REGULAR ARTICLE. Wei Xue

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1 Plnt Soil (2018) 428: REGULAR ARTICLE Density-dependency nd plnt-soil feedbck: former plnt bundnce influences competitive interctions between two grsslnd plnt species through plnt-soil feedbcks Wei Xue & T. Mrtijn Bezemer & Frnk Berendse Received: 26 Februry 2018 /Accepted: 17 My 2018 /Published online: 28 My 2018 # The Author(s) 2018 Abstrct Bckgrounds nd ims Negtive plnt-soil feedbcks (PSFs) re thought to promote species coexistence, but most evidence is derived from theoreticl models nd dt from plnt monoculture experiments. Methods We grew Anthoxnthum odortum nd Centure jce in field plots in monocultures nd in mixtures with three rtios (3:1, 2:2 nd 1:3) for three yers. We then tested in greenhouse experiment the performnce of A. odortum nd C. jce in pots plnted with monocultures nd 1:1 mixtures nd filled with live nd sterile soils collected from the field plots. Responsible Editor: W Richrd Whlley. Electronic supplementry mteril The online version of this rticle ( contins supplementry mteril, which is vilble to uthorized users. W. Xue (*): T. M. Bezemer Deprtment of Terrestril Ecology, Netherlnds Institute of Ecology (NIOO-KNAW), PO Box 50, 6700 AB Wgeningen, The Netherlnds e-mil: W.Xue@nioo.knw.nl T. M. Bezemer Institute of Biology, Section Plnt Ecology nd Phytochemistry, Leiden University, PO Box 9505, 2300 RA Leiden, The Netherlnds F. Berendse Nture Conservtion nd Plnt Ecology Group, Wgeningen University, Droevendlsesteeg 3, 6708 PB Wgeningen, The Netherlnds Results In the greenhouse experiment, C. jce produced less boveground biomss in soil conditioned by C. jce monocultures thn in soil conditioned by A. odortum monocultures, while the boveground biomss of A. odortum in generl did not differ between the two monospecific soils. The negtive PSF effect ws greter in the 1:1 plnt mixture thn in plnt monocultures for A. odortum but did not differ for C. jce. In the greenhouse experiment, the performnce of C. jce reltive to A. odortum in the 1:1 plnt mixture ws negtively correlted to the bundnce of C. jce in the field plot where the soil ws collected from. This reltionship ws significnt both in live nd sterile soils. However, there ws no reltionship between the performnce of A. odortum reltive to C. jce in the 1:1 plnt mixture in the greenhouse experiment nd the bundnce of A. odortum in the field plots. Conclusions The response of plnt to PSF depends on whether the focl species grows in monocultures or in mixtures nd on the identity of the species. Interspecific competition cn excerbte the negtive plnt-soil feedbcks compred to intrspecific competition when plnt competes with stronger interspecific competitor. Moreover, the bundnce of species in mixed plnt communities, vi plnt-soil feedbck, negtively influences the reltive competitiveness of tht species when it grows lter in interspecific competition, but this effect vries between species. This phenomenon my contribute to the coexistence of competing plnts under nturl conditions through preventing the dominnce of prticulr plnt species.

2 442 Plnt Soil (2018) 428: Keywords Interspecific competition. Intrspecific competition. Plnt bundnce. Plnt density. Plnt-soil feedbcks. Plnt-soil interctions. Soil biot Introduction Plnts cn lter soil biotic nd biotic properties. These chnges in the soil cn subsequently influence the performnce of the sme or other plnt species tht grow on this substrte, which is known s plnt-soil feedbck (Bever et l. 1997; Ehrenfeld et l. 2005; vn der Putten et l. 2013). Plnt-soil feedbcks cn influence plnt growth positively through the ccumultion of soil nutrients (Berendse 1990; Chpmn et l. 2006; Wrdle et l. 1999) or symbiotic mutulists (Klironomos 2002; vn der Putten et l. 2016) nd negtively by nutrient immobiliztion or depletion (Berendse 1994), or ccumultion of soil pthogens (vn der Putten et l. 2016). Positive feedbcks re thought to promote plnt dominnce nd homogenize plnt communities (Hrtnett nd Wilson 1999; O Connor et l. 2002), while negtive feedbcks llow species coexistence nd increse plnt species diversity (Bever 2003; Bever et l. 1997; Petermnn et l. 2008). Plnt-soil feedbcks of prticulr plnt species re generlly tested by compring the performnce of tht species on soils tht were plnted with monocultures of the sme species nd on soils plnted with monocultures of the other species (Bever et l. 1997; Brinkmnetl. 2010; Kulmtiski et l. 2008). However, in the field, plnts rrely grow in monocultures nd often compete with other plnt species. The presence of other species will not only ffect the soil resources tht re vilble for ech of the component species (Csper nd Jckson 2002; Hwkesetl.2005), but lso ffect the composition of the soil community including both mutulistic nd pthogenic orgnisms (Brtelt-Ryser et l. 2005; Eisenhuer 2016; Husmnn nd Hwkes 2009). Conspecific plnt-soil feedbck effects my be weker in soils conditioned by plnt mixtures thn in soils conditioned by monocultures of tht species, due to the lower bundnce of the focl species in plnt mixtures (Hwkes et l. 2013). Severl studies hve suggested tht negtive plnt-soil feedbcks in nturl systems might be density-dependent (Bgchi et l. 2010; Bell et l. 2006; Comitetl.2014; Kos et l. 2013; vnde Voorde et l. 2011). If the locl density of species in plnt community increses, species-specific soil pthogens re expected to increse s well, thus decresing the per cpit fitness of tht plnt species (Bgchi et l. 2010). However, only one study hs empiriclly exmined this so fr (Dudenhöffer et l. 2018). The response of plnt to plnt-soil feedbck depends on whether the plnt grows individully or in competition with other plnts, nd severl studies hve shown tht negtive plnt-soil feedbcks re generlly enhnced in the presence of competitors (e.g. Cllwy et l. 2004; Hol et l. 2013; Kulmtiski et l. 2008; Shnnon et l. 2012). However, whether plnts grown in monocultures (nd hence experience intrspecific competition) nd grown in plnt mixtures (nd experience interspecific competition) respond differently to plnt-soil feedbcks is poorly understood. Csper nd Cstelli (2007) proposed tht negtive conspecific plntsoil feedbcks re expected to be more pronounced when plnts compete with the sme species (intrspecific competition) thn with other plnt species (interspecific competition). However, Krdol et l. (2007)nd Petermnn et l. (2008) reported tht the negtive response of plnts to plnt-soil feedbck is stronger when the plnts grew in interspecific competition thn when grew in intrspecific competition. Recently, Jing et l. (2015) demonstrted tht when two plnts compete, the soil feedbck effects of one species cn negtively influence the other competing species more thn tht it influences the conspecific species, even though the conspecific species suffers from negtive plnt-soil feedbcks when grown lone. Hence, in interspecific competition, it cn be either dvntgeous or disdvntgeous for species to grow in the soil conditioned by the sme species (Jing et l. 2015). It remins unresolved how the density of plnt species in mixed plnt community, vi plnt-soil feedbck, influences the competition between two plnt species when they grow lter in the soil where these plnts were previously growing. Mny plnt-soil feedbck studies compre the growth of plnt in sterilised soils with nd without ddition of soil inoculum (e.g. vn der Putten et l. 1993; Krdol et l. 2006; Kos et l. 2013). However, dding smll mount of live soil to lrge mount of sterilised bulk soil my not result in representtive soil communities. For exmple, the density of the soil community my be very different from tht observed outdoors in the field (Brinkmn et l. 2010). Alterntively, plnt-soil feedbcks cn be determined by compring plnt growth in sterilised nd unsterilised pure soils. Sterilising typiclly results in incresed vilbility of

3 Plnt Soil (2018) 428: soil nutrients (Brinkmn et l. 2010). Plnt-soil feedbcks cn be driven simultneously by biotic nd biotic chnges in the soil. Therefore, the difference between the performnce of plnt in unsterilised nd sterilised soil would be net effect of the elimintion of soil biot nd the increse in soil nutrients. The im of the present study ws to investigte how, vi plnt-soil feedbcks, the bundnce of species in plnt community consisting of two species influences the growth nd competition between these two species when they grow lter in the soil. We grew the grss Anthoxnthum odortum nd the forb Centure jce in field plots in monocultures nd in mixtures with three rtios (3:1, 2:2 nd 1:3) for three yers. We then tested the performnce of A. odortum nd C. jcee in greenhouse experiment with the two species grown in monocultures nd in 1:1 mixtures in pots filled with either unsterilised or sterilized soils collected from the field plots. We specificlly hypothesised tht: (1) plnts will produce less biomss in Bown^ soil (conditioned by conspecific monocultures) thn in Bforeign^ soil (conditioned by heterospecific monocultures) s conspecific plnt-soil feedbcks re generlly negtive. As consequence, when two plnt species grow in mixtures (interspecific competition), the plnt species tht encounters its Bown^ soil will be t competitive disdvntge. (2) Negtive conspecific plnt-soil feedbck effects will increse with greter bundnce of tht species during the previous growth phse (i.e. conditioning phse) in the plnt community, e.g. due to the build-up of speciesspecific soil pthogens in the soil. (3) Negtive conspecific plnt-soil feedbcks will be stronger when plnts grow in 1:1 plnt mixtures thn when they grow in monocultures, s the competing species will not suffer from negtive plnt-soil feedbcks nd hence will be stronger competitor. (4) Plnt-soil feedbcks will be stronger in live soil thn in sterile soil s steriliztion will eliminte the soil biot tht cn drive the plnt-soil feedbcks. Methods nd mterils Plnt species Our study species were Anthoxnthum odortum L. (Pocee) nd Centure jce L. (Astercee). A. odortum is perennil grss tht produces closely connected rmets, while C. jce is long-lived perennil herb tht hs monocrpic shoots nd cn form extensive belowground brnches (Jongejns nd de Kroon 2005). Both species re ntive grsslnd species in western Europe. They hve similr life history strtegies, i.e., with clonl growth s well s sexul reproduction (Hrtemink et l. 2004) nd commonly coexist in medows (vn Ruijven nd Berendse 2003). Grden experiment We performed long-term competition experiment with A. odortum nd C. jce in field plots from April 2013 to September In this experiment, we plnted A. odortum nd C. jce in monocultures s well s in mixtures t three plnting rtios (3:1, 2:2 nd 1:3) in plots (1 1 m 2 ). Blck soil (totl N: 2.13 g kg 1 ;totlc: 28.2 g kg 1 ; totl P: 2.39 g kg 1 ) ws used in ech plot. Soils collected from these experimentl plots were coded s Ao soil (conditioned by monocultures of A. odortum), Cj soil (conditioned by monocultures of C. jce), 3Ao/1Cj soil (conditioned by 3:1 mixture of A. odortum nd C. jce), 2Ao/2Cj soil (conditioned by 2:2 mixture of A. odortum nd C. jce) nd 1Ao/ 3Cj soil (conditioned by 1:3 mixture of A. odortum nd C. jce), respectively. The totl number of seedlings plnted in ech plot ws 144. Ech tretment hd five replicte blocks, yielding 25 plots. Plots were weeded regulrly. In September 2015, we clipped ech plnt in the centrl cm 2 t height of 1 cm nd determined the boveground biomss of ech of the two plnt species in ech plot fter oven-drying it to constnt weight. In Februry 2016, we collected the soil from the centrl re of cm 2, to depth of 20 cm of ech experimentl plot. The soil from ech plot ws sieved (1.5 cm mesh) nd seprted in two prts. Hlf of the soil from ech plot ws sterilized by γ-irrdition (minimum 25KGry, Isotron, Ede, the Netherlnds) so tht there were 50 different conditioned soils (5 plnting tretments 2 steriliztion tretments 5 replicte blocks). Greenhouse experiment Ech of the 50 soil smples ws used to fill three pots (21 cm in top-dimeter nd 18 cm in height) with 5.6 kg soil in ech pot (Fig. 1) so tht the entire experiment consisted of 150 pots. Pots filled with soils collected in the sme field block were llocted to the sme block in the greenhouse experiment so tht there were five blocks

4 444 Plnt Soil (2018) 428: corresponding to the blocks in the field experiment. Pots of different tretments were rndomized within ech block. Before filling the pots, we plced piece of filter pper (15 cm in dimeter) t the bottom of ech pot to prevent soil from pssing through holes in the bottom of the pot but llowing verticl movement of wter. Ech pot ws plced on try to prevent possible contmintion through lechte. For soil chemicl nlysis, we rndomly selected three blocks, nd took soil smples (5 plnting tretments 2 steriliztion tretments) from ech selected block. Unsterilised soils (not sterilised by γ-irrdition; live soil) nd sterile soils (sterilized by γ-irrdition) were nlysed seprtely. We mesured soil orgnic mtter content, nutrient content (NH 4,NO 3 nd PO 4 ), wter content nd ph (Tble 1; Methods S1). We purchsed seeds of A. odortum nd C. jce from specilized compny (Cruydthoeck, Nijeberkoop, the Netherlnds). All seeds of ech plnt species were evenly sown on plstic trys filled with stemed potting soil (3 N-3P-3 K, Seed Strting Potting Mix, Mircle-Gro Lwn Products, Inc., Mrysville) tht fcilittes fst root development in heted greenhouse (2 C verge temperture, 70.2% verge reltive humidity). The trys were wtered dily. One week fter germintion, the trys with seedlings were moved to n unheted greenhouse (12.8 C verge temperture, 70.3% verge reltive humidity) until they were trnsplnted into the pots. We plnted similr-sized seedlings of A. odortum nd C. jce in ech pot in either monocultures or 1:1 mixtures (Fig. 1). In monocultures, we plnted 16 seedlings of A. odortum or C. jce in ech pot. In the 1:1 mixtures, we plnted eight seedlings of A. odortum nd eight seedlings of C. jce in lternting positions (Fig. 1). After one week, we replced ded seedlings. All other species emerging from the seed bnk of the soil were removed mnully during the experiment. The experiment ws mintined for 90 dys (from 11 April to 11 July 2016) in the sme unheted greenhouse. During the experiment, the men temperture nd the reltive humidity in the greenhouse were 17.4 C nd 67.5%. Wter ws dded to ll pots three times per week. Hrvest nd mesurement Ninety dys fter trnsplnting, we clipped ll plnts t the soil level. The two different plnt species in the 1:1 mixtures were hrvested seprtely. We lso took four soil cores (4.0 cm dimeter, stright down to the bottom of pot) in ech pot to mesure the root mss (Fig. 1). We only took soil cores from pots plnted with monocultures becuse it ws not possible to seprte roots of the two different plnt species in the mixtures. We then wshed ll root smples over 0.5 mm sieve. Aboveground prts nd belowground prts of ech plnt species in ech pot were oven-dried t 70 C for 48 h nd weighted. Dt nlysis In the grden experiment, we used replcement digrms to show the biomss of the two species in ll plnting tretments (i.e., monocultures nd mixtures t three different rtios: 3:1, 2:2 nd 1:3), nd used the reltive crowding coefficient (k) of species to ssess its competitive bility in the mixtures reltive to tht in the monocultures (De Wit 1960). We clculted k s: ð ðz 1Þ =zþ ðo=mþ O M 1 1,inwhichz is the plnting frequency of species in the mixtures, O nd M re the boveground biomss of tht species in mixtures nd in monocultures, respectively. We then used liner regressions to ssess whether k ws dependent on the plnting frequencies of ech species. In the greenhouse experiment, we first clculted boveground biomss per plnt of A. odortum nd C. jce in ech pot, since monocultures hd twice s mny individuls per species t the strt of the experiment s mixtures. As belowground biomss ws determined by tking soil cores, it ws clculted s the men of the root biomss in the four soil cores nd not s the root biomss per pot. Dt of boveground nd belowground biomss were log trnsformed to improve the normlity nd homogeneity of vrince. We first nlysed the boveground nd belowground biomss of ech plnt species on the two soils collected from the monospecific plots in the field (i.e., Ao soil nd Cj soil collected from the grden experiment; monospecific soil) to test whether there ws soil type effect on the performnce of the two species. We first performed full-model nlysis including species (A. odortum vs. C. jce), soil type (soil type ws tested s Bown^ soil vs. Bforeign^ soil), steriliztion (live vs. sterile), competition (monocultures vs. mixtures; only for boveground

5 Plnt Soil (2018) 428: Conditioning phse Soil tretments in the conditioning phse Live Sterile Live Sterile Live Sterile Live Sterile Live Sterile 2. Test phse A. odortum in monoculture Fig. 1 Schemtic representtion of the experimentl design. (1) Conditioning phse: conditioned soils were collected from threeyer field experiment, in which soils were conditioned seprtely by monocultures of A. odortum nd C. jce, s well s mixtures of these two species t three plnting rtios (3:1, 2:2 nd 1:3). Conditioned soils were either sterilized or not (i.e., live nd sterile), resulting in 10 soil tretments. (2) Test phse: we plnted either 16 A. odortum nd C. jce in 1:1 mixture C. jce in monoculture plnts of species A. odortum or species C. jce in monocultures, or eight plnts of ech of the species in mixtures in ech of the ten soil tretments in greenhouse experiment. White nd blck dots represent the initil positions where A. odortum nd C. jce were grown. The shded circles within ech pot represent the positions where we took soil smples biomss) nd their interctions s fixed fctors, with block s rndom fctor. Subsequently, we seprtely nlysed biomss of ech species using mixed-effect ANOVA with soil type, steriliztion, competition (only for boveground biomss) nd their interctions s fixed fctors, nd block s rndom fctor. To test if plnt-soil feedbck (PSF) differed in response to competition mode nd steriliztion tretment, we clculted the PSF s the log-rtio of plnt biomss on Bown^ nd Bforeign^ soils (ln Biomss own Biomss foreign ) for ech combintion of species, competition nd steriliztion. PSFs were clculted seprtely for ech replicte nd bsed on boveground biomss (boveground PSF) nd belowground biomss (belowground PSF). We nlysed the PSF-vlues using full-model nlysis including species, steriliztion, competition (only for boveground PSF) nd their interctions s fixed fctors, with block s rndom fctor, followed by seprte nlyses using mixed-effect ANOVA with steriliztion, competition (only for boveground PSF) nd the interction (only for boveground PSF) s fixed fctors, nd block s rndom fctor. Since in the pots plnted with plnt mixtures the growth of the two species is not independent, we evluted the competition between the two species by clculting for ech pot the competitive blnce index (CB). The CB ws clculted s: ln MIX Ao MIX Cj with MIX Ao nd MIX Cj representing the biomss of A. odortum nd C. jce in the 1:1 mixtures in the greenhouse experiment, respectively. Using this index, the performnce of the two species in pot ws combined. CB will be equl to zero if the two species perform eqully well in mixtures; CB

6 446 Plnt Soil (2018) 428: Tble 1 Abiotic chrcteristics of live nd sterile soils collected from the field plots Steriliztion Soil P-PO 4 (mg/kg) N-NO 3 (mg/kg) 1 N-NH 4 (mg/kg) ph (H 2 O) Moisture (%) Orgnic Mtter (%) Live soils Ao soil 0 ± 0 d ± 4.00 b 6.85 ± 0.11 b ± ± Ao/1Cj soil 0.16 ± 0.12 bcd 0.50 ± ± 4.91 b 6.97 ± 0.16 b ± ± Ao/2Cj soil 6 ± 6 cd 0.57 ± ± 3.80 b 6.95 ± 0.15 b ± ± Ao/3Cj soil 6 ± 6 cd 0.56 ± ± 4.99 b 7.02 ± 0.11 b ± ± 0.58 Cj soil 0.25 ± 0.12 bcd 0.66 ± ± 3.89 b 6.98 ± 0.20 b ± ± 0.16 Sterile soils Ao soil 0.67 ± 0.21 bc 0.90 ± ± ± 5 b ± ± Ao/1Cj soil 0.22 ± 0.12 bcd 0.50 ± ± 1.30 b 7.15 ± ± ± Ao/2Cj soil 0.73 ± 0.15 b 0.54 ± ± 1.13 b 7.19 ± ± ± Ao/3Cj soil 0.49 ± 0.16 bcd 0.58 ± ± 0.82 b 7.16 ± ± ± 0.23 Cj soil 1.09 ± ± ± 5.17 b 7.17 ± ± ± 0.55 ANOVA Steriliztion 37.10*** *** 21.17*** Soil 3.36* Interction Mens (±SE), nd F- ndp-vlues of two-wy ANOVAs re given. Men vlues shring the sme superscript (-d) re not significntly different mong the ten soils in ech column (Tukey post hoc tests). Ao soil nd Cj soil represent soils conditioned by monocultures of A. odortum nd C. jce, respectively, while 3Ao/1Cj soil, 2Ao/2Cj soil nd 1Ao/3Cj soil represent the soils conditioned by 3:1, 2:2 nd 1:3 mixtures of A. odortum nd C. jce, respectively. *** P <01, ** P <1, * P <5 1 Dt ws log-trnsformed. Dt of N-NO 3 in the live soil conditioned by monoculture of A. odortum (Ao soil) ws bsed on only one smple will be positive if the biomss of A. odortum is higher thn C. jce nd negtive if C. jce biomss is higher. A one-smple t-test ws used to test whether the CB differed from zero. We used two-wy ANOVA to test the effects of soil type (Ao soil vs. Cj soil), steriliztion nd their interction on the CB on the two monospecific soil types. Block ws included s rndom fctor. Mens of the CB vlues on different monospecific soils were compred using post-hoc test for pirwise comprison. Further, the reltionship between the growth of either A. odortum or C. jce in the greenhouse experiment nd its former bundnce in the field plots ws nlysed using liner regression for ech species, steriliztion nd competition (only for boveground biomss) combintion. The reltionship between the CBs between the two species in the greenhouse experiment nd the former bundnce of either A. odortum or C. jce in the field plots ws lso nlysed using liner regression seprtely for live nd sterile soils. We performed ll dt nlysis using R (version 3.3.2) ( in RStudio (version ) ( Liner mixed-effect models were fitted with nlme (version ) (Pinheiro et l. 2016). Post-hoc comprisons were tested s plnned contrsts using the multcomp pckge (version 1.4 6) in R (Hothorn et l. 2008). All dt were checked grphiclly for normlity nd homogeneity for vrince. Results Biomss of the two plnt species nd soil properties in the field plots In ll mixtures, the totl boveground biomss of C. jce per plot ws significntly greter thn tht of A. odortum (Fig. S1). A. odortum showed n inverse sigmoid curve in the replcement digrm (Fig. S1)nd its competitive bility (reltive crowding coefficient, k) decresed with incresing frequency (Fig. S2A). There ws no significnt reltionship between the competitive bility of C. jce nd its plnting frequency (Fig. S2B). The mount of P-PO 4, N-NH 4,ndthepH(H 2 O) were significntly higher in sterile soil thn in live soil but there ws no difference in the mount of N-NO 3,in soil moisture nd in orgnic mtter between live nd sterile soils (Tble 1). Overll, none of the mesured properties except P-PO 4 ws different mong the five soils (Ao soil, 3Ao/1Cj soil, 2Ao/2Cj soil, 1Ao/3Cj soil

7 Plnt Soil (2018) 428: nd Cj soil; Tble 1). The mount of P-PO 4 ws overll higher in Cj soil thn in other soils (Tble 1). Plnt-soil feedbck effects in monospecific soils in the greenhouse experiment In the greenhouse experiment, C. jce overll produced less boveground biomss when grown in Bown^ soil (Cj soil) thn in Bforeign^ soil (Ao soil), while boveground biomss of A. odortum did not differ between the two soils (Tble S1A, S2A; Fig. 2, b). A. odortum produced more boveground biomss in sterile soil thn in live soil in both plnt monocultures nd the 1:1 plnt mixture, but the difference ws much bigger in the 1:1 plnt mixture thn in plnt monocultures (Tble S2A; Fig. 2). In monocultures, C. jce lso produced more boveground biomss in sterile soil thn in live soil, but in the 1:1 plnt mixture, there ws no difference between these two steriliztion tretments (Tble S2A;Fig.2b). The belowground biomss of A. odortum ws significntly greter in live Bforeign^ soil thn in live Bown^ soil, but did not differ in sterile Bforeign^ nd Bown^ soil (Tble S2B; Fig. 2c). In contrst, belowground biomss of C. jce did not differ between Bforeign^ nd Bown^ soil in either live or sterile soils (Tble S1B, S2B; Fig. 2d). The boveground PSF of A. odortum tended to be lower in the1:1 plnt mixture thn in the plnt monoculture independent of steriliztion tretment (Tble S3A; Fig. S3A). Generlly, the boveground PSF of C. jce ws A. odortum C. jce 1.0 (A) 1.0 (B) b b d c c c b bc bc c Live Sterile Live Sterile Live Sterile Live Sterile 1.0 (C) 1.0 (D) b b 0.2 c b 0.2 Live Sterile Live Sterile Fig. 2 Aboveground biomss per plnt ( nd b), nd belowground biomss per soil core (c nd d) ofa. odortum ( nd c) nd C. jce (b nd d) on Bown^ (soil conditioned by monocultures of the sme species) nd Bforeign^ soils (soil conditioned by monocultures of the other species) in the greenhouse experiment. BSterile^ nd BLive^ indicte sterilized soil nd non-sterilized soil respectively. Plnts were grown in monocultures nd in 1:1 mixtures in the greenhouse experiment. Men vlues (± 1 SE) re presented. Letters bove the brs indicte significnt differences in boveground biomss mong ech pnel

8 448 Plnt Soil (2018) 428: negtive, but there ws no difference between plnt monocultures nd 1:1 plnt mixtures (Tble S3A;Fig. S3B). The belowground PSF of A. odortum ws significntly greter in sterile soil thn in live soil but there ws no difference between these two soil types for C. jce (Tble S3B;Fig. S3C, D). Competitive blnce between the two species grown in the 1:1 plnt mixture in monospecific soils in the greenhouse experiment The competitive blnce index (CB: performnce of A. odortum in the 1:1 mixture reltive to tht of C. jce) ws greter in sterile soil thn in live soil (Fig. 3). Overll, C. jce ws superior to A. odortum in live soil while the reverse ws true in sterile soil (Fig. 3). The competitive blnce, CB ws significntly smller in live Ao soil thn in live Cj soil, but there ws no significnt difference in CB between sterile Ao nd sterile Cj soil. CB ws significntly smller thn zero in live Ao soil, but did not differ from zero in live Cj soil, indicting tht C. jce ws competitively superior in live Ao soil, but not in live Cj soil. In sterile Competitive blnce between A. odortum nd C. jce Ao soil Cj soil * ns c b Soil * ST *** -2.0 Live Sterile MIX Ao Fig. 3 Competitive blnce (CB; lnmix Cj ) between A. odortum nd C. jce in the 1:1 mixture on Ao soil (soils collected from field plots with A. odortum monocultures) nd Cj soil (soils collected from field plots with C. jce monocultures) in the greenhouse experiment in sterile nd live soil. Men vlues (± 1 SE) nd significnt effects of two-wy ANOVA with soil type (Soil), steriliztion (ST) nd the interction re presented, the superscript sterisks give P: *P < 5 nd *** P <01. Brs tht shre the sme letters re not significnt different bsed on Tukey post-hoc comprison. Negtive CB vlues indicte tht the biomss of C. jce is higher thn tht of A. odortum, while positive CB vlues indicte tht A. odortum biomss is higher. The sterisk t the strt of the first br indicte tht the vlues differ from zero (P < 5) bsed on one-smple t-test, ns indictes not significnt b ns ns soil, the pttern ws similr but A. odortum ws superior over C. jce (Fig. 3). Reltionships between the growth nd competitive blnce in the greenhouse nd bundnce (biomss) in the field plots For both species, there ws no significnt reltionship between the growth (boveground biomss nd belowground biomss) of the species in the greenhouse experiment nd the bundnce of either species in the field experiment (ll P >5;Fig.S4-S6). The CB between A. odortum nd C. jce in the greenhouse experiment ws negtively correlted to the bundnce of A. odortum in the field experiment in live soil (Fig. 4), but not in sterile soil (Fig. 4b). However, this pttern ws cused by one dt point nd ws no longer significnt fter removing this point (Fig. S7). There ws significnt positive reltionship between the CB between A. odortum nd C. jce in the greenhouse experiment nd the bundnce of C. jce in the field experiment in both live (Fig. 4c) nd sterile soil (Fig. 4d). Discussion In the present study, we show tht the competitive blnce (the performnce of A. odortum reltive to C. jce) in the greenhouse ws relted to the former bundnce of C. jce, while it ws independent of the former bundnce of A. odortum in the field. This result implies tht the bundnce of plnt species in mixed communities cn influence the competitive interctions of lter growing plnts vi plnt-soil feedbck effects, but tht these effects vry between species. Negtive plnt-soil feedbck strength is often ssumed to increse with previous plnt density, but this hs been rrely tested (e.g., Bgchi et l. 2010; Bell et l. 2006; Comit et l. 2014; Kos et l. 2013). In the present study, we therefore expected negtive reltionship between the growth of species in the greenhouse experiment nd its former bundnce in the field. However, we did not find such reltionship for either of the two species. A possible explntion is tht C. jce ws competitively superior in ll field plots nd produced much more biomss thn A. odortum, even t low plnting densities (Fig. S1). Hence, C. jce my hve plyed dominnt role in conditioning the soils in ll mixtures, which my explin

9 Plnt Soil (2018) 428: Live soil Monocultures in field Mixtures in field Sterile soil Fig. 4 Reltionship between the biomss of A. odortum ( nd b) orc. jce (c nd d) in the field plots nd the competitive MIX Ao blnce (CB;lnMIX Cj )betweena. odortum nd C. jce in the 1:1 plnt mixture in the greenhouse experiment. For the CB, negtive vlues indicte tht the biomss of C. jce is higher thn tht of A. odortum, while positive vlues indicte A. odortum biomss is higher. Blck nd white dots represent soils collected from field plots plnted with monocultures nd mixtures, respectively. The F-, R 2 -ndp-vlues obtined from liner regressions re lso presented the lck of reltionship between the growth of species in the greenhouse experiment nd its former bundnce in the field. However, it is lso importnt to note tht low-productive plnt species my hve much lrger impct on the soil thn highly productive species. Another possible explntion my relte to the nondditivity of plnt-soil feedbcks (Hwkes et l. 2013; Kuebbing et l. 2014). Growth of test plnt species in soil conditioned by different plnt species simultneously is not necessrily the sme s the verged effects those species hve in monocultures. We expected tht the former plnt bundnce of one species my hve negtive influence on its competitive performnce lter on. Indeed we observed tht there ws negtive reltionship between the density in the field nd the competitive performnce for both A. odortum nd C. jce lthough the significnce of the reltionship for A. odortum ws determined by one dt point. In the present study, the two plnts my hve conditioned the soil differently, it is possible tht the conditioning effects of A. odortum on the soil were overll wek even though its biomss vried strongly mong the field plots (Fig. S4). Remrkbly, the negtive effects of the former bundnce of C. jce on its competitive performnce occurred both in live nd sterile soils. In this study, A. odortum benefited more from higher soil nutrient vilbility thn C. jce s indicted by the positive impct of steriliztion on the performnce of A. odortum reltive to C. jce. Potentilly, C. jce

10 450 Plnt Soil (2018) 428: which ws more productive thn A. odortum in the field my hve produced more lbile soil orgnic mtter leding to incresed soil nutrient vilbility (Berendse 1990), which, in turn, could fvour A. odortum more thn C. jce (Fig. S8). However, in our study, we did not observe n increse in vilbility of nutrients in C. jce soils (Tble 1). Alterntively, we speculte tht these negtive plnt-soil feedbck effects my be driven by llelopthic effects (Cllwy nd Aschehoug 2000). It is possible tht the root exudtes of C. jce in both live nd sterile soils reduced the performnce of C. jce reltive to A. odortum. Our results would then suggest tht llelopthy my inhibit or slow down the dominnce of prticulr species in interspecific competition, promoting the coexistence of species. We hypothesized tht negtive plnt-soil feedbcks would be stronger in the 1:1 plnt mixture thn in plnt monocultures (Krdol et l. 2007; Petermnn et l. 2008; vn der Putten nd Peters 1997). We found only limited evidence for this. The performnce of A. odortum ws reduced more in live Bown^ soil thn in live Bforeign^ soil when grown in competition i.e., in the 1:1 plnt mixture thn when grown in plnt monoculture nd similr trend ws observed for C. jce.in the 1:1 plnt mixture in the greenhouse experiment, C. jce ws competitively superior to A. odortum in live soil, nd the performnce of C. jce in its Bown^ soil ws less reduced when grown together with A. odortum, while the performnce of A. odortum in its Bown^ soil ws much more reduced when grown with C. jce. These results would suggest tht interspecific competition cn excerbte negtive plnt-soil feedbck effects compred to intrspecific competition, but only when plnt competes with stronger competitor. We expected tht negtive plnt-soil feedbcks would be stronger in live soil thn in sterile soil. In greement with our hypothesis, the negtive plnt-soil feedbck effects of A. odortum were smller or less negtive in sterile soil thn in live soil, but for C. jce this ws not true. This result indictes tht the negtive feedbcks encountered by A. odortum ppers to be biotic while tht by C. jce is biotic. However, it should be noted tht steriliztion of soils cn chnge soil fetures such s nutrient vilbility (Brinkmn et l. 2010; Jkobsen nd Andersen 1982; Powlson nd Jenkinson 1976), nd fst-growing species of microorgnisms cn develop rpidly in sterilized soil (Brinkmn et l. 2010; de Boer et l. 2003). Overll, our results regrding the effects of steriliztion on plntsoil feedbcks effects re inconclusive, even though, steriliztion per se, hd lrge effect on plnt growth nd plnt competition. We conclude tht conspecific plnt-soil feedbcks cn negtively influence plnt growth nd tht the negtive effects tend to be stronger when the test plnts grow in interspecific competition thn when they grow in intrspecific competition. Moreover, the former bundnce of species in mixed plnt communities, vi plnt-soil feedbck, cn negtively influence the reltive competitiveness of tht species when it grows lter in interspecific competition. However, our study lso shows tht these plnt-soil feedbck effects depend on the identity of the plnt species. In broder context, the density dependent feedbck effects my prevent the dominnce of one species nd promote the coexistence of competing plnt species in nturl systems. Acknowledgements We thnk Jn vn Wlsem nd Frns Möller for helping with the estblishment of the experiment, Peiyu Zhng, Cong Chen nd Ningjing Liu for helping with the hrvest of the experiment, nd two nonymous reviewers for very useful comments on erlier versions of the mnuscript. This work ws funded by the Chin Scholrship Council (No ). This is publiction xxxx of the Netherlnds Institute of Ecology (NIOO-KNAW). Open Access This rticle is distributed under the terms of the Cretive Commons Attribution 4.0 Interntionl License ( cretivecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, nd reproduction in ny medium, provided you give pproprite credit to the originl uthor(s) nd the source, provide link to the Cretive Commons license, nd indicte if chnges were mde. References Bgchi R, Swinfield T, Gllery RE, Lewis OT, Gripenberg S, NrynL,FreckletonRP(2010)TestingtheJnzen- Connell mechnism: pthogens cuse overcompensting density dependence in tropicl tree. Ecol Lett 13: Brtelt-Ryser J, Joshi J, Schmid B, Brndl H, Blser T (2005) Soil feedbcks of plnt diversity on soil microbil communities nd subsequent plnt growth. Perspect Plnt Ecol Evol Syst 7:27 49 Bell T, Freckleton RP, Lewis OT (2006) Plnt pthogens drive density-dependent seedling mortlity in tropicl tree. Ecol Lett 9: Berendse F (1990) Orgnic mtter ccumultion nd nitrogen minerliztion during secondry succession in hethlnd ecosystems. J Ecol 78:

11 Plnt Soil (2018) 428: Berendse F (1994) Litter decomposbility- neglected component of plnt fitness. J Ecol 82: Bever JD (2003) Soil community feedbck nd the coexistence of competitors: conceptul frmeworks nd empiricl tests. New Phytol 157: Bever JD, Westover KM, Antonovics J (1997) Incorporting the soil community into plnt popultion dynmics: the utility of the feedbck pproch. J Ecol 85: Brinkmn EP, vn der Putten WH, Bkker E-J, Verhoeven KJF (2010) Plnt-soil feedbck: experimentl pproches, sttisticl nlyses nd ecologicl interprettions. J Ecol 98: Cllwy RM, Aschehoug ET (2000) Invsive plnts versus their new nd old neighbors: mechnism for exotic invsion. Science 290: Cllwy RM, Thelen GC, Brth S, Rmsey PW, Gnnon JE (2004) Soil fungi lter interctions between the invder Centure mculos nd North Americn ntives. Ecology 85: Csper BB, Cstelli JP (2007) Evluting plnt-soil feedbck together with competition in serpentine grsslnd. 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