The role of plant soil feedbacks and land-use legacies in restoration of a temperate steppe in northern China

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1 Eol Res (21) 25: DOI 1.17/s x ORIGINAL ARTICLE Lili Jing Xingguo Hn Gungming Zhng Pul Krol The role of plnt soil feeks n ln-use legies in restortion of temperte steppe in northern Chin Reeive: 24 Jnury 21 / Aepte: 16 My 21 / Pulishe online: 2 July 21 Ó The Eologil Soiety of Jpn 21 Astrt Plnt soil feeks ffet plnt performne n plnt ommunity ynmis; however, little is known out their role in eologil restortion. Here, we stuie plnt soil feeks in restortion of steppe vegettion fter griulturl isturne in northern Chin. First, we nlyze ioti n ioti soil properties uner mono-ominnt plnt pthes in n olfiel restortion site n in trget steppe site. Seon, we teste plnt soil feeks y growing plnt speies from these two sites on soils from on- n heterospeifi origin. Soil properties generlly i not iffer etween the ol-fiel site n steppe site, ut there were signifint ifferenes mong mono-ominnt plnt pthes within the sites. While soil speies origin (i.e., the plnt speies eneth whih the soil ws ollete) ffete iomss of iniviul plnt speies in the feek experiment, speies-level plnt soil feeks were neutrl. Soil site origin (ol-fiel, steppe) signifintly ffete iomss of ol-fiel n steppe speies. For exmple, ol-fiel speies h higher iomss in ol-fiel soils thn in steppe soils, initing positive ln-use legy. However, soil site origin effets epene on the L. Jing Æ X. Hn (&) Æ G. Zhng Stte Key Lortory of Vegettion n Environmentl Chnge, Institute of Botny, Chinese Aemy of Sienes, Xingshn, Beijing 193, Chin E-mil: xghn@is..n Tel.: Fx: L. Jing Grute University of the Chinese Aemy of Sienes, Yuqunlu, Beijing 149, Chin P. Krol Environmentl Sienes Division, Ok Rige Ntionl Lortory, One Bethel Vlley Ro, Ok Rige, TN 37831, USA P. Krol Deprtment of Forest Eology n Mngement, Sweish University of Agriulturl Sienes, Ume, Sween plnt speies eneth whih the soils were ollete. The preitive vlue of ioti n ioti soil properties in explining plnt iomss iffere etween n within groups of ol-fiel n steppe speies. We onlue tht the ourrene of positive ln-use legies for ol-fiel speies my retr suessionl replement of ol-fiel speies y steppe speies. However, high levels of iiosynrsy in responses of ol-fiel n steppe plnt speies to on- n heterospeifi soils inite interspeifi vrition in the extent to whih soil legies n plnt soil feeks ontrol suessionl speies replements in Chinese steppe eosystems. Keywors Aioti n ioti soil properties Æ Biogeohemistry Æ Ln-use history Æ Nturl experiment pproh Æ Ol-fiel Æ Seonry suession Æ Soil hemistry Introution The temperte steppe in northern Chin, s ominnt form of lnspe, onstitutes n integrl prt of the Eursin grssln n plys importnt roles in serviing the eologil environment n soio-eonomis of the region; the steppe systems hve tritionlly een mjor soure of niml prouts (Kng et l. 27). Moreover, steppe systems hve the potentil to sequester lrge mounts of ron. However, griulturl exploittion hve h etrimentl impts on physil n hemil soil onitions, n out 9% of the temperte steppe in northern Chin no longer resemles originl steppe vegettion (Liu n Tong 23; You et l. 23; Ding et l. 26). In 2, in reognition of the prolems use y griulturl exploittion of the lns, progrms were impose to restore the eologil lne of the Chinese steppe y reuing grzing pressure or y turning low-yieling frmln k to steppe (Chen et l. 29). The min ojetive of these progrms is to remove griulturl isturne regimes n promote the re-estlishment of nturl steppe

2 112 vegettion. Restortion efforts though hve not lwys een suessful; fter esstion of griulturl isturnes, ompositionl evelopment of plnt ommunities towrs typil steppe vegettion is often retre (Rong 24; Jing et l. 26). So fr, restortion efforts in Chinese steppe systems hve primrily fouse on restoring physil n hemil soil onitions without expliitly onsiering the role of intertions etween ovegroun n elowgroun eosystem omponents. Aovegroun elowgroun linkges hve strong impts on temporl shifts in ommunity omposition n ssoite eosystem proesses (e.g., Wrle 22; Vn er Putten et l. 29), suggesting tht they re importnt to the restortion of steppe eosystems fter griulturl isturne. Prtiulrly, feeks etween plnts n soil oul e influentil in the reovery of isture plnt ommunity s suh feeks hve een shown to ffet plnt performne, plnt-ompetitive intertions, ommunity evenness, n suessionl plnt ommunity ynmis (e.g., Vn er Putten et l. 1993; Bever 1994; Reynols et l. 23; Krol et l. 26, 27; Csper et l. 28; Hrrison n Brgett 21). Generlly, plnt soil feeks re efine y the iomss of onspeifis to plnt speies-speifi hnges in soil properties reltive to iomss responses of heterospeifi ompetitors (Bever et l. 1997). Importntly, plnt soil feeks re not restrite to speies level, ut n lso operte t high levels of orgniztion, suh s plnt funtionl or suessionl groups (Bezemer et l. 26; Krol et l. 27). Positive feek n result from N-fixing miroorgnisms or enhne symioses with myorrhizl fungi (Sprent 1993; Klironomos 22; Krol et l. 26), while negtive feek n result from umultion of soil pthogens, suh s prsiti nemtoes or fungl oomyetes (Vn er Putten et l. 1993; Vn er Putten 1997; Reinhrt et l. 25). Feeks etween plnts n soil orgnisms n lso operte through the eomposition pthwy (Vn Breemen n Finzi 1998; Dorrepl et l. 27). Plnt speies iffer in the qulity n quntity of resoures they eliver to or tke up from the soil (Hoie 1996), potentilly reting feeks through regulting nutrients ville for susequent plnt growth (e.g., Berense 1994; Vivno n Austin 28; Ayres et l. 29; MCrthy- Neumnn n Koe 21). Finlly, plnt soil feeks n lso iretly e ue to plnt speies-speifi nutrient epletion (Bezemer et l. 26), or through speies-speifi effets on physil soil properties suh s moisture ontent, temperture, or texture (s reviewe in Ehrenfel et l. 25). Previous stuies hve shown tht plnt soil feeks n generte suessionl replements of unwnte, erly-suessionl speies y lte-suessionl trget speies (Krol et l. 26, 27). For exmple, in seonry suession fter griulturl ln nonment in the Netherlns, negtive plnt soil feeks enhne suession uring erly stges of suession, while positive feeks retre suession in lter stges. Erly seonry suession plnt speies (pioneers, ruerls) my e prtiulrly suseptile to the uil-up of soil pthogens euse of their fst growth n poor efene (Prie 1984). On the other hn, lte seonry suession plnt speies re generlly thought to epen more on mutulisti ssoitions with myorrhizl fungi thn erly speies (Jnos 198; Smith n Re 1997), n re generlly slowgrowing; therefore lte-suessionl speies re more likely to experiene positive feek (Krol et l. 26). However, so fr, only few stuies hve teste effets of plnt soil feeks in vegettion restortion fter griulturl isturnes, n little is known out the generlity of the suggeste priniples. Also, previous plnt soil feek stuies show strong is towrs grsslns n ol-fiels in Europe n North-Ameri, n more stuies re neee to test the vliity of previous finings for eosystems in other iogeogrphil regions. Here, we report the results of feek experiment onute in temperte steppe eosystem in Duolon ounty, northern Chin. Until 1978, the mjor isturnes in the steppe eosystem were low-intensity grzing y ntelopes n rits, n wilfire (Zhou et l. 27). After 1978, s result of mrket-se eonomi reforms, lrge res of steppe were onverte to rop ln, or to grzing systems. In our experiment, we inlue two sites tht use to e prt of the sme steppe eosystem: n ol-fiel tht ws none from griulture in 21 (the restortion site, representing n erly stge of seonry suession), n steppe site whih h een grze y ttle n sheep until 21, ut still oul e onsiere s typil steppe (the trget site ) (for etils, see Xu et l. 21). Plnt ominne ptterns iffere etween the two sites; the ol-fiel ws ominte y erly suessionl pioneer speies, while the steppe ws ominte y K-strtegi plnt speies pte to unisture ompetition (Bi et l. 24; Zhng 25; Niu et l. 28; Xu et l. 21). We selete mono-ominnt plnt pthes for three ol-fiel speies n for three steppe speies. First, for eh of the plnt speies, we mesure ioti n ioti soil properties. Seon, soils ollete eneth the mono-ominnt plnt pthes (i.e., with known plnt growth histories) were use in n outoor feek experiment, i.e., the Nturl Experiment Approh (Kulmtiski n Krol 28). Speies-level plnt soil feeks were ssesse y ompring plnt growth on on- n heterospeifi soils. Bse on their growth strtegies, we hypothesize negtive feeks for the ruerl ol-fiel speies n positive plnt soil feeks for the slow-growing steppe speies. We lso teste ln-use legy effets, i.e., ompring growth on ol-fiel soils with growth on steppe soils. Finlly, we use multiple regressions to eluite the ontriution of eh of ioti n ioti soil properties to plnt growth.

3 113 Mterils n methos Site esription n experimentl esign Our experimentl site ws lote in Duolun County (42 27 N, E, 1,38 m.s.l.), Inner Mongoli in northern Chin. Men monthly ir tempertures rnge from 17.5 C in Jnury to 18.9 C in July, with men nnul temperture of 2.1 C. Men nnul preipittion in this re is mm (67% flls from June to August). The soils in this re re hestnut soils (Chinese lssifition), or Hpli Clisols oring to the FAO lssifition (Niu et l. 28). Within the experimentl site, we selete two sites tht use to e prt of the sme steppe eosystem: (1) n ol-fiel tht ws none from griulturl use in 21 (the restortion site ), n (2) jent to the ol-fiel typil steppe (the trget site ) (see Introution ). First, we selete monoominnt plnt pthes for three of the ominnt speies t eh of the two sites (Appenix 1). At the olfiel site we selete pthes of Artemisi pillris (Art p; perennil C 3 -for), Artemisi lvnulefoli (Art lv; perennil C 3 -for), n Pennisetum entrsitium (Pen en; perennil C 4 -grss) (herefter referre to s ol-fiel speies ); these speies re typilly foun on none griulturl ln in northern Chin (Zhng et l. 24; Zhng 25; Niu n Wn 28; Wng et l. 29; Xu et l. 21). At the steppe site we selete pthes of Artemisi frigi (Art fri; short-stture, perennil su-shru (C 3 )), Leymus hinensis (Ley hi; perennil rhizome grss (C 3 )), n Stip krylovii (Sti kry; perennil unhgrss (C 3 )) (herefter referre to s steppe speies ) whih re typil ominnt plnt speies in steppe in this region n re onsiere trget speies in restortion of egre steppe (Eitoril Committee for Vegettion of Chin 198; Bi et l. 24; Niu et l. 28). For eh plnt speies we selete six replite pthes n 2 2 m plots were estlishe in eh pth. Aross ll plnt speies, the pthes were rnomly istriute in the ol-fiel n steppe sites; n ll pthes were istriute within 6 m. Soil olletion n nlyses In April 27, lrge soil smple (5 5 1 m) ws ollete from orner position in eh plnt pth, mixe n sieve (5-mm mesh) to remove lrge roots n stones. From eh soil smple, one susmple ws ir-rie (<3 C), sieve (2-mm mesh) n nlyze for ph, totl ron (C), totl nitrogen (N), inorgni nitrogen (NO 3 N n NH 4 + N), totl phosphorus (P), n plnt-ville P. Soil ph ws mesure t soil: wter rtio of 1:2.5. Totl C ws nlyze using H 2 SO 4 K 2 Cr 2 O 7 oxition metho (Nelson n Sommers 1982). Totl N ws nlyze using the Kjelhl igestion metho with n Alpkem utonlyzer (Kjekte System126 Distilling Unit, Sween). Inorgni nitrogen ws extrte with 2 M KCl. Totl P ws etermine y igesting the soil smple with 18 M H 2 SO 4 following the metho of Prkinson n Allen (1975). Plnt-ville P ws etermine using the Kelown metho (Vnlierop 1988). From eh soil smple, seon susmple (15 g ry weight) ws use for nlysis of miroil iomss C n N using hloroform fumigtion extrtion metho (Vne et l. 1987). Miroil iomss C n N were etermine from the ifferenes etween extrtle C n N onentrtions in the fumigte n the unfumigte smples using onversion ftors (k EC n k EN ) of.38 n.45 (Lovell et l. 1995), respetively. All results were expresse on n oven-rie soil sis. Feek experiment For eh of the six plnt speies, the remining soil ws ulke n homogenize to give six types of soils eh representtive for the mono-ominnt plnt pthes from whih they were ollete. The soils were then use to estlish n outoor feek experiment in whih we teste plnt performne on onspeifi n heterospeifi soils. We ssume tht ifferenes in soil onitions uner ifferent plnt speies reflete previous plnt growth (i.e., plnt speies-speifi effets) n not site onitions, suh s prent mteril; soils in our fiel sites were homogeneous, n the plnt pthes hve een stle for t lest five yers (Lili Jing, unpulishe t). The experiment involve fiel-ollete seelings plnte into PVC tues (pots) (imeter 11 m n 5- m epths) whih were fille with the fiel soils. The ottom of the pots ws overe with perforte plsti film to keep soils in ple. The pots were ple in exvte holes in fiel out 2 m from the ol-fiel n steppe sites, leving pproximtely 1 m of the pot ove groun level. At the sme time the soil smples were ollete, we ollete seelings for use in the feek experiment. We use fiel-ollete seelings euse previous trils showe high mortlity of lortory germinte seelings, proly ue to the hrsh limti onitions uring Inner Mongolin spring. Smll seelings (verge shoot height (m): Art p = 1.4, Art lv = 2.8, Pen en =.5, Art fri = 1.3, Ley hi = 5., n Sti kry = 4. m) from the ol-fiel n steppe speies were ollete jent to the respetive mono-ominnt plnt pthes. Seelings were refully remove from the soil, n roots were thoroughly (ut refully) wshe with tp wter (Niu et l. 28; Niu n Wn 28; Zho et l. 28). Prior to trnsplnting, eh iniviul ws mesure to ensure tht within speies ll seelings were of similr size (height, weight). Eh pot ws plnte with one seeling. The experiment ws set up in ftoril esign (n = 9) with two ftors: soil type (ol-fiel [Art p, Art lv, Pen en], steppe [Art fri, Ley hi, Sti kry]) n plnt speies (ol-fiel [Art p, Art lv, Pen en], steppe

4 114 [Art fri, Ley hi, Sti kry]). Pots were rrnge in nine replite loks (6 6 gri esign; tues were t 1-m istne from eh other). Within loks, pots were rnomly istriute. Bloks were seprte y 1-m wie orriors. In totl, the experimentl esign involve 6 plnt speies 6 soil types 9 replite loks = 324 pots. In generl, seeling survivl ws high; however, seelings tht ie uring the first week of the experiment were reple. Plnts were wtere regulrly uring the first month; plnts were not wtere therefter. Plnts were grown for 18 weeks, fter whih shoot iomss ws hrveste. Pots were remove from the fiel n roots were wshe from the soils. Plnt mteril ws oven-rie t 7 C for minimlly 48 h, n weighe. Dt nlyses Aioti n ioti soil properties mesure eneth mono-ominnt plnt pthes were nlyze using twowy nlysis of vrine (ANOVA) with soil site origin (ol-fiel, steppe) s fixe ftor, n plnt speies neste within soil site origin s rnom ftor. If signifint plnt speies effets were oserve, Dunn s HSD post ho tests were use to etermine ifferenes mong speies. Beuse of the low numer of speies within plnt groups, n euse of the ul sttus of heterospeifi soil in our experiment (ol-fiel soils, steppe soils), we eie not to lulte integrte mesures of plnt soil feek (e.g., perentge ifferene in iomss etween onspeifi n heterospeifi soil). As rgue y MCrthy-Neumnn n Koe (21), lumping ll heterospeifi speies into single group, oul osure omplex reltionships mong plnt speies s meite through hnges in soil properties. Inste, inresing the trnspreny of t nlysis, we teste iomss responses in one-wy ANOVA with soil speies origin (i.e., the plnt speies eneth whih the soil ws ollete) s fixe ftor, n we use Dunn HSD post ho tests to test ifferenes mong soil speies origins (onspeifi origin n five ifferent types of heterospeifi origin). Ln-use legy effets were nlyze using three-wy ANOVA with plnt speies, soil site origin, n soil speies origin neste within soil site origin s fixe ftors. Responses of iniviul plnt speies to soil site origin were nlyze using two-wy ANOVA with soil site origin n soil speies origin neste within soil site origin s fixe ftors. For ll ANOVA s, the ssumption of normlity ws heke with Kolmogorov Smirnov tests n the ssumptions of homogeneity of vrines ws heke using Levene s test. If the ssumptions were not met, t were logtrnsforme prior to nlysis. Forwr stepwise multiple regressions were use to etermine reltionships etween soil properties n plnt iomss. All univrite nlyses were performe using SPSS, version 15. (SPSS In, Chigo, Illinois). Results Soil ioti n ioti vriles uner mono-ominnt plnt pthes Soil ioti n ioti properties i not iffer signifintly etween ol-fiel soils n steppe soils, exept tht the soil N/P rtio tene to e higher in steppe soils thn in ol-fiel soils (Tle 1). However, within soil histories, ioti n ioti soil properties iffere signifintly epening on the plnt speies eneth whih Tle 1 Results from ANOVA testing effets of soil site origin (ol-fiel, steppe) n plnt speies on ioti n ioti soil properties Soil site origin ws inlue s fixe ftor, n plnt speies neste within soil site origin s rnom ftor * Inites signifint effet Soil properties Effet f F p Totl C (g kg 1 ) Soil site origin Speies (soil site origin) <.1* Totl N (g kg 1 ) Soil site origin Speies (soil site origin) <.1* Totl P (g kg 1 ) Soil site origin Speies (soil site origin) <.1* Plnt-ville P (mg kg 1 ) Soil site origin Speies (soil site origin) <.1* Soil N/P Soil site origin Speies (soil site origin) * Soil ph Soil site origin Speies (soil site origin) <.1* Bulk ensity (g m 3 ) Soil site origin Speies (soil site origin) <.1* Inorgni N (mg kg 1 ) Soil site origin Speies (soil site origin) <.1* Miroil C (mg kg 1 ) Soil site origin Speies (soil site origin) <.1* Miroil N (mg kg 1 ) Soil site origin Speies (soil site origin) <.1* Miroil C/N Soil site origin Speies (soil site origin) <.1*

5 - 115 Totl C (g kg -1 ) A B Totl N (g kg -1 ) N/P Totl P (g kg -1 ) C E D F Aville P ph (mg kg -1 ) NH 4 + -N (mg kg -1 ) G Art p Art lv Pen en Art fri Ley hi Sti kry Ol fiel Steppe Soil origin H Art p Art lv Pen en Art fri Ley hi Sti kry Ol fiel Steppe Soil origin NO 3 - -N (mg kg -1 ) Fig. 1 Soil ioti ftors s mesure eneth mono-ominnt plnt pthes for ol-fiel speies n steppe speies. Dt re men ± SE (n = 6). Art p Artemisi pillris, Art lv Artemisi lvnulefoli, Pen en Pennisetum entrsitium, Art fri Artemisi frigi, Ley hi Leymus hinensis, Sti kry Stip krylovii the soil ws ollete (Figs. 1, 2, n illustrte in Fig. 4). For exmple, ross ll soils, the highest levels of totl C, totl N, n totl P were foun in soils eneth the steppe speies A. frigi, while the lowest levels were foun in soils eneth the steppe speies L. hinensis. Similrly, ross ll soils, the highest levels of plntville P were foun in soils eneth the ol-fiel speies A. pillris, while the lowest levels were foun in soils eneth the ol-fiel speies P. entrsitium. Soils eneth P. entrsitium h the highest levels of miroil C, while the lowest levels were foun in soils eneth the ol-fiel speies A. pillris n A. lvnulefoli (Fig. 2). Plnt soil feeks Soil speies origin, i.e., the plnt speies eneth whih the soil ws ollete, signifintly ffete iomss of iniviul plnt speies in the feek experiment (Fig. 3, Appenix 2). For exmple, iomss of the olfiel speies A. pillris ws pproximtely two-fol higher in soils previously olonize y onspeifis, A. lvnulefoli, nl. hinensis thn in soils previously olonize y P. entrsitium, A. frigi,ns. krylovii (Fig. 3). However, oth for ol-fiel speies n for steppe speies, plnt soil feeks (iomss on onspeifi soils ompre to iomss on heterospeifi soils) were neutrl (Fig. 3). For ol-fiel speies, plnt iomss on own soils ws not ifferent from plnt iomss on soils on whih other ol-fiel speies h een growing. Similrly, for steppe speies, plnt iomss on own soils ws not ifferent from plnt iomss on soils on whih other steppe speies h een growing (Fig. 3). Soil site origin (i.e., ol-fiel or steppe) signifintly ffete iomss of ol-fiel n steppe speies (Tle 2; Fig. 3). On verge, iomss of ol-fiel speies ws 34% higher on ol-fiel soils thn on steppe soils. For steppe speies, iomss ws on verge 13% higher on ol-fiel soils thn on steppe soils. However, oth for ol-fiel speies n steppe speies, soil site origin effets epene strongly on the plnt speies eneth whih the soils were ollete. Moreover, within plnt groups, iniviul plnt speies showe ifferentil responses to soil site origin n soil speies origin s inite y signifine of the intertion effets etween plnt speies n soil speies origin neste within soil site origin (Tle 2). Tests for iniviul plnt speies showe tht iomss of the ol-fiel speies P. entrsitium ws signifintly higher on ol-fiel soils thn on steppe soils. On verge, the iomss of the two other ol-fiel speies, A. pillris n A. lvnulefoli, ws lso higher

6 116 Miroil iomss C (mg kg -1 ) Miroil iomss N (mg kg -1 ) Miroil iomss C/N A B C Art p Art lv Pen en Art fri Ley hi Sti kry Ol fiel Soil origin Steppe Fig. 2 Soil miroil C, N, n C/N s mesure eneth monoominnt plnt pthes for ol-fiel speies n steppe speies. Dt re men ± SE (n = 6). Art p Artemisi pillris, Art lv Artemisi lvnulefoli, Pen en Pennisetum entrsitium, Art fri Artemisi frigi, Ley hi Leymus hinensis, Sti kry Stip krylovii on ol-fiel soils thn on steppe soils, lthough there ws vrition within soil site origin groups epening on the plnt speies eneth whih the soil ws ollete s inite y signifint effets of soil speies origin neste within soil site origin (Tle 3; Fig. 3). On verge, iomss of the steppe speies S. krylovii ws 37% lower in steppe soils thn in ol-fiel soils, ut the ifferene ws not onsistent ross soil speies origins (Tle 3; Fig. 3). Biomss of the other two steppe speies, A. frigi n L. hinensis, i not iffer etween steppe soils n ol-fiel soils. Reltionships etween soil properties n plnt iomss Stepwise forwr multiple regressions showe tht the orreltion etween ioti n ioti soil properties n plnt iomss iffere mrkely etween ol-fiel speies n steppe speies, n lso mong speies within sites (Tle 4). Totl C negtively orrelte with plnt iomss n oul explin out 46 n 39% of the vrition of iomss of the ol-fiel speies A. pillris n A. lvnulefoli, respetively. Aitionl vrition in iomss of these ol-fiel speies oul e expline y miroil iomss C; these orreltions were negtive. Soil N/P orrelte negtively with plnt iomss of the ol-fiel speies P. entrsitium, ounting for 19% of the vrition. There ws signifint positive orreltion etween plnt-ville P n iomss of the steppe speies A. frigi n L. hinensis, Biomss (g) Ol fiel speies Art p Steppe speies Art fri Biomss (g) Biomss (g) 1 5 Art lv Ley hi Biomss (g) Biomss (g) Pen en Sti kry 4 2 Biomss (g) Art p Art lv Pen en Art fri Ley hi Sti kry Ol fiel Steppe Soil origin Art p Art lv Pen en Art fri Ley hi Sti kry Ol fiel Steppe Soil origin Fig. 3 Biomss proution of ol-fiel speies n steppe speies grown in soils previously olonize y onspeifis (white r) n in soils previously olonize y heterospeifis (grey rs). Dt re men ± SE (n = 9). Art p Artemisi pillris, Art lv Artemisi lvnulefoli, Pen en Pennisetum entrsitium, Art fri Artemisi frigi, Ley hi Leymus hinensis, Sti kry Stip krylovii

7 Tle 2 Results from three-wy ANOVA testing effets of plnt speies, soil site origin, n soil speies origin neste within soil site origin on plnt iomss Plnt group Effet f F p Ol-fiel Plnt speies <.1* Soil site origin <.1* Soil speies origin (soil site origin) <.1* Plnt speies soil site origin <.1* Plnt speies soil speies origin (soil site origin) * Steppe Plnt speies <.1* Soil site origin * Soil speies origin (soil site origin) <.1* Plnt speies soil site origin Plnt speies soil speies origin (soil site origin) * All terms were inlue s fixe ftors Soil site origin: ol-fiel or steppe; Soil speies origin: plnt speies eneth whih the soil ws ollete * Inites signifint effet 117 Tle 3 Results from two-wy ANOVA testing effets of soil site origin n soil speies origin neste within soil site origin on plnt iomss Plnt group Plnt speies Effet f F p Ol-fiel Art p Soil site origin * Soil speies origin (soil site origin) <.1* Art lv Soil site origin <.1* Soil speies origin (soil site origin) <.1* Pen en Soil site origin * Soil speies origin (soil site origin) Steppe Art fri Soil site origin Soil speies origin (soil site origin) <.1* Ley hi Soil site origin Soil speies origin (soil site origin) Sti kry Soil site origin <.1* Soil speies origin (soil site origin) * Both terms were inlue s fixe ftors Soil site origin: ol-fiel or steppe; Soil speies origin: plnt speies eneth whih the soil ws ollete Art p Artemisi pillris, Art lv Artemisi lvnulefoli, Pen en Pennisetum entrsitium, Art fri Artemisi frigi, Ley hi Leymus hinensis, Sti kry Stip krylovii * Inites signifint effet Tle 4 Moels preiting plnt iomss from ioti n ioti soil properties lulte y forwr stepwise multiple regressions with p vlue of.5 s the inlusion riterion Plnt group Plnt speies Preitor vrile r 2 Sign F p Ol-fiel Art p Totl C <.1 Soil miroil iomss C Art lv Totl C <.1 Soil miroil iomss C Pen en Soil N/P Steppe Art fri Plnt-ville P Totl C Ley hi Plnt-ville P Sti kry Soil miroil iomss C <.1 The r 2 vlues re the oeffiients of etermintion, i.e., the proportion of vriility tht is ounte for y the moel; the signs inite the iretion of the reltionships etween the vriles. Ftors inlue in the nlyses were: soil totl C, N, P, soil N/P, soil ph, soil NH 4 + N, soil NO 3 N, plnt-ville P, soil miroil iomss C, N n C/N Art p Artemisi pillris, Art lv Artemisi lvnulefoli, Pen en Pennisetum entrsitium, Art fri Artemisi frigi, Ley hi Leymus hinensis, Sti kry Stip krylovii ounting for 19 n 13% of the vrition, respetively. For A. frigi, n itionl 17% of the vrition oul e expline negtively y totl C. Miroil iomss C ws signifintly negtively orrelte with the iomss of the steppe speies S. krylovii, ounting for 38% of the vrition.

8 118 Ol-fiel site Plnt speies omposition A B Steppe site Grzing C D E F Vrition in ioti n ioti soil properties Time Fig. 4 Coneptul igrm showing temporl ptterns of plnt ommunity omposition in reltion to ln-use history. The steppe site n the ol-fiel site use to e prt of the sme steppe eosystem. Between 1978 n 21, the two sites iffere in lnuse; the ol-fiel site ws ultivte with rye (Aven hinensis), while the steppe site ws grze. After esstion of griulturl Disussion Plnt speies iffer in their effets on soil properties (e.g., Bezemer et l. 26; Hrrison n Brgett 21), whih, in turn my ffet susequent growth of on- n heterospeifis. Suh plnt soil feeks hve een suggeste to e importnt for the rte n iretion of suessionl plnt speies replements fter ln-use hnge (Krol et l. 26, 27). For restortion of Chinese steppe fter esstion of griulturl prties, we showe tht plnt speies from n ol-fiel restortion site n from typil steppe site (the trget site ) exerte speies-speifi effets on oth ioti n ioti soil properties (Fig. 4). In following feek experiment, using soils ollete eneth the ol-fiel n steppe speies, we teste reiprol iomss responses. With respet to onspeifiity n heterospeifiity, soil speies origin effets were iiosynrti, i.e., no speieslevel plnt soil feeks were oserve. However, with respet to soil site origin (i.e., ol-fiel or steppe) we oserve n interesting pttern. Generlly, ol-fiel speies performe etter in ol-fiel soils thn in steppe soils; in ontrst, steppe speies were not muh ffete y soil speies origin. Our hypothesis tht the ruerl ol-fiel speies show negtive plnt soil feeks ws not supporte. Previous stuies hve inite tht in ol-fiel suession, erly-suessionl ruerls ten to experiene negtive plnt soil feeks, enhning their replement y lter-suessionl speies (Krol et l. 26). Fstgrowing, poorly efene ruerls my e prtiulrly vulnerle to umultion of soil pthogens (Coley et l. 1985; Buron 1987; Vn er Putten 23), whih oul result in speies-speifi uil-up of soil pthogens in their rhizosphere (Vn er Putten et l. 1993; Bever 1994). The ol-fiel speies in our stuy pprently i not suffer from speies-speifi soil pthogens. While negtive plnt soil feeks re ommonly oserve for ol-fiel prties, ifferent plnt speies ominte the ol-fiel site (,, ) n the steppe site (, e, f). Aioti n ioti soil properties iffere etween ol-fiel soils n steppe soils, ut there ws strong inter-speifi vrition within groups of soils epening on the plnt speies eneth whih the soils were ollete speies (Kulmtiski et l. 28), it hs lso een shown tht plnt soil feeks re highly speies-speifi; negtive feeks for some ol-fiel speies my e very smll or even non-existing (e.g., Bever 1994; Krol et l. 27). Moreover, plnt soil feeks re the outome of multiple intertions. So, it oul lso e tht pthogeni effets were ompenste for y positive feeks with the ioti soil omponent, or y speies-speifi ssoitions with mutulisti soil orgnisms. As we use fiel-ollete seelings (see Methos ), plnts in our feek experiment my still hve h some of their own rhizosphere orgnisms; in prtiulr, even though seelings were thoroughly (ut refully) wshe, roots my lrey hve een olonize y myorrhizl fungi upon trnsplnttion. Although suh unintentionl myorrhizl infetions oul hve ffete plnt performne, it is not ler how this my hve ffete ifferentil plnt growth on on- n heterospeifi soils. Previous stuies hve suggeste tht lte seonry suession speies enefit more from host-speifi ssoitions with myorrhizl fungi thn erly-suessionl speies (Reeves et l. 1979; Jnos 198), n therefore woul e likely to show positive plnt soil feeks (Krol et l. 26). However, we i not fin support for our hypothesis tht the lte-suessionl steppe speies in our experiment show positive plnt soil feeks. All three speies re esrie s myorrhizl plnts (Bo n Yn 24; Bo et l. 25), ut we o not hve t on the reiprol reltionships etween these three plnt speies n their ssoite myorrhizl fungi. It oul e tht the host-speifiity of the myorrhizl ssoitions involve in our experimentl system ws low. It oul lso e tht other effets, suh s ioti soil onitions, hve outweighe positive effets of myorrhizl fungi. In ny se, ontrry to wht hs een suggeste for Europen grsslns (Krol et l. 26), positive speies-level plnt soil feeks i not pper to ontriute to persistene of lte-suessionl trget speies in Chinese steppe eosystems.

9 119 The oserve lk of speies-level feeks in our experiment is no reson to elieve tht plnt soil intertions re not importnt to plnt ommunity ynmis in restortion of steppe eosystems. In the ontext of suessionl replements n eosystem restortion, ln-use legy effets, i.e., ontrsting iomss responses to ol-fiels soils n steppe soils, re more relevnt thn speies-level feeks. Olfiel speies generlly performe etter on ol-fiel soils thn on steppe soils. These iomss responses suggest tht hnges in soil properties towrs those foun in steppe soils oul stimulte replement of unwnte ol-fiel speies with trget steppe speies, n hene, enhne steppe restortion. In our stuy, ln-use legies for ol-fiel soils shoul e interprete s omine effet of previous griulturl prties suh s plowing n fertiliztion, n plnt speies-speifi effets of the plnts growing on the soils fter esstion of griulturl prties. No onsistent ifferenes were foun in soil properties etween olfiel n steppe soils n iomss of ol-fiel speies showe interspeifi vrition in orreltions with soil properties. Hene, whih hnges in soil properties woul e most likely to ontrol suessionl replements of ol-fiel speies remins somewht speultive. We suggest tht suessionl uil-up in soil totl C n soil miroil iomss C might ply role s two of the three ol-fiel speies showe negtive orreltions with these prmeters. As illustrte in Fig. 4, within groups of ol-fiel speies n steppe speies, we showe strong speiesspeifi effets on oth ioti n ioti soil properties. While we nnot fully exlue tht speies-speifi vrition in plnt soil reltionships were influene y unerlying soil heterogeneity, these speies-speifi effets strongly suggest tht plnt speies provie unique soil legies whih, in turn, n ffet plnts olonizing these soils fterwrs. Previous stuies hve shown high levels of iiosynrsy in plnt speies responses to heterospeifi soil legies (Bezemer et l. 26; Csper et l. 28; MCrthy-Neumnn n Koe 21). Inee, in our stuy, the legy effets of ol-fiel speies were generlly iiosynrti, i.e., the three steppe speies showe vrile responses to soils of the three olfiels speies. Notwithstning, in our stuy, some soil legy effets were onsistent ross the three steppe speies. For exmple, ll three steppe speies showe the highest iomss proution when grown on soils with history of A. pillris, n ol-fiel for. Soils ollete eneth A. pillris h the highest vlues of plnt-ville P, n plnt-ville P ws the est preitor of iomss for two of the three steppe speies. Similr orreltions etween plnt iomss n ifferenes in nutrient vilility generte y plnts previously growing on the soils hve een shown y Mnning et l. (28). While the orreltive nture of our stuy oes not llow tests for usl effets, these reltionships suggest tht suess of the trget steppe speies epens on the ientity of the ol-fiel speies previously olonizing the soils. Implitions n onlusions Despite the limittion of our experiment (notly, the use of fiel-ollete seelings, n potentil onfouning effets of unerlying soil heterogeneity), the oserve positive effet of ol-fiel soils on ol-fiel speies lerly point t soil-meite retrtion of suessionl evelopment towrs the trget steppe plnt ommunities. This implies tht simultneous ovegroun n elowgroun interventions (Krol n Wrle 21) my e neee to enhne the effiy of suessionl-se restortion progrms in typil Chinese steppe eosystems. However, given the smll numer of plnt speies use in our stuy (three ol-fiel speies, three steppe speies), we shoul e pruent in how we generlize our finings. While our results she some light on the potentil role of plnt soil feeks in restortion of steppe eosystems, the overll high level of iiosynrsy in responses of olfiel n steppe plnt speies to on- n heterospeifi soil legies, inites high interspeifi vrition in the effets of plnt soil feeks on rte n iretion of suessionl replement of unwnte ol-fiel speies y trget steppe speies. Restortion efforts oul gin from improve unerstning of the mehnisms unerlying this interspeifi vrition in plnt soil feek (Suing et l. 24). Rther thn using ro lssifitions s ol-fiel speies n steppe speies, or lterntively, erly-suessionl speies n lte-suessionl speies, it might e more eologilly meningful to lssify speies se on their funtionl trits. Notly, reent stuies inite the ritil importne of plnt funtionl trits in their reltionship to soil orgnisms n soil proesses (e.g., Ehrenfel et l. 25; Queste et l. 27; De Deyn et l. 28). Therefore, we suggest tht more trit-se pprohes in future plnt soil feek stuies re neee to further enhne our unerstning of the role of plnt soil feek in restortion of temperte steppe n other humnisture eosystems. Aknowlegments This reserh ws supporte y the Stte Key Bsi Reserh Development Progrm of Chin (27CB1681) n the Ntionl Nturl Siene Fountion of Chin (38326, ). The uthors thnk Shiqing Wn, Shuli Niu, Jinyng Xi, Weixing Liu, Wenhu Xu, Zhe Zhng, Yng Li, Hijun Yng, n Tingting Li for the help in setting up the experiment n for omments on previous rfts of the mnusript.

10 111 Appenix 1 Men perentge iomss of the ominnt speies in the mono-ominnt plnt pthes Ol-fiel speies Steppe speies Art p Art lv Pen en Art fri Ley hi Sti kry Perentge of iomss ± ± ± ± ± ± 2.7 Art p Artemisi pillris, Art lv Artemisi lvnulefoli, Pen en Pennisetum entrsitium, Art fri Artemisi frigi, Ley hi Leymus hinensis, Sti kry Stip krylovii Appenix 2 Result from one-wy ANOVAs testing effets of soil speies origin (Art p, Art lv, Pen en, Art fri, Ley hi, Sti Kry) on plnt iomss Ol-fiel speies Steppe speies Art p Art lv Pen en Art fri Ley hi Sti kry f F p <.1* <.1*.9 <.1*.5 <.1* Shown re f, F n p vlues Art p Artemisi pillris, Art lv Artemisi lvnulefoli, Pen en Pennisetum entrsitium, Art fri Artemisi frigi, Ley hi Leymus hinensis, Sti kry Stip krylovii * Inites signifint effet Referenes Ayres E, Steltzer H, Simmons BL, Simpson RT, Steinweg JM, Wllenstein MD, Mellor N, Prton WJ, Moore JC, Wll DH (29) Home-fiel vntge elertes lef litter eomposition in forests. Soil Biol Biohem 41:66 61 Bi YF, Hn XG, Wu JG, Chen ZZ, Li LH (24) Eosystem stility n ompenstory effets in the Inner Mongoli grssln. Nture 431: Bo YY, Yn W (24) Arusulr myorrhize n their struturl types on ommon plnts in grsslns of mi-western Inner Mongoli. Bioivers Si 12:51 58 Bo YY, Sun F, Yn W (25) Preliminry stuy on rusulr myorrhizes n their morphologil types of ommon plnts in Inner Mongoli esert region. J Ari Ln Resour Environ 19: Berense F (1994) Litter eomposility neglete omponent of plnt fitness. J Eol 82: Bever JD (1994) Feek etween plnts n their soil ommunities in n ol fiel ommunity. Eology 75: Bever JD, Westover KM, Antonovis J (1997) Inorporting the soil ommunity into plnt popultion ynmis: the utility of the feek pproh. J Eol 85: Bezemer TM, Lwson CS, Helun K, Ewrs AR, Brook AJ, Igul JM, Mortimer SR, Vn er Putten WH (26) Plnt speies n funtionl group effets on ioti n miroil soil properties n plnt-soil feek responses in two grsslns. J Eol 94: Buron JJ (1987) Diseses n plnt popultion iology. Cmrige University Press, Cmrige Csper BB, Bentiveng SP, Ji BM, Doherty JH, Eenorn HM, Gustfson DJ (28) Plnt-soil feek: testing the generlity with the sme grsses in serpentine n pririe soils. Eology 89: Chen X, Lu PF, He G, Ou YZ, Liu J (29) Ftors ffeting ln reonversion plns following pyment for eosystem servie progrm. Biol Conserv 142: Coley PD, Brynt JP, Chpin FS (1985) Resoure vilility n plnt ntiherivore efense. Siene 23: De Deyn GB, Cornelissen JHC, Brgett RD (28) Plnt funtionl trits n soil ron sequestrtion in ontrsting iomes. Eol Lett 11: Ding Y, Niu J, Yng C (26) Stuy on the teneny n formtion uses of grssln egrtion, esertifition n the sustinle evelopment in northern hin: The se of Duolun ounty, Inner Mongoli. J Inn Mong Univ 37: Dorrepl E, Cornelissen JHC, Aerts R (27) Chnging lef litter feeks on plnt proution ross ontrsting surti petln speies n growth forms. Oeologi 151: Eitoril Committee for Vegettion of Chin (198) Vegettion of Chin. Siene Press, Beijing Ehrenfel JG, Rvit B, Elgersm K (25) Feek in the plnt soil system. Annu Rev Environ Resour 3: Hrrison KA, Brgett RD (21) Influene of plnt speies n soil onitions on plnt-soil feek in mixe grssln ommunities. J Eol 98: Hoie SE (1996) Temperture n plnt speies ontrol over litter eomposition in Alskn tunr. Eol Monogr 66: Jnos DP (198) Myorrhize influene tropil suession. Biotropi 12:56 64

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