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Soil acidity and nutrient deficiency in central amazonian

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  • 1. ORIGINAL PAPERSoil acidity and nutrient deficiency in central Amazonianheath forest soilsFla´vio J. Luiza˜o Æ Regina C. C. Luiza˜o ÆJohn ProctorReceived: 21 February 2007 / Accepted: 21 May 2007 / Published online: 21 June 2007Ó Springer Science+Business Media B.V. 2007Abstract Experiments were carried out to test theeffects of liming and nutrient additions on plantgrowth and soil processes such as C and N miner-alisation in three contrasting forest types in centralAmazonia: the stunted facies of heath forest (SHF),the tall facies of heath forest (THF) and thesurrounding lowland evergreen rain forest (LERF).Calcium-carbonate additions increased soil respira-tion in the field plots in the SHF; in laboratoryincubations, soil respiration was higher in the SHFwhen soils were fertilised with N, and in THF andLERF after S additions. The addition of N alone or indifferent combinations generally induced a netimmobilisation of soil N. Net nitrification increasedduring the incubation in SHF and THF soils fertilisedwith N+P, and in LERF soils fertilised with either N,or P, or CaCO3. In a field experiment using ingrowthbags, a higher fine root production was observed inall forest types when bags were fertilised with CaCl2or CaCO3, suggesting that Ca may be a limitingnutrient in these soils. Calcium-carbonate addition ina glasshouse bioassay experiment with rice showedan overall positive effect on the survival and growthof the seedlings. In other treatments where soil pHwas not raised, the rice showed acute toxicitysymptoms, poor root and shoot growth and highmortality. Similar results were yielded in a fieldexperiment, using naturally established seedlings inthe field plots in SHF, THF and LERF. It is concludedthat the acute H+ion toxicity is a major growth-limiting factor for non-adapted plants in heath forestsoils in central Amazonia.Keywords Campina Á Campinarana Á Heath forest ÁNutrient limitation Á Soil acidityIntroductionMost of Amazonia that is not seasonally flooded iscovered by lowland evergreen rain forest (sensuWhitmore 1984), often referred to in Brazil as terrafirme forest, and characterised by high speciesdiversity (Pires and Prance 1985). However otherforest formations that have a low species diversity,low stature and high presence of scleromorphicleaves, associated with white sandy soils (Spodosols),occur locally throughout Amazonia in Brazil, south-ern Venezuela, Ecuador, north-eastern Peru (Klingeand Medina 1979; Anderson 1981; Proctor 1999), aswell as in Guyana and Suriname (Heyligers 1963;Whitmore 1984). Several of these forest formationsF. J. Luiza˜o (&) Á R. C. C. Luiza˜oDepartamento de Ecologia, Instituto Nacional dePesquisas da Amazoˆnia, Caixa Postal 478, 69011-970Manaus, Amazonas, Brasile-mail: fluizao@inpa.gov.brJ. ProctorSchool of Biological and Environmental Sciences,University of Stirling, Stirling FK9 4LA, Scotland, UK123Plant Ecol (2007) 192:209–224DOI 10.1007/s11258-007-9317-6
  • 2. present distinctive situations (e.g., caatinga locatedon waterlogged sites in Venezuela vs. campina incentral Amazon on sites not subject to flooding).However, these forest formations from the neotropics(which could be collectively called caatinga), shownoticeable similarities in structure and physiognomyamongst themselves, and to kerangas from thepalaeotropics, in Southeast Asia (Bru¨nig 1968,1970; Proctor et al. 1983; Whitmore 1984). Takinginto account that in Brazil there is another well-known biome named caatinga (covering large areasof the semi-arid region in north-eastern Brazil), theuse of an international nomenclature such as ‘heathforest’ (sensu Whitmore 1984) seems more conve-nient, and will be used henceforth. About 5–6% ofAmazonia is covered by heath forest (Anderson 1981;Whitmore 1984) occurring on Spodosols with a layerof mor humus of varying thickness. The stuntedfacies of heath forest (referred to as SHF in thisarticle) is called campina in Brazil and often lacks themor humus layer; the taller facies (THF) is calledcampinarana, and occurs next to high LERF. Thephysiognomy of the SHF and THF formations couldcorrespond to facies of ‘caatinga’ in Venezuela(Anderson 1981).Heath forests grow on bleached white sands(Richards 1996) and are generally characterised bytheir short stature, slender trunks, thick leaves andlow species richness. There are several views as tothe causes of heath forests, but it is unlikely that asingle causal factor acts in isolation (Bru¨nig 1968,1970; Richards 1996). The four factors most com-monly cited are: (i) drought (Bru¨nig 1968; Klinge andMedina 1979); (ii) waterlogging (Bru¨nig 1968;Bongers et al. 1985; Klinge and Medina 1979); (iii)low nutrients (Bru¨nig 1973, 1974; Jordan 1985;Medina and Cuevas 1989; Richards 1996); and, (iv)soil acidity and phenolics (Bru¨nig 1968; Janzen 1974;Proctor et al. 1983; Whitmore 1984; Proctor 1999).However, the main factor or factors causing thisforest formation remain unclear (Miyamoto et al.2007) and require further investigation.The first two of the above hypotheses, drought andwaterlogging, are difficult to investigate experimen-tally. However, on the basis of observations made inheath forests occurring under different hydrologicalsituations, they have been discarded as the principalcausal factors. For example why does seasonalwaterlogging tend to cause savanna in much ofBrazil and not heath forests if waterlogging is animportant cause of heath forests?The second two hypotheses (low nutrients, soilacidity and phenolics) are more amenable to exper-imental tests. Moreover, field studies in heath forestin Brunei, analysing soil and litterfall nutrientcontents, have indicated a possible limitation by N,but not by P for heath forest growth (Moran et al.2000). In experimental tests, Ca addition (liming) hasgenerally been used to reduce acidity and fertiliserapplications to the soil can directly stimulate micro-bial population and allow plant growth. The rootingrowth technique, despite its shortcomings, offersan opportunity to study fine root growth in relation tomineral nutrient availability, and is particularly usefulfor within-site comparisons amongst treatments(Steen et al. 1991).In order to test the hypothesis that nutrients, or lowpH, or both limited soil processes (such as soilrespiration and N transformations), fine root and plantgrowth and survival were compared after the additionof nutrients in two types of heath forest and in LERF.It was hypothesised that (a) soil respiration, Ntransformations, and roots and seedling growth wouldrespond to N but not P or other nutrient addition; and(b) increasing soil pH through liming would cause asignificant response in soil processes, root growth,and seedling growth and survival, and (c) the additionof both lime and nutrients should produce the bestresponses.Materials and methodsStudy siteThe field study was carried out in central Amazonia(2o360S; 60o010W), 60 km north of Manaus,Amazonas State, Brazil, on a gradient of naturalvegetation from SHF through THF to high LERF.The average annual rainfall in the area is 2,300 mm,and a dry season occurs from June to November. Thesoils are classified as Spodosols (SHF and THF) andUltisols (LERF). Selected features for soil profilesunder each forest type are given in Table 1. Speciesrichness in both heath forests is low (seven species haÀ1in SHF and 24 in THF) compared with 82 species haÀ1in the LERF. Above-ground biomass was estimated at71 Mg haÀ1in SHF, 152 Mg haÀ1in THF and210 Plant Ecol (2007) 192:209–224123
  • 3. 409 Mg haÀ1in LERF (Luiza˜o 1996). The Fabaceae(Caesalpinioideae) has the highest basal area in allthree-forest types, followed by the Sapotaceae in theSHF, by the Euphorbiaceae in the THF, and by theBurseraceae in the LERF. A full description of the siteproperties and the forests is given by Luiza˜o (1996).For soil and vegetation studies, three 50 m · 50 m plotswere delimited and used in each forest type. In eachplot, the four quadrants, measuring 25 m · 25 m, werealso marked. In the present work, two experimentswere carried out in the field (experiments 1 and 2) andtwo in the laboratory (experiments 3 and 4).Field experimentsExperiment 1: root ingrowth bags in the fieldNylon ingrowth bags of 12 cm · 12 cm and 1-mmmesh were used. Two growth media were used in theingrowth bags: medium-sized vermiculite (3À6 mm)and sieved sand from open SHF sites. They con-trasted in that sand is inert with virtually no exchangecapacity, whilst vermiculite being a clay mineral hasa large exchange capacity (100–150 meq/100 g), itspH is between 7 and 10, and naturally containsexchangeable K+, Mg2+and Fe2+ions. The bags withsand were placed on the soil surface (after the removalof the litter layer) and the bags with vermiculite wereplaced on the soil surface, and in the soil to a depth of10 cm. In the SHF, the 10 cm depth corresponded toeither white sand in the open patches, or under closedcanopy, it incorporated the layer where organicmatter and fine roots concentrated. In the THF at10 cm depth ingrowth bags were almost exclusivelyin the litter layer and in the LERF, mostly in theupper litter layer where a well-developed root matoccurred.There were six nutrient addition treatments(Table 2), where the growth media were treated withdistilled water (control) or by either solutions orsuspensions of one of five nutrients: KCl, CaCO3,NaHPO4, CaCl2 and urea (NH2CONH2). After 24 himbibition, the growth media were placed in thenylon ingrowth bags. In each 25 m · 25 m quadrantof the main field study plots (50 m · 50 m), one bagwas randomly placed, making it four replicate soilbags of each nutrient treatment per plot. The bagswere left undisturbed for 117 d (all in the rainyseason) from 2 January to 19 May 1993. Then, all thebags were removed, any outside roots shaved, and theroots inside the bags (all <2-mm diameter) separatedby sieving and flotation. The roots were dried(1058C) and weighed.Experiment 2: the effect of nutrient addition on nativetree seedlingsIn each forest type, two 8 m · 5 m plots weredelimited, either in small natural gaps (THF andLERF) or in open areas alongside the ‘islands’ ofTable 1 Nutrient and acidity analyses of soil from the upper layers from the SHF, THF and LERF. Values are means of three pits(Source: Luiza˜o 1996, modified)Depth*(cm)pHH2O N(mg gÀ1)C:N Ptotal(mg gÀ1)K+(m-eqiv100 gÀ1)Na+(m-eqiv100 gÀ1)Ca2+(m-eqiv100 gÀ1)Mg2+(m-eqiv100 gÀ1)CEC(m-eqiv100 gÀ1)H+/Al3+(m-eqiv100 gÀ1)SHF 0–5 3.7 0.28 25.4 165 0.15 0.03 0.08 0.26 1.84 >67.05–10 4.3 0.20 2.0 48 0.03 0.0 0.15 0.04 0.66 >24.020–30 4.9 0.30 0.5 17 0.0 0.0 0.08 0.01 0.28 7.50THF 0–9 3.5 1.24 24.3 623 0.36 0.45 0.02 0.38 7.06 25.89–20 4.2 0.05 18.8 26 0.06 0.0 0.14 0.04 1.08 8.7020–30 4.2 0.02 61.0 19 0.03 0.0 0.18 0.03 1.05 9.10LERF 0–6 3.9 1.08 21.0 419 0.05 0.05 0.02 0.06 7.82 0.217–20 4.1 0.70 18.6 305 0.02 0.01 0.34 0.06 19.4 0.4020–30 4.3 0.30 37.0 214 0.02 0.0 0.36 0.05 19.3 0.10* The layer thickness varied according to the distribution of organic and mineral layers. The first of the three above layers waspredominantly organic (H); the second, mixed organic/mineral, and the third, an intrinsically mineral layer. Note that in SHF anyvestige of organic mixing in soil profile had disappeared after 10 cm in depthPlant Ecol (2007) 192:209–224 211123
  • 4. vegetation (SHF). Only two replicate plots were usedbecause of the shortage of suitable natural gaps in theTHF and LERF. Fourteen 1 m · 1 m quadrats in eachplot were selected for experimental treatments onseedlings already existing and measuring up to 30 cmin height (thus, a wide variety of seedling species, andlikely of ages as well, was included in the experiment).Seven nutrient addition treatments were applied (Table2): (1) NH2CONH2, (2) Na2PO4, (3) KCl, (4) CaCl2,(5) CaCO3, (6) a combination of 1, 2, 3 and 5, and acontrol (no added nutrients). Two replicates of each ofthe seven treatments were applied in each plot.Treatments were randomly located in each plot.Rates of fertilisation (Table 2) were similar to thosegenerally recommended by forestry nurseries inBrazil (Reis 1989), and fell within the lower part ofranges commonly used for mature trees elsewhere(Tanner et al. 1990). The nutrients were added to thesoil on 1 March 1993, during the rainy season toensure that native seedlings did not dry out in themonths following treatment. Seedlings were assessedat the beginning of the experiment and after 180 d,and survival rate (final/initial numbers) and growthquotient (final/initial height) determined.The same 8 m · 5 m plots were used for soilrespiration measurements in response to nutrientadditions. Three composite samples (made up of fivesub-samples taken at random within the 1 m · 1 mquadrats) were collected from the upper soil layer (0–20 cm) from each treatment. In the SHF, the 0–20 cmlayer was generally mineral, slightly mixed withsome organic matter in the top 1–2 cm; in the THFand the LERF, it generally included a humic layerand a mixed organo-mineral layer, as well as a rootmat. Samples were cleaned of roots and litter, and thefresh soil transferred into glass bottles. Bottles wereincubated in the dark for 10 d at 248C, and theevolved carbon dioxide measured by using thefumigation–incubation method of Jenkinson andPowlson (1976). Sampling and measurements wererepeated after 60 d and 180 d from the beginning ofthe experiment.Laboratory experimentsExperiment 3: effect of nutrient addition on C and Nmineralisation and net nitrificationTo test the effects of soil nutrient limitation on soilrespiration and N transformations nutrient additionswere made to soil under laboratory conditions. Soilmineral samples were taken from the top 10 cm ineach of the three 50 m · 50 m plots of the three foresttypes, bulked per forest type and carefully mixed. A50-g sub-sample of each bulked sample was ran-domly allocated to one of 12 treatments (Table 2).The flasks were incubated in the dark at 248Cfor 10 d, and the evolved CO2 was measured bytitration according to the fumigation-incubationmethod of Jenkinson and Powlson (1976). Forcalculations of the N transformation N was extractedfrom 5-g sub-samples, at the start of the incubationTable 2 Nutrient addition treatments (all expressed on a kg haÀ1basis) applied to soils (and root ingrowth media in Experiment 1)in the four experiments made in the field and in the laboratoryTreatment Experiment 1 (field)Root ingrowth bagsExperiments 2 and 3 (field, nativeseedlings; and lab, rice)Experiment 4 (lab) Soil C and Nmineralisation1 N as 150 kg of NH2CONH2 N as 150 kg of NH2CONH2 N as 150 kg of NH2CONH22 P as 50 kg of NaH2PO4 P as 50 kg of NaH2PO4 P as 50 kg of NaH2PO43 K as 60 kg of KCl K as 60 kg of KCl K as 60 kg of KCl4 Ca as 2 000 kg of CaCl2 Ca as 2 000 kg of CaCl2 Ca as 2 000 kg of CaCO35 Ca as 2 000 kg of CaCO3 Ca as 2 000 kg of CaCO3 Ca as 2 000 kg of CaSO46 No added nutrients (control) NPKCa—combination of 1, 2, 3 and 5 S as 500 kg of Na2SO47 – No added nutrients (control) NP (combination of 1 + 2)8 – – NK (combination of 1 + 3)9 – – NCa (combination of 1 + 4)10 – – NCa (combination of 1 + 5)11 – – NS (combination of 1 + 6 above)12 – – No added nutrients (control)212 Plant Ecol (2007) 192:209–224123
  • 5. (initial mineral N), and after 10 d (incubated mineralN) with 50-ml 2 M KCl. Concentrations of theammonium ion were determined colorimetrically byflow injection, using a modified indophenol bluemethod and the concentrations of nitrate ions weredetermined by a similar technique using a modifiedcadmium reduction method (Gine et al. 1980). Netmineralisation and net nitrification were calculatedfollowing Keeney (1982) and included the subtrac-tion of the amount of nitrogen added in the Ntreatments.Experiment 4: glasshouse bioassay experimentHumus (decomposing litter and raw humus material)and the upper mineral soil layer were collectedseparately from SHF, THF and LERF, air-dried andsieved through a 2-mm mesh. Eight 7-cm diameter(200-ml volume) pots were prepared for each ofseven treatments, and for each forest type and soildepth. The seven treatments (Table 2) were the sameas those applied in the field (Experiment 2) and thepots were watered with 20 ml freshly made nutrientsolutions or suspensions (Table 2). The pots wererandomly located on wooden benches inside aglasshouse. Except for CaCl2, the rates of nutrientadditions were at the lower end of the recommendedrange for cultivating acidic soils in Brazil (Anghinoniand Volkeweiss 1984). Directly after applying thenutrients, 10 seeds of dryland rice (Brazilian varietyIAC-47) were placed in the top 1-cm of soil. The potswere kept moist and 10 d after planting germinationwas assessed; 40 d later rice plants were assessed andharvested. Shoot and root biomass, and plant survivaland mortality were determined.Dryland rice was chosen as the test plant after anattempt to grow a native tree species in fieldconditions was unsuccessful due to heavy seedlingpredation, despite showing high rates of germinationin all three forest types (Luiza˜o 1996). Dryland riceas a test plant is usually disease free, has a low soilnutrient demand, and its seeds are readily available.Despite that the Iban word kerangas (for heath forestsin Indonesia) means a site/soil where rice cannotgrow (Whitmore 1984), the authors considered its useappropriate, since eventual positive responses in SHFand THF soils could be attributed to the soilamendments provided by nutrient additions.Statistical analysesIn the field assays, nested analyses of variance (treat-ments nested in plots) using GLM (General LinearModel) were performed. In the laboratory incubations,two-way analyses of variance were performed withnutrient treatment and forest type as fixed factors. Toassess the effects of the nutrient additions in relationtothecontrol,one-way analysesofvariancefollowedbythe Dunnett’s test were used to compare treatments tocontrol within each forest type. Data were transformed(using square-root, logarithmic or arcsine transforma-tions) to assure homogeneity of variance (Zar 1984).ResultsField experimentsExperiment 1: root ingrowth bags at field plotsThere was a large variability in the results obtainedfrom ingrowth bags. Significantly fewer roots werefound in the ingrowth bags in the SHF (nestedANOVA, d.f. = 12; P < 0.001) than in the THF andLERF. Fine root mass was significantly lower in thebags filled with sand compared with those withvermiculite (P < 0.001; Fig. 1). Within the vermiculitebags, those buried within the soil showed a higherproduction of fine roots compared with those placed onthe litter layer surface. In the SHF, the vermiculitebags placed on the soil surface showed a significantlyhigher production of fine roots than both the vermic-ulite bags buried within the soil and the sand bags onthe soil surface (P < 0.001). Although variability washigh, CaCO3, CaCl2 and KCl increased fine rootgrowth in the THF (P < 0.05). In the LERF, CaCl2 andCaCO3 were the only treatments which significantlyincreased (both P < 0.001) fine root growth invermiculite-filled bags and at both depths.Experiment 2: Effect of nutrient addition on thegrowth of native tree seedlingsIn the SHF plots, nutrient additions did not signifi-cantly increase seedling survival compared to con-trols (Fig. 2) and CaCl2 addition (nested ANOVA,d.f. = 21; F = 6.52; P < 0.001) killed all the seedlings.Plant Ecol (2007) 192:209–224 213123
  • 6. In the THF seedling survival was also significantlyreduced by CaCl2 (F = 4.0; P < 0.01), but increasedby NPK+CaCO3. In the LERF plots, none of thenutrient additions influenced the survival rate of theseedlings. The quotient of final/initial height wassignificantly increased in SHF by NPK+CaCO3(+27%). Nitrogen addition alone caused a meanincrease of 22% in seedling growth in relation to thecontrol, but the difference was not statisticallysignificant. In the THF, the final height of theseedlings was generally lower than the initial height(except after addition of NPK+CaCO3), but onlysignificantly so with CaCl2. In LERF no significantdifferences in height were found between treatments.No significant differences were found amongsttreatments for soil respiration (Table 3), with theexception of the 60-d sampling time in SHF, whererespiration was significantly higher with the additionof NPK+CaCO3 (nested ANOVA, d.f. = 21;P < 0.05). In the same soil, there was a concomitantincrease (P < 0.001) in soil pH under the sametreatment.SHF012345KCl CaCO3 CaCl2 Urea NaH2PO4 ControlRotomass(gabg1-)vermiculite, on surfacevermiculite, 10 cm deepsand, on surfaceTHF0246810KCl CaCO3 CaCl2Urea NaH2PO4ControlRootmass(gbag1-)LERF0246810KCl CaCO3CaCl2Urea NaH2PO4ControlTreatmentstooRsams(ggab1-)* ***** ********* *******Fig. 1 Ingrowth bag experiment: dry mass of roots per bagafter 117 d in the bags containing vermiculite on the soilsurface, vermiculite at 10 cm depth in the soil and sand on thesoil surface, under different nutrient addition treatments. Barsare means ± SE of four bags in each experiment and treatmentin each of the three replicate plots in the SHF, THF and LERF.Significance levels for nested ANOVA with Dunnet’s test forcomparisons with the control are: *, 0.05; **, 0.01; ***, 0.0010.00.40.81.21.62.0NPKaCl2CaCO3CPNKI+CaCO3CtnorolGrowthnidex(fina/lnitiiahleightSHF THF LERF0.00.20.40.60.81.01.21.4NPKaCl2CaCO3CKPNI+CaCO3CtnorolTreatmentsuSvrivlaaretSHF THF LERF************Fig. 2 Field experiment: survival rate (quotient of final/initialnumber of living native seedlings), and the growth (quotient offinal/initial height of the native seedlings) 180 d after nutrientaddition in the SHF, THF and LERF. Values are means withSE (n values are variable and indicated above the bars). Thesurvival rate varies from 0 (no survival of seedlings) to 1 (allsurvived). Growth quotients <1 indicate negative growth on theaverage of the plots: quotients >1 indicate actual growth ofseedlings. Significant differences in relation to the control(from nested ANOVA followed by Dunnet’s test) are indicatedby asterisks: *,0.05; **, 0.01; ***, 0.001214 Plant Ecol (2007) 192:209–224123
  • 7. Laboratory experimentsExperiment 3: effect of nutrient addition on C and NmineralisationSoil respiration. Soil respiration measurements variedwidely amongst soil types and treatments. Greaterincreases in respiration after nutrient additions inrelation to the control were visible in SHF (Fig. 3),but the differences were only significant in thetreatments N+P and N+Na2SO4 (one-way ANOVA,P < 0.05). In the THF soils, respiration was signif-icantly higher than the control in the treatments S andN+S (P < 0.001). In the LERF soils, respiration wassignificantly higher than the control in the treatmentsS and N+K (P < 0.001) (Fig. 3).Net nitrogen mineralisation and net nitrification.The addition of N alone, or in all combinations (N +Na2SO4; N+K; N+CaCO3; N+CaSO4; N+P) inducednet N immobilisation (P < 0.001) in SHF and THFsoils (Fig. 4). In the LERF soils, six out of the 12treatments caused significant net immobilisation ofN: the addition of N alone; N+P; N+K; N+CaCO3;N+CaSO4; N+Na2SO4 (P < 0.001), whereas twotreatments caused net mineralisation: CaSO4 andCaCO3 (all P < 0.001) (Fig. 4).Net nitrification rates were not affected by any ofthe treatments in SHF soils (Fig 5). In the THFsoils, only N+P increased significantly net nitrifica-tion (P < 0.001). In the LERF, the rates of netnitrification were significantly different from thecontrol in seven out of the 12 treatments: anincrease with N, P and CaCO3; and a decrease withKCl, Na2SO4, N+CaSO4 and N+Na2SO4 (allP < 0.001) (Fig. 5).Experiment 4: glasshouse bioassay experimentSoil type and nutrient addition treatment generally hada significant influence on the germination, survival andgrowth of the dryland rice (Fig. 6). There was anextreme stunting and early death of seedlings in SHFand THF soils that had not received CaCO3. Asignificantly higher shoot biomass of rice was foundwith CaCO3 alone and with NPK+CaCO3 (F = 16.1;P < 0.001) in SHF soils. In THF soils, only the additionof CaCO3 (F = 7.66; P < 0.001) and in the LERF, onlythe addition of NPK+CaCO3 increased shoot biomasssignificantly. Root biomass was also significantlyhigher after the addition of both CaCO3 and NPK+Ca-CO3 (F = 9.23; P < 0.001) in SHF soil; after addition ofCaCO3 in THF soil (F = 5.91; P < 0.001); and nosignificant effects of nutrient addition were found inthe LERF soils. The addition of CaCl2 inhibitedgermination and killed most seedlings even in theLERF soils (Fig. 6), although the few seedlings whichdid survive in the SHF and THF soil grew well. Theaddition of CaCl2 significantly increased seedlingmortality in all three soil types (F = 14.4, SHF;F = 10.3, THF; F = 24.3, LERF; P < 0.001). In THFsoils, addition of NH2CONH2 also significantlyincreased mortality (F = 10.3; P < 0.001).Table 3 Soil respiration (mg C gÀ1oven-dry soil) 60 d and 180 d after nutrient addition to field plots with already existing seedlingsin SHF, THF and LERFTreatment Forest typesSHF THF LERF60 d 180 d 60 d 180 d 60 d 180 dN 56.0 ± 25.6 20.0 ± 2.20 91.4 ± 32.6 101 ± 22.4 52.1 ± 15.6 111 ± 3.70P 20.1 ± 4.08 na 83.7 ± 12.2 na 57.3 ± 20.3 naK 68.9 ± 17.0 na 60.9 ± 15.2 na 52.1 ± 11.3 naNPK + CaCO3 104 ± 15.7*66.6 ± 14.5 93.3 ± 21.6 110 ± 12.7 86.5 ± 8.45 103 ± 13.2CaCl2 70.1 ± 20.6 na 91.1 ± 23.6 na 69.5 ± 17.3 naCaCO3 41.9 ± 5.18 100 ± 3.43 105.5 ± 25.3 128 ± 20.6 92.3 ± 22.8 135 ± 41.6Control 30.5 ± 6.12 57.1 ± 20.8 48.5 ± 11.3 128 ± 13.4 66.5 ± 6.12 90.4 ± 21.8Values are treatment means ± SE at each time in each forest type of two replicate sub-plots within each of two plots (n = 4).na = not analysed; *significant difference among treatments (P < 0.05)Plant Ecol (2007) 192:209–224 215123
  • 8. DiscussionThe pH in the three forest types was amongst thelowest recorded for rain forests on acidic soils, butthe concentrations of nutrients (except for Na in SHF,and Ca in all three forest types) in the surface soilsSHF020406080100120 ***************** ******tCrlN+NP+NK+NaCCO3+NaCSO4+NSO4PKaCCO3aCSO4Na2SO4Na2SO4Na2SO4Solirespriat(noiµgCg1-)THF0306090120tCrlN+NP+NK+NCaCO3+NSaCO4+NSO4PKO3CaCSaCO4Solirespirtaoi(nµgCg1-)LERF0306090120tCrlN+NP+NK+NaCCO3+NaCSO4+NSO4PKaCCO3aCSO4TreatmentsSoilrespiration(µCg-g)1Fig. 3 Laboratory experiment: soil respiration (mg C gÀ1oven-dry soil 10 dÀ1) under different nutrient additiontreatments (explained in the text) in SHF, THF and LERFsoils. Values are means ± SD (n = 3). Significance levels forANOVA within each forest type with Dunnet’s test forcomparisons with the control are: *, 0.05; **, 0.01; ***, 0.001SHF-120-100-80-60-40-200204060CtrlNN+PN+KN+CaCO3N+CaSO4N+SO4PKCaCO3CaSO4Na2SO4Na2SO4Na2SO4Nmineralization(µNg-1)Nmineralization(µgNg-1)Nmineralization(µgNg-1)******************THF-120-100-80-60-40-200204060CtrlNN+PN+KN+CaCO3N+CaSO4N+SO4PKCaCO3CaSO4*********************LERF-120-100-80-60-40-200204060CtrlNN+PN+KN+CaCO3N+CaSO4N+SO4PKCaCO3CaSO4************************Fig. 4 Laboratory experiment: net nitrogen mineralisation(mg N gÀ1oven-dry soil 10 dÀ1) under different nutrientaddition treatments in the SHF, THF and LERF soils. Valuesare means ± SE (n = 9). Significance levels for ANOVA withDunnet’s test for comparisons with the control are: *, 0.05;**, 0.01; ***, 0.001216 Plant Ecol (2007) 192:209–224123
  • 9. are not exceptionally low (Luiza˜o 1996). The moststriking difference observed between the heath forestand the LERF soils was the dominance of H+(insteadof Al3+) in the exchange complex, especially in theSHF, where Al3+concentrations were negligible andthe H+/Al3+quotient was much higher (more than 300times in upper soil layer) than in the LERF soils(Luiza˜o 1996; Proctor 1999; Table 1). However, thebiomass estimated for the LERF (409 Mg haÀ1),slightly higher than the range reported for forests onOxisols in Amazonia (Jordan 1985) suggests that-7-5-3-1135 SHFtCrlN+NP+NK+NCO3aC+NSaCO4+NSO4PKCaCO3SaCO4Na2SO4Na2SO4Na2SO4Nettinrficiatnoi(µgN1-)-3036912 THFtCrlN+NP+NK+NCaCO3+NCaSO4+NSO4PKaCCO3aCSO4Netintrifictaion(µNgg1-)-505101520 LERFtCrlN+NP+NK+NCaCO3+NCaSO4+NSO4PKCO3aCSO4aCTreatmentseNtnitrficitanoi(µNgg1-)************************Fig. 5 Laboratory experiment: net nitrification (mg N gÀ1oven-dry soil 10 dÀ1) under different nutrient additiontreatments in the SHF, THF and LERF soils. Values aremeans ± SE (n = 9). Significance levels for ANOVA withDunnet’s test for comparisons with the control are: *, 0.05;**, 0.01; ***, 0.0010246***************************************810Mortatilyu-NreaCKlaCCl2aCCO3PNK+aCO3CConrtolConrtolConrtolSHF THF LERF020406080100120N-ruaeNaH2PO4NaH2PO4CKlaCl2CaCO3CPNK+aCO3CSoohtibmo(ssagm2-)020406080100N-ruaeaNH2O4PCKlaCl2CaCO3CPNK+aCO3CTreatmentsRomoibto(ssagm2-)Fig. 6 Glasshouse experiment: number of dead rice seedlings,and shoot and root dry mass (g mÀ2) in each treatment after50 d, using soils from the SHF, THF and LERF. Values aremeans and SE (n = 8), and significant differences in relation tothe control (from one-way ANOVA followed by Dunnet’s test)are indicated by asterisks: *, 0.05; **, 0.01; ***, 0.001Plant Ecol (2007) 192:209–224 217123
  • 10. there are no limitations for tree growth in that foresttype.Two nutrient combinations caused a significantincrease in the SHF soil respiration: urea withNa2PO3, and urea with Na2SO4 suggesting that N islimiting microbial activities in the SHF. In turn, P andS seemed to be important when enough N wassupplied. In THF soils, S, especially when combinedwith N, seemed to be the nutrient which mostlystimulated the activity of the microorganismswhereas in LERF soils, additions of S, and thecombination N+K, stimulated soil respiration. En-hanced microbial activity could be caused either by Sor by the added Ca or Na (Persson et al. 1989).However, the latter is unlikely to be the case since Nais at most a micronutrient whilst Ca did not produceso positive a response when added as CaCO3. Thus,the increase in microbial activity might be caused byadditions of S, which was somehow unexpected,since over 95% of the forest topsoil S is organicallybound (David et al. 1982). These results indicate thatunder certain conditions (e.g. adequate supply ofother nutrients) S may limit microbial decomposition.Another possible explanation could be a potentialliming effect of S in the soil, but unfortunately therewas no separate S treatment in the experiments toconfirm the results.High soil acidity has often been considered to be astrong microbial inhibitor. When acidity is reducedby liming a more diverse decomposer communitymay establish, allowing a more efficient substrateutilisation (Insam 1990). Contrary to that expectation,though CaCO3 addition increased soil pH in the SHF,its initial positive effect on soil respiration at the 60-dsampling was not apparent at 180 d. In THF andLERF soil respiration was not significantly influencedby CaCO3, a similar result to that found by Perssonet al. (1990) in coniferous forest in Scandinavia.They found no significant difference in soil respira-tion between the controls and mineral soils whichreceived CaCO3, and that may indicate that notenough liming material was applied to increase soilpH in those forest types.Low concentrations of N found in heath forestleaves (Coomes and Grubb 1996) and litterfall(Luiza˜o 1996; Proctor 1999) have been used tosuggest that N may be unusually low in heath forests,thus limiting plant growth (Coomes and Grubb 1996).However, low N availability of soils may occurbecause of immobilisation by microorganisms (Pers-son et al. 1990). In the present study, in the soils of allforest types, all treatments including N additionsresulted in a high net N immobilisation, which is aconsequence of increased activity of the soilmicrobes (Persson et al. 1990). Since in the SHFsoils a significant pH increase was not followed byenhanced net N mineralisation, it seems that low pHis not the only factor influencing the N transforma-tions. The addition of CaCO3 alone was effective inenhancing net N mineralisation only in the LERFsoils. The general lack of an increase in net Nmineralisation in both the SHF and THF soils whenonly CaCO3 was applied may be explained by anincrease in bacterial relative to fungal decomposition,since there are strong indications that liming of forestsoils stimulates bacterial activity more than that offungi (Griffin 1985). In the present study N wasadded as urea, and no significant changes in soil pHwere observed in the urea treatments, despite itspotential acidifying effect, as pointed out in exper-iments made in eastern Amazonia in soils with asimilar texture and chemistry (Ludwig et al. 2001).As an intermediate in microbial metabolism, ureaapplied to the soil is very readily hydrolysed, andmuch of it is transformed to ammonium ions andimmobilised in a few days.Net nitrate production can only increase whenthere is ammonium available for nitrifying microor-ganisms. Therefore, the extent to which nitrateproduction and leaching may increase depends onwhether liming stimulates mineralisation or immo-bilisation of ammonium. An experiment using soilsolution concentration of nitrate in soil profile toestimate nitrate leaching in Scandinavian forest soilsshowed that leaching of NO3-N occurred in higherconcentrations below pH 4.5 as a direct effect of thepH more than any other factors (Falkengren-Grerupet al. 2006). In the present study, as the pH was notelevated substantially in the SHF soils, nitrateleaching may have occurred in the field assays, butnot in the 10-d incubation experiment in laboratory.In this case, since N mineralisation was inhibited bymany of the added nutrients, no ammonium was leftfor the nitrification process. In both SHF and THFsoils, net nitrification was inhibited (although notsignificantly) by nearly all nutrients applied. Even theaddition of urea did not increase nitrification. Studieshave suggested that labile inhibitors of nitrification218 Plant Ecol (2007) 192:209–224123
  • 11. may be responsible for delays in nitrate production(Vitousek and Matson 1985) or for its completeinhibition (White 1988).The Ca status of the SHF, THF and LERF soilswas very low and the overall positive response of fineroot growth (in all bag positions, media and foresttypes) to both CaCO3 and CaCl2 addition, suggeststhat fine root growth is restricted by both soil pH andlow Ca. However, the positive effect of both Catreatments on the root mass in the heath forest soilsmay have another explanation. First, increased fineroot production does not necessarily imply increasedplant growth (E.V.J. Tanner, pers. comm. 2002).Plants might respond to fertilisation by first increas-ing root production, and only much later showing anyincrease in above-ground biomass (Silver 1994).Also, the general increase in root growth in the bagsfilled with vermiculite, especially in those buried inthe soil, suggest that the alkaline vermiculite used inBrazil (pH = 8.8) had a positive effect on fine rootgrowth. The vermiculite used in the present work wasacquired from the only supplier in Brazil and with itshigh pH value and an unquantified amount of cationsin its composition, certainly represented a confound-ing factor for evaluating the effects of the nutrientadditions. However, it must be pointed out that thetwo cations generally present in higher concentrationsin vermiculite (Mg2+and Fe2+) were not evaluated inthe present work. Also, there was a control for theexperiment using vermiculite bags with no nutrientaddition, and further, the effect of nutrient additionson vermiculite bags placed on soil surface were notstrikingly different from the ones with sand.The results of the present study contrast with that ofCuevas and Medina (1988), who worked in differenttypes of rain forest (tierra firme, tall caatinga and lowbana) at San Carlos, Venezuela. They found fine rootgrowth stimulated by the addition of N in tall caatingaand low bana forests only on top of the root mat andby P in tierra firme and bana forests and by Ca only inthe tierra firme forest (&LERF). Proctor (1995)pointed out that owing to the very poor root growthin the unfertilised treatments of Cuevas and Medina(1988) their study did not allow them to reach firmconclusions on the limiting nutrients in the tierra firmeand bana forests. Their data lend no support to theview that N, P or K, are limiting for plant growth inlowland evergreen rain forests, which confirms theresults of the present study.The lack of response of fine roots to N, P and Kaddition observed here is not surprising, and corrob-orates the results of several recent ingrowth bagstudies carried out in tropical and temperate soils.Studies carried out in Borneo at Barito Ulu, CentralKalimantan, Indonesia (J. Proctor, unpublished),found no response in a heath forest to P (but therewas a significantly increased fine root growth inLERF in the presence of P). It seems that soil aciditynot only controls nutrient effects on plant growth butit is also important for maintaining differences inspecies composition such as was observed by Roemet al. (2002) in heath land on nutrient-poor sandy soilin the Netherlands. They showed that the influence ofnutrient availability on species composition in heath-land was less important than soil acidity. To whatextent that control by acidity is effective is notprecisely known as in harsh environments, such asthe heath forests, some native species are able to dealwith nutrient limitations (stress tolerators), but mayrapidly respond in an opportunistic way when thelimitation is removed, assuming a behaviour properlycalled as ‘latent competitors’ (Nagy and Proctor1997). Such a strategy by certain heath forest specieswould help explain the surprising results found byMiyamoto et al. (2007) in a Bornean heath forest insouthern Central Kalimantan (basal area of21.8 m2haÀ1) on bleached white sand, under anannual rainfall regime of 3,200 mm. They recorded aquick recovery in wood biomass after a strongdrought, caused by the El Nin˜o phenomenon. Usingpulses of nutrients (in this case, possibly released bydead wood and the extra litterfall produced by thedrought) the heath forest apparently became a moreproductive system in the following years, allowing anincrease in primary productivity in response toincreased nutrient availability. The increase in nutri-ent availability in this case may be paralleled by anincrease in soil pH caused by the release of Ca andMg from the dead wood as illustrated in former worksinvolving clearings produced by selective logging inBrazilian Amazon. They showed that together withsome short term release of N and P from extra finelitterfall, a considerable increase in Ca and Mgavailability in upper soil layer was observed after1.5 years in response to the decomposition of deadwood accumulated in patches of the clearingsproduced by selective logging (Yano 2001; Pauletto2006). These two basic cations, Ca and Mg, as well asPlant Ecol (2007) 192:209–224 219123
  • 12. Mn, are present in higher concentrations in the coarselitter fraction 2–10 cm in diameter (Pauletto 2006)which may be decomposed within a couple of years,resulting in a slight but important increase in soil pH,causing a positive response in seedling and treegrowth.In the present study, native seedlings in the fieldexperiment showed either no or a negative responseto N, P and K addition, as well as a high mortalitywhen CaCl2 was applied. The results in SHF and THFwere very similar to those of other studies carried outin temperate forests on acidic sandy soils in Sweden(Brunet and Neymark 1992; Falkengren-Krerup andTyler 1992, 1993; Staaf 1992) or elsewhere (Proctor1999; Roem et al. 2002). They all found that anyaddition of mineral nutrients was unsuccessful inpromoting plant survival or growth, unless thetreatment involved an increase in soil pH.In the present study, overall, there were nobeneficial effects of the nutrient addition in the SHFand THF, if not accompanied by an increase in soilpH (by the addition of CaCO3), and a very limitedeffect in the LERF. Thus, there was no directevidence of nutrient limitation for seedling growthin the SHF and THF, and other factors must beinvolved. The high toxicity induced by soil aciditywas likely to be the main cause for the death or poorgrowth of seedlings in the nutrient addition treat-ments.In soils well supplied with Al, pH is controlled bya complex hydrated Al-ion buffer system which sets alower limit to pH, preventing extreme acidity (withvalues much below 4.0) and high H+concentrations(Rowell 1988; Fitter and Hay 1991). For soils ofsimilar pH there are large differences betweenmineral and organic soils. In mineral soils exchange-able Al limits exchangeable acidity, whilst in organicsoils the pH is maintained by the buffering ability ofthe organically complexed Al. Along a transitionfrom mineral to organic soils the decrease inexchangeable Al with increasing organic matter, isparalleled by an increase in the exchangeable acidity.The removal of the Al complexes by the addition ofbases (especially CaCl2, which was used in muchlarger concentrations than the other major nutrients inthe present study) may have caused a decrease in thesoil pH, increasing the H+toxicity. It must beremembered that the amelioration of H+toxicity byAl3+ions has been shown experimentally (Kinraide1993), and that in acidic soils Al3+ions may preventH+from becoming an intrinsic toxin (Kinraide 2003).Thus, Al3+ions decrease solute leakage at low pH,producing a growth enhancement (Foy 1984; Rowell1988). In studies of Haplic Podzols in a borealconiferous forest in Sweden, Skyllberg (1991, 1999)found that the humus layer (O horizon) had a pHpositively correlated with Al. In line with otherabove-mentioned authors (e.g. Proctor 1999; Kinra-ide 1993; 2003) Skyllberg suggested that in acidhumus layers and organic horizons with a pH below4.0, Al cations act as any ‘base cation’ through an H+-displacement at cation exchange sites. Thus, insteadof acidifying effects, Al ions in soil (at adequateconcentrations) would be beneficial, buffering the pHat levels not toxic to plants, and the lack ofdisplacement of such ions cause strong toxicity forplant roots. In Scotland, addition of low concentra-tions of Al (2–5 mg lÀ1) to soils poor in Al ionsenhanced the growth of two races of Betula pendulaRoth originating from Al-poor soils (Kidd andProctor 2000). In Scandinavia, a pot experimentusing acid soil and raising its pH from 3.3 bycarbonate additions showed that the growth ofBromus benekenii (Lange) Trimen. and nine otherspecies (out of a total of 17) was limited at pH <4.1and the toxicity of H-ions to Bromus was confirmedat pH 4.2 or lower (Falkengren-Grerup et al. 1995). Inthe present study, the very low concentration of Al inthe heath forest soils, especially in the SHF, wherethe mor humus is often lacking, may be a majorreason for the poor control of H+toxicity.The results of the glasshouse experiment using riceseedlings overall confirmed those found in the fieldstudy on native tree seedlings: the only generalpositive effect on growth was caused by the additionof CaCO3, whilst the addition of CaCl2 had a generaldeleterious effect on seedlings, inducing high mor-tality rates. The general coincidence of the resultsobserved in the glasshouse (using a cultivated crop)with the field experiment (using several nativespecies) was reassuring.The apparent contradiction of the strongly nega-tive results for seedling growth in relation to thepositive responses of fine root growth to the additionof CaCl2 (in the ingrowth bags) may have twoexplanations. These results may indicate that most ofthe roots penetrating the bags and responding posi-tively to the CaCl2 additions originated from mature220 Plant Ecol (2007) 192:209–224123
  • 13. plants (not seedlings), which might respond differ-ently to nutrient addition. Most likely, though, thefine roots were not adversely affected because therewas enough time for part of the CaCl2 (mainly thechloride fraction) to be leached from the bags byrainwater. In fact, 1,440 mm of rain fell during theexperiment, and January, the first month of theexperiment, had a rainfall mean of 108 mm per week.After such selective leaching, the residual Ca mayhave been beneficial for fine root growth.The positive responses of fine root growth and thesoil respiration to additions of Ca to the soil seem tobe further pieces of evidence of limitations by thiselement in the heath forest soils, after the apparentlimiting effect of Ca and Mn for soil and litterorganisms (Luiza˜o 1994; 1996). However, that doesnot imply that these elements are also limiting forplant growth as a whole, since other factors may beinvolved (Attiwill and Adams 1993). For instance,Grubb (1989) suggested that in nutrient-poor soils, animportant interaction between shade and nutrients(especially for P) occurs, and that was partlyconfirmed in later bioassays in lowland dipterocarprain forests in Singapore. Highly positive responsesof two shrubby species were found when P was added(Burslem et al. 1994), but seedlings of four shade-tolerant species showed either no response or anegative response to P additions (Burslem et al.1995). They suggested P and major cations aslimiting factors in nutrient-poor soils (Burslemet al. 1994), and those shade-tolerant tree seedlingswhich have mycorrhizas are not limited by P supplybecause of the mycorrhizas or because they have alow demand for nutrients when growing in the shade(Burslem et al. 1995). The latter suggestion was alsomade by Denslow et al. (1987), who found positiveresponses of seedling growth with complete nutrientfertilisation on nutrient-richer soils, but no responsesof shrubby species to P additions. In fact, theassessment of the actual nutrient requirements oftrees would be necessary for nutrient addition exper-iments, but these requirements are virtually impossi-ble to ascertain.The results found in the present study for theseedling survival and growth agree notably withanother study on Central Kalimantan heath forestsoils, also growing dryland rice in a pot experiment.No seedling root growth was found in any treatmentin the heath forest organic soil, except when CaCO3was added (Proctor 1999). It was speculated that poorgrowth of rice on heath forest soils was due to toxinsin the soil and not due to a low soil nutrient status.The negative effects of the humus layer includedin part of the pots in the present study may also be theresult of phenolic compounds (leached by thefrequent watering of the pots), affecting seedlingroots, especially in the heath forest soils. In Sarawak,Bru¨nig (1968, 1974) reported that heath forest soilshave high concentrations of secondary metabolites,which may have two effects: production of toxiceffects on the vegetation, and reduction of availableN in the soil. Whitmore (1990) indicated that phenolsare abundant in heath forest leaves and litter, andthese may be toxic or inhibit uptake when they leachinto the soil. Soil phenolics directly affect germina-tion and especially the growth of higher plants, andconcentrations of soluble phenolics are correlatedwith organic matter content, and highest in thesuperficial L and F organic layers (Kuiters 1990). Inthe organic layers of the THF soils, evidence wasfound of phenolic leachates, in the form of green-brownish bubbles (Luiza˜o 1994), certainly releasedby the decomposition of either the litter on the soilsurface or the fine roots, the main originators ofphenolics in soil (Kuiters 1990).However, in the field experiment, using pre-exist-ing natural seedlings, and where controls showed nostrong mortality, the putative toxicity of phenoliccompounds would have interacted with the addednutrients, making it still more difficult to explain themechanisms involved. The phenolic substances areclosely related to pH and soil nutrient status, andalthough phenolics are generally not high enough to bestrongly acidic, they are more physiologically activewith H+to produce the high mortality of seedlings inthe SHF and THF when the pH buffer was probablyswamped by the large additions of CaCl2.ConclusionsItispossiblethatthesoilsintheSHFarenutrientlimited,considering that they have virtually no top organic layer(wheremostofthe nutrientsare found inTHFsoils), andthata betterresponse,thoughnotalwayssignificant,wasobserved for SHF soils than for THF soils whennutrients were added. Seedling mortality was less inthe SHF than in THF when N, P or NPK + CaCO3 werePlant Ecol (2007) 192:209–224 221123
  • 14. added, whilst the shoot and root mass were higher inSHF than in THF soils when NPK + CaCO3 were added.There was little evidence of N or P limitation, asgenerally suggested for acidic tropical soils, as the chiefcause of poor plant growth in SHF and THF. It ispossible to speculate that there was some evidence oftoxic effects of soil pH and secondary compounds, asillustrated by the slight negative responses to theinclusion of humus layer in the pots with heath forestsoils, and by the largely positive response to the additionof CaCO3 to the soils. However, the question of limitingfactors for plant growth in heath forest soils is still anunresolved one, and, thus, the view of Whitmore (1984)that heath forests occur on sites which have a number ofunfavourable characteristics, acting together or sepa-rately,issubstantiated.Evennotbeingfrequent,droughtmay occur; the extremely acid soils, with pH <4 atsurface would be toxic to many plants; the soil has lowamounts of Al and Fe sesquioxides, and consequently alow ability to absorb H+; phenols occur at high levels inleaves and litter, leaching into the soil; and, the amountsof nutrients in fine litter are low and slowly cycling. Allthese severe conditions, together or separately, restrictthe production of heath forest and select only thosespecies which are resistant to its many adverse condi-tions.Acknowledgements We wish to thank Claudio Yano andCilene Palheˆta Soares for helping in the laboratory and in the field;two anonymous reviewers and Laszlo Nagy provided helpfulcomments to improve the manuscript. The work was funded byINPA/DFID (National Institute for Amazonian Research/Department for International Development, UK) through theproject BIONTE (Biomass and Nutrients in the Tropical RainForest) and by the European Community through the project‘Organic Matter as Basis for Sustainable Use of Soils in Amazon’.ReferencesAnderson AB (1981) White-sand vegetation of BrazilianAmazonia. Biotropica 13:199–210Anghinoni I, Volkweiss SJ (1984) Recomendac¸o˜es de uso defertilizantes no Brasil. In: Espinoza W, Oliveira AJ (eds)Anais do simpo´sio sobre fertilizantes na agricultura Bra-sileira. EMBRAPA, Brası´liaAttiwill PM, Adams MA (1993) Nutrient cycling in forests.New Phytol 124:561–582Bongers F, Engelen D, Klinge H (1985) Phytomass structure ofnatural plant communities on spodosols in southernVenezuela: the bana woodland. Vegetatio 63:13–34Brunet J, Neymark M (1992) Importance of soil acidity to thedistribution of rare forest grasses in south Sweden. Flora187:317–326Bru¨nig EF (1968) On the limits of vegetable productivity in thetropical rain forest and the boreal coniferous forest. IndBot Soc 46:314–322Bru¨nig EF (1970) Stand structure, physiognomy, and envi-ronmental factors in some lowland forests in Sarawak.Trop Ecol 11:26–43Bru¨nig EF (1973) Species richness and stand diversity inrelation to site and succession of forests in Sarawak andBrunei (Borneo). Amazoniana 4:293–320Bru¨nig EF (1974) Ecological studies in the kerangas forests ofSarawak and Brunei. Borneo Literature Bureau, KuchingBurslem DFRP, Grubb PJ, Turner IM (1995) Responses tonutrient addition among shade-tolerant tree seedlings oflowland tropical rain forest in Singapore. J Ecol 83:113–122Burslem DFRP, Turner IM, Grubb PJ (1994) Mineral nutrientstatus of coastal hill dipterocarp forest and adinandrabelukar in Singapore: bioassays of nutrient limitation. JTrop Ecol 10:579–600Coomes DA, Grubb PJ (1996) Amazonian caatinga and relatedcommunities at La Esmeralda, Venezuela: forest struc-ture, physiognomy and floristics, and control by soil fac-tors. Vegetatio 122:167–191Cuevas E, Medina E (1988) Nutrient dynamics within Ama-zonian forest. II. Fine root growth, nutrient availabilityand leaf litter decomposition. Oecologia 76:222–235David MB, Mitchell MJ, Nakas JP (1982) Organic and inor-ganic sulfur constituents of a forest soil and their rela-tionship to microbial activity. Soil Sci Soc Amer J46:847–852Denslow JS, Vitousek PM, Schultz JC (1987) Bioassays ofnutrient limitation in a tropical rainforest soil. Oecologia74:370–376Falkengren-Grerup U, Tyler G (1992) Nutrient conditionslimiting survival and growth of Galium odoratum (L.)Scop. in acid forest soil. Acta Oecol 13:169–180Falkengren-Grerup U Tyler G (1993) Experimental evidencefor the relative sensitivity of deciduous forest plants tohigh soil acidity. For Ecol Manage 60:311–326Falkengren-Grerup U, Brunet J Quist ME (1995) Sensitivity ofplants to acidic soils exemplified by the forest grassBromus benekenii. Water Air Soil Poll 85:1233–1238Falkengren-Grerup U, ten Brink DJ Brunet J (2006) Land useeffects on soil N, P, C and pH persist over 40–80 years offorest growth on agricultural soils. For Ecol Manag225:74–81Fitter AH, Hay RKM (1991) Environmental physiology ofplants, 2nd edn. Academic Press, OxfordFoy CD (1984) Physiological effects of hydrogen, aluminium,and manganese toxicities in acid soil. In: Adams F (ed)Soil acidity and liming, 2nd edn. American Society ofAgronomy, MadisonGine MF, Bergamin-Filho H, Zagatto EAG et al (1980)Simultaneous determination of nitrate and nitrite by flowinjection analysis. Anal Chim Acta 114:192–197Griffin DM (1985) A comparison of the roles of bacteria andfungi. In: Leadetter ER, Poindexter ED (eds) Bacteria innature: bacterial acitivities in perspective. Plenum Press,New YorkGrubb PJ (1989) The role of mineral nutrients in the tropics: aplant ecologist’s view. In: Proctor J (ed) Mineral nutrients222 Plant Ecol (2007) 192:209–224123
  • 15. in tropical forests and savannas. Blackwell ScientificPublications, OxfordHeyligers PC (1963) Vegetation and soil of a white-sand sa-vanna in Suriname. Verhandelingen der koninklijke Ne-derlandse Akademie van Wetenschappen, AFD.Natuurkunde. N.V. Noord-Hollandshce, Uitgevers Ma-atschappij, AmsterdamInsam H (1990) Are the soil microbial biomass and basalrespiration governed by climatic regimes? Soil Biol Bio-chem 22:525–532Janzen DH (1974) Tropical blackwater rivers, animals and mastfruiting by the Dipterocarpaceae. Biotropica 6:69–103Jenkinson DS, Powlson DS (1976) The effects of biocidaltreatments on metabolism in soil. V. A method for mea-suring soil biomass. Soil Biol Biochem 8:209–213Jordan CF (1985) Nutrient cycling in tropical forest ecosys-tems. John Wiley and Sons, ChichesterKeeney DR (1982) Nitrogen availability indices. In: Page AL,Miller RH, Keeney DR (eds) Methods of soil analysis Part2, 2nd edn. American Society of Agronomy, MadisonKidd PS, Proctor J (2000) Effects of aluminium on the growthand mineral composition of Betula pendula Roth. J ExpBot 51:1057–1066Kinraide TB (1993) Aluminium enhancement of plantgrowth in acid rooting media. A case of reciprocalalleviation of toxicity by two toxic cations. PhysiolPlanta 88:619–625Kinraide TB (2003) Toxicity factors in acidic forest soils: at-tempts to evaluate separately the toxic effects of excessiveAl3+and H+and insufficient Ca2+and Mg2+upon rootelongation. Eur J Soil Sci 54:323–333Klinge H, Medina E (1979) Rio Negro caatingas and camp-inas. Amazonas states of Venezuela and Brazil. In:Spetch RL (ed) Heathland and related shrublands. Eco-systems of the World 9A. Elsevier Scientific, Amster-dam. pp 483–487Kuiters AT (1990) Role of phenolic substances from decom-posing forest litter in plant-soil interactions. Acta BotNeerl 39:329–348Ludwig B, Khanna PK, Anurugsa B et al (2001) Assessment ofcation and anion exchange and pH buffering in an Ama-zonian Ultisol. Geoderma 102:27–40Luiza˜o FJ (1996) Ecological studies in three contrasting foresttypes in central Amazonia. Ph.D. thesis, University ofStirlingLuiza˜o RCC (1994) Soil biological studies in contrasting typesof vegetation in central Amazonian Rain Forests. Ph.D.thesis, University of StirlingMedina E, Cuevas E (1989) Patterns of nutrient accumulationand release in Amazonian forests of the upper Rio Negrobasin. In: Proctor J (ed) Mineral nutrients in tropicalforests and savannas. Blackwell Scientific Publications,OxfordMiyamoto K, Rahajoe JS, Kohyama T (2007) Forest structureand primary productivity in a Bornean heath forest. Bio-tropica 39:35–42Moran JA, Barker MG, Moran AJ et al (2000) A comparison ofthe soil water, nutrient status, and litterfall characteristicsof tropical heath and mixed-dipterocarp forest sites inBrunei. Biotropica 32:2–13Nagy L, Proctor J (1997) Plant growth and reproduction on atoxic alpine ultramafic soil: adaptation to nutrient limita-tion. New Phytol 137:267–274Pauletto D (2006) Estoque e produc¸a˜o de liteira grossa emsubmetida ao manejo florestal no noroeste de MatoGrosso. Dissertac¸a˜o de mestrado, Universidade doAmazonasPersson T, Wire´n A, Andersson S (1990) Effects of liming oncarbon and nitrogen mineralization in coniferous forest.Water Air Soil Poll 54:351–354Pires JM, Prance GT (1985) The vegetation types of BrazilianAmazon. In: Prance GT, Lovejoy TE (eds). Amazonia.Pergamon Press, OxfordProctor J (1995) Rainforests and their soils. In: Primack RB,Lovejoy TE (eds) Ecology, conservation, and manage-ment of Southeast Asian rainforests. Yale UniversityPress, New HavenProctor J (1999) Heath forests and acid soils. Bot J Scotl51:1–14Proctor J, Anderson JM, Chai P et al (1983) Ecological studiesin four contrasting lowland rain forests in Gunung MuluNational Park, Sarawak. I. Forest environment, structureand floristics. J Ecol 71:237–260Reis EL (1989) Processo de obtenc¸a˜o de mudas de seringueiraem tubetes. 1. Avaliac¸a˜o do desenvolvimento das plaˆn-tulas com diferentes adubac¸o˜es. Agrotropica 1:194-197Richards PW (1996) The tropical rain forest: an ecologicalstudy, 2nd edn. Cambridge University Press, CambridgeRoem WJ, Klees H, Berendse F (2002) Effects of nutrientaddition and acidification on plant species diversity andseed germination in heathland vegetation. J Appl Ecol39:937–948Rowell DL (1988) Soil acidity and alkalinity. In: Wild A (ed)Russel’s soil conditions and plant growth. Longman Sci-entific, EssexSilver WL (1994) Is nutrient availability related to plantnutrient use in humid tropical forests? Oecologia 98:336–343Skyllberg U (1991) Seasonal variation of pHH2O and pHCaCl2 incentimeter-layers of mor humus in a Picea abies (L.)Karst. stand on till soils in northern Sweden. Scand J ForRes 6:3–18Skyllberg U (1999) pH and solubility of aluminium in acidforest soils: a consequence of reactions between organicacidity and aluminium alkalinity. Europ J Soil Sci 50:95–106Staaf H (1992) Performance of some field-layer vegetationspecies introduced into an acid beech forest with mor soil.Acta Oecologica 13:753-765Steen E (1991) Usefulness of the mesh bag method in quan-titative root studies. In: Atkinson D (eds) Plant rootgrowth: an ecological perspective. Blackwell ScientificPublications, OxfordTanner EVJ, Kapos V, Freskos S et al (1990) Nitrogen andphosphorus fertilization of Jamaican montane forest trees.J Trop Ecol 6:231–238Vitousek PM, Matson PA (1985) Causes of delayed nitrateproduction in two Indiana forests. For Sci 31:122–131Yano CY (2001) Efeitos da liteira fina sobre a disponibilidadede nutrientes e o crescimento de plaˆntulas em a´reas dePlant Ecol (2007) 192:209–224 223123
  • 16. extrac¸a˜o seletiva de madeira na Amazoˆnia Central.Dissertac¸a˜o de mestrado, Universidade do AmazonasWhite CS (1988) Nitrification inhibition by monoterpenoids:theoretical mode of action based on molecular structures.Ecology 69:1631–1633Whitmore TC (1984) Tropical rain forests of the Far East, 2ndedn. Clarendon Press, OxfordWhitmore TC (1990) An introduction to tropical rain forests.Clarendon Press, OxfordZar JH (1984) Biostatistical analysis. Prentice-Hall, Engle-wood Cliffs224 Plant Ecol (2007) 192:209–224123