Root plasticity of native and invasive Great Basin species in response to soil nitrogen heterogeneity

Transcription

1 Plnt Ecol (2009) 202: DOI /s #625 Root plsticity of ntive nd invsive Gret Bsin species in response to soil nitrogen heterogeneity J. J. Jmes Æ J. M. Mngold Æ R. L. Sheley Æ T. Svejcr Received: 29 Octoer 2006 / Accepted: 27 June 2008 / Pulished online: 6 July 2008 Ó Springer Science+Business Medi B.V Astrct Soil nutrients re heterogeneously distriuted in nturl systems. While mny species respond to this heterogeneity through root system plsticity, little is known out how the mgnitude of these responses my vry etween ntive nd invsive species. We quntified root morphologicl nd physiologicl plsticity of co-occurring ntive nd invsive Gret Bsin species in response to soil nitrogen heterogeneity nd determined if trde-offs exist etween these forging responses nd species reltive growth rte or root system iomss. The nine study species included three perennil unchgrsses, three perennil fors, nd three invsive perennil fors. The plnts were grown in lrge pots outdoors. Once week for 4 weeks equl mounts of 15 NH 15 4 NO 3 were distriuted in the soil either evenly through the soil profile, in four ptches, or in two ptches. All species cquired more N in ptches compred to when N ws pplied evenly through the soil profile. None of the species incresed root length density in enriched ptches compred to control ptches ut ll species incresed root N uptke rte in enriched ptches. There ws positive reltionship etween N uptke rte, reltive growth rte, nd root system iomss. Pth J. J. Jmes (&) J. M. Mngold R. L. Sheley T. Svejcr USDA-Agriculturl Reserch Service, Estern Oregon Agriculturl Reserch Center, AHwy 205, Burns, OR 97720, USA e-mil: jeremy.jmes@oregonstte.edu nlysis indicted tht these positive interreltionships mong trits could provide one explntion of how invsive fors were le to cpture 2 nd 15-fold more N from enriched ptches compred to the ntive grsses nd fors, respectively. Results from this pot study suggest tht plnt trits relted to nutrient cpture in heterogeneous soil environments my e positively correlted which could potentilly promote size-symmetric competition elowground nd fcilitte the spred of invsive species. However, field experiments with plnts in different neighor environments ultimtely re needed to determine if these positive reltionships mong trits influence competitive ility nd invder success. Keywords Bunchgrsses Fors Nutrients Rngelnd Root forging Weeds Introduction Sptil nd temporl vrition in nutrient vilility is common feture of soils in nturl systems (Strk 1994; Gross et l. 1995; Frley nd Fitter 1999). While numer of studies hve shown tht plnts cn increse resource cpture in heterogeneous soil environments y mking morphologicl nd physiologicl djustments to the root system (Hodge 2004) the mgnitude of these forging responses vries sustntilly mong species (Roinson 1994). Severl hypotheses hve een proposed to explin this

2 212 Plnt Ecol (2009) 202: vrition in plsticity mong species. For exmple, it hs een hypothesized tht species with high reltive growth rtes (RGR) will demonstrte greter degree of morphologicl plsticity in response to soil nutrient heterogeneity thn species with low RGR, tht demonstrte greter degree of physiologicl plsticity compred to species with high RGR (Grime 1979; Cmpell nd Grime 1989). Likewise, trdeoff etween root system size nd the ility of species to selectively plce roots in nutrient rich ptches (root forging precision) hs een proposed, with species of smll root systems predicted to forge more precisely for nutrients thn species with lrger root systems (Cmpell et l. 1991). Whether or not trde-offs exist etween root trits hs decidedly different ecologicl implictions. If there re trde-offs mong trits, then different species my e fvored in different soil environments nd heterogeneity in soil nutrient vilility could potentilly fcilitte species coexistence. Alterntively, if there re positive reltionships etween trits, then heterogeneity in soil nutrient vilility could promote size symmetric competition elowground, potentilly inhiiting coexistence (Schwinning nd Weiner 1998; Frnsen et l. 2001; Rjniemi nd Reynolds 2004). Given the impct nutrient heterogeneity my hve on plnt growth nd species interctions it is not surprising tht much reserch hs focused on understnding the mechnisms of plnt response to this vrition. However, the mjority of this reserch hs een centered on crop species or compred species from different hitts or successionl stges (e.g., Drew nd Sker 1975; Cmpell et l. 1991; Roinson 1994). Less is known out how root response to nutrient heterogeneity vries mong species within community nd in prticulr, how nutrient heterogeneity my influence interctions etween ntive nd invsive species (Einsmnn et l. 1999; Rjniemi nd Reynolds 2004; Stevens nd Jones 2006; Pdill et l. 2007). The rod ojective of this study ws to quntify vrition in root morphologicl nd physiologicl plsticity of co-occurring ntive nd invsive species in response to soil nitrogen (N) heterogeneity nd determine if trde-offs exist etween these forging responses nd species RGR or root system size. The species selected for this study re widely distriuted in the sgerush steppe of the Gret Bsin. Nutrients in these resource-poor systems re typiclly supplied in short-lived ptches (Jckson nd Cldwell 1993; Ryel et l. 1996). The ephemerl nture of nutrient supply in the sgerush steppe suggests tht the ility of species to respond rpidly to nutrient ptches through root plsticity my e n importnt trit influencing competitive ility nd survivl in this system. The nine species chosen for this study represent three importnt functionl groups in this system, ntive perennil unchgrsses, ntive perennil fors, nd invsive perennil fors introduced from Eursi nd the Mediterrnen region (Tle 1). We hypothesize tht: (1) ll species will cquire more N when N is pplied in ptches compred to when N is pplied evenly through the soil profile, (2) ntive grsses nd fors, which generlly hve lower RGR thn invsive fors, will respond to N heterogeneity through physiologicl plsticity wheres invsive fors will respond to N heterogeneity primrily Tle 1 List of the nine species used in this study Functionl group Common nme Species Species revition Bunchgrss Blueunch whetgrss Pseudoroegenri spict (Pursh) A. Löve PSSP Thurer s needlegrss Achntherum thurerinum (Piper) Brkworth ACTH Idho fescue Festuc idhoensis Elmer FEID Ntive for Arrowlef lsmroot Blsmorhiz sgittt (Pursh) Nutt. BASA Grey hwkserd Crepis intermedi Gry CRIN Long-lef phlox Phlox longifoli Nutt. PHLO Invsive for Diffuse knpweed Centure diffus Lm. CEDI Rush skeletonweed Chondrill junce L. CHJU Dlmtin todflx Linri dlmtic (L.) P. Mill. LIDA Nomenclture follows the USDA PLANTS dtse (

3 Plnt Ecol (2009) 202: through morphologicl plsticity, nd (3) trde-off will exist etween root system size nd forging precision. Methods Study system nd mterils In spring 2005, smll plnts of the ntive nd invsive fors (cnopy dimensions c cm) or tillers of the ntive unchgrsses (cnopy dimensions c cm) were plnted individully into lrge pots (25 cm di 9 30 cm deep). All plnts were collected from locl popultions except Blsmorhiz sgittt which ws purchsed s seedlings from commercil grower. Pots were filled with 1:1 mixture of field soil nd corse snd to provide low N soil medi. Field soil ws collected from the top 20 cm t the Northern Gret Bsin Experimentl Rnge ( N, W; c m elev.), out 56 km west of Burns, Oregon, USA. The soils t the site re sndy lom to lomy snd, Typic Durixerolls (Lentz nd Simonson 1986) with totl N verging round 0.08%. Pots were plced in n outdoor grden t the Estern Oregon Agriculturl Reserch Center, Burns, OR, USA. Plnts were llowed to grow for month efore tretments were pplied. During this period plnts were kept well-wtered nd received 200 ml ppliction of one-eighth strength of Hoglnd s solution to promote estlishment (Epstein 1972). Plnts tht died within week of the plnting were replced. Experimentl design nd N ptch tretments Within ech of eight locks, three plnts of ech species were rndomly ssigned to receive one of three sptil ptterns of N supply for totl of 216 pots (9 species 9 3 sptil N ptterns 9 8 locks = 216). Ech plnt received mmol of 20 tom% 15 NH 4 15 NO 3 ech week for 4 weeks either homogenously, in four ptches, or in two ptches. In the homogenous tretment 1 l of mm 15 NH 4 15 NO 3 ws pplied evenly over the soil surfce every week. A needle nd syringe were used to crete ptches in the two- nd four-ptch tretments. Ech ptch ws centered 7 cm from the se of the plnt. Ech ptch ws creted y evenly distriuting 25 ml of the leled solution in five injection points over 5 cm re. The 15 N solution ws injected through the 5 15 cm soil lyer. Injections were mde in the sme loctions ech week creting ephemerl nutrient ptches with diffuse orders, s they occur likely in the field. Tretments ssigned to two ptches received 25 ml of 4.16 mm 15 NH 4 15 NO 3 in ech ptch nd tretments with four ptches received the sme volume of solution in ech ptch t hlf the concentrtion. Plnts ssigned to ptch tretments received pproximtely 1 l of wter the dy efore ech lel ppliction to mke the soil wter content comprle to the homogenous tretment. Bsed on soil ulk density nd the initil inorgnic N concentrtion of the potting medi, the N dditions in the two- nd four-ptch tretments were expected to increse soil N to round 10 nd 5 mg kg -1, respectively, which ws within the rnge tht inorgnic N cn vry in sgerush steppe systems (Cui nd Cldwell 1997; Peek nd Forseth 2003). Hrvest nd mesurements At the eginning of the experiment, 15 dditionl plnts of ech species were hrvested to develop regression equtions to estimte initil iomss of ech plnt. These initil iomss estimtes nd the finl plnt iomss hrvested t the end of the study were used to clculte RGR for ech species during the experiment using the formul: RGR = [ln(m f ) - ln(m i )]/t 2 - t 1 ] where M f nd M i re finl nd initil plnt iomss. Aout 5 weeks fter the sptil N supply tretments were initited, pots were hrvested y lock. Aove ground iomss ws clipped nd seprted into leves nd stems. Leves nd stems were then triple rinsed with distilled wter, dried t 65 C, weighed nd ground to fine powder. Tissue N concentrtion nd 15 N enrichment were mesured on n isotope rtio mss spectrometer (Fisons Instruments, Beverly, MA) t the University of Cliforni Dvis Stle Isotope Fcility. Clcultions of 15 N content followed Ndelhoffer nd Fry (1994) where 15 N content (mg plnt -1 )=m f 9 [(N f - N i )/(N l - N i )], where m f is the mss of the N pool (mg), N f nd N i re the finl nd initil tom% 15 N of the smple, nd N l is the tom% 15 N of the leled solution. Soil cores (5 cm di from the 5 to 15 cm soil lyer) were collected from the enriched ptches to quntify

4 214 Plnt Ecol (2009) 202: root length density (RLD). Two control cores were collected from these pots t similr depth nd distnce from the plnt se. Soil cores were collected in the homogenous tretment in similr fshion. Roots were gently wshed from the soil in the cores over fine meshed screen to recover very fine lterl roots. Roots were then stored t 4 C until they were scnned for length with WinRHIZO (Regent Instruments Inc., Sint-Foy, Cnd) to determine RLD (Boum et l. 2000). The ility of species to selectively llocte root length to nutrient rich ptches (i.e., root forging precision) ws clculted using log response rtio where lnrr = ln(rld enriched /RLD control ) (Hedges et l. 1999; Rjniemi nd Reynolds 2004) nd RLD enriched nd RLD control re RLD in the nutrient nd control ptches, respectively. Incresing positive vlues of lnrr indicted incresing precision in root plcement. A one smple t-test ws conducted to determine if lnrr ws significntly greter thn zero. Root NO - 3 nd NH + 4 uptke rtes were mesured in the two-ptch tretment. Two susmples of fine roots (\1 mm di, pproximtely 15 mg dry weight) were removed from oth the enriched nd nonenriched ptches in the two-ptch tretment. These susmples were immeditely plced in tegs nd equilirted in 0.5 mm CCl 2 t 20 C. Within 30 min of smpling, the susmples were sumerged in solutions contining either 500 lm 15 NH 4 Cl or K 15 NO 3 for 30 min. The uptke solutions were well-mixed, erted nd contined 1% sucrose nd 0.5 mm CCl 2 (Jckson et l. 1990). After the incution period, ll smples were wshed in series of 2 mm KCl solutions nd finl rinse in distilled wter to remove ny 15 N dsored to the root surfce. The N uptke ssys were completed within n hour fter hrvesting to minimize the effect of root excision on N uptke cpcity (Bloom nd Cldwell 1988). Roots were dried t 65 C, ground to fine powder nd nlyzed for N concentrtion nd 15 N enrichment following the sme procedure used to quntify lef nd stem 15 N. Root NO nd NH 4 uptke rtes were expressed on root dry mss sis (lmol g -1 h -1 ). Root system iomss ws used s n index of root system size (Einsmnn et l. 1999; Rjniemi nd Reynolds 2004). To quntify root system iomss nd mount of 15 N retined in roots, pots were sliced open nd the rest of the root system ws wshed from the soil. After drying, the ulk roots were weighed nd susmple ws ground to fine powder for 15 N nlysis. Totl plnt 15 N cpture ws clculted y summing the 15 N content of shoots nd roots. Sttisticl nlysis nd pth model development Mesurements tht did not involve repeted smpling of the sme plnt were nlyzed with ANOVA (SAS 2001). Assumptions of ANOVA were evluted using the Shpiro Wilk test for normlity nd Levene s test for homogeneity of vrince. When these ssumptions were not met, dt were weighted y the inverse of the vrince (Neter et l. 1990). Repeted mesures ANOVA ws used when compring root responses of the sme individul plnt in control nd enriched ptches. The etween-suject effects were lock nd species. Becuse the root system of the sme plnt ws smpled in the control nd ptch tretment, within-suject effects were ptch type nd the interction etween ptch type nd the etween-suject effects. Following ANOVA, liner contrsts were used to test priori hypotheses out differences in N cpture nd root responses etween functionl groups. When these comprisons were not orthogonl, sequentil Bonferroni corrections were mde to mintin n experiment-wise error rte of = 0.05 (Rice 1989). Becuse we hd no priori sis for predicting individul species responses we compred species responses within functionl groups using Tukey s studentized rnge test. Pth nlysis nd structurl eqution modeling were used to determine how RGR, root system scle, nd root system plsticity influence N cpture in sptilly heterogeneous environments. This model ws sed on previous mthemticl models nd empiricl results of nutrient flow to roots nd plnt nutrient cpture in reltion to root length, growth rte nd physiology (Cmpell et l. 1991; Brer 1995). Pth coefficients, their significnce level nd the fit of the structurl model to the dt were evluted with the CALIS procedure in SAS. The totl correltions etween independent nd dependent vriles were decomposed into direct nd indirect effects with direct effects indicted y single heded rrows in the pth digrm. Indirect effects occurred when vrile ws linked to dependent vrile through one or more intermediry vriles. Model fit ws

5 Plnt Ecol (2009) 202: evluted y compring the predicted covrince mtrix sed on the specified model with the oserved covrince structure from our dt. We used the Goodness of Fit Index (GFI) nd Normed Fit Index (NFI) s indices of model fit. Vlues of GFI nd NFI [ 0.9 re generlly considered indictive of good greement etween the mtrices (Htcher 1994; Schumcker nd Lomx 2004). Results Functionl group nd species ttriutes The three functionl groups (unchgrss, ntive for, nd invsive for) differed in RGR during the experiment nd there ws lso significnt vrition in RGR within functionl groups (Fig. 1). Invsive fors hd greter RGR thn unchgrsses nd ntive fors (P \ 0.01) nd unchgrsses hd greter RGR thn ntive fors (P = 0.01). An effect of sptil pttern of N supply on RGR ws not oserved (P [ 0.05). While species within functionl groups differed in root iomss, there were lso significnt differences in root iomss etween functionl groups (Fig. 1). Invsive fors hd greter root iomss thn unchgrsses (P = 0.04) nd ntive fors (P \ 0.01) nd unchgrsses hd greter root iomss thn ntive fors (P \ 0.01). These differences were not ffected y the sptil pttern of N supply (P [ 0.05). The mount of iomss llocted to roots reltive to totl plnt iomss (RMR) tended to e similr mong species within functionl groups (Fig. 1c) ut unchgrsses nd ntive fors hd greter RMR thn invsive fors (P \ 0.01). Plnt N cpture All species cptured more N when N ws supplied in ptches compred to when N ws supplied homogenously (P \ 0.01; Fig. 2). Likewise, unchgrsses, ntive fors, nd invsive fors cptured more N when N ws supplied in two ptches compred to when the sme mount of N ws distriuted mong four ptches (P \ 0.01, P = 0.03, nd P \ 0.01, respectively). Invsive fors cptured more N from ptches compred to unchgrsses nd ntive fors (P \ 0.01). RGR ( g g -1 d -1 ) Root iomss ( g) RMR ( g g -1 ) () () (c) Root responses c c PSSP ACTH FEID BASA PHLO CRIN CEDI LIDA CHJU Bunchgrsses Ntive fors Invsive fors Fig. 1 ( c) Reltive growth rte (RGR), root iomss nd root mss rtio (RMR) for ech study species within the three functionl groups (men ± SE, n = 18 24). Vlues re verged over the different N supply tretments. Brs with different letters indicte significnt differences within functionl groups (P \ 0.05, Tukey s studentized rnge test) While RLD ws not significntly different etween unchgrsses nd invsive fors (P = 0.23), ntive fors hd lower RLD thn unchgrsses nd invsive fors (P \ 0.01; Fig. 3). Root length density did not differ etween the four-ptch nd two-ptch tretment for ny species (P [ 0.05) nd RLD ws not greter in enriched ptches compred to control c

6 216 Plnt Ecol (2009) 202: Plnt N cpture (mg plnt -1 ) 9 Homogeneous 4 ptches 2 ptches 6 3 PSSP ACTH FEID BASA CRIN PHLO CEDI CHJU LIDA Bunchgrsses Ntive fors Invsive fors Root forging precision (lnrr) PSSP ACTH FEID BASA PHLO CRIN CEDI LIDA CHJU Bunchgrsses Ntive fors Invsive fors Fig. 2 Effect of the sptil pttern of N supply on N cpture y the nine study species (men ± SE, n = 6 8). The sme totl mount of N ws pplied in ll tretments Root length denisty (km m -3 ) 40 Control ptch Enriched ptch PSSP ACTH FEID BASA PHLO CRIN CEDI LIDA CHJU Bunchgrsses Ntive fors Invsive fors Fig. 3 Root length density (RLD) of the study species in control nd enriched ptches. Species responses re verged cross oth ptch tretments (men ± SE, n = 12 16) ptches (P = 0.53). As result, root forging precision did not differ significntly from zero for ny functionl group or study species within functionl group (P [ 0.05, one smple t-test for men; Fig. 4). Root uptke rtes for NH 4 + nd NO 3 - in the twoptch tretment did not differ significntly for ny species so vlues for root uptke rtes for ll species were verged over oth N forms. Ntive fors hd lower uptke rtes in control ptches compred to unchgrsses nd invsive fors (P \ 0.01) ut root N uptke rte in control ptches did not differ etween unchgrsses nd invsive fors (Fig. 5; P = 0.32). While ll species hd greter root uptke Fig. 4 Root forging precision of the study species clculted using log response rtio where lnrr = ln (RLD enriched / RLD control ). Species responses re verged cross oth ptch tretments (men ± SE, n = 12 16). Positive vlues indicte greter precision in root plcement while vlues not significntly different from zero indicte tht root plcement ws similr in enriched nd non-enriched soil ptches N uptke rte (µmol g -1 h -1 ) Control ptch Enriched ptch PSSP ACTH FEID BASA CRIN PHLO CEDI CHJU LIDA Bunchgrsses Ntive fors Invsive fors Fig. 5 Nitrogen uptke rte (NO NH 4 + ) of roots growing in control or enriched ptch (men ± SE, n = 6 8). Uptke rtes were mesured on the two-ptch tretment only rtes in enriched ptches compred to control ptches (P \ 0.01) this vried y species (ptch type 9 species; P = 0.02). Invsive fors hd greter root uptke rtes in enriched ptches compred to unchgrsses nd ntive fors (P \ 0.01). There ws trend for unchgrsses to hve higher uptke rtes thn ntive fors in enriched ptches (P = 0.08). There ws lso trend for root system mss to e positively correlted with uptke rte (r = 0.56, P = 0.11).

7 Plnt Ecol (2009) 202: Pth nlysis The model fit indices, GFI nd NFI, were 0.93 nd 0.93, respectively, indicting tht the pth model fit the dt to resonle level. The vriles included in the model explined 73% of the vritions in plnt N cpture (Fig. 6). Root system mss nd root N uptke rte hd strong nd significnt pths to plnt N cpture (P \ 0.01) while the pth from root forging precision to plnt N cpture ws not significnt (P = 0.15). Reltive growth rte hd significnt pth to root N uptke rte nd root system mss nd explined 32% nd 19% of the vrition in these vriles, respectively. Discussion All species cquired more N when N ws supplied in ptches compred to when N ws supplied uniformly, supporting our first hypothesis. These oservtions re consistent with previous work on perennil unchgrsses from nutrient-poor nd -rich hitts (Frnsen et l. 1999) nd re likely due to n effect of soil N concentrtion on N cpture nd greter N uptke rtes of roots growing in ptches. Nmely, N uptke rte is expected to increse linerly s soil N concentrtion increses. Therefore, in this experiment, concentrting the sme mount of N in ptches could result in greter N cpture thn the uniform supply tretment even without physiologicl djustments to the root system (Brer nd Silerush 1984). In ddition, for ll species, roots growing in ptches hd greter N uptke rte thn roots growing outside of the ptches. With this physiologicl djustment, higher N concentrtions re needed to sturte N uptke cpcity (Brer 1995), likely llowing these species to cpture more N in the ptch tretments compred to when N ws supplied uniformly. Our hypothesis tht ntive species with low RGR would respond to nutrient ptches primrily through physiologicl plsticity while invsive species with high RGR would respond to nutrient heterogeneity through morphologicl plsticity ws not supported. While ll species hd greter root N uptke rtes in enriched ptches compred to control ptches, none of the species hd greter root length density in enriched ptches reltive to control ptches. In ddition, invsive fors, which hd higher RGR thn ntives, lso hd higher root N uptke rtes thn the ntives in enriched ptches. These oservtions lrgely contrst with previous theoreticl nd empiricl work. For exmple, the C S R model of plnt strtegies developed y Grime (1979) predicts tht species with low RGR mintin slow-growing, long-lived root system nd should therefore exhiit greter root physiologicl plsticity thn species with high RGR. In review of 27 species with different RGR, Roinson nd Vn Vuuren (1998) found tht the increse in root nutrient uptke rtes in enriched ptches compred to controls verged round 2.4- fold for slow-growing species ut only out 1.3-fold for fst-growing species, supporting the initil predictions of Grime (1979) N uptke rte (µmol g - 1 h -1 ) 0.70*** 0.57*** 0.19 Reltive growth rte (g g -1 d -1 ) 0.43** Root system mss (g) 0.78*** 0.73 Plnt N cpture (mg plnt -1 ) Root forging precision (response rtio) 0.08 Fig. 6 Pth model to determine how vrition in RGR, root system mss, nd root forging precision nd root N uptke rte contriutes to vrition in N cpture in sptilly heterogeneous environments. For ech pth effect the stndrdized prtil regression coefficient is given nd the significnce of the pth is indicted s *** P\0.0001, ** P\ Numers in old re the totl vrince explined (r 2 ) for ech dependent vrile

8 218 Plnt Ecol (2009) 202: The reltionship etween RGR nd physiologicl plsticity in root nutrient uptke cpcity hs een lrgely unexplored in the context of invsive species nd the results from this current study suggest lterntive hypotheses out the reltionship etween RGR nd root physiologicl plsticity need to e considered. For exmple, reserch in cropping systems hs demonstrted tht during periods of rpid iomss production root N uptke rtes re often elevted due to greter plnt N demnd (Siddiqi et l. 1990; Mttsson et l. 1992; Schenk 1996). Therefore, insted of trde-off etween RGR nd physiologicl plsticity, invsive species with high RGR my e le to increse root N uptke rte to greter degree thn ntive species with low RGR due to greter plnt N demnd. Becuse of the lck of forging precision demonstrted y our study species under these experimentl conditions, our hypothesis out trde-off etween root system sizes nd forging precision could not e evluted. In contrst to our study, the mjority of experiments investigting plnt responses to nutrient ptches hve demonstrted vrious degrees of forging precision in rnge of species (Roinson 1994; Roinson nd Vn Vuuren 1998). One of the species used in this study, P. spict, hs demonstrted sustntil forging precision in some previous studies (Eissenstt nd Cldwell 1988; Blck et l. 1994; Lriguderie nd Richrds 1994) ut not others (Jckson nd Cldwell 1989; Ivns et l. 2003). One fctor tht my contriute to these oserved discrepncies in forging responses, even when the sme species is considered, my e the level of mycorrhizl coloniztion. While we did not quntify mycorrhizl ssocition in this study, mycorrhize cn gretly increse the ility of plnts to cpture nutrients nd my dmpen the degree to which plnts forge for nutrients (Koide nd Elliot 1989). Most evidence, however, indictes tht while mycorrhize my e importnt for phosphorous cpture they contriute sustntilly less to the ility of plnt to cpture N from ptches (Hodge 2004). Therefore, differences in mycorrhizl coloniztion etween experiments pper to e less likely explntion for the lck of root prolifertion oserved in this experiment. One likely reson tht root prolifertion ws not oserved in this study ut hs een commonly oserved in other studies my e due to how the nutrient ptches were creted. In our study, we injected N t weekly intervls tht likely resulted in firly ephemerl N ptches. Cui nd Cldwell (1997) nd Ivns et l. (2003) showed tht plnts in the Gret Bsin respond to rief pulses of N vilility minly through chnges in root N uptke rte with new root growth either gretly lgging the nutrient flush or not occurring t ll if the pulse is too rief. Most experiments on plnt response to nutrient heterogeneity hve generlly utilized more constnt form of nutrient enrichment (e.g., slow-relese fertilizer or frequent injections of nutrient solution) resulting in reltively long-lived nutrient ptches (e.g., Cmpell et l. 1991; Blck et l. 1994; Rjniemi nd Reynolds 2004). The ephemerl nture of nutrient ptches hs een recognized (Lm et l. 2004), prticulrly in rid nd semi-rid systems (Cui nd Cldwell 1997; Jmes nd Richrds 2006). Results from this pot study, s well s previous field studies in the Gret Bsin, suggest root prolifertion my e miniml when N is restricted to rief pulses. Results from our pth nlysis identified comintions of trits tht my contriute to the success of invsive fors in the heterogeneous, nutrient poor soils of the sgerush steppe s well s other ecosystems. For exmple, in our study there ws positive correltion etween root system mss nd root N uptke rte with invsive fors hving higher RGR, greter root iomss nd higher N uptke rtes per unit root iomss thn the ntive species. Vrition in oth root iomss nd N uptke rte per unit root iomss were importnt in contriuting the vrition in ility of species to cpture N from ephemerl ptches. Vrition in oth vriles, in turn, ws influenced y vrition in RGR. The interreltionship mong trits descried in this working model provides one possile explntion of how invsive fors were le to cpture 2 nd 15-fold more N from enriched ptches compred to the ntive grsses nd fors, respectively. Although identifying trits of invding species hs een n re of intense reserch interest, often these trits re considered in reltion to the individul effects they my hve on invsion. Our results suggest tht it my e useful to plce some emphsis on understnding how the interreltionship etween suites of trits my influence the success of invsive plnts. In this study, we oserved positive reltionship etween RGR, root system size nd plsticity in root N uptke rte. Insted of trde-off etween trits, these

9 Plnt Ecol (2009) 202: results suggest tht within plnt community, trits relted to nutrient cpture my e positively correlted, potentilly promoting size-symmetric competition elowground (Einsmnn et l. 1999; Frley nd Fitter 1999; Rjniemi nd Reynolds 2004). This my e one mechnism fcilitting the spred of invsive species in nutrient-poor systems. Importntly, however, we lso oserved sustntil vrition in some of these trits mong species within functionl group (i.e., ntive nd invsive fors). The limittions of using conventionl functionl clssifiction schemes (e.g., for, grss, or shru) to predict ecosystem properties such s invsion resistnce hs een demonstrted (Wright et l. 2006). In support of this ide, our results suggest tht root trits relted to N cpture my e more similr etween invsive fors nd ntive unchgrsses thn etween invsive fors nd ntive fors. This suggests ntive unchgrsses might e more importnt in interfering with invsive for estlishment nd growth thn would otherwise e predicted sed on conventionl functionl clssifiction schemes. It is importnt to note, however, tht this study only evluted plstic root responses of individul plnts in pots. While the pots used in this study were reltively lrge, this pproch cn induce numer of experimentl rtifcts (e.g. Brown et l. 1991) suggesting tht these results should e interpreted with some cution. In ddition, our experiment did not determine how these responses vry in the presence of neighors. The enefits of these vrious trits my chnge depending on interctions with neighoring plnts nd composition of the nutrient ptch (Chill nd Csper 1999; Roinson et l. 1999). Ultimtely, field experiments with plnts in different neighor environments will provide n importnt next step in determining how these positive reltionships mong trits influence competitive ility nd invder success. References Brer SA (1995) Soil nutrient iovilility: mechnistic pproch. Wiley, New York Brer SA, Silerush M (1984) Plnt root morphology nd nutrient uptke. In: Brer SA, Bouldin DR (eds) Roots, nutrient nd wter influx, nd plnt growth. ASA Specil Puliction 49, Mdison, pp Blck RA, Richrds JH, Mnwring JH (1994) Nutrient uptke from enriched soil microsites y three Gret Bsin perennils. Ecology 75: doi: / Bloom AJ, Cldwell RM (1988) Root excision decreses nutrient sorption nd gs fluxes. Plnt Physiol 87: Boum TJ, Nielsen KL, Koustl B (2000) Smple preprtion nd scnning protocol for computerized nlysis of root length nd dimeter. Plnt Soil 218: doi: /A: Brown DP, Prtum TK, Bledsoe CS, Forde ED, Cothern JS, Perry D (1991) Noninvsive studies of conifer roots: nucler mgnetic resonnce (NMR) imging of douglsfir seedlings. Cn J For Res 21: doi: / x Chill JF, Csper BB (1999) Growth consequences of soil nutrient heterogeneity for two old-field hers, Amrosi rtemisiifoli nd Phytolcc mericn, grown individully nd in comintion. Ann Bot (Lond) 83: doi: /no Cmpell BD, Grime JP (1989) A comprtive study of plnt responsiveness to the durtion of episodes of minerl nutrient enrichment. New Phytol 112: doi: /j t02382.x Cmpell BD, Grime JP, Mckey JML (1991) A trde-off etween scle nd precision in resource forging. Oecologi 87: doi: /bf Cui MY, Cldwell MM (1997) A lrge ephemerl relese of nitrogen upon wetting of dry soil nd corresponding root responses in the field. Plnt Soil 191: doi: /A: Drew MC, Sker LR (1975) Nutrient supply nd the growth of seminl root systems in rely II. Loclized compenstory increses in lterl root growth nd rtes of nitrte uptke when nitrte supply is restricted to only one prt of the root system. J Exp Bot 26: doi: /jx/ Einsmnn JC, Jones RH, Pu M, Mitchell RJ (1999) Nutrient forging trits in 10 co-occurring plnt species of contrsting life forms. J Ecol 87: doi: /j x Eissenstt DM, Cldwell MM (1988) Sesonl timing of root growth in fvorle microsites. Ecology 69: doi: / Epstein E (1972) Minerl nutrition of plnts: principles nd perspectives. Wiley, New York Frley RA, Fitter AH (1999) Temporl nd sptil vrition in soil resources in deciduous woodlnd. J Ecol 87: doi: /j x Frley RA, Fitter AH (1999) The response of seven co-occurring woodlnd herceous perennils to loclized nutrientrich ptches. J Ecol 87: doi: /j x Frnsen B, Blijjenerg J, De Kroon H (1999) Root morphologicl nd physiologicl plsticity of perennil grss species nd the exploittion of sptil nd temporl heterogeneous nutrient ptches. Plnt Soil 211: doi: /a: Frnsen B, de Kroon H, Berendse F (2001) Soil nutrient heterogeneity lters competition etween two perennil grss species. Ecology 82: Grime JP (1979) Plnt strtegies nd vegettion processes. Wiley, Chichester Gross KL, Pregitzer KS, Burton AJ (1995) Sptil vrition in nitrogen vilility in three successionl plnt communities. J Ecol 83: doi: /

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