Stoichiometry of ferns in Hawaii: implications for nutrient cycling

Transcription

1 Oecologi (2008) 157: DOI /s ECOSYSTEM ECOLOGY - ORIGINAL PAPER Stoichiometry of ferns in Hwii: implictions for nutrient cycling Kthryn L. Amtngelo Peter M. Vitousek Received: 3 July 2007 / Accepted: 24 June 2008 / Pulished online: 23 July 2008 Springer-Verlg 2008 Astrct We sked if element concentrtions in ferns diver systemticlly from those in woody dicots in wys tht could inxuence ecosystem properties nd processes. Phylogeneticlly, ferns re deeply seprted from ngiosperms; for our nlyses we dditionlly seprted leptosporngite ferns into polypod ferns, monophyletic clde of ferns which rdited fter the rise of ngiosperms, nd ll other leptosporngite (non-polypod) ferns. We smpled oth non-polypod nd polypod ferns on nturl fertility grdient nd within fertilized nd unfertilized plots in Hwii, nd compred our dt with shru nd tree smples collected previously in the sme plots. Non-polypod ferns in prticulr hd low C concentrtions under ll conditions nd less plsticity in their N nd P stoichiometry thn did polypod ferns or dicots. Polypod ferns were prticulrly rich in N nd P, with low N:P rtios, nd their stoichiometry vried sustntilly in response to diverences in nutrient vilility. Distinguishing etween these two groups hs the potentil to e useful oth in nd out of Hwii, s they hve distinct properties which cn Vect ecosystem function. These diverences could contriute to the widespred undnce of polypod ferns in n ngiosperm-dominted world, nd to ptterns of nutrient cycling nd limittion in sites where ferns re undnt. Keywords Pteridophyte Angiosperm Plsticity Phylogeny Nitrogen-to-phosphorus rtio Communicted y Todd Dwson. K. L. Amtngelo (&) P. M. Vitousek Deprtment of Biologicl Sciences, Stnford University, Stnford, CA 94305, USA e-mil: kmtng@gmil.com Introduction Structures nd metolic pthwys common to ll plnts provide some underlying consistency to the concentrtions nd reltive undnces the stoichiometry of the elements they contin. However, terrestril plnts diver more sustntilly in stoichiometry within nd mong species nd higher phylogenetic groupings thn do other groups of orgnisms (Sterner nd Elser 2002). Cuses of this vrition include diverences in: structure, storge, nd defense (Aerts nd Chpin 1999; Reiners 1986); growth form nd growth rte (Meerts 1997; Shver nd Chpin 1980; Vn Arendoonk nd Poorter 1994); nd element vilility in the environment (Bowmn et l. 2003; Vitousek et l. 1995). This vrition hs often een correlted with phylogeny (Brodley et l. 2004, 2001; KerkhoV et l. 2006; Thompson et l. 1997). Plnts diver not only in their element contents under dewned conditions, ut lso in the plsticity of their stoichiometry in divering environments (Knecht nd Gornsson 2004). Element stoichiometry inxuences element cycling, trophic interctions, nd decomposition; s such it hs long een of interest to gronomists nd ecologists (Grten 1976; Wksmn nd Tenney 1928). The elementl composition of herivores nd decomposers divers sustntilly from those of the plnts they consume nd the litter they decompose (Sterner nd Elser 2002; Vitousek 2003). These diverences Vect the iologicl vilility of essentil plnt nutrients nd ultimtely the success of plnts tht diver in element requirements. Reserch in phytoplnkton hs demonstrted tht element concentrtion nd rtios re conserved in some phylogenetic groups mirroring the conditions under which those groups evolved (Quigg et l. 2003). Mny rtios tht re conserved within phylogenetic phytoplnkton groups

2 620 Oecologi (2008) 157: re lso conserved mong vsculr plnts. Among ngiosperms, concentrtions nd rtios of some undnt elements (se ctions nd Si) vry mong orders ut re reltively consistent within them (Brodley et l. 2004, 2001; Chenery nd Sporne 1976; Hodson et l. 2005); similr phylogenetic signls hve een oserved for N nd P in seed plnts (KerkhoV et l. 2006). This conservtion of element prowles within plnt groups could llow us to predict nutrient-medited impcts of prticulr species on nutrient cycling nd other ecosystem processes. For exmple, high concentrtions of Si in commelinoid monocots nd high N in legumes hve signiwcnt, ut opposite, evects on pltility to herivores nd decomposers (Cornelissen nd Thompson 1997; M nd Ymji 2006; Ritchie et l. 1998). Ferns represent prticulrly interesting group in which to evlute oth phylogenetic correltes with stoichiometry nd the consequences of this vrition for ecologicl processes. Ferns diver sustntilly from ngiosperms in structure nd iochemistry, nd their ecologicl uniqueness nd importnce is well recognized (Pge 2002; Rthinspthi 2006; Rothwell 1996). Fern phylogenies distinguish monophyletic clde clled polypod ferns, consisting of the order Polypodiles, tht rdited while ngiosperms were ecoming dominnt (Pryer et l. 2004; Schneider et l. 2004; Smith et l. 2006). All other leptosporngite ferns cn e grouped into non-polypod ferns (including tree ferns, Wlmy ferns, wter ferns, gleichenioid, osmundceous, nd schizeoid ferns); the mjor rdition in non-polypod orders pre-dted the diversiwction of ngiosperms y tens of millions of yers. The nutrient physiology of ferns hs received reltively little ttention (lthough see Hohne nd Richter 1981; Richrdson et l. 2005; Wegner et l. 2003), nd only As ccumultion hs een ddressed from phylogenetic perspective (Mehrg 2002). Both non-polypod nd polypod ferns re widespred nd undnt, nd even co-dominnt with ngiosperms in some ecosystems prticulrly forested ecosystems where woody dicots comprise much of the overstory. To the extent tht polypod nd non-polypod ferns diver in stoichiometry nd plsticity from ech other nd from ngiosperm forest dominnts, this widespred co-occurrence overs the opportunity to determine how phylogenetic group diverences in element contents cn inxuence ecosystems. In this pper, we sk if ferns generlly, nd polypod ferns in prticulr, diver from other plnt groups in element concentrtions nd/or rtios in wys tht could inxuence the functioning of ecosystems in which ferns re undnt. We ddress two min questions in this study 1. Are there diverences etween ferns nd woody dicots, nd etween fern groups, with regrds to stoichiometry when ll re grown on the sme sustrte? 2. Are there diverences in the plsticity of element concentrtions nd rtios mong plnt groups, when compred cross sites tht diver sustntilly in nutrient vilility or in response to soil fertiliztion? Mterils nd methods We crried out this reserch in the Hwiin Islnds for severl resons. First, ferns re undnt in mny ecosystems cross the rchipelgo, with vriety of species dominting the sucnopy or ground lyer of forests. The nonpolypod ferns Ciotium spp. nd Dicrnopteris lineris in prticulr cn contriute sustntilly (35 75%) to stndlevel productivity nd nutrient cycling (Rich et l. 1997; Vitousek et l. 1995), nd severl polypod gener including Elphoglossum, Diplzium, nd Dryopteris dominte the understory of other stnds. Second, the vilility of nutrients vries sustntilly, ut in well-understood nd well-chrcterized wys, cross the forests of the Hwiin rchipelgo (Crews et l. 1995; Vitousek 2004) llowing us to ddress plsticity of folir nutrient content. Finlly, we hve mintined long-term soil fertiliztion experiments in three sites for t lest 13 yers, further expnding the rnge of soil nutrient vilility ccessile to this nlysis. Fern species were smpled from four sites rryed long soil development sequence in which ll sites re ner 1,200 m elevtion nd 2,500 mm nnul rinfll, ut on sustrtes tht rnge in ge from 300 yers to 4.1 million yers (0.3 4,100 kyers) (Crews et l. 1995). Soils nd dominnt trees of the 0.3 kyer site re rich in ctions nd Si, low in ville N nd P (0.98 kg m 2 N, kg m 2 orgnic P in 50-cm soil prowles, Crews et l. 1995), nd production there is limited y N (Vitousek et l. 1993). Both the 20- nd 150 kyer sites re low in ctions nd Si nd rich in N nd P (1.56 kg m 2 N, kg m 2 orgnic P, 1.46 kg m 2 N, kg m 2 orgnic P, respectively). The 4,100 kyer site is modertely rich in N nd P (1.13 kg m 2 N, kg m 2 orgnic P), low in ctions nd Si, nd P supply limits plnt production (Herert nd Fownes 1995). The 0.3-, 20-, nd 4,100 kyer sites contin replicted fctoril fertiliztion experiments tht hve een ongoing since 1985, 1993, nd 1991, respectively (Vitousek 2004). In ddition to unfertilized plots, we smpled ferns from plots fertilized with N (100 kg h 1 yer 1 ), P (100 kg h 1 yer 1 ) nd tretment consisting of ll other essentil plnt nutrients (T) tht included K (100 kg h 1 yer 1 ), C (100 kg h 1 yer 1 ), Mg (58 kg h 1 yer 1 ), S (40 kg h 1 yer 1 ), Fe (8 kg h 1 yer 1 ), Mo (0.01 kg h 1 yer 1 ), nd mixed micronutrient supplement contining Mn, Mo, Zn, Cu, nd B. We collected young, fully developed leves from the terrestril ferns tht were undnt within ech site (Tle 1);

3 Oecologi (2008) 157: these were clipped, dried t 60 C nd ground to 40 mesh in Wiley mill. C nd N were nlyzed on Crlo Er NA 1500 elementl nlyzer. Ction digests (P, C, K, Mg, Al) were performed y wet shing of smples in HNO 3 nd H 2 O 2 ; extrcts were Wltered nd nlyzed on Thermo ScientiWc inductively coupled plsm spectrometer (ICP). A suset of smples ws sent to the Mrine Science Deprtment nlyticl l t University of Hwii Hilo for Si nlysis. Smples were dry shed in muze furnce, followed y HF digestion nd ICP nlysis Element dt for mcronutrients (N, P, C, K, Mg) for 20 ntive terrestril fern species (Wve non-polypod, Wfteen polypod) were compred with dt from six common, dominnt woody dicot species collected t the four chronosequence sites nd from the ntive dominnt tree Metrosideros polymorph collected from ll the fertilizer plots. M. polymorph folige ws collected nd nlyzed t Tle 1 Species included in nlyses; dicot species from Vitousek et l. 1995,. Voucher specimens re not ville Non-polypod ferns Ciotium glucum (Sm.) Hook. & Arn. (A, B, C, D) Ciotium menziesii Hook. (A, B, C, D) Dicrnopteris lineris Und. (A, C, D) Diplopterygium pinntum (Kunze) Nki (B, D) Sticherus owyhensis (Hook.) Ching (D) Dicots Metrosideros polymorph Gudich. (A, B, C, D) Cheirodendron trigynum A.Heller (A, B, C, D) Ilex noml Hook. & Arn. (A, B, C, D) Coprosm spp. (A, B, C, D) Vccinium clycinum Sm. (A, B, C, D) Myrsine lessertin A.DC. (A, B, C) Polypod ferns Asplenium normle D.Don (B, D) Asplenium polyodon G.Forst. (B, C, D) Athyrium microphyllum (Sm.) Alston (B, C, D) Diplzium sndwichinum (Pr.) Diels (B, C, D) Dryopteris fusco-tr Roinson (C) Dryopteris glr (Brck.) Kuntze (B, C, D) Dryopteris wllichin (Spreng.) Hyl. (B) Elphoglossum crssicule Copel. (D) Elphoglossum pleceum (Hook. & Grev.) Sledge (A, C, D) Elphoglossum prvisqumeum Skotts. (A) Nephrolepis cordifoli (L.) C.Presl (C, D) Pteridium quilinum (L.) Kuhn (D) Sdleri cytheoides Kulf. (D) Sdleri pllid Hook. & Arn. (A) Sdleri souleyetin (Gud.) T.Moore (A, D) Sites t which species were collected re indicted y letters in prentheses [0.3 kyers (A), 20 kyers (B), 150 kyers (C), 4,100 kyers (D)] the sme time s these fern collections, nd found not to diver signiwcntly from erlier pulictions (Vitousek 1998; Vitousek et l. 1995). The smpled dicot species include oth forest shrus nd trees, nd comprise much of the overstory iomss in Hwiin forests. To evlute chnges of nutrient content, we clculted species phenotypic plsticity indices (PPI) (Vlldres et l. 2000). PPI rnges from 0 to 1 nd is clculted s the diverence etween species mximum nd minimum men vlues, divided y the mximum. Environmentl PPI (PPI e ) vlues were clculted sed on etween-site diverences in element concentrtions for ech species tht occurred t multiple sites in control (unfertilized) plots. In ddition, fertiliztion PPIs (PPI f ) were clculted for species tht occurred in oth control nd fertiliztion plots t the sme site where species occurred in control nd fertiliztion plots t multiple sites, the lrgest PPI f for those species ws used. DiVerences mong plnt groups in nutrient concentrtions nd PPI within sites were evluted with t-tests djusted for multiple comprisons. As not ll species were found t ll sites, signiwcnt inxuences of site nutrient vilility on plnt concentrtion of n element or rtio were evluted with mixed-model nlysis of covrince (ANCOVA) on ech plnt group seprtely, with species s rndom evect nd nutrient vilility of tht element s Wxed evect. To detect seprtion of groups sed on nutrient concentrtions, we sumitted men nutrient concentrtion dt (N, P, C, K) for species in control plots t the four sites to principl component nlysis. All sttistics were performed on log-trnsformed dt. All sttisticl nlyses were performed in JMP (SAS Institute, Cry, N.C.). Results DiVerences mong groups within sites At ech of the four chronosequence sites, concentrtions of some of the mcronutrients divered mong dicots, nonpolypod ferns, nd polypod ferns (Tle 2). At the reltively N- nd P-rich 20- nd 150 kyer sites, polypod ferns hd signiwcntly more folir N nd P thn dicots nd nonpolypod ferns, which did not diver signiwcntly from ech other. DiVerences mong plnt groups for those elements were smller t the low N (0.3 kyers) site, where nonpolypod ferns hd the highest N, nd t the low P (4,100 kyers) site, where non-polypod ferns hd the highest P. Across ll four sites, polypod ferns hd the highest K content, nd t ll four sites non-polypod ferns hd extremely low C nd Mg content (less thn 0.1% folir C t the two oldest sites). Totl mcronutrient ction (C + K + Mg) content ws signiwcntly lower in non-polypod ferns thn in polypod ferns or dicots t ll sites. Dicots,

4 622 Oecologi (2008) 157: Tle 2 Folir nutrient concentrtions (% dry mss) of nonpolypod ferns, polypod ferns, nd dicots cross grdient of soil development. DiVerent letters indicte signiwcnt diverences mong groups within site, clculted y t-tests djusted for multiple comprisons * P < 0.05 (signiwcnt evect of site nutrient vilility on group nutrient concentrtion or rtio from mixed-evects nlysis of covrince) Soil is rich in ctions nd reltively low in N nd P Soil is high in N nd P nd lower in ctions c Soil is low in P nd ctions d Mcronutrient ctions include C, Mg, nd K Element Group Site 0.3 kyers 20 kyers 150 kyers 4,100 kyers c N Dicots* Polypod* Non-polypod P Dicots* Polypod* Non-polypod* C Dicots* Polypod Non-polypod c c K Dicots* Polypod Non-polypod* Mg Dicots Polypod Non-polypod Mcro-nutrient Dicots* ctions d Polypod* Non-polypod* c N:P Dicots* Polypod* Non-polypod polypod ferns, nd non-polypod ferns seprted with principl components nlyses using N, P, C, nd K (Fig. 1) t ll four sites, lthough t the youngest site polypod ferns were reltively similr to dicots. Principl components xis 1 (PCA1) explined 46% of the vrition, nd ws PCA D D D D N PCA1 N N 0.3 ky 20 ky 150 ky 4100 ky Fig. 1 Principl component nlysis of log element concentrtions in dicots (D), non-polypod ferns (N), nd polypod ferns (P) t four sites, projected onto plne dewned y the Wrst two principl components. The Wrst principl components xis (PCA1) nd second principl components xis (PCA2) explin 46.8 nd 26.4% of the vrition, respectively: PCA1 = 0.57 N P 0.15C K, PCA2 = 0.18 N P C K P N P P 1.5 P dominted y N nd P; principl components xis 2 (PCA2) explined n dditionl 26% nd ws dominted y C nd to lesser extent K. DiVerences within groups mong sites on nturl fertility grdient Folir nutrient concentrtions vried signiwcntly (P < 0.05) with chnging nutrient vilility long the ge grdient cross the Hwiin Islnds (Tle 2). P nd totl mcronutrient ction concentrtions divered signiwcntly in ll groups. Individul ctions were vrily Vected, with Mg content not divering signiwcntly in ny group, vrition in C signiwcnt only in dicots, nd vrition in K signiwcnt only in non-polypod ferns nd dicots. In contrst to polypod ferns nd dicots, N in non-polypod ferns did not vry signiwcntly cross the sites. The plsticity of element concentrtions within species cross sites (s mesured y PPI) divered mong the three groups (Tle 3). Non-polypod ferns vried lest in N nd P content. Dicots hd prticulrly high PPI with regrds to K, s did polypod ferns with regrds to P. P concentrtion more thn douled in polypod ferns in the richest site reltive to the poorest, wheres concentrtions in non-polypod ferns nd dicots incresed round 50%. However, principl components nlysis (ove) demonstrted tht groups hd lrger nd more consistent evect on mcronutrient concentrtions thn

5 Oecologi (2008) 157: Tle 3 Phenotypic plsticity indices for species cross sites tht diver in soil fertility (PPI e ), or with fertiliztion (PPI f ). See text for clcultion. DiVerent letters indicte signiwcnt diverences (P < 0.05) in PPI mong groups Group EVect N P C Mg K Non-polypod PPI e Polypod PPI e Dicots PPI e Non-polypod PPI f Polypod PPI f did plsticity in response to vrition in nutrient vilility (sites), nd the three groups seprted out signiwcntly t ll four sites (Fig. 1). Element rtios N:P rtios were vrile nd did not diver signiwcntly mong groups t ny site, lthough there were diverences mong sites in dicots nd polypod ferns (Tle 2). The N:P rnge for polypod ferns cross sites ws greter (7.5) thn tht of dicots nd non-polypod ferns (oth 4.5). We lso investigted rtios etween mcronutrient ctions tht my sustitute for C in plnt structures. K:C nd Mg:C rtios in ferns were signiwcntly wider thn rtios in dicots t ll sites. Polypod nd non-polypod fern K:C rtios verged 7.2 nd 14.4 times wider thn dicot rtios, respectively, nd Mg:C rtios verged 2.4 nd 5.8 times wider. Responses to fertiliztion Fertiliztion Vected folir nutrient concentrtions signiwcntly in oth groups of ferns for ll Wve mcronutrients (P < 0.05). Plsticity in response to fertiliztion (PPI f ) ws similr to plsticity in response to diverences in nutrient vilility mong sites (PPI e ), lthough fertiliztion hd lrger evects on P content, nd generlly smller evects on mcronutrient ctions (Tle 3). For seven species tht grew t the 150 kyer fertile site (the site nturlly richest in P), the 4,100 kyer site (the poorest in P), nd in P-fertilized plots in the 4,100 kyer site, P content incresed signiwcntly etween sites nd with fertiliztion in ll Wve polypod species, nd incresed only in one of the two nonpolypod ferns (nd then only with fertiliztion) (Fig. 2). Polypod fern P concentrtions incresed from 85 to 250%, wheres non-polypod fern P incresed from 2 to 55%. Other elements Silic concentrtions vried sustntilly mong fern species, ut the diverences did not segregte etween non-polypod nd polypod ferns. Three polypod species (Elphoglossum pleceum, Dryopteris glr, nd Asplenium polyodon) hd P concentrtion (%) Fig. 2 Responses of P concentrtions of eight fern species to diverences etween sites (150 nd 4,100 kyers) tht diver sustntilly in nutrient vilility, nd with P fertiliztion t the 4,100-kyer, P-limited site. DiVerent letters indicte signiwcnt diverences within species (P <0.05). CG Ciotium glucum; CM Ciotium menziesii; DL Dicrnopteris lineris; AP Asplenium polyodon; AM Athyrium microphyllum; DS Diplzium sndwichinum; DG Dryopteris glr; NC Nephrolepis cordifoli; CG, CM, DL non-polypod fern species very low Si content while the other species contined ove 0.3% Si. Si concentrtions decresed with incresing site ge in ll eight species investigted (Tle 4), consistent with declining Si in soils cross this grdient (Vitousek 2004). Al content ws very low in ll species except Dicrnopteris lineris; s result, Al:Si rtios were >1 in tht species nd fr lower in the others. Two other species in the Gleichenicee (Sticherus owyhensis nd Diplopterygium pinntum) lso ccumulted high levels of Al (unpulished dt), ut the non-polypod Ciotium species did not. The Si:C rtio, n indiction of potentil nutrient sustitution (nd reltive Si ccumultion) vried widely etween species nd cross groups, from 1.2 to 10.2 in non-polypod ferns nd from 0.03 to 3.1 in polypod ferns. Discussion 150 ky 4100ky 4100ky fert CG CM DL AP AM DS DG NC Species Woody dicots, polypod ferns, nd non-polypod ferns hve sustntilly diverent prowles of element concentrtions for c c

6 624 Oecologi (2008) 157: Tle 4 Si (% dry mss), Al (p.p.m.), Al:Si, nd C:Si of severl widely distriuted ferns t three sites. n.d. Non-detectle Ciotium Dicrnopteris Athyrium Asplenium Dryopteris Elphoglossum Sdleri menziesii lineris microphyllum polyodon glr pleceum souleyetin Site Ciotium glucum 0.3 kyers Si kyers Si ,100 kyers Si kyers Al kyers Al ,100 kyers Al n.d kyers Al:Si < kyers Al:Si ,100 kyers Al:Si n.d kyers Si:C kyers Si:C ,100 kyers Si:C Non-polypod ferns Polypod ferns elements tht contriute sustntilly to ecosystem structure nd functioning. While non-polypod fern N nd P concentrtions were comprle to those of dicots, s hs een demonstrted previously (Richrdson et l. 2005; Vitousek et l. 1995), we oserved tht polypod ferns often hve signiwcntly higher folir N nd P concentrtions thn other plnt groups tested from the sme site. Herceous ngiosperms tend to hve higher N nd P concentrtions thn woody ngiosperms (KerkhoV et l. 2006); polypod ferns my function more like herceous ngiosperms thn do tree ferns nd other non-polypod ferns. Both non-polypod nd polypod ferns resor similr proportions of N nd P s do ngiosperms (Allison nd Vitousek 2004), nd polypod fern litter is often high in N nd P content t these sites (unpulished dt). Rtes of oth production nd litter decomposition re demonstrly nutrient limited in the infertile 0.3- nd 4,100 kyer sites (Hrrington et l. 2001; Hoie nd Vitousek 2000), nd rpid decomposition of polypod ferns with nutrient-rich litter could increse locl nutrient vilility. In contrst to N nd P, ll mesured ferns hd low C concentrtions, remrkly so in the non-polypod ferns. Even the reltively C-rich polypod ferns hd N:C rtios verging 7 cross ll sites, higher thn ngiosperms nd even higher thn the rtio of those elements in grsses mesured t nutrient-rich site (NeV et l. 2006). C concentrtions in non-polypod ferns in two sites were elow 0.1%, comprle to C concentrtions in the most nutrient-poor monocots (Brodley et l. 2003; McLughlin nd Wimmer 1999; White nd Brodley 2003). Low concentrtions of divlent ctions in non-polypod ferns re not limited to Hwii: tree ferns nd gleichenioid ferns elsewhere lso exhiit low divlent ctions ut re reltively rich in K compred to co-occurring dicots (Enright nd Ogden 1987; Tnner 1977; Vitousek 2003). The vilility of C cn Vect the multiple ecosystem functions, including limittions on decomposition rte nd interctions with invertertes (Hoie et l. 2006; McLughlin nd Wimmer 1999; Silver nd Miy 2001). C-poor non-polypod ferns often decompose slowly in Hwii nd t other sites, in wys not well explined y trditionl predictors of decomposition rte (Allison nd Vitousek 2004; Scowcroft 1997; Wrdle et l. 2002). Low C concentrtions in non-polypod fern folige could slow decomposition nd dely the relese of nutrients from litter. C concentrtions were once thought to e pssively controlled y trnspirtion rtes (Bngerth 1979), nd indeed they my e when the concentrtion of C in the xylem is high (White nd Brodley 2003). However, ctive exclusion of C from the xylem, nd so decoupling from trnspirtion rte, ppers to e more importnt in regulting C concentrtions (White nd Brodley 2003). C concentrtions s low s those we oserve in non-polypod

7 Oecologi (2008) 157: ferns imply sustntil physiologicl diverences from dicots. A mjor pool of C in plnts is in cell wlls, where C crosslinks nd stilizes pectins. Some plnts my form covlent crosslinks with phenolic cids in their cell wlls, reducing relince on C stiliztion (Fry 1986). Extremely low C in monocots my lso rexect the sustitution of Si for C in cell wlls (Brodley et l. 2003; Cornelissen nd Thompson 1997). A survey of Si:C in plnts demonstrted tht mny ferns hve high rtios, potentilly indictive of monocot-like sustitution, nd Si:C generlly decresed etween erly vsculr plnts nd polypod ferns (M nd Tkhshi 2002). In prticulr, species in the non-polypod fern group nd the group of polypod ferns designted Athyriles until recently (Smith et l. 2006) were considered Si ccumultors (Si:C > 1). We oserved reltively high Si nd Si:C in oth of those groups, in contrst to the other species investigted (Tle 3). In ddition to Si, other ctions my sustitute for C in some processes, nd K:C nd Mg:C re oth signiwcntly wider in non-polypod ferns thn polypod ferns, which in turn hve wider rtios thn ngiosperms (McLughlin nd Wimmer 1999). Although non-polypod ferns my use unique comintion of ctions for essentil cell functions, their totl ction content is consistently lower thn tht of polypod ferns nd dicots, even when environmentl vilility is high. This oservtion rises the possiility tht the environments in which ncient ferns nd their reltives evolved nd diversi- Wed were low in ville ctions, necessitting the evolution of structures requiring few ctions or lterntively, tht wys of using C in structure hd not yet evolved. Conversely, ncient ecosystems my hve hd high concentrtions of toxic multivlent ctions. Non-polypod ferns my hve retined some ncestrl chrcteristics, s they often persist in environments edphiclly inhospitle to other plnts due to either extremely low nutrient concentrtion or high concentrtions of toxic elements (Gltier nd Phillips 1996; Pge 2002). Low reltive growth rtes re common in plnts from nutrient-poor soils, nd they often correlte with low element concentrtions (Meerts 1997). Ferns re reltively slow growing (Pge 2002; Wlker nd Aplet 1994) low growth rtes, or ctive selection t the roots, could reduce toxicity due to elements such s iron (Fe) nd Al (Snowden nd Wheeler 1993). Additionlly, Si in plnts provides protection ginst high concentrtions of toxic metls (Foy et l. 1978), nd high-al plnts generlly lso hve high Si levels (Hodson nd Evns 1995). Al ccumultion is considered primitive trit in the ngiosperms (Chenery nd Sporne 1976), nd in fct, we only oserved Al ccumultion in the Gleicheniles in the non-polypod fern grde. Locl Si nd mcronutrient ction concentrtions my Vect the success of non-polypod ferns cross the rnge of soil properties in Hwii; tree ferns generlly ecome decresingly importnt with sustrte ge, lthough gleichenioid ferns re common in ptches, prticulrly on slopes, t ll ut the nutrient-rich 20-kyer-old site. Polypod ferns re rich nd reltively plstic in N nd P compred to non-polypod ferns, consistent with their diversiwction fter the rise of ngiosperms. Angiosperm dominnce likely provided more complex, nutrient-rich, nd competitive environment (Schneider et l. 2004), nd polypod ferns evolved in direct competition with fst-growing ngiosperms in the densely shded understory of forests (Feild et l. 2003; Feild et l. 2004). As result, polypod ferns my hve evolved incresed resource cpture, in ddition to the evolution of novel photoreceptor necessry for life in shde (Kwi et l. 2003). Non-polypod ferns, in contrst, exhiit lower levels of nutrient plsticity consistent with evolution in hrsh, nutrient-poor environment (NeV et l. 2006). In our sites, polypod ferns re nerly sent t the N- nd P-poor youngest site, ut increse in importnce in older sites. In low-nutrient, prticulrly low- P understories, disturnces my relese pulses of nutrients, which smller, more quickly growing polypod ferns cn cquire. Additionlly, the ility to store luxury nutrients when they ecome ville, nd quickly return them to the roots through rpid decomposition rtes, could contriute to the trnsition in understory dominnce from nonpolypod to polypod ferns long the soil chronosequence. Edphic grdients inxuence fern diversity nd composition in tropicl forests outside of Hwii s well (Tuomisto nd Poulsen 1996; Tuomisto et l. 2002). Leptosporngite ferns in Hwii cn e seprted into t lest two su-groups, distinct from ech other nd co-occurring dicots, sed on mcronutrient concentrtion nd phenotypic plsticity. The reltively smll numer of nonpolypod ferns in Hwii prevents certinty tht monggroup diverences occur in other systems; however, ville dt from the literture demonstrte mcronutrient ction trends re consistent where non-polypod ferns dominte (Enright nd Ogden 1987; Tnner 1977). Contrsts in element concentrtions etween ferns nd ngiosperms, nd etween non-polypod nd polypod ferns, hve the potentil to Vect ecosystem-level nutrient cycling. Plnt groups cn replce ech other s understory dominnts in spce (long environmentl grdients) nd time (in succession nd ecosystem development) in Hwii nd mny other tropicl nd sutropicl environments. Moreover, in mny res the ferndominted understories of Hwiin forests re eing replced y ngiosperm invders high-nutrient (N, P, nd ctions), fst-growing, esily decomposle plnts tht re dpted to humn-ltered environments (Allison nd Vitousek 2004; Thompson et l. 1997). These ngiosperm invsions into non-polypod fern-dominted systems could lter the cycling of C nd other ctions sustntilly. Distinguishing mong plnt groups hs proved useful in

8 626 Oecologi (2008) 157: ecosystem-scle reserch when groups re correctly designted in regrds to the question eing sked (Petchey nd Gston 2006; Violle et l. 2007). Identifying generlizle chrcteristics of groups such s non-polypod nd polypod ferns cn e useful for predicting how communities nd ecosystems chnge in response to humn-induced ltertions. Acknowledgements We thnk R. Aguriuj, L. Arnold, H. Frrington, M. Meyer, nd D. Turner for help in the Weld nd in the l, nd J. Benner, C. Lunch, J. Funk, K. Pryer, nd two nonymous reviewers for comments on drft of the mnuscript. This work ws supported y NSF DEB nd NSF DEB References Aerts R, Chpin FS (1999) The minerl nutrition of wild plnts revisited: re-evlution of processes nd ptterns. In: Fitter AH, RVelli DG (eds) Advnces in ecologicl reserch, vol 30. Acdemic Press, London, pp 1 67 Allison SD, Vitousek PM (2004) Rpid nutrient cycling in lef litter from invsive plnts in Hwii. Oecologi 141: Bngerth F (1979) Clcium-relted physiologicl disorders of plnts. Annu Rev Phytopthol 17: Bowmn WD, Bhnj L, Dmm M (2003) Alpine lndscpe vrition in folir nitrogen nd phosphorus concentrtions nd the reltion to soil nitrogen nd phosphorus vilility. Arct Antrct Alp Res 35: Brodley MR, Willey NJ, Wilkins JC, Bker AJM, Med A, White PJ (2001) Phylogenetic vrition in hevy metl ccumultion in ngiosperms. New Phytol 152:9 27 Brodley MR et l (2003) Vrition in the shoot clcium content of ngiosperms. J Exp Bot 54: Brodley MR et l (2004) Phylogenetic vrition in the shoot minerl concentrtion of ngiosperms. J Exp Bot 55: Chenery EM, Sporne KR (1976) A note on the evolutionry sttus of Aluminum ccumultors mong dicotyledons. New Phytol 76: Cornelissen JHC, Thompson K (1997) Functionl lef ttriutes predict litter decomposition rte in herceous plnts. New Phytol 135: Crews TE et l (1995) Chnges in soil-phosphorus frctions nd ecosystem dynmics cross long chronosequence in Hwii. Ecology 76: Enright N, Ogden J (1987) Decomposition of litter from common woody species of Kuri (Agthis strlis Slis) forest in northern New Zelnd. Aust J Ecol 12: Feild TS, Arens NC, Dwson TE (2003) The ncestrl ecology of ngiosperms: emerging perspectives from extnt sl lineges. Int J Plnt Sci 164:S129 S142 Feild TS, Arens NC, Doyle JA, Dwson TE, Donoghue MJ (2004) Drk nd distured: new imge of erly ngiosperm ecology. Pleoiology 30: Foy CD, Chney RL, White MC (1978) Physiology of metl toxicity in plnts. Annu Rev Plnt Physiol Plnt Mol Biol 29: Fry SC (1986) Cross-linking of mtrix polymers in the growing cell wlls of ngiosperms. In: Briggs WR (ed) Annul review of plnt physiology, vol 37. Annul Reviews, Plo Alto, pp Gltier J, Phillips TM (1996) Structure nd evolutionry signiwcnce of erly ferns. In: Cmus JM, Giy M, Johns RJ (eds) Pteridology in perspective. Royl Botnic Grdens, Kew, pp Grten C (1976) Correltions etween concentrtions of elements in plnts. Nture 261: Hrrington R, Fownes J, Vitousek P (2001) Production nd resource use eyciencies in N- nd P-limited tropicl forests: comprison of responses to long-term fertiliztion. Ecosystems 4: Herert DA, Fownes JH (1995) Phosphorus limittion of forest lef re nd net primry production on highly wethered soil. Biogeochemistry 29: Hoie S, Vitousek P (2000) Nutrient limittion of decomposition in Hwiin forests. Ecology 81: Hoie SE, et l. (2006) Tree species evects on decomposition nd forest Xoor dynmics in common grden. Ecology 87: Hodson MJ, Evns DE (1995) Aluminium/silicon interctions in higher plnts. J Exp Bot 46: Hodson MJ, White PJ, Med A, Brodley MR (2005) Phylogenetic vrition in the silicon composition of plnts. Ann Bot 96: Hohne H, Richter B (1981) Investigtions on the minerl element nd nitrogen content in ferns. Flor 171:1 10 Kwi H, et l. (2003) Responses of ferns to red light re medited y n unconventionl photoreceptor. Nture 421: KerkhoV AJ, Fgn WF, Elser JJ, Enquist BJ (2006) Phylogenetic nd growth form vrition in the scling of nitrogen nd phosphorus in the seed plnts. Am Nt 168:E103 E122 Knecht MR, Gornsson A (2004) Terrestril plnts require nutrients in similr proportions. Tree Physiol 24: M JF, Tkhshi E (2002) Soil, fertilizer, nd plnt silicon reserch in Jpn. Elsevier, Amsterdm M JF, Ymji N (2006) Silicon uptke nd ccumultion in higher plnts. Trends Plnt Sci 11: McLughlin SB, Wimmer R (1999) Tnsley review no. 104: clcium physiology nd terrestril ecosystem processes. New Phytol 142: Meerts P (1997) Folir mcronutrient concentrtions of forest understorey species in reltion to Ellenerg s indices nd potentil reltive growth rte. Plnt Soil 189: Mehrg AA (2002) Arsenic nd old plnts. New Phytol 156:1 4 NeV JC, Reynolds R, Snford RL, Fernndez D, Lmothe P (2006) Controls of edrock geochemistry on soil nd plnt nutrients in southestern Uth. Ecosystems 9: Pge CN (2002) Ecologicl strtegies in fern evolution: neopteridologicl overview. Rev Pleoot Plynol 119:1 33 Petchey OL, Gston KJ (2006) Functionl diversity: ck to sics nd looking forwrd. Ecol Lett 9: Pryer KM, Schuettpelz E, Wolf PG, Schneider H, Smith AR, CrnWll R (2004) Phylogeny nd evolution of ferns (monilophytes) with focus on the erly leptosporngite divergences. Am J Bot 91: Quigg A et l (2003) The evolutionry inheritnce of elementl stoichiometry in mrine phytoplnkton. Nture 425: Rich JW, Russell AE, Vitousek PM (1997) Primry productivity nd ecosystem development long n elevtionl grdient on Mun Lo, Hwii. Ecology 78: Rthinspthi B (2006) Ferns represent n untpped iodiversity for improving crops for environmentl stress tolernce. New Phytol 172: Reiners WA (1986) Complementry models for ecosystems. Am Nt 127:59 73 Richrdson SJ, Peltzer DA, Allen RB, McGlone MS (2005) Resorption prowciency long chronosequence: responses mong communities nd within species. Ecology 86:20 25 Ritchie ME, Tilmn D, Knops JMH (1998) Herivore evects on plnt nd nitrogen dynmics in ok svnn. Ecology 79: Rothwell GW (1996) Pteridophytic evolution: n often underpprecited phytologicl success story. Rev Pleoot Plynol 90: Schneider H, Schuettpelz E, Pryer KM, CrnWll R, Mgllon S, Lupi R (2004) Ferns diversiwed in the shdow of ngiosperms. Nture 428:

9 Oecologi (2008) 157: Scowcroft P (1997) Mss nd nutrient dynmics of decying litter from PssiXor mollissim nd selected ntive species in Hwiin montne rin forest. J Trop Ecol 13: Shver GR, Chpin FS (1980) Response to fertiliztion y vrious plnt-growth forms in n Alskn tundr nutrient ccumultion nd growth. Ecology 61: Silver WL, Miy RK (2001) Glol ptterns in root decomposition: comprisons of climte nd litter qulity evects. Oecologi 129: Smith AR, Pryer KM, Schuettpelz E, Korll P, Schneider H, Wolf PC (2006) A clssiwction for extnt ferns. Txon 55: Snowden RED, Wheeler BD (1993) Iron toxicity to fen plnt species. J Ecol 81:35 46 Sterner R, Elser J (2002) Ecologicl stoichiometry: the iology of elements from molecules to the iosphere. Princeton University Press, Princeton Tnner E (1977) Four montne rin forests of Jmic quntittive chrcteriztion of Xoristics, soils, nd folir minerl levels, nd discussion of interreltions. J Ecol 65: Thompson K, Prkinson JA, Bnd SR, Spencer RE (1997) A comprtive study of lef nutrient concentrtions in regionl herceous Xor. New Phytol 136: Tuomisto H, Poulsen AD (1996) InXuence of edphic speciliztion on pteridophyte distriution in neotropicl rin forests. J Biogeogr 23: Tuomisto H et l (2002) Distriution nd diversity of pteridophytes nd Melstomtcee long edphic grdients in Ysuni Ntionl Prk, Ecudorin Amzoni. Biotropic 34: Vlldres F, Wright SJ, Lsso E, Kitjim K, Percy RW (2000) Plstic phenotypic response to light of 16 congeneric shrus from Pnmnin rinforest. Ecology 81: Vn Arendoonk JJCM, Poorter H (1994) The chemicl composition nd ntomicl structure of leves of grss species divering in reltive growth rte. Plnt Cell Environ 17: Violle C, et l. (2007) Let the concept of trit e functionl! Oikos 116: Vitousek P (1998) Folir nd litter nutrients, nutrient resorption, nd decomposition in Hwiin Metrosideros polymorph. Ecosystems 1: Vitousek P (2003) Stoichiometry nd Xexiility in the Hwiin model system. In: Melillo J, Field C, Moldn B (eds) SCOPE 61: interctions of the mjor iogeochemicl cycles. Islnd Press, Wshington D.C., pp Vitousek P (2004) Nutrient cycling nd limittion. Princeton University Press, Princeton Vitousek P, Wlker L, Whiteker L, Mtson P (1993) Nutrient limittions to plnt growth during primry succession in Hwii Volcnoes Ntionl Prk. Biogeochemistry 23: Vitousek P, Gerrish G, Turner D, Wlker L, Muellerdomois D (1995) Litterfll nd nutrient cycling in 4 Hwiin montne rin forests. J Trop Ecol 11: Vitousek PM, Turner DR, Kitym K (1995) Folir nutrients during long-term soil development in Hwiin montne rinforest. Ecology 76: Wksmn SA, Tenney FG (1928) Composition of nturl orgnic mterils nd their decomposition in the soil. III. The inxuence of nture of plnt upon the rpidity of its decomposition. Soil Sci 26: Wlker L, Aplet G (1994) Growth nd fertiliztion responses of Hwiin tree ferns. Biotropic 26: Wrdle D, Bonner K, Brker G (2002) Linkges etween plnt litter decomposition, litter qulity, nd vegettion responses to herivores. Funct Ecol 16: Wegner C, Wunderlich M, Kessler M, Schwe M (2003) Folir C:N rtio of ferns long n Anden elevtionl grdient. Biotropic 35: White PJ, Brodley MR (2003) Clcium in plnts. Ann Bot 92: