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ORIGINAL PAPER
Soil acidity and nutrient deficiency in central Amazonianheath forest soils
Flavio J. Luizao Æ Regina C. C. Luizao ÆJohn Proctor
Received: 21 February 2007 / Accepted: 21 May 2007 / Published online: 21 June 2007
� 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 CaCl2or 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 � Campinarana � Heath forest �Nutrient limitation � 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. Luizao (&) � R. C. C. Luizao
Departamento de Ecologia, Instituto Nacional de
Pesquisas da Amazonia, Caixa Postal 478, 69011-970
Manaus, Amazonas, Brasil
e-mail: [email protected]
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
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 (Brunig 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 (Brunig 1968,
1970; Richards 1996). The four factors most com-
monly cited are: (i) drought (Brunig 1968; Klinge and
Medina 1979); (ii) waterlogging (Brunig 1968;
Bongers et al. 1985; Klinge and Medina 1979); (iii)
low nutrients (Brunig 1973, 1974; Jordan 1985;
Medina and Cuevas 1989; Richards 1996); and, (iv)
soil acidity and phenolics (Brunig 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
(2o360 S; 60o010 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 ha�1
in SHF and 24 in THF) compared with 82 species ha�1
in the LERF. Above-ground biomass was estimated at
71 Mg ha�1 in SHF, 152 Mg ha�1 in THF and
210 Plant Ecol (2007) 192:209–224
123
409 Mg ha�1 in LERF (Luizao 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 Luizao (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 (3�6 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: Luizao 1996, modified)
Depth*
(cm)
pHH2O N
(mg g�1)
C:N Ptotal
(mg g�1)
K+
(m-eqiv
100 g�1)
Na+
(m-eqiv
100 g�1)
Ca2+
(m-eqiv
100 g�1)
Mg2+
(m-eqiv
100 g�1)
CEC
(m-eqiv
100 g�1)
H+/Al3+
(m-eqiv
100 g�1)
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
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 248Cfor 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 ha�1 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
(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 (Luizao 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
to the control, one-way analyses of variance followed by
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
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
Ro
tom
ass
(gabg
1-)
vermiculite, on surface
vermiculite, 10 cm deep
sand, on surface
THF
0
2
4
6
8
10
KCl CaCO3 CaCl2 Urea NaH2PO4 Control
Roo
tm
ass
(gba
g1-)
LERF
0
2
4
6
8
10
KCl CaCO3 CaCl2 Urea NaH2PO4 Control
Treatments
tooR
sam
s(g
gab1-)
* *
**
** *
**
****** *****
**
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
aC
l 2C
aC
O3
C
PN
KI+
CaC
O3
Ctn oro
l
Gro
wth
nid
ex(f
ina
/lni
tiia
hlei
gh
t
SHF THF LERF
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
N P K
aC
l 2C
aC
O3
C
KP
NI+
CaC
O3
Ctnoro
l
Treatments
uS
vriv
laar
et
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
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 g�1 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
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 *
*
***
***
******
*** ***
***
tC
rl N +N
P
+N
K
+N
aC
CO
3
+N
aC
SO
4
+N
SO
4 P K
aC
CO
3
aC
SO
4
Na 2
SO
4N
a 2S
O4
Na 2
SO
4
So
lire
spria
t(
noi
µg
Cg
1-)
THF
0
30
60
90
120
tC
rl N +N
P
+N
K
+N
Ca
CO
3
+N
Sa
CO
4
+N
SO
4 P K O3
Ca
C
Sa
CO
4
So
lire
spir
ta
oi(
nµ
gC
g1-)
LERF
0
30
60
90
120
tC
rl N +N
P
+N
K
+N
aC
CO
3
+N
aC
SO
4
+N
SO
4 P K
aC
CO
3
aC
SO
4
Treatments
Soi
lres
pira
tion
(µC
g-g
)1
Fig. 3 Laboratory experiment: soil respiration (mg C g�1
oven-dry soil 10 d�1) 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
Ctr
l N
N+
P
N+
K
N+
Ca
CO
3
N+
Ca
SO
4
N+
SO
4 P K
Ca
CO
3
Ca
SO
4
Na 2S
O4
Na 2S
O4
Na 2S
O4
N m
iner
aliz
atio
n (µ
N g
-1)
N
min
eral
izat
ion
(µg
N g
-1)
N
min
eral
izat
ion
(µg
N g
-1)
***
***
***
***
***
***
THF
-120
-100
-80
-60
-40
-20
0
20
40
60
Ctr
l N
N+
P
N+
K
N+
Ca
CO
3
N+
Ca
SO
4
N+
SO
4 P K
Ca
CO
3
Ca
SO
4
***
***
***
***
****
**
***
LERF
-120
-100
-80
-60
-40
-20
0
20
40
60
Ctr
l N
N+P
N+K
N+C
aCO
3
N+C
aSO
4
N+S
O4 P K
CaC
O3
CaS
O4
***
***
***
***
***
***
***
***
Fig. 4 Laboratory experiment: net nitrogen mineralisation
(mg N g�1 oven-dry soil 10 d�1) 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
are not exceptionally low (Luizao 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
(Luizao 1996; Proctor 1999; Table 1). However, the
biomass estimated for the LERF (409 Mg ha�1),
slightly higher than the range reported for forests on
Oxisols in Amazonia (Jordan 1985) suggests that
-7
-5
-3
-1
1
3
5 SHF
tC
rl N +N
P
+N
K
+N
CO
3a
C +N
Sa
CO
4
+N
SO
4 P K
Ca
CO
3
Sa
CO
4
Na 2
SO
4N
a 2S
O4
Na 2
SO
4
Ne
tti
nr
ficia
tn
oi(µ
gN
1-)
-3
0
3
6
9
12 THF
tC
rl N +N
P
+N
K
+N
CaC
O3
+N
CaS
O4
+N
SO
4 P K
aC
CO
3
aC
SO
4
Net
intr
ific
taio
n(µ
Ng
g1-)
-5
0
5
10
15
20 LERF
tC
rl N +N
P
+N
K
+N
Ca
CO
3
+N
Ca
SO
4
+N
SO
4 P K
CO
3a
C
SO
4a
C
Treatments
eN
tnitr
fici
ta
noi
(µN
gg
1-)
***
***
***
***
***
***
***
***
Fig. 5 Laboratory experiment: net nitrification (mg N g�1
oven-dry soil 10 d�1) 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
Mor
tatily
u-N
rea C
Kl
aC
Cl 2
aC
CO
3
PN
K+
aC
O3
C
Con
rtol
Con
rtol
Con
rtol
SHF THF LERF
0
20
40
60
80
100
120
N-
ruae
NaH
2PO
4N
aH2P
O4
CK
l
aC
l 2C
aC
O3
C
PN
K+
aC
O3
C
Sooht
ibmo
(ssa
gm
2-)
0
20
40
60
80
100
N-
ruae
aN
H2
O4
P
CK
l
aC
l 2C
aC
O3
C
PN
K+
aC
O3
C
Treatments
Ro
moibto(
ssag
m2-)
Fig. 6 Glasshouse experiment: number of dead rice seedlings,
and shoot and root dry mass (g m�2) 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
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
(Luizao 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
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 ha�1) 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 Nino 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
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 l�1) 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
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 (Luizao 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,
Brunig (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 (Luizao 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
It is possible that the soils in the SHF are nutrient limited,
considering that they have virtually no top organic layer
(where most of the nutrients are found in THF soils), and
that a better response, though not always significant, 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
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, is substantiated. Even not being frequent, 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 Palheta 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’.
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