ASPECTS OF RAINFOREST REGENERATION III. THE INTERACTION OF PHENOLS, LIGHT AND NUTRIENTS
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1 New Phytl. (1982) 92, ASPECTS OF RAINFOREST REGENERATION III. THE INTERACTION OF PHENOLS, LIGHT AND NUTRIENTS BY G. CHANDLER AND S. GOOSEM Btany Department, University f Queensland, St. Lucia, Q, 4067, Australia (Accepted 15 July 1982) SUMMARY Measurements in tw sub-trpical rainfrests demnstrated that (i) in ne rainfrest successin, ttal sil phenls varied dramatically thrughut the study year with sils frm the 'climax' rainfrest exhibiting highest phenl levels, the nature f these phenlic cmpunds was nt investigated; (ii) in the ther rainfrest successin, the 55-year-id regrwth exhibited highest ttal phenls, but the level f cndensed tannins increased thrughut the successin. The highest level f nitrificatin was bserved in sils cntaining highest ttal phenls but the additin f ferulic acid decreased nitrificatin. Studies n Argyrdendrn triflilatum demnstrated that additin f the phenl, caffeic acid, t nutrient media enhanced leaf cncentratins f Zn, Mn and P. Increasing light intensities, hwever, decreased fliar cncentratins f Fe, Zn, Mn and P but had n effect n Ca r N. Plants raised n ammnium -N exhibited higher levels f Fe, Zn, Mn and P than thse raised n nitrate-n. Glasshuse trials shwed that at lw light intensities missin f N, P and N + P did nt dramatically enhance leaf phenl prductin. Almst invariably, an increase in light intensity increased leaf phenls but nly ne f the fur species examined (Syzygium firibundum) exhibited marked respnses t nutrient deficiencies at high light intensities, with the missin f nitrgen leading t highest leaf phenls. INTRODUCTION Phenls, armatic rings bearing ne r mre hydrxyl and/r ther substituents, are a class f secndary plant metablites which until recently were thught f as being relatively unimprtant with regard t cntrlling plant metablism, r adapting a plant t its envirnment. Since phenls prvide the building blcks (i.e. the hydrxycinnamic acids-ferulic, sinapic, cumaric and ^-cumaric acids) fr lignin synthesis and there is n cnvincing evidence fr unanimity f physilgical cntrl f phenlic accumulatin (McClure, 1979), the nly limitatin n phenl synthesis is that the prducts d nt impede nrmal cellular metablism. Given the ptential array f prducts, therefre, many authrs hypthesize that phenls may be agents invlved in allelpathic respnses (Whittaker and Feeny, 1971; Ldhi, 1978) whereby phenlic phyttxins, nce released frm leaves r rts, play a key rle in cntrlling sil prperties and the assciated vegetatin under dminant tree species. Several authrs (Odum, 1969; Rice and Panchly, 1974; Wdwell, 1974) argue that as an ecsystem matures, nutrient cycling becmes 'less leaky'; yung cmmunities therefre exhibit pen nutrient cycles, whereas in mature r climax cmmunities, mechanisms exist fr retaining nutrients, particularly n pr sils (internal cycling, reduced herbivry, thick rt mat, etc.; Jrdan and Herrera, X/82/ X/82/ $03.00/ The New Phytlgist
2 37O G. CHANDLER AND S. GOOSEM 1981), which lead t clsed nutrient cycles. Phenlics and their derivatives are implicated in this prcess since they inhibit bacteria invlved in nitrificatin (Ldhi and Killingbeck, 1980). This is manifested in a predminance f ammnium-n ver nitrate-n in the climax cmmunity, the NH4"*' being less easily leached frm the sil. Lamb (1980) argues, hwever, that nitrificatin inhibitin is nt an invariable cnsequence f successinal develpment and that the pattern f N mineralizatin is prbably related t verall sil fertility because f the infiuence this has n phenlic develpment in leaves. Nevertheless, even n eutrphic sils a rle fr phenls cannt be discunted, since average levels f leaf phenls increase with later successinal species (Neldner, 1980). Besides affecting the frm f available N, phenls als affect the availability f ther plant nutrients but in a manner which is nt yet clear. Davies (1971) reprted phenlic cfnpunds as water-suble chelating agents implicated in the slutin and transprt f Fe. Additin f chelatrs t nutrient slutins can reduce metal activity and uptake (Fy, Chaney and White, 1978) but Wallace et al. (1974) suggest that uptake f metal chelates by snap beans may accunt fr the high levels f Cu, C and Cd in plants raised n chelatr ammended sils. Glass (1973, 1974) demnstrated that in shrt-term experiments, uptake f K and phsphate was inhibited by phenlic cmpunds which strngly infiuenced cell membrane ptentials. Glass and Dunlp (1974) supprt the hypthesis that phenlic infiuence n in uptake is mediated thrugh direct nn-specific effects upn cell membrane permeability. Stwe and Osbrn (1980) als reprted an interactin between phenlics and nutrients; phyttxicity f cumaric and vanillic acids increased at lw nutrient levels. Since phenl prductin is exacerbated by lw nutrient levels (Lehman and Rice, 1972; Del Mral, 1972; McKey et al., 1978) and phenlic cmpunds are fund in sils underlying natural vegetatin types (Whitehead, 1964; MuUer and Chu, 1972) it is surprising that s little wrk is reprted dealing with nutrient phenl interactins. This study investigates seasnal and successinal variatins in sil phenls and the effect f a simple phenl n sil nitrificatin rates. In additin, the effect f light intensity and nutrients n leaf phenl levels and the effect f light and phenls n fliar nutrient levels are investigated in rder t examine sme f the diverse effects f phenls in rainfrest plants. MATERIALS AND METHODS Sil phenls and site descriptins Sil samples were cllected frm three successinal sites thrughut 1980 in a study area at Mt. Glrius, S. Queensland (latitude 27 2O'S, lngitude 'E, altitude 635 m): site 1, a virgin, mist sub-trpical rainfrest n a basaltic kraznzem (Webb, Tracey and Williams, 1972); site 2, a 22-year-ld regrwth frm an riginal 0-16 ha clearing in the mature rainfrest; site 3, a sclerphytic Eucalyptus-Tristania dminated frest int which rainfrest elements appear t be encraching. At each site 5x10 cm cres were cllected and bulked fr analysis. Samples were extracted in 80 % ethanl under refiux fr 8 h and ttal phenls estimated by the methd f Swain and Hillis (1959). In December 1981, sil samples were als cllected frm a sub-trpical rainfrest successin previusly described by Lamb (1980). Sils (5x10 cm cres) frm each successinal stage were bulked and extracted fr cndensed tannins and
3 Aspects f rainfrest regeneratin 371 tannin derivatives (Rice and Panchly, 1973) and phenlic acids (Ldhi,. 1975). Phenlic prducts were estimated as befre. Labratry incubatins Labratry sil incubatins t estimate nitrificatin fllwed the methd f Lamb (1980). After establishing levels f simple phenlic acids in successinal sils (Lamb's successin), ferulic acid was added t varius incubatins at 0, x 0-5, x 1 and X 2 the cncentratins f simple phenlic acids riginally present in the sils. Each treatment cmprised three replicate incubatins and subsequent duplicate determinatins. Grwth cnditins Seeds f Argyrdendrn triflilatum F. Muell. (a climax rainfrest species) were germinated in trays f vermiculite (28 C) and 12 weeks after germinatin seedlings were transferred t 6-5 cm pts cntaining acid-washed sand. Plants were raised under shade clth creating fur shade regimes: (a) zer shade, (b) 50% shade, (c) 75% shade and (d) 98% shade (irradiance apprximately 100, 50, 25 and 2 ne cm"^ s~\ respectively). Under each shade regime plants were supplied with either (a) ammnium (plus nitrificatin inhibitr, 'N-serve') r (b) nitratetype nutrient slutin (Lng Ashtn) and after 4 weeks establishment time varius cncentratins f caffeic acid were added t nutrient media supplied t grups f five plants: 0, 6-09 x 10-^ M and x 10"^ M caffeic acid (0, 10 and 50 p.p.m. respectively). After 6 mnths grwth leaf samples were ven dried (60 C) and subjected t (i) micr Kjeldahl N estimatins, and (ii) nitric/perchlric acid digest with subsequent estimatins f Mn, Mg, Fe, K, Zn and Causing atmic absrptin spectrscpy. Phsphate was als determined in this digest (Oweczkin and Kervin, 1980). Seedlings (apprximately 5 mnths ld) f Brachychitn aceriflius F. Muell., Syzygium firibundum F. Muell. {Eugenia ventenatii Benth.), Eupmatia laurina R.Br. and Archntphenix cunninghamiana Wendl. and Drude were als raised in sand cultures (20 weeks) under the shade regimes described abve. Plants were supplied twice weekly with ne f fur ammnium-nitrate-type nutrient slutins (Lng Ashtn frmula, Hewitt and Smith, 1975) and ph adjusted t 6-6 with KOH r HCl prir t applicatin. These slutins were (a) cmplete (b) cmplete minus P (c) cmplete minus N (d) cmplete minus P and N. At harvest leaf phenls were extracted and estimated as described previusly (Swain and Hillis, 1959). RESULTS Variatins in sil phenls with time Large variatins in ttal sil phenls were bserved in all successinal sites at Mt. Glrius thrughut the year [Fig. 1 (b)]. All exhibited a phenl peak m March f relatively shrt duratin, whilst mature rainfrest and frmge-site sils exhibited high sil phenls fr an extended perid later in the year. Bth peaks ccurred at times f lw rainfall [Fig. 1(«)] althugh sil misture per se was lwest in April and Octber (unpublished data).,, In the successin described by Lamb (1980), ttal phenls peaked m the 55-year-ld regrwth, but thereafter declined in the mature climax site (Fig. 2). This pattern was mimicked by simple phenlic acids and tannin derivatives but the level f cndensed tannins increased thrughut the successin.
4 372 G. GHANDLER AND S. GOOSEM 1980 Fig. 1. Seasnal changes at the Mt. Glrius study sites: (a) rainfall 1980, M; lng-term average rainfall, \I\; x (y) = rainy daj's per mnth 1980 (lng-term average number f rainy days per mnth); (b) ttal sil phenls: fringe site, O; mature frest. A; regrwth site, D- Althugh cmparisns f ttal sil phenls reprted by different authrs are difficult t make (different extractin techniques, etc.) the levels in these rich rainfrest sils appeared lw (apprximately 10 t 30%) cmpared with values reprted in presumably less-fertile sils (Whitehead, 1964; Ldhi, 1975, 1978; McKey et al, 1978). Labratry incubatins Prir t incubatin the levels f NH4"'" N and NOg^-N in sils thrughut the successin were similar (Fig. 3). Fllwing incubatin, hwever, NOg^-N increased dramatically, with maximum NOg~-N ccurring in the sil which exhibited highest levels f phenlic acids and tannin derivatives (Fig. 2). There was n significant change in the amunts f ammnium present in sils after incubatin (Fig. 3). Additin f ferulic acid t sils generally decreased NOg^-N present fllwing incubatin (Fig. 4). On a percentage basis, nitrificatin was affected mst in the climax cmmunity sil where a twfld increase in simple phenlics decreased NOg~-N by abut 45 %. Only small decreases in NOg^-N were bserved when the amunt f ferulic acid was increased frm ne t twfld ver initial simple phenl cncentratins. Effect f caffeic acid and light intensity n leaf nutrients in Argyrdendrn triflilatum Increasing light intensity significantly decreased leaf Fe, Zn, Mn and P but had n effect n leaf Ca r N (Table 1) (tw- way analysis f variance, 95 % level f prbability). Lwer levels f K and Mg were bserved at intermediate light
5 Aspects f rainfrest regeneratin cr O c 0) 300- t U/D Age f successin (years) Fig. 2. Cbanges in pbenls in rainfrest sils frm varius successinal stages and frm an undisturbed cmmunity (U/D) at tbe Lamingtn Natinal Park. Simple pbenlic acids (/tg ferulic acid equivalents), O; tannic derivatives {/ig ellagic acid equivalents). A; cndensed tannins (jig catecbin equivalents), D; ttal phenls (sum f O + A + D), Standard errrs sbwn by vertical bars. intensity. Plants supplied with ammnium-n (Table 1) exhibited higher levels f Fe, Zn, Mn and P cmpared with thse raised n nitrate-n (paired t test). Applicatin f caffeic acid t nutrient media (Table 1) influenced the levels f sme elements als affected by light; levels f Zn, P and Mn were enhanced (90 % level f prbability). Levels f P and Mn were maximal at 10 p.p.m. caffeic acid, but higher cncentratins decreased leaf cntent f these nutrients. Whilst nt statistically significant, caffeic acid als appeared t increase the level f Fe in leaves f Argyrdendrn triflilatum. Effect f light intensity and nutrients n leaf phenls The effect f changes in light intensity n leaf phenl levels varied dramatically between species (Fig. 5). In B. aceriflius small changes in light intensity (e.g. 98 t 75% shade) increased leaf phenl cntent by ver 100% but with further increases in light, the levels flattened ut [Fig. 5(a)]. Omissin f nutrients did nt significantly affect leaf phenls in this species. In S. firibundum, increasing light
6 374 G. CHANDLER AND S. GOOSEM E d. Q. r O E Q. d Age f successin (years) 50 U/D Fig. 3. Mineral N present in rainfrest sils cllected frm the Lamingtn Natinal Park successin. NH4+-N and NO3~-N present at cllectin, O; after incubatin, #. Standard errrs shwn by vertical bars. intensity increased leaf phenls nly when nutrients were mitted frm the culture medium [Fig. 5(b)]. This was the nly species examined where missin f nutrients significantly affected leaf phenls but this effect was nly bserved at higher light intensities. Fr E. laurina and Archntphenix cunninghamiana increasing light intensity increased leaf phenls but missin f nutrients did nt [Fig. 5 (c), (d)]. DISCUSSION Reprts supprting the cntentin that nitrificatin is inhibited in sils frm 'climax' cmmunities generally relate t successins n relatively infertile sils (Lamb, 1980). The Mt. Glrius and Lamingtn successins, hwever, ccur n relatively fertile kraznzems where the level f ttal phenls is lw (Figs 1 and 2).
7 Aspects f rainfrest regeneratin E Q. d. I I t O Ferulic acid added l incubatins (^g g Fig. 4. Effect f ferulic acid n sil mineralizatin/nitrificatin. Sils were cllected frm the Lamingtn successin and incubated with ferulic acid as described in the text: 0,12-year-ld site; #, 17-year-ld; A, 45-year-Id; A, 55-year-ld; Q, undisturbed site. Standard errrs shwn by verical bars. Seasnal variatins in sil phenls (Fig. 1), which are implicated in nitrificatin inhibitin, were in fact quite marked, and althugh all sites exhibited peaks, the 'climax' cmmunity exhibited the highest phenl level ver an extended perid. Whilst this is cnsistent with higher average levels f leaf phenls in * climax' rainfrest species cmpared with ther serai stage species (Neldner, 1980), the 'climax' sils in Lamb's successin did nt shw this althugh they did exhibit highest levels f cndensed tannins (Fig. 2). Peaks in sil phenls (Fig. 1) were nt crrelated with rainfall maxima, suggesting that leaching frm attached leaves did nt cntribute significantly t sil phenls in the shrt term, althugh sme phenls are knwn t be water sluble. The ccurrence f high sil phenls at all sites in March and substantial levels in ' climax' and fringe sites later in the year are pxbably related t metablic events within the sil, cued by sme yet-t-be-established envirnmental factrs. Litterfall in this frest peaked in December (rainy seasn); the sil phenl peak in March may refiect phenl release as decay f these leaves ccurs. The high levels f sil phenls later in the year may refiect the breakdwn f litter accumulated thrugh the dry seasn, althugh there is n reasn t suspect that the ccurrence f sil phenls at different times is due t the same envirnmental (r ther) factr. The apparent disappearance f phenls culd be due either t phenlase activity r t the cmplexing f phenlic cmpunds with humic acid and rganic cllids reprted t ccur in sils with a high natural rganic cntent (MuUer and Chu, 1972). sil)
8 376 G. CHANDLER AND S. GOOSEM IT) O vo O ri fo tsi m > l Ti- 00 vo r-i T- TH f^ p p O O 6 O O O CS m in O -a '3 a u +-> C u T-l in 00 vd t^ rtin t^ OS O> f^ fs ^ T-l P p 6 \O m m c^ m T-c (S O t^ rh t^ O fn) T I n T < O n CS CN m P CS CS CO CN rj CN m <N CS CN CN CS vari nalvsis m m O O 00 O in CS m in d -71 T< p P P P CS r^ CS r» CS rp p in p r CS CS CS CS CS I 2 a a 3c I s c*) m v r^ n t^ m CS r^ m r^ CS r-c T-l p p p p Tt- in <* c^ '^ O T-l O^ 10 TJ- r CS T7< p p p p p in O in O t^ t^ f7* '^^ CS CS CS CS 0 vo p CS CS CS CS pi u 01 V CO c S U 4.* <» <; g 8 m m m in ri- CSt CS f^ ^^i f^^ ^ ^ 7*^ 00 in ^ CS '^ ^ <N c a d O vo O s CS r "^ CO r CS 00 CSO 1*^ 00 rh T 1 T 1 TH y-m d OS \O "^ CS O ^ in so CS CS fo CS SO O 00 O O CN r-* T 1 TH t I Ti rh CS be O 00 O T-i so O rht-l O r^ vo CS O OS O^ so S r O 00 rh in * OS 00 OS 00 O 00 r s rh -.j- -.^ CS OS m m s 00 r^ >$ CO CS t^ r- Ti< s CS CN OS vo <* OS O m in CS CO 1-1 so m a dry wt u ^ i ^ I' + I + I + I + I + I + I ^ m ** «^ I CO.^ «'C II Ji irt m CS CS O O in m l-i S a 8
9 Aspects f rainfrest regeneratin Irradiance (ne cm" Fig. 5. Effect f light intensity and nutrient deficiencies n leaf phenls in (a) Brachychitn aceriflius, (b) Syzygiumflribundum, (c) Eupmatia laurina, (d) Archntphenix cunninghamiana. Plants were raised as described in the text. Symbls: O, full nutrients; #, full nutrients minus N; A, full nutrients minus P; A, full nutrients minus N and P. 100 Rice and Panchly (1973, 1974) suggest that inhibitin f nitrificatin in climax cmmunities, mediated thrugh secndary plant metablites, makes the ecsystem 'less leaky' with regard t nitrgen. Lamb (1980) argues that whether r nt ecsystem maturity leads t N cnservatin is dependent upn the nature f the nutrient stress experienced by plants during the successin. Fr fertile rainfrest sils. Lamb (1980) reprted increasing amunts f nitrate N in each lder successinal stage. On nutrient-rich sites, therefre, nitrificatin inhibitin did nt appear t ccur. In ur studies at Lamingtn, nitrificatin patterns were essentially similar t thse reprted by Lamb (1980). Nitrificatin did nt appear t be inhibited in the 'climax' sils (Fig. 3) althugh ur study did shw a reductin f nitrificatin in the climax cmm.unity cmpared with the successinal stage prir t 'climax'. Inevitably, therefre, we cnclude that nitrificatin inhibitin is nt necessarily a cnsequence f ecsystem develpment. Further, the generally lw level f inhibitin f nitrificatin by ferulic acid (Fig. 4) and the fact that maximum nitrificatin (Fig. 3) ccurred in sils cntaining the highest levels f simple phenls and tannin derivatives (Fig. 2) suggests that at cncentratins fund in these sils (and at cnsiderably higher cncentratins) these cmpunds are nt
10 378 G. CHANDLER AND S. GOOSEM imprtant in inhibiting nitrificatin. The psitin f cndensed tannins remains unclear; if they cntinue t increase as the ecsytem matures (Fig. 2) they may play a critical rle nt nly in inhibiting nitrificatins but als in binding essential nutrients. While the shrt-term effect f simple phenls n phsphate and K uptake by barley rts is ne f inhibitin (Glass, 1973, 1974) there is the pssibility that phenls act as water-sluble chelating agents making sme nutrients mre available t plants (Davies, 1971). With Argyrdendrn triflilatum (Table 1) caffeic acid enhanced fliar cncentratins f Zn, P, Mn and pssibly Fe. Althugh the mechanism f actin is unclear, the simple phenls which are cmmn cnstituents f sils (Ldhi, 1978), may play a mre imprtant rle in nutrient mbilizatin at lw cncentratins than they d in preventing germinatin r evkitig allelpathic respnses. Grubb (1977) cntends that shading is an imprtant variable with regard t fliar nutrient cncentratins; he reprted that shade and sun leaves cntained similar cncentratins f N, P, S, Fe and Cu, but that shade leaves usually cntained appreciably mre K, Mg, Zn and M. Fr Argyrdendrn, hwever, (Table 1) shade leaves cntained higher levels f Fe, Zn, P and Mn. Plants raised n NOg" in full sunlight, fr example, cntained 0-02 % manganese n a dry wt basis, which crrespnds t the average value reprted by Grubb (1977). Plants raised n NH4+ in full light, hwever, almst duble that value, whilst under shade cnditins, a furfld increase in Mn was fund (Table 1). The high levels f ins under shade cnditins may arise as a cnsequence f reduced grwth because f a lack f carbhydrate, r the accumulatin f ins may be an eclgically significant mechanism allwing fr rapid grwth f rainfrest seedlings shuld favurable light cnditins permit grwth. This hypthesis wuld have mre appeal if N were mbilized under shade cnditins. Althugh the shade leaves f Argyrdendrn d cntain appreciably mre nutrients than sun leaves, the elements invlved differ frm thse reprted by Grubb (1977). Presumably, species differences r the cmplicating effects f sils (and presumably phenls) n nutrient availability accunts fr these discrepancies. Higher levels f nutrients in plants raised n NH4''' nutrient slutin (Table 1) may refiect n adaptatin f this species t better grwth n NH4+ versus NOg". A similar adaptatin was nted fr S. firibundum (Chandler, 1981). Given the high levels f NH4''" in many rainfrest sils (Tanner, 1977) and the apparent adaptatin f rainfrest plants t grwth n ammnium nutrient slutins, the hypthesis (see Hewitt and Smith, 1975) that mst species grw better with nitrate than with ammnium-n needs clser examinatin with regard t a cmplex rainfrest ecsystem. High levels f phenlics in rainfrest plants are assciated with lw sil fertility (McKey et al., 1978). At lw light intensities, hwever, missin f varius nutrients (Fig. 5) did nt always appear t enhance leaf phenl prductin significantly. This may refiect lw activity f light-activated enzymes invlved in phenl synthesis (Schiitte, 1978). Almst invariably, an increase in light intensity increased leaf phenls, but nly ne f the fur species examined (S. firibundum) exhibited marked respnses t nutrient deficiencies, with the missin f N leading t high leaf phenls. Variatins in light intensity, therefre, appeared t infiuence phenls mre drastically than missin f plant nutrients, and in fact the suggestin that phenl levels invariably increase with decreasing nutrient levels may apply t an ecystem as a whle, but nt fr individual species. This
11 Aspects f rainfrest regeneratin 379 hypthesis is supprted by Neldner (1980), wh reprted that sme rainfrest species actually exhibited higher levels f leaf phenls when plants were raised n basaltic kraznzems cmpared with thse raised n white sands. In cnsidering an envirnmental rle fr phenlic metablites the nature and tempral distributin f these cmpunds and their effects n prcesses in the envirnment must be ascertained. This has nt been clearly demnstrated t date. Certainly, n ligtrphic sils, cmplex phenls inhibit nitrificatin (Rice and Panchly, 1973) and may limit nutrient release by their tanning effects. An essential manifestatin f the psitive feedback effects f phenlics wuld appear t be the black-water rivers (Janzen, 1974). On eutrphic sils, hwever, the sequence f events invlving phenls remains unclear. If simple phenls are the majr phenlic prduct, then nutrient acquisitin thrugh a chelating effect may be mre imprtant than slight inhibitin f nitrificatin. If, as Alexander (1977) reprted, simple phenls are a carbn surce fr bacterial and fungal grwth then the phenls may indirectly aid mineralizatin/nitrificatin. Data (Figs 2 and 3) supprt this cntentin, since nitrificatin was mst rapid in sils with the highest levels f simple phenls and tannin derivatives. Presumably ther mechanisms perate t prevent lss f NOg" frm the system. Certainly the failure f many rainfrest species t increase phenl prductin significantly under nutrient limiting cnditins, tgether with the lw levels f ttal sil phenls in the tw subtrpical systems examined, suggests that a rle prpsed fr phenls n infertile sils is nt perating in this system. Pssibly the slw accumulatins f cndensed tannins with increasing maturity will mdify that situatin. ACKNOWLEDGEMENTS The authrs wuld like t thank Ms Jill Landsberg and Mr Peter Ft fr their expert technical assistance thrughut the prject. Thanks are als due t Dr David Lamb and Dr Hck Ng wh read an earlier draft f the manuscript and made many helpful cmments. The wrk was supprted in part by an Australian Research Grants Cmmittee grant (D R). Stephen Gsem was the hlder f a Cmmnwealth Pstgraduate Schlarship. REFERENCES ALEXANDER, M. (1977). Sil Micrbilgy. Wiley and Sns, New Yrk. 2nd editin, p CHANDLER, G. E. (1981). Physilgical aspects f rainfrest regeneratin. L Effects f light and nitrgen surce n grwth and nitrgen assimilating enzymes f Slanum mauritianum and Syzygium firibundum. New Phytlgist, 87, DAVIES, R. L (1971). Relatin f plyphenls t decmpsitin f rganic matter and t pedgenetic prcesses. Sil Science, 111, DEL MORAL, R. (1972). On the variability f chlrgenic acid cncentratin. Oeclgia, 9, FY, C. D., CHANEY, R. L. & WHITE, M. C. (1978). The physilgy f metal txicity in plants. Annual Review f Plant Physilgy, 29, GLASS, A. D. M. (1973). Influence f phenlic acids n in uptake. L Inhibitin f phsphate uptake. Plant Physilgy, 51, GLASS, A. D. M. (1974). Influence f phenlic acids n in uptake. III. Inhibitin f ptassium absrptin. Jurnal f Experimental Btany, 25, GLASS, A. D. M. & DUNLOP, J. (1974). Influence f phenlic acids n in uptake. IV. Deplarizatin f membrane ptentials. Plant Physilgy, 54, GRUBB, P. J. (1977). Cntrl f frest grwth and distributin n wet trpical muntains with special reference t mineral nutritin. Annual Review f Eclgy and Systematics, 8, HEWITT, E. J. & SMITH, T. A. (1975). Plant Mineral Nutritin. Unibks, English Universities Press. p. 32.
12 380 G. CHANDLER AND S. GOOSEM JANZEN, D. H. (1974). Trpical blackwater rivers; animals and mast fruiting by Diptercarpaceae. Bitrpica, 6, JORDAN, C. F. & HERRERA, R. (1981). Trpical rain frests. Are nutrients really critical? American Naturalist, 117, LAMB, D. (1980). Sil nitrgen mineralizatin in a secndary rainfrest successin. Oeclgia, 47, LEHMAN, R. H. & RICE, E. L. (1972). Effect f deficiencies f nitrgen, ptassium and sulphur n chlrgenic acid and scplin in sunflwer. American Midland Naturalist, 87, LDHi, M. A. K. (1975). Sil-plant phyttxicity and its pssible significance in patterning f herbaceus vegetatin in a bttmland frest. American Jurnal f Btany, 62, LODHI, M. A. K. (1978). AUelpathic effects f decaying litter f dminant trees and their assciated sil in a lwland frest cmmunity. American Jurnal f Btany, 65, LDHi, M. A. K. & KiLLiNGBECK, K. T. (1980). AUelpathic inhibitin f nitrificatins and nitrifying bacteria in a pndersa pine cmmunity. American Jurnal f Btany, 67, MCCLURE, J. W. (1979). Phenlics in the envirnment. In: Bichemistry f Phenlics (Ed. by T. Svi^ain, J. B. Harbrne & C. F. Van Sumere), pp Plenum Press, New Yrk. MCKEY, D., WATERMAN, P. G., GARTLAN, J. S. & STRUHSAKE, T. T. (1978). Phenlic cntent f vegetatin in tw African frests; eclgical implicatins. Science, 202, MuLLER, C. H. & CHOU, C. H. (1972). Phyttxins: an eclgical phase in phytchcmistry. In: Phytchemical Eclgy (Ed. by J. B. Harbrne), pp Academic Press, New Yrk and Lndn. NELDNER, V. J. (1980). The eclgical rle f phenlics in plant/animal interactins and rainfrests in S.E Queensland. Hnurs thesis. University f Queensland, p. 12. ODUM, E. P. (1969). The strategy f ecsystem develpment. Science, 164, OwECZKiN, J. & KERVEN, G. (1980). Methds f Analysis fr Nitrgen, Phsphrus, Sulphur and Ptassium in Plant Tissue. Department f Agriculture, University f Queensland. RICE, E. L. & PANCHOLY, S. K. (1973). Inhibitin f nitrificatin by climax ecsystems. II. Additinal evidence and a pssible rle f tannins. American Jurnal f Btany, 60, RICE, E. L. & PANCHOLY, S. K. (1974). Inhibitin f nitrificatin by climax ecsystems. III. Inhibitrs ther than tannins. American Jurnal f Btany, 61, ScHUTTE, H. R. (1978). Secndary plant substances; special tpics f the phenylprpanid metablism. Prgress in Btany, 40, STOWE, L. G. & OsBORN, A. (1980). The infiuence f nitrgen and phsphrus levels n the phyttxicity f phenlic cmpunds. Canadian Jurnal f Btany, 58, SWAIN, T. & HILLIS, W. E. (1959). The phenlic cnstituents i Prunus dmestica. I. Quantitative analysis f phenlic cnstituents. Jurnal f Science, Fd and Agriculture, 10, TANNER, E. V. J. (1977). Fur mntane rainfrests f Jamaica: a quantitative characterizatin f the flristics, the sil and the fliar mineral levels and a discussin f the interrelatins. Jurnal f Eclgy, 65, WALLACE, A., MUELLER, R. T., CHA, J. W. & Alexander, G. V. (1974). Sil ph, excess lime and chelaing agents n micrnutrients in sybeans and bush beans. Agrnmy Jurnal, 66, WEBB, L. J., TRACEY, G. & WILLIAMS, W. T. (1972). Regeneratin and pattern in the subtrpical rainfrest. Jurnal f Eclgy, 60, WHITEHEAD, D. C. (1964). Identificatin f p-hydrxybenzic, vanillic, p-cumaric and ferulic acids in sils. Nature, 202, 417^18. WHITTAKER, R. H. & FEENY, P. P. (1971). Allclchemics; chemical interactin between species. Science, 171, WOODWELL, G. M. (1974). Success, successin and Adam Smith. Biscience, 24,
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