUS NTIVE SPECIES Our results show tht plstic responses cn e chnged y previous environmentl experiences, nd suggest tht the ility of species to regulte their plsticity is relted to the hitts in which they occur, nd whether they re invsive or ntive species. Invsive species hve een hypothesized to e more plstic thn ntives, ut we found little evidence for this. Contrry to some predictions (Mrshll & Jin 1968; Dehler 2003) nd some empiricl results (Dvidson et l. 2011), our four invsive species were not different thn their four ntive counterprts in their responses to wter conditions, s found in other studies (rock, Weinig & Glen 2005; Funk 2008; Plcio-Lopez & Ginoli 2011). Plsticity is highly trit dependent, nd high degree of plsticity in one trit my e ssocited with low plsticity in other trits (Vlldres et l. 2000). This suggests tht integrted mesures of plnt performnce my e more importnt for understnding the role of plsticity in invsion thn quntifying the degree of plsticity 2016 The uthors. Journl of Ecology 2016 ritish Ecologicl Society, Journl of Ecology, 105, 176 187
Erly experience lters lter responses 185 (or metplsticity) in individul trits (Hulme 2008). sed on our composite mesure of reltive growth, the invsive species enefitted from erly inundtion more thn ntive species did, wheres ntive species enefited more from erly drought. Comprison of lrger numer of ntive nd invsive species is needed to drw stronger conclusions. DPTIVE METPLSTICITY VERSUS CONSTRINTS ND DMGE Since.D. rdshw s lndmrk pper over hlf century go (rdshw 1965), there hve een extensive discussions nd detes concerning the relevnt trits, mesurement, evolutionry nd ecologicl significnce of phenotypic plsticity, s well its costs nd mechnisms. It my e premture to theorize out these sme issues with respect to the higher-order phenomenon of metplsticity (Novoplnsky 2009). Still, the current study suggests some theoreticl considertions: 1. It is importnt to distinguish etween dptive ehviours nd those tht re inevitle results of plnt growth form, unvoidle constrints or dmge. If plnt suffers from phosphorus deficiency, its leves will e purple, nd it my hve difficulty deling with dditionl stresses. It does not seem useful to interpret this s dptive plsticity/metplsticity. Similrly, plnt growth is llometric, nd plnt s reltive growth rte decreses with size. Therefore, ny tretment tht reduces plnt growth ut hs no other negtive effects will result in higher reltive growth under etter environmentl conditions lter when compred to plnts tht did not suffer from reduced growth erlier (Weiner 2004). This is etter interpreted in terms of llometry thn s metplsticity. 2. When should plnts evolve metplsticity rther thn simple plsticity? ssuming tht there is cost of plsticity nd tht this cost increses with the redth of plstic responses of which the plnt is cple, we would expect metplsticity to evolve when specific environmentl conditions re predictly ssocited with specific lter environmentl conditions. Under such scenrio, plnts could reduce the cost of future rod plsticity y mintining more limited plsticity for the predicted environment. The life spn of the plnt reltive to the temporl vrition in its environment ecomes importnt here. We would expect metplsticity to evolve when the lifespn of plnt is long enough for it to experience different environmentl conditions during its life, ut not if its lifespn covers mny such chnges in different directions (unless the metplsticity is temporry). Thus, metplsticity would e expected to evolve in short-lived plnts, ut not those with the very shortest lifespn, for exmple desert nnuls. Conclusions This study demonstrtes tht erly experience of drought or inundtion cn modify responses to drought or inundtion lter in life. The ility to modulte susequent plsticity in response to erly experience is ffected y the species hitt, whether it is invsive or ntive, nd the type of environmentl experience. dptive metplsticity my e ssocited with greter stress tolernce nd reduced costs. Species from different hydrologicl hitts not only showed different short-term responses to wter conditions t oth stges, ut lso showed differences in the vrition in lter plsticity in response to the erly tretments, nd these differences were usully interpretle in terms of their hitts. Species from hydric nd xeric hitts enefitted most from erly inundtion nd drought experiences, respectively, while evidence of lter costs of such exposure ws found in one species from mesic hitts. Invsive species did not show higher short-term plsticity thn ntive species, ut the effects of erly inundtion versus drought on lter growth were different for these two groups. Flexiility in producing different degrees of plsticity my e s importnt for dpttion to environmentl heterogeneity s plsticity t one point in time. Future reserch should focus on the development of generl theory for the evolution of plsticity nd metplsticity of trits, nd on the mechnisms involved. cknowledgements We thnk Giles C. Thelen nd other memers of the Cllwy L t the University of Montn for help with the experiment, Erik schehoug nd Dniel twter for help with sttisticl nlyses nd comments on the mnuscript. This reserch ws supported y the Ntionl Nturl Science Foundtion of Chin (NSFC), grnt No. 30970493 to D.-W.Z. nd the U.S. Ntionl Science Foundtion DE 0614406, NSF EPSCoR Trck-1 EPS-1101342 (INSTEP 3), nd the Interntionl Progrms t the University of Montn to R.M.C. Dt ccessiility ll dt re present in the pper nd its supporting informtion. References grwl,.. (2000) Overcompenstion of plnts in response to herivory nd the y-product enefits of mutulism. 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Received 11 Mrch 2016; ccepted 22 July 2016 Hndling Editor: Jmes Chill 2016 The uthors. Journl of Ecology 2016 ritish Ecologicl Society, Journl of Ecology, 105, 176 187