Soil acidity and nutrient deficiency in central amazonian


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Soil acidity and nutrient deficiency in central amazonian

  1. 1. ORIGINAL PAPER Soil acidity and nutrient deficiency in central Amazonian heath forest soils Fla´vio J. Luiza˜o Æ Regina C. C. Luiza˜o Æ John Proctor Received: 21 February 2007 / Accepted: 21 May 2007 / Published online: 21 June 2007 Ó Springer Science+Business Media B.V. 2007 Abstract Experiments were carried out to test the effects of liming and nutrient additions on plant growth and soil processes such as C and N miner- alisation in three contrasting forest types in central Amazonia: the stunted facies of heath forest (SHF), the tall facies of heath forest (THF) and the surrounding lowland evergreen rain forest (LERF). Calcium-carbonate additions increased soil respira- tion in the field plots in the SHF; in laboratory incubations, soil respiration was higher in the SHF when soils were fertilised with N, and in THF and LERF after S additions. The addition of N alone or in different combinations generally induced a net immobilisation of soil N. Net nitrification increased during the incubation in SHF and THF soils fertilised with N+P, and in LERF soils fertilised with either N, or P, or CaCO3. In a field experiment using ingrowth bags, a higher fine root production was observed in all forest types when bags were fertilised with CaCl2 or CaCO3, suggesting that Ca may be a limiting nutrient in these soils. Calcium-carbonate addition in a glasshouse bioassay experiment with rice showed an overall positive effect on the survival and growth of the seedlings. In other treatments where soil pH was not raised, the rice showed acute toxicity symptoms, poor root and shoot growth and high mortality. Similar results were yielded in a field experiment, using naturally established seedlings in the field plots in SHF, THF and LERF. It is concluded that the acute H+ ion toxicity is a major growth- limiting factor for non-adapted plants in heath forest soils in central Amazonia. Keywords Campina Á Campinarana Á Heath forest Á Nutrient limitation Á Soil acidity Introduction Most of Amazonia that is not seasonally flooded is covered by lowland evergreen rain forest (sensu Whitmore 1984), often referred to in Brazil as terra firme forest, and characterised by high species diversity (Pires and Prance 1985). However other forest formations that have a low species diversity, low stature and high presence of scleromorphic leaves, associated with white sandy soils (Spodosols), occur locally throughout Amazonia in Brazil, south- ern Venezuela, Ecuador, north-eastern Peru (Klinge and Medina 1979; Anderson 1981; Proctor 1999), as well as in Guyana and Suriname (Heyligers 1963; Whitmore 1984). Several of these forest formations F. J. Luiza˜o (&) Á R. C. C. Luiza˜o Departamento de Ecologia, Instituto Nacional de Pesquisas da Amazoˆnia, Caixa Postal 478, 69011-970 Manaus, Amazonas, Brasil e-mail: J. Proctor School of Biological and Environmental Sciences, University of Stirling, Stirling FK9 4LA, Scotland, UK 123 Plant Ecol (2007) 192:209–224 DOI 10.1007/s11258-007-9317-6
  2. 2. present distinctive situations (e.g., caatinga located on waterlogged sites in Venezuela vs. campina in central Amazon on sites not subject to flooding). However, these forest formations from the neotropics (which could be collectively called caatinga), show noticeable similarities in structure and physiognomy amongst themselves, and to kerangas from the palaeotropics, in Southeast Asia (Bru¨nig 1968, 1970; Proctor et al. 1983; Whitmore 1984). Taking into account that in Brazil there is another well- known biome named caatinga (covering large areas of the semi-arid region in north-eastern Brazil), the use of an international nomenclature such as ‘heath forest’ (sensu Whitmore 1984) seems more conve- nient, and will be used henceforth. About 5–6% of Amazonia is covered by heath forest (Anderson 1981; Whitmore 1984) occurring on Spodosols with a layer of mor humus of varying thickness. The stunted facies of heath forest (referred to as SHF in this article) is called campina in Brazil and often lacks the mor humus layer; the taller facies (THF) is called campinarana, and occurs next to high LERF. The physiognomy of the SHF and THF formations could correspond to facies of ‘caatinga’ in Venezuela (Anderson 1981). Heath forests grow on bleached white sands (Richards 1996) and are generally characterised by their short stature, slender trunks, thick leaves and low species richness. There are several views as to the causes of heath forests, but it is unlikely that a single 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 and Medina 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 this forest formation remain unclear (Miyamoto et al. 2007) and require further investigation. The first two of the above hypotheses, drought and waterlogging, are difficult to investigate experimen- tally. However, on the basis of observations made in heath forests occurring under different hydrological situations, they have been discarded as the principal causal factors. For example why does seasonal waterlogging tend to cause savanna in much of Brazil and not heath forests if waterlogging is an important cause of heath forests? The second two hypotheses (low nutrients, soil acidity and phenolics) are more amenable to exper- imental tests. Moreover, field studies in heath forest in Brunei, analysing soil and litterfall nutrient contents, 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) has generally been used to reduce acidity and fertiliser applications to the soil can directly stimulate micro- bial population and allow plant growth. The root ingrowth technique, despite its shortcomings, offers an opportunity to study fine root growth in relation to mineral nutrient availability, and is particularly useful for within-site comparisons amongst treatments (Steen et al. 1991). In order to test the hypothesis that nutrients, or low pH, or both limited soil processes (such as soil respiration and N transformations), fine root and plant growth and survival were compared after the addition of nutrients in two types of heath forest and in LERF. It was hypothesised that (a) soil respiration, N transformations, and roots and seedling growth would respond to N but not P or other nutrient addition; and (b) increasing soil pH through liming would cause a significant response in soil processes, root growth, and seedling growth and survival, and (c) the addition of both lime and nutrients should produce the best responses. Materials and methods Study site The field study was carried out in central Amazonia (2o 360 S; 60o 010 W), 60 km north of Manaus, Amazonas State, Brazil, on a gradient of natural vegetation 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. The soils are classified as Spodosols (SHF and THF) and Ultisols (LERF). Selected features for soil profiles under each forest type are given in Table 1. Species richness in both heath forests is low (seven species haÀ1 in SHF and 24 in THF) compared with 82 species haÀ1 in the LERF. Above-ground biomass was estimated at 71 Mg haÀ1 in SHF, 152 Mg haÀ1 in THF and 210 Plant Ecol (2007) 192:209–224 123
  3. 3. 409 Mg haÀ1 in LERF (Luiza˜o 1996). The Fabaceae (Caesalpinioideae) has the highest basal area in all three-forest types, followed by the Sapotaceae in the SHF, by the Euphorbiaceae in the THF, and by the Burseraceae in the LERF. A full description of the site properties and the forests is given by Luiza˜o (1996). For soil and vegetation studies, three 50 m · 50 m plots were delimited and used in each forest type. In each plot, the four quadrants, measuring 25 m · 25 m, were also marked. In the present work, two experiments were carried out in the field (experiments 1 and 2) and two in the laboratory (experiments 3 and 4). Field experiments Experiment 1: root ingrowth bags in the field Nylon ingrowth bags of 12 cm · 12 cm and 1-mm mesh were used. Two growth media were used in the ingrowth bags: medium-sized vermiculite (3À6 mm) and sieved sand from open SHF sites. They con- trasted in that sand is inert with virtually no exchange capacity, whilst vermiculite being a clay mineral has a large exchange capacity (100–150 meq/100 g), its pH is between 7 and 10, and naturally contains exchangeable K+ , Mg2+ and Fe2+ ions. The bags with sand were placed on the soil surface (after the removal of the litter layer) and the bags with vermiculite were placed on the soil surface, and in the soil to a depth of 10 cm. In the SHF, the 10 cm depth corresponded to either white sand in the open patches, or under closed canopy, it incorporated the layer where organic matter and fine roots concentrated. In the THF at 10 cm depth ingrowth bags were almost exclusively in the litter layer and in the LERF, mostly in the upper litter layer where a well-developed root mat occurred. There were six nutrient addition treatments (Table 2), where the growth media were treated with distilled water (control) or by either solutions or suspensions of one of five nutrients: KCl, CaCO3, NaHPO4, CaCl2 and urea (NH2CONH2). After 24 h imbibition, the growth media were placed in the nylon ingrowth bags. In each 25 m · 25 m quadrant of the main field study plots (50 m · 50 m), one bag was randomly placed, making it four replicate soil bags of each nutrient treatment per plot. The bags were left undisturbed for 117 d (all in the rainy season) from 2 January to 19 May 1993. Then, all the bags were removed, any outside roots shaved, and the roots inside the bags (all <2-mm diameter) separated by sieving and flotation. The roots were dried (1058C) and weighed. Experiment 2: the effect of nutrient addition on native tree seedlings In each forest type, two 8 m · 5 m plots were delimited, either in small natural gaps (THF and LERF) or in open areas alongside the ‘islands’ of Table 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-eqiv 100 gÀ1 ) Na+ (m-eqiv 100 gÀ1 ) Ca2+ (m-eqiv 100 gÀ1 ) Mg2+ (m-eqiv 100 gÀ1 ) CEC (m-eqiv 100 gÀ1 ) H+ /Al3+ (m-eqiv 100 gÀ1 ) SHF 0–5 3.7 0.28 25.4 165 0.15 0.03 0.08 0.26 1.84 >67.0 5–10 4.3 0.20 2.0 48 0.03 0.0 0.15 0.04 0.66 >24.0 20–30 4.9 0.30 0.5 17 0.0 0.0 0.08 0.01 0.28 7.50 THF 0–9 3.5 1.24 24.3 623 0.36 0.45 0.02 0.38 7.06 25.8 9–20 4.2 0.05 18.8 26 0.06 0.0 0.14 0.04 1.08 8.70 20–30 4.2 0.02 61.0 19 0.03 0.0 0.18 0.03 1.05 9.10 LERF 0–6 3.9 1.08 21.0 419 0.05 0.05 0.02 0.06 7.82 0.21 7–20 4.1 0.70 18.6 305 0.02 0.01 0.34 0.06 19.4 0.40 20–30 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 was predominantly organic (H); the second, mixed organic/mineral, and the third, an intrinsically mineral layer. Note that in SHF any vestige of organic mixing in soil profile had disappeared after 10 cm in depth Plant Ecol (2007) 192:209–224 211 123
  4. 4. vegetation (SHF). Only two replicate plots were used because of the shortage of suitable natural gaps in the THF and LERF. Fourteen 1 m · 1 m quadrats in each plot were selected for experimental treatments on seedlings already existing and measuring up to 30 cm in height (thus, a wide variety of seedling species, and likely of ages as well, was included in the experiment). Seven nutrient addition treatments were applied (Table 2): (1) NH2CONH2, (2) Na2PO4, (3) KCl, (4) CaCl2, (5) CaCO3, (6) a combination of 1, 2, 3 and 5, and a control (no added nutrients). Two replicates of each of the seven treatments were applied in each plot. Treatments were randomly located in each plot. Rates of fertilisation (Table 2) were similar to those generally recommended by forestry nurseries in Brazil (Reis 1989), and fell within the lower part of ranges commonly used for mature trees elsewhere (Tanner et al. 1990). The nutrients were added to the soil on 1 March 1993, during the rainy season to ensure that native seedlings did not dry out in the months following treatment. Seedlings were assessed at the beginning of the experiment and after 180 d, and survival rate (final/initial numbers) and growth quotient (final/initial height) determined. The same 8 m · 5 m plots were used for soil respiration measurements in response to nutrient additions. Three composite samples (made up of five sub-samples taken at random within the 1 m · 1 m quadrats) were collected from the upper soil layer (0– 20 cm) from each treatment. In the SHF, the 0–20 cm layer was generally mineral, slightly mixed with some organic matter in the top 1–2 cm; in the THF and the LERF, it generally included a humic layer and a mixed organo-mineral layer, as well as a root mat. Samples were cleaned of roots and litter, and the fresh soil transferred into glass bottles. Bottles were incubated in the dark for 10 d at 248C, and the evolved carbon dioxide measured by using the fumigation–incubation method of Jenkinson and Powlson (1976). Sampling and measurements were repeated after 60 d and 180 d from the beginning of the experiment. Laboratory experiments Experiment 3: effect of nutrient addition on C and N mineralisation and net nitrification To test the effects of soil nutrient limitation on soil respiration and N transformations nutrient additions were made to soil under laboratory conditions. Soil mineral samples were taken from the top 10 cm in each of the three 50 m · 50 m plots of the three forest types, bulked per forest type and carefully mixed. A 50-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 248C for 10 d, and the evolved CO2 was measured by titration according to the fumigation-incubation method of Jenkinson and Powlson (1976). For calculations of the N transformation N was extracted from 5-g sub-samples, at the start of the incubation Table 2 Nutrient addition treatments (all expressed on a kg haÀ1 basis) applied to soils (and root ingrowth media in Experiment 1) in the four experiments made in the field and in the laboratory Treatment Experiment 1 (field) Root ingrowth bags Experiments 2 and 3 (field, native seedlings; and lab, rice) Experiment 4 (lab) Soil C and N mineralisation 1 N as 150 kg of NH2CONH2 N as 150 kg of NH2CONH2 N as 150 kg of NH2CONH2 2 P as 50 kg of NaH2PO4 P as 50 kg of NaH2PO4 P as 50 kg of NaH2PO4 3 K as 60 kg of KCl K as 60 kg of KCl K as 60 kg of KCl 4 Ca as 2 000 kg of CaCl2 Ca as 2 000 kg of CaCl2 Ca as 2 000 kg of CaCO3 5 Ca as 2 000 kg of CaCO3 Ca as 2 000 kg of CaCO3 Ca as 2 000 kg of CaSO4 6 No added nutrients (control) NPKCa—combination of 1, 2, 3 and 5 S as 500 kg of Na2SO4 7 – 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) 192:209–224 123
  5. 5. (initial mineral N), and after 10 d (incubated mineral N) with 50-ml 2 M KCl. Concentrations of the ammonium ion were determined colorimetrically by flow injection, using a modified indophenol blue method and the concentrations of nitrate ions were determined by a similar technique using a modified cadmium reduction method (Gine et al. 1980). Net mineralisation and net nitrification were calculated following Keeney (1982) and included the subtrac- tion of the amount of nitrogen added in the N treatments. Experiment 4: glasshouse bioassay experiment Humus (decomposing litter and raw humus material) and the upper mineral soil layer were collected separately from SHF, THF and LERF, air-dried and sieved through a 2-mm mesh. Eight 7-cm diameter (200-ml volume) pots were prepared for each of seven treatments, and for each forest type and soil depth. The seven treatments (Table 2) were the same as those applied in the field (Experiment 2) and the pots were watered with 20 ml freshly made nutrient solutions or suspensions (Table 2). The pots were randomly located on wooden benches inside a glasshouse. Except for CaCl2, the rates of nutrient additions were at the lower end of the recommended range for cultivating acidic soils in Brazil (Anghinoni and Volkeweiss 1984). Directly after applying the nutrients, 10 seeds of dryland rice (Brazilian variety IAC-47) were placed in the top 1-cm of soil. The pots were kept moist and 10 d after planting germination was assessed; 40 d later rice plants were assessed and harvested. Shoot and root biomass, and plant survival and mortality were determined. Dryland rice was chosen as the test plant after an attempt to grow a native tree species in field conditions was unsuccessful due to heavy seedling predation, despite showing high rates of germination in all three forest types (Luiza˜o 1996). Dryland rice as a test plant is usually disease free, has a low soil nutrient demand, and its seeds are readily available. Despite that the Iban word kerangas (for heath forests in Indonesia) means a site/soil where rice cannot grow (Whitmore 1984), the authors considered its use appropriate, since eventual positive responses in SHF and THF soils could be attributed to the soil amendments provided by nutrient additions. Statistical analyses In the field assays, nested analyses of variance (treat- ments nested in plots) using GLM (General Linear Model) were performed. In the laboratory incubations, two-way analyses of variance were performed with nutrient treatment and forest type as fixed factors. To assess the effects of the nutrient additions in relation tothecontrol,one-way analysesofvariancefollowedby the Dunnett’s test were used to compare treatments to control within each forest type. Data were transformed (using square-root, logarithmic or arcsine transforma- tions) to assure homogeneity of variance (Zar 1984). Results Field experiments Experiment 1: root ingrowth bags at field plots There was a large variability in the results obtained from ingrowth bags. Significantly fewer roots were found in the ingrowth bags in the SHF (nested ANOVA, d.f. = 12; P < 0.001) than in the THF and LERF. Fine root mass was significantly lower in the bags filled with sand compared with those with vermiculite (P < 0.001; Fig. 1). Within the vermiculite bags, those buried within the soil showed a higher production of fine roots compared with those placed on the litter layer surface. In the SHF, the vermiculite bags placed on the soil surface showed a significantly higher production of fine roots than both the vermic- ulite bags buried within the soil and the sand bags on the soil surface (P < 0.001). Although variability was high, CaCO3, CaCl2 and KCl increased fine root growth in the THF (P < 0.05). In the LERF, CaCl2 and CaCO3 were the only treatments which significantly increased (both P < 0.001) fine root growth in vermiculite-filled bags and at both depths. Experiment 2: Effect of nutrient addition on the growth of native tree seedlings In 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) 192:209–224 213 123
  6. 6. In the THF seedling survival was also significantly reduced by CaCl2 (F = 4.0; P < 0.01), but increased by NPK+CaCO3. In the LERF plots, none of the nutrient additions influenced the survival rate of the seedlings. The quotient of final/initial height was significantly increased in SHF by NPK+CaCO3 (+27%). Nitrogen addition alone caused a mean increase of 22% in seedling growth in relation to the control, but the difference was not statistically significant. In the THF, the final height of the seedlings was generally lower than the initial height (except after addition of NPK+CaCO3), but only significantly so with CaCl2. In LERF no significant differences in height were found between treatments. No significant differences were found amongst treatments for soil respiration (Table 3), with the exception of the 60-d sampling time in SHF, where respiration was significantly higher with the addition of NPK+CaCO3 (nested ANOVA, d.f. = 21; P < 0.05). In the same soil, there was a concomitant increase (P < 0.001) in soil pH under the same treatment. SHF 0 1 2 3 4 5 KCl CaCO3 CaCl2 Urea NaH2 PO4 Control Rotomass(gabg 1- ) vermiculite, on surface vermiculite, 10 cm deep sand, on surface THF 0 2 4 6 8 10 KCl CaCO3 CaCl2 Urea NaH2 PO4 Control Rootmass(gbag1- ) LERF 0 2 4 6 8 10 KCl CaCO3 CaCl2 Urea NaH2 PO4 Control Treatments tooRsams(ggab 1- ) * * * * * * * * * * ** * * * * * * ** ** Fig. 1 Ingrowth bag experiment: dry mass of roots per bag after 117 d in the bags containing vermiculite on the soil surface, vermiculite at 10 cm depth in the soil and sand on the soil surface, under different nutrient addition treatments. Bars are means ± SE of four bags in each experiment and treatment in each of the three replicate plots in the SHF, THF and LERF. Significance levels for nested ANOVA with Dunnet’s test for comparisons with the control are: *, 0.05; **, 0.01; ***, 0.001 0.0 0.4 0.8 1.2 1.6 2.0 N P K aCl2C aCO3C PNKI+CaCO3 Ctnorol Growthnidex(fina/lnitiiahleight SHF THF LERF 0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 N P K aCl2C aCO3C KPNI+CaCO3 Ctnorol Treatments uSvrivlaaret SHF THF LERF * * *** * *** * ** Fig. 2 Field experiment: survival rate (quotient of final/initial number of living native seedlings), and the growth (quotient of final/initial height of the native seedlings) 180 d after nutrient addition in the SHF, THF and LERF. Values are means with SE (n values are variable and indicated above the bars). The survival rate varies from 0 (no survival of seedlings) to 1 (all survived). Growth quotients <1 indicate negative growth on the average of the plots: quotients >1 indicate actual growth of seedlings. Significant differences in relation to the control (from nested ANOVA followed by Dunnet’s test) are indicated by asterisks: * ,0.05; ** , 0.01; *** , 0.001 214 Plant Ecol (2007) 192:209–224 123
  7. 7. Laboratory experiments Experiment 3: effect of nutrient addition on C and N mineralisation Soil respiration. Soil respiration measurements varied widely amongst soil types and treatments. Greater increases in respiration after nutrient additions in relation to the control were visible in SHF (Fig. 3), but the differences were only significant in the treatments 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 and N+S (P < 0.001). In the LERF soils, respiration was significantly higher than the control in the treatments S 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) induced net N immobilisation (P < 0.001) in SHF and THF soils (Fig. 4). In the LERF soils, six out of the 12 treatments caused significant net immobilisation of N: the addition of N alone; N+P; N+K; N+CaCO3; N+CaSO4; N+Na2SO4 (P < 0.001), whereas two treatments caused net mineralisation: CaSO4 and CaCO3 (all P < 0.001) (Fig. 4). Net nitrification rates were not affected by any of the treatments in SHF soils (Fig 5). In the THF soils, only N+P increased significantly net nitrifica- tion (P < 0.001). In the LERF, the rates of net nitrification were significantly different from the control in seven out of the 12 treatments: an increase with N, P and CaCO3; and a decrease with KCl, Na2SO4, N+CaSO4 and N+Na2SO4 (all P < 0.001) (Fig. 5). Experiment 4: glasshouse bioassay experiment Soil type and nutrient addition treatment generally had a significant influence on the germination, survival and growth of the dryland rice (Fig. 6). There was an extreme stunting and early death of seedlings in SHF and THF soils that had not received CaCO3. A significantly higher shoot biomass of rice was found with CaCO3 alone and with NPK+CaCO3 (F = 16.1; P < 0.001) in SHF soils. In THF soils, only the addition of CaCO3 (F = 7.66; P < 0.001) and in the LERF, only the addition of NPK+CaCO3 increased shoot biomass significantly. Root biomass was also significantly higher after the addition of both CaCO3 and NPK+Ca- CO3 (F = 9.23; P < 0.001) in SHF soil; after addition of CaCO3 in THF soil (F = 5.91; P < 0.001); and no significant effects of nutrient addition were found in the LERF soils. The addition of CaCl2 inhibited germination and killed most seedlings even in the LERF soils (Fig. 6), although the few seedlings which did survive in the SHF and THF soil grew well. The addition of CaCl2 significantly increased seedling mortality in all three soil types (F = 14.4, SHF; F = 10.3, THF; F = 24.3, LERF; P < 0.001). In THF soils, addition of NH2CONH2 also significantly increased mortality (F = 10.3; P < 0.001). Table 3 Soil respiration (mg C gÀ1 oven-dry soil) 60 d and 180 d after nutrient addition to field plots with already existing seedlings in SHF, THF and LERF Treatment Forest types SHF THF LERF 60 d 180 d 60 d 180 d 60 d 180 d N 56.0 ± 25.6 20.0 ± 2.20 91.4 ± 32.6 101 ± 22.4 52.1 ± 15.6 111 ± 3.70 P 20.1 ± 4.08 na 83.7 ± 12.2 na 57.3 ± 20.3 na K 68.9 ± 17.0 na 60.9 ± 15.2 na 52.1 ± 11.3 na NPK + CaCO3 104 ± 15.7* 66.6 ± 14.5 93.3 ± 21.6 110 ± 12.7 86.5 ± 8.45 103 ± 13.2 CaCl2 70.1 ± 20.6 na 91.1 ± 23.6 na 69.5 ± 17.3 na CaCO3 41.9 ± 5.18 100 ± 3.43 105.5 ± 25.3 128 ± 20.6 92.3 ± 22.8 135 ± 41.6 Control 30.5 ± 6.12 57.1 ± 20.8 48.5 ± 11.3 128 ± 13.4 66.5 ± 6.12 90.4 ± 21.8 Values 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) 192:209–224 215 123
  8. 8. Discussion The pH in the three forest types was amongst the lowest recorded for rain forests on acidic soils, but the concentrations of nutrients (except for Na in SHF, and Ca in all three forest types) in the surface soils SHF 0 20 40 60 80 100 120 * * * * * * * * * * * * * * * * * * * * * * * tCrl N +NP +NK +NaCCO3 +NaCSO4 +NSO4 P K aCCO3 aCSO4 Na2SO4 Na2SO4Na2SO4 Solirespriat(noiµgCg1- ) THF 0 30 60 90 120 tCrl N +NP +NK +NCaCO3 +NSaCO4 +NSO4 P K O3CaC SaCO4 Solirespirtaoi(nµgCg1- ) LERF 0 30 60 90 120 tCrl N +NP +NK +NaCCO3 +NaCSO4 +NSO4 P K aCCO3 aCSO4 Treatments Soilrespiration(µCg-g)1 Fig. 3 Laboratory experiment: soil respiration (mg C gÀ1 oven-dry soil 10 dÀ1 ) under different nutrient addition treatments (explained in the text) in SHF, THF and LERF soils. Values are means ± SD (n = 3). Significance levels for ANOVA within each forest type with Dunnet’s test for comparisons with the control are: *, 0.05; **, 0.01; ***, 0.001 SHF -120 -100 -80 -60 -40 -20 0 20 40 60 Ctrl N N+P N+K N+CaCO3 N+CaSO4 N+SO4 P K CaCO3 CaSO4 Na2 SO4 Na2 SO4Na2 SO4 Nmineralization(µNg-1 )Nmineralization(µgNg-1 ) Nmineralization(µgNg-1 ) * * * * * * * * * * * * * * * * * * THF -120 -100 -80 -60 -40 -20 0 20 40 60 Ctrl N N+P N+K N+CaCO3 N+CaSO4 N+SO4 P K CaCO3 CaSO4 * * * * * * * * * * * * ** * * * * * * * LERF -120 -100 -80 -60 -40 -20 0 20 40 60 Ctrl N N+P N+K N+CaCO3 N+CaSO4 N+SO4 P K CaCO3 CaSO4 * * * * * * * * * * * * * * * * * * * * * * * * Fig. 4 Laboratory experiment: net nitrogen mineralisation (mg N gÀ1 oven-dry soil 10 dÀ1 ) under different nutrient addition treatments in the SHF, THF and LERF soils. Values are means ± SE (n = 9). Significance levels for ANOVA with Dunnet’s test for comparisons with the control are: *, 0.05; **, 0.01; ***, 0.001 216 Plant Ecol (2007) 192:209–224 123
  9. 9. are not exceptionally low (Luiza˜o 1996). The most striking difference observed between the heath forest and the LERF soils was the dominance of H+ (instead of Al3+ ) in the exchange complex, especially in the SHF, where Al3+ concentrations were negligible and the H+ /Al3+ quotient was much higher (more than 300 times in upper soil layer) than in the LERF soils (Luiza˜o 1996; Proctor 1999; Table 1). However, the biomass estimated for the LERF (409 Mg haÀ1 ), slightly higher than the range reported for forests on Oxisols in Amazonia (Jordan 1985) suggests that -7 -5 -3 -1 1 3 5 SHF tCrl N +NP +NK +NCO3aC +NSaCO4 +NSO4 P K CaCO3 SaCO4 Na2SO4Na2SO4 Na2SO4 Nettinrficiatnoi(µgN1- ) -3 0 3 6 9 12 THF tCrl N +NP +NK +NCaCO3 +NCaSO4 +NSO4 P K aCCO3 aCSO4 Netintrifictaion(µNgg1- ) -5 0 5 10 15 20 LERF tCrl N +NP +NK +NCaCO3 +NCaSO4 +NSO4 P K CO3aC SO4aC Treatments eNtnitrficitanoi(µNgg1- ) * * * * * * * * * * * * * * * * * * * * * * * * Fig. 5 Laboratory experiment: net nitrification (mg N gÀ1 oven-dry soil 10 dÀ1 ) under different nutrient addition treatments in the SHF, THF and LERF soils. Values are means ± SE (n = 9). Significance levels for ANOVA with Dunnet’s test for comparisons with the control are: *, 0.05; **, 0.01; ***, 0.001 0 2 4 6 *** *** *** * * * ** * * * ** * * * ** * ** * * *** * * * * * * * 8 10 Mortatily u-Nrea CKl aCCl2 aCCO3 PNK+aCO3 C Conrtol ConrtolConrtol SHF THF LERF 0 20 40 60 80 100 120 N-ruae NaH2 PO4 NaH2 PO4 CKl aCl2 C aCO3 C PNK+aCO3 C Soohtibmo(ssagm 2- ) 0 20 40 60 80 100 N-ruae aNH2 O4 P CKl aCl2 C aCO3 C PNK+aCO3 C Treatments Romoibto(ssagm 2- ) Fig. 6 Glasshouse experiment: number of dead rice seedlings, and shoot and root dry mass (g mÀ2 ) in each treatment after 50 d, using soils from the SHF, THF and LERF. Values are means and SE (n = 8), and significant differences in relation to the control (from one-way ANOVA followed by Dunnet’s test) are indicated by asterisks: *, 0.05; **, 0.01; ***, 0.001 Plant Ecol (2007) 192:209–224 217 123
  10. 10. there are no limitations for tree growth in that forest type. Two nutrient combinations caused a significant increase in the SHF soil respiration: urea with Na2PO3, and urea with Na2SO4 suggesting that N is limiting microbial activities in the SHF. In turn, P and S seemed to be important when enough N was supplied. In THF soils, S, especially when combined with N, seemed to be the nutrient which mostly stimulated the activity of the microorganisms whereas in LERF soils, additions of S, and the combination N+K, stimulated soil respiration. En- hanced microbial activity could be caused either by S or by the added Ca or Na (Persson et al. 1989). However, the latter is unlikely to be the case since Na is at most a micronutrient whilst Ca did not produce so positive a response when added as CaCO3. Thus, the increase in microbial activity might be caused by additions of S, which was somehow unexpected, since over 95% of the forest topsoil S is organically bound (David et al. 1982). These results indicate that under certain conditions (e.g. adequate supply of other nutrients) S may limit microbial decomposition. Another possible explanation could be a potential liming effect of S in the soil, but unfortunately there was no separate S treatment in the experiments to confirm the results. High soil acidity has often been considered to be a strong microbial inhibitor. When acidity is reduced by liming a more diverse decomposer community may establish, allowing a more efficient substrate utilisation (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-d sampling was not apparent at 180 d. In THF and LERF soil respiration was not significantly influenced by CaCO3, a similar result to that found by Persson et al. (1990) in coniferous forest in Scandinavia. They found no significant difference in soil respira- tion between the controls and mineral soils which received CaCO3, and that may indicate that not enough liming material was applied to increase soil pH in those forest types. Low concentrations of N found in heath forest leaves (Coomes and Grubb 1996) and litterfall (Luiza˜o 1996; Proctor 1999) have been used to suggest that N may be unusually low in heath forests, thus limiting plant growth (Coomes and Grubb 1996). However, low N availability of soils may occur because of immobilisation by microorganisms (Pers- son et al. 1990). In the present study, in the soils of all forest types, all treatments including N additions resulted in a high net N immobilisation, which is a consequence of increased activity of the soil microbes (Persson et al. 1990). Since in the SHF soils a significant pH increase was not followed by enhanced net N mineralisation, it seems that low pH is not the only factor influencing the N transforma- tions. The addition of CaCO3 alone was effective in enhancing net N mineralisation only in the LERF soils. The general lack of an increase in net N mineralisation in both the SHF and THF soils when only CaCO3 was applied may be explained by an increase in bacterial relative to fungal decomposition, since there are strong indications that liming of forest soils stimulates bacterial activity more than that of fungi (Griffin 1985). In the present study N was added as urea, and no significant changes in soil pH were observed in the urea treatments, despite its potential acidifying effect, as pointed out in exper- iments made in eastern Amazonia in soils with a similar texture and chemistry (Ludwig et al. 2001). As an intermediate in microbial metabolism, urea applied to the soil is very readily hydrolysed, and much of it is transformed to ammonium ions and immobilised in a few days. Net nitrate production can only increase when there is ammonium available for nitrifying microor- ganisms. Therefore, the extent to which nitrate production and leaching may increase depends on whether liming stimulates mineralisation or immo- bilisation of ammonium. An experiment using soil solution concentration of nitrate in soil profile to estimate nitrate leaching in Scandinavian forest soils showed that leaching of NO3-N occurred in higher concentrations below pH 4.5 as a direct effect of the pH more than any other factors (Falkengren-Grerup et al. 2006). In the present study, as the pH was not elevated substantially in the SHF soils, nitrate leaching may have occurred in the field assays, but not in the 10-d incubation experiment in laboratory. In this case, since N mineralisation was inhibited by many of the added nutrients, no ammonium was left for the nitrification process. In both SHF and THF soils, net nitrification was inhibited (although not significantly) by nearly all nutrients applied. Even the addition of urea did not increase nitrification. Studies have suggested that labile inhibitors of nitrification 218 Plant Ecol (2007) 192:209–224 123
  11. 11. may be responsible for delays in nitrate production (Vitousek and Matson 1985) or for its complete inhibition (White 1988). The Ca status of the SHF, THF and LERF soils was very low and the overall positive response of fine root growth (in all bag positions, media and forest types) to both CaCO3 and CaCl2 addition, suggests that fine root growth is restricted by both soil pH and low Ca. However, the positive effect of both Ca treatments on the root mass in the heath forest soils may have another explanation. First, increased fine root production does not necessarily imply increased plant growth (E.V.J. Tanner, pers. comm. 2002). Plants might respond to fertilisation by first increas- ing root production, and only much later showing any increase in above-ground biomass (Silver 1994). Also, the general increase in root growth in the bags filled with vermiculite, especially in those buried in the soil, suggest that the alkaline vermiculite used in Brazil (pH = 8.8) had a positive effect on fine root growth. The vermiculite used in the present work was acquired from the only supplier in Brazil and with its high pH value and an unquantified amount of cations in its composition, certainly represented a confound- ing factor for evaluating the effects of the nutrient additions. However, it must be pointed out that the two cations generally present in higher concentrations in vermiculite (Mg2+ and Fe2+ ) were not evaluated in the present work. Also, there was a control for the experiment using vermiculite bags with no nutrient addition, and further, the effect of nutrient additions on vermiculite bags placed on soil surface were not strikingly different from the ones with sand. The results of the present study contrast with that of Cuevas and Medina (1988), who worked in different types of rain forest (tierra firme, tall caatinga and low bana) at San Carlos, Venezuela. They found fine root growth stimulated by the addition of N in tall caatinga and low bana forests only on top of the root mat and by P in tierra firme and bana forests and by Ca only in the tierra firme forest (&LERF). Proctor (1995) pointed out that owing to the very poor root growth in the unfertilised treatments of Cuevas and Medina (1988) their study did not allow them to reach firm conclusions on the limiting nutrients in the tierra firme and bana forests. Their data lend no support to the view that N, P or K, are limiting for plant growth in lowland evergreen rain forests, which confirms the results of the present study. The lack of response of fine roots to N, P and K addition observed here is not surprising, and corrob- orates the results of several recent ingrowth bag studies carried out in tropical and temperate soils. Studies carried out in Borneo at Barito Ulu, Central Kalimantan, Indonesia (J. Proctor, unpublished), found no response in a heath forest to P (but there was a significantly increased fine root growth in LERF in the presence of P). It seems that soil acidity not only controls nutrient effects on plant growth but it is also important for maintaining differences in species composition such as was observed by Roem et al. (2002) in heath land on nutrient-poor sandy soil in the Netherlands. They showed that the influence of nutrient availability on species composition in heath- land was less important than soil acidity. To what extent that control by acidity is effective is not precisely known as in harsh environments, such as the heath forests, some native species are able to deal with nutrient limitations (stress tolerators), but may rapidly respond in an opportunistic way when the limitation is removed, assuming a behaviour properly called as ‘latent competitors’ (Nagy and Proctor 1997). Such a strategy by certain heath forest species would help explain the surprising results found by Miyamoto et al. (2007) in a Bornean heath forest in southern Central Kalimantan (basal area of 21.8 m2 haÀ1 ) on bleached white sand, under an annual rainfall regime of 3,200 mm. They recorded a quick recovery in wood biomass after a strong drought, caused by the El Nin˜o phenomenon. Using pulses of nutrients (in this case, possibly released by dead wood and the extra litterfall produced by the drought) the heath forest apparently became a more productive system in the following years, allowing an increase in primary productivity in response to increased nutrient availability. The increase in nutri- ent availability in this case may be paralleled by an increase in soil pH caused by the release of Ca and Mg from the dead wood as illustrated in former works involving clearings produced by selective logging in Brazilian Amazon. They showed that together with some short term release of N and P from extra fine litterfall, a considerable increase in Ca and Mg availability in upper soil layer was observed after 1.5 years in response to the decomposition of dead wood accumulated in patches of the clearings produced by selective logging (Yano 2001; Pauletto 2006). These two basic cations, Ca and Mg, as well as Plant Ecol (2007) 192:209–224 219 123
  12. 12. Mn, are present in higher concentrations in the coarse litter 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 tree growth. In the present study, native seedlings in the field experiment showed either no or a negative response to N, P and K addition, as well as a high mortality when CaCl2 was applied. The results in SHF and THF were very similar to those of other studies carried out in temperate forests on acidic sandy soils in Sweden (Brunet and Neymark 1992; Falkengren-Krerup and Tyler 1992, 1993; Staaf 1992) or elsewhere (Proctor 1999; Roem et al. 2002). They all found that any addition of mineral nutrients was unsuccessful in promoting plant survival or growth, unless the treatment involved an increase in soil pH. In the present study, overall, there were no beneficial effects of the nutrient addition in the SHF and THF, if not accompanied by an increase in soil pH (by the addition of CaCO3), and a very limited effect in the LERF. Thus, there was no direct evidence of nutrient limitation for seedling growth in the SHF and THF, and other factors must be involved. The high toxicity induced by soil acidity was likely to be the main cause for the death or poor growth of seedlings in the nutrient addition treat- ments. In soils well supplied with Al, pH is controlled by a complex hydrated Al-ion buffer system which sets a lower limit to pH, preventing extreme acidity (with values much below 4.0) and high H+ concentrations (Rowell 1988; Fitter and Hay 1991). For soils of similar pH there are large differences between mineral and organic soils. In mineral soils exchange- able Al limits exchangeable acidity, whilst in organic soils the pH is maintained by the buffering ability of the organically complexed Al. Along a transition from mineral to organic soils the decrease in exchangeable Al with increasing organic matter, is paralleled by an increase in the exchangeable acidity. The removal of the Al complexes by the addition of bases (especially CaCl2, which was used in much larger concentrations than the other major nutrients in the present study) may have caused a decrease in the soil pH, increasing the H+ toxicity. It must be remembered that the amelioration of H+ toxicity by Al3+ ions has been shown experimentally (Kinraide 1993), and that in acidic soils Al3+ ions may prevent H+ from becoming an intrinsic toxin (Kinraide 2003). Thus, Al3+ ions decrease solute leakage at low pH, producing a growth enhancement (Foy 1984; Rowell 1988). In studies of Haplic Podzols in a boreal coniferous forest in Sweden, Skyllberg (1991, 1999) found that the humus layer (O horizon) had a pH positively correlated with Al. In line with other above-mentioned authors (e.g. Proctor 1999; Kinra- ide 1993; 2003) Skyllberg suggested that in acid humus layers and organic horizons with a pH below 4.0, Al cations act as any ‘base cation’ through an H+ - displacement at cation exchange sites. Thus, instead of acidifying effects, Al ions in soil (at adequate concentrations) would be beneficial, buffering the pH at levels not toxic to plants, and the lack of displacement of such ions cause strong toxicity for plant roots. In Scotland, addition of low concentra- tions of Al (2–5 mg lÀ1 ) to soils poor in Al ions enhanced the growth of two races of Betula pendula Roth originating from Al-poor soils (Kidd and Proctor 2000). In Scandinavia, a pot experiment using acid soil and raising its pH from 3.3 by carbonate additions showed that the growth of Bromus benekenii (Lange) Trimen. and nine other species (out of a total of 17) was limited at pH <4.1 and the toxicity of H-ions to Bromus was confirmed at pH 4.2 or lower (Falkengren-Grerup et al. 1995). In the present study, the very low concentration of Al in the heath forest soils, especially in the SHF, where the mor humus is often lacking, may be a major reason for the poor control of H+ toxicity. The results of the glasshouse experiment using rice seedlings overall confirmed those found in the field study on native tree seedlings: the only general positive effect on growth was caused by the addition of CaCO3, whilst the addition of CaCl2 had a general deleterious effect on seedlings, inducing high mor- tality rates. The general coincidence of the results observed in the glasshouse (using a cultivated crop) with the field experiment (using several native species) was reassuring. The apparent contradiction of the strongly nega- tive results for seedling growth in relation to the positive responses of fine root growth to the addition of CaCl2 (in the ingrowth bags) may have two explanations. These results may indicate that most of the roots penetrating the bags and responding posi- tively to the CaCl2 additions originated from mature 220 Plant Ecol (2007) 192:209–224 123
  13. 13. plants (not seedlings), which might respond differ- ently to nutrient addition. Most likely, though, the fine roots were not adversely affected because there was enough time for part of the CaCl2 (mainly the chloride fraction) to be leached from the bags by rainwater. In fact, 1,440 mm of rain fell during the experiment, and January, the first month of the experiment, had a rainfall mean of 108 mm per week. After such selective leaching, the residual Ca may have been beneficial for fine root growth. The positive responses of fine root growth and the soil respiration to additions of Ca to the soil seem to be further pieces of evidence of limitations by this element in the heath forest soils, after the apparent limiting effect of Ca and Mn for soil and litter organisms (Luiza˜o 1994; 1996). However, that does not imply that these elements are also limiting for plant growth as a whole, since other factors may be involved (Attiwill and Adams 1993). For instance, Grubb (1989) suggested that in nutrient-poor soils, an important interaction between shade and nutrients (especially for P) occurs, and that was partly confirmed in later bioassays in lowland dipterocarp rain forests in Singapore. Highly positive responses of 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 a negative response to P additions (Burslem et al. 1995). They suggested P and major cations as limiting factors in nutrient-poor soils (Burslem et al. 1994), and those shade-tolerant tree seedlings which have mycorrhizas are not limited by P supply because of the mycorrhizas or because they have a low demand for nutrients when growing in the shade (Burslem et al. 1995). The latter suggestion was also made by Denslow et al. (1987), who found positive responses of seedling growth with complete nutrient fertilisation on nutrient-richer soils, but no responses of shrubby species to P additions. In fact, the assessment of the actual nutrient requirements of trees 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 the seedling survival and growth agree notably with another study on Central Kalimantan heath forest soils, also growing dryland rice in a pot experiment. No seedling root growth was found in any treatment in the heath forest organic soil, except when CaCO3 was added (Proctor 1999). It was speculated that poor growth of rice on heath forest soils was due to toxins in the soil and not due to a low soil nutrient status. The negative effects of the humus layer included in part of the pots in the present study may also be the result of phenolic compounds (leached by the frequent watering of the pots), affecting seedling roots, especially in the heath forest soils. In Sarawak, Bru¨nig (1968, 1974) reported that heath forest soils have high concentrations of secondary metabolites, which may have two effects: production of toxic effects on the vegetation, and reduction of available N in the soil. Whitmore (1990) indicated that phenols are abundant in heath forest leaves and litter, and these may be toxic or inhibit uptake when they leach into the soil. Soil phenolics directly affect germina- tion and especially the growth of higher plants, and concentrations of soluble phenolics are correlated with organic matter content, and highest in the superficial L and F organic layers (Kuiters 1990). In the organic layers of the THF soils, evidence was found of phenolic leachates, in the form of green- brownish bubbles (Luiza˜o 1994), certainly released by the decomposition of either the litter on the soil surface or the fine roots, the main originators of phenolics in soil (Kuiters 1990). However, in the field experiment, using pre-exist- ing natural seedlings, and where controls showed no strong mortality, the putative toxicity of phenolic compounds would have interacted with the added nutrients, making it still more difficult to explain the mechanisms involved. The phenolic substances are closely related to pH and soil nutrient status, and although phenolics are generally not high enough to be strongly acidic, they are more physiologically active with H+ to produce the high mortality of seedlings in the SHF and THF when the pH buffer was probably swamped by the large additions of CaCl2. Conclusions ItispossiblethatthesoilsintheSHFarenutrientlimited, considering that they have virtually no top organic layer (wheremostofthe nutrientsare found inTHFsoils), and thata betterresponse,thoughnotalwayssignificant,was observed for SHF soils than for THF soils when nutrients were added. Seedling mortality was less in the SHF than in THF when N, P or NPK + CaCO3 were Plant Ecol (2007) 192:209–224 221 123
  14. 14. added, whilst the shoot and root mass were higher in SHF than in THF soils when NPK + CaCO3 were added. There was little evidence of N or P limitation, as generally suggested for acidic tropical soils, as the chief cause of poor plant growth in SHF and THF. It is possible to speculate that there was some evidence of toxic effects of soil pH and secondary compounds, as illustrated by the slight negative responses to the inclusion of humus layer in the pots with heath forest soils, and by the largely positive response to the addition of CaCO3 to the soils. However, the question of limiting factors for plant growth in heath forest soils is still an unresolved one, and, thus, the view of Whitmore (1984) that heath forests occur on sites which have a number of unfavourable characteristics, acting together or sepa- rately,issubstantiated.Evennotbeingfrequent,drought may occur; the extremely acid soils, with pH <4 at surface would be toxic to many plants; the soil has low amounts of Al and Fe sesquioxides, and consequently a low ability to absorb H+ ; phenols occur at high levels in leaves and litter, leaching into the soil; and, the amounts of nutrients in fine litter are low and slowly cycling. All these severe conditions, together or separately, restrict the production of heath forest and select only those species which are resistant to its many adverse condi- tions. Acknowledgements We wish to thank Claudio Yano and Cilene Palheˆta Soares for helping in the laboratory and in the field; two anonymous reviewers and Laszlo Nagy provided helpful comments to improve the manuscript. The work was funded by INPA/DFID (National Institute for Amazonian Research/ Department for International Development, UK) through the project BIONTE (Biomass and Nutrients in the Tropical Rain Forest) and by the European Community through the project ‘Organic Matter as Basis for Sustainable Use of Soils in Amazon’. References Anderson AB (1981) White-sand vegetation of Brazilian Amazonia. Biotropica 13:199–210 Anghinoni I, Volkweiss SJ (1984) Recomendac¸o˜es de uso de fertilizantes no Brasil. In: Espinoza W, Oliveira AJ (eds) Anais do simpo´sio sobre fertilizantes na agricultura Bra- sileira. EMBRAPA, Brası´lia Attiwill PM, Adams MA (1993) Nutrient cycling in forests. 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