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FEC534.fm Page 378 Friday, May 4, 2001 3:00 PM
Functional
Ecology 2001
15, 378 – 387
Leaf respiration in two tropical rainforests: constraints
on physiology by phosphorus, nitrogen and temperature
Blackwell Science, Ltd
P. MEIR,*† J. GRACE* and A. C. MIRANDA‡
*Institute of Ecology and Resource Management, University of Edinburgh, The King’s Buildings, Mayfield Road,
Edinburgh EH9 3JU, UK, and ‡Departamento de Ecologia, Universidade Nacional de Brasilia, 70910-900, Brasilia
DF, Brazil
Summary
1. Leaf respiration is a major component of the terrestrial carbon cycle, but is poorly
quantified for tropical forests. We measured dark respiration, R, and nutrient concentration (nitrogen, N and phosphorus, P) of leaves within two forest canopies: in
Reserva Jarú, south-west Brazil; and Mbalmayo Reserve, central Cameroon. The data,
expressed on a leaf area basis (Ra, Na, Pa ) and a leaf mass basis (Rm, Nm, Pm ), were
used to quantify the temperature sensitivity of R and to test the hypothesis that leaf
metabolism is more strongly constrained by phosphorus than by nitrogen in these
lowland rainforests.
2. Leaf respiration rate (Ra, at 25 °C) at Jarú was nearly half that at Mbalmayo (the
range in Ra from near the ground to the upper canopy was 0·11–0·78 µmol m–2 s–1 at
Jarú versus 0·22–1·19 µmol m–2 s–1 at Mbalmayo), and the mean Q10 for respiration at
each site was 2·3 ± 0·9 (1 SD) and 2·0 ± 0·5 (1 SD), respectively. There were significant
differences (P < 0·01) between sites in leaf phosphorus concentration, but not in
leaf nitrogen concentration: Pm was very low at Jarú (0·2–0·7 mg g–1) but higher at
Mbalmayo (0·5–2·4 mg g–1), whilst Nm was similar at both forests (10–45 mg g–1).
3. Rm was not significantly associated with canopy position or specific leaf area (SLA,
m2 g–1) in either forest, but a significant relationship between SLA and Nm was found
for both sites (P < 0·05), consistent with existing data. At Jarú, Rm was strongly related
to Pm (P < 0·001) and less strongly related to Nm (P < 0·05), but at Mbalmayo, Rm was
not significantly related to either Pm or Nm.
4. Ra was linearly related to Na and Pa at both sites (P < 0·01), principally because
of changes in leaf mass per area (LMA, g m–2) associated with canopy position. At
Mbalmayo, LMA explained 70% of the variation in Ra, but only 20% at Jarú. For Jarú,
the strongest relationship with Ra was obtained by combining LMA with Pm in a
multiple regression (r2 = 0·53); further inclusion of Nm did not improve the regression.
At Mbalmayo neither Nm or Pm improved the regression of Ra on LMA.
5. These results indicate a strong influence of LMA on the relative rates of Ra within the
vertical gradient of each canopy. They also suggest that at Jarú Pm constrains respiration more strongly than Nm, and further, that the very low Pm at Jarú may explain the lower
absolute values of respiration there relative to Mbalmayo, where Pm was higher. The
leaves at both sites are typical of lowland tropical rainforests in not having particularly low
Nm, and consistent with this, Nm was a weaker predictor of respiration than Pm or LMA.
Key-words: Leaf mass per area, leaf nitrogen, leaf phosphorus, nutrient constraints, Q10, temperature sensitivity
Functional Ecology (2001) 15, 378 – 387
Introduction
The dark respiration of leaves plays a key role in the
carbon economy of plants, but is poorly understood
© 2001 British
Ecological Society
†Author to whom correspondence should be addressed. E-mail:
[email protected]
in comparison to photosynthesis. Leaf respiration in
forest canopies may consume 9–22% of gross primary
production, and comprise 50–70% of above-ground
(autotrophic) respiration (Linder 1985; Malhi et al.
1999; Yoda 1983). This large component of the carbon
cycle is also sensitive to temperature and nutrient
availability, and its consequent variation in response
378
FEC534.fm Page 379 Friday, May 4, 2001 3:00 PM
379
Leaf respiration in
tropical forests
to climate can be critical in determining the carbon
balance of vegetation (Ryan 1991).
The rates of dark respiration, R, and maximum
photosynthesis, Amax, are strongly correlated in leaves
on a mass and area basis (Amthor 1989). These physiological parameters are also closely tied to leaf nutrient
concentration (James 1953), and a strong correlation
between Amax and leaf nitrogen concentration, N, has
been found amongst different species and biomes,
especially when expressed on a dry-mass basis (e.g. Field
& Mooney 1986; Reich et al. 1997). More recently, a
similar relationship has also been reported between
N and R (Reich et al. 1998). However, a significant
relationship between leaf physiological capacity (e.g.
Amax ) and leaf phosphorus concentration, P, has rarely
been observed in temperate, e.g. Pinus (Reich & Schoettle
1988) or tropical forests (e.g. Raaimakers et al. 1995).
This may reflect either a lack of studies in appropriate
regions, or the lack of a phosphorus constraint.
A central role for nitrogen in determining R and
Amax is well recognized (Kawahara et al. 1976; Reich
et al. 1998; Ryan 1995), although a few studies have
shown no correlation (e.g. Byrd et al. 1992). Respiratory
and photosynthetic enzymes are nitrogen-rich and
energetically expensive to maintain: 30–50% of leaf
nitrogen is found in Rubisco (Lawlor 1993), and 50–
60% of maintenance respiration is used in protein
turnover (Penning de Vries 1975). However, phosphorus
also influences productivity (Smeck 1985) and may
be the key limiting nutrient, in place of nitrogen, in
lowland tropical rainforests where soils are highly
weathered, phosphorus availability is very low, and
nitrogen is relatively abundant (Tanner et al. 1998;
Vitousek & Sanford 1986). In addition to its requirement in nucleic acid and protein structures, phosphorus
is needed for the phosphorylation of ADP in respiration (Amthor 1989) and for the production of triose
phosphate, the principal chloroplastic export product
(Stitt 1990). Deficiencies in phosphorus can therefore
be expected to influence physiological capacity, and do
limit the rates of RuBP regeneration and CO2 assimilation (Jacob & Lawlor 1992; Kirschbaum & Tomkins
1990).
For whole plants, true nutrient limitation is shown
only if the rate of a (growth) process is increased by the
addition of that nutrient (Chapin et al. 1986; Tanner
et al. 1998). However, such fertilization experiments
may not always be conclusive. Some early successional
species in tropical rainforest respond more to phosphorus
supplements than do late successional species, whilst
others, apparently adapted to low phosphorus availability, may not be capable of responding to nutrient
supplements, making nutrient limitation more difficult
to identify (e.g. Huante et al. 1995; Veenendaal et al.
1996). In these latter circumstances a longer-term change
in community composition may be a possible response
to a change in nutrient availability (Berendse 1993).
In the absence of clear experimental results, data on
tissue nutrient concentration, physiological activity and
minimal critical requirements can provide an indication
of the relative constraints imposed by different nutrients
in natural systems (e.g. Marschner 1995; Raaimakers
et al. 1995).
In this study we present data on dark respiration
rates and the concentrations of nitrogen and phosphorus
in leaves from the canopies of two tropical rainforests,
in Brazil and Cameroon. In addition to measuring the
temperature response in leaf respiration, we investigated
the extent to which respiration is constrained by nitrogen
or phosphorus, and tested the hypothesis that if phosphorus is more limiting than nitrogen, as has been
suggested for many lowland rainforests (e.g. Martinelli
et al. 1999; Tanner et al. 1998), then we should observe
a stronger influence of leaf phosphorus concentration
than nitrogen concentration on leaf respiration rate.
Materials and methods
 
The site characteristics for each forest are summarized
in Table 1. The first site was at Jarú Biological Reserve,
Rondonia State, south-west Brazil (10°05′ S, 61°55′ W)
and is referred to here as ‘Jarú’. The forest is classed as
undisturbed open forest grading to dense forest in places
(IBGE 1993). The second site was at the Mbalmayo
Reserve, Central Province of Cameroon (3°23′ N, 11°30′ W)
and is referred to here as ‘Mbalmayo’. This is a secondary deciduous forest that was selectively logged in 1988
(Lawson 1995).
Table 1. Site characteristics for Reserva Jarú, Brazil (undisturbed forest) and Mbalmayo Reserve, Cameroon (secondary forest).
© 2001 British
Ecological Society,
Functional Ecology,
15, 378 – 387
Character
Jarú, Brazil
Mbalmayo, Cameroon
Dominant tree families
Mean canopy height (m)
Leaf area index (m2 m–2)
Total soil organic carbon (%)
Total soil nitrogen (%)
Total soil phosphorus (%)
Rainfall (mm year–1)
Above-ground biomass (t ha–1)
Moraceae, Leguminoseae, Palmeae
35*
4·0*
1·18†
0·10†
0·011†
1900§
220*
Sterculiaceae, Ulmaceae, Leguminoseae
36*
4·4*
1·83‡
0·16‡
0·018‡
1520‡
90*
Sources for data: *Meir, 1996; †Amaral Filho et al. (1978); ‡Ngeh (1989); §Culf et al. (1996).
FEC534.fm Page 380 Friday, May 4, 2001 3:00 PM
380
P. Meir et al.
Table 2. Species sampled at Jarú, Brazil and Mbalmayo, Cameroon
Species
Family
Ra
M
H
Jarú, Brazil
Maximiliana maripa (Corre Serra) Drude
Naucleopsis krunni (Standl) C.C. Berg
Theobroma microcarpum Mart.
Erythroxylum cf. macrophyllum Cav·
Leonia glycicarpa Ruiz
Leonia glycicarpa Ruiz
Derris pterocarpa (DC) Killip
Protium polybotrium (Turcz) Engl.
Inga sp.
Strychnos amazonicus Krukoff *
Inga sp.
Cedrela odorata L.
Palmae
Moraceae
Sterculiaceae
Erythroxylaceae
Violaceae
Violaceae
Leguminoseae
Burseraceae
Leguminoseae
Loganaceae
Leguminoseae
Meliaceae
0·11 (0·03)
0·13 (0·02)
0·24 (0·03)
0·22 (0·06)
0·24 (0·03)
0·23 (0·04)
0·37 (0·07)
0·39 (0·14)
0·43 (0·06)
0·78 (0·08)
0·57 (0·01)
0·55 (0·03)
2
1
1
2
2
2
1
2
1
2
1
1
1
1
1
3
10
16
20
20
26
30
32
36
Mbalmayo, Cameroon
Hypsodelphis violacea (Ridl.) M-Redh
Dichapetalum sp.
Afromomum giganteum (Oliv. & Harb.) K. Schum.
Trichilia sp.
Musanga cecropioides R. Br.
Haumania dankelmaniana M-Redh.
Staudtia stipitata Warb.
Celtis adolfi-friderici Engl.
Celtis adolfi-friderici Engl.
Musanga cecropioides R. Br.
Musanga cecropioides R. Br.
Amphimas pterocarpoides Harms.
Amphimas pterocarpoides Harms.
Marantaceae
Dichapetalaceae
Zingiberaceae
Meliaceae
Moraceae
Marantaceae
Myristicaceae
Ulmaceae
Ulmaceae
Moraceae
Moraceae
Leguminoseae
Leguminoseae
0·22 (0·09)
0·31 (0·11)
0·61 (0·06)
0·39 (0·04)
0·55 (0·08)
0·51 (0·10)
0·40 (0·11)
0·50 (0·02)
0·53 (0·01)
0·90 (0·02)
1·19 (0·02)
0·71 (0·03)
0·83 (0·04)
2
U
2
1
2
2
1
1
1
2
2
1
1
1
1
1
1
1
3
7
12
14
22
26
36
40
Ra (±1 SD; n = 2 – 4) is mean leaf respiration rate (µmol m–2 s–1), corrected to 25 °C as described in Materials and methods.
M denotes likely arbuscular mycorrhizal associations for each species: 1 = known, 2 = probable, U = unknown; no likely nonor ectomycorrhizal species were identified (I. Alexander, personal communication); H, height (m); *denotes climber species.
-  
© 2001 British
Ecological Society,
Functional Ecology,
15, 378 – 387
Measurements were made on fully expanded (but not
senescing) leaves from throughout the vertical profile
of each canopy. Access to the canopy was via a throughcanopy tower, and measurements were made at all
available heights on adjacent leaves (n = 2–4) of each
accessible species (Table 2). Gas-exchange measurements
were made under similar climatic conditions (clear skies,
low wind speeds) in Jarú, Brazil on the nights of 25
May and 4 June 1993, and in Mbalmayo, Cameroon,
on 11 and 22 March 1994.
Respiration measurements were made at ambient
temperature and humidity by sealing attached leaves
inside a chamber (Licor, Nebraska, USA) connected
in a closed circuit to an infra-red gas analyser (Licor
6200); leaf temperature was measured using a calibrated
leaf-chamber thermocouple. Where possible, measurements were made at 2 h intervals during the night.
Measurements (three to six) were made during the night
for a subset of leaves, and for these leaves (six species,
two to four leaves per species; Table 3), the temperature
response in respiration was also determined. Leaves
were kept in the chamber for 60 s, during which the
CO2 concentration rose to ≈50 times the sensitivity of
the gas analyser (≈5·0 µmol mol–1; Licor 1990). The
efflux rate of CO2 from the leaves was assumed to
represent the rate of leaf respiration and was calculated
on an area basis according to:
Ra (µmol m–2 s–1) = ∆[CO2]Vch /(AchVT)
eqn 1
where ∆[CO2] is the change in concentration of CO2
in chamber (µmol mol–1 s–1), Vch and Ach are chamber
volume (m3) and enclosed leaf area (m2), respectively,
and VT is the volume of one mole of gas at ambient
temperature and pressure.
    

Fresh leaf area was measured using a precalibrated
Delta-T leaf-area meter (Delta-T Devices Ltd, Cambridge, UK). A leaf corer was used to obtain 10–30
discs (diameter = 16 mm) from each fresh sample, and
the leaf material was oven-dried at 70 °C to constant
mass. Specific leaf area (SLA, m2 g–1) determinations
were made using a precision balance (Sauter Re1614,
Albstadt, Switzerland; maximum sensitivity = 0·1 mg).
Leaf nitrogen and phosphorus concentrations for the
leaves from Mbalmayo were determined using an acid
digestion followed by colorimetric analysis (Grimshaw
et al. 1989), and for those from Jarú using a Carlo –Erba
elemental analyser and an ammonium molybdate
FEC534.fm Page 381 Friday, May 4, 2001 3:00 PM
381
Leaf respiration in
tropical forests
Table 3. Temperature responses for night-time leaf respiration
at Jarú and Mbalmayo
Species
Q10
r2
Jarú, Brazil
Maximiliana maripa
Theobroma microcarpum
Naucleopsis krunnii
Inga sp.
Leonia glycicarpa
Derris pterocarpa
Mean
1·5 (0·5)
2·1 (0·2)
2·9 (0·8)
1·7 (0·7)
1·9 (0·3)
4·1 (1·8)
2·3 (0·9)
0·66 (0·23)
0·56 (0·14)
0·64 (0·24)
0·70 (0·15)
0·84 (0·20)
0·47 (0·31)
0·65 (0·11)
Mbalmayo, Cameroon
Amphimas ptercarpoides
Musanga cecropoides
Afromomum giganteum
Staudtia stipitata
Hypsodelphis violacea
Celtis adolphi-friderici
Mean
1·8 (0·2)
1·6 (0·3)
2·1 (0·5)
3·1 (0·4)
1·7 (1·1)
1·9 (0·6)
2·0 (0·5)
0·87 (0·10)
0·65 (0·23)
0·58 (0·16)
0·54 (0·18)
0·57 (0·42)
0·41 (0·35)
0·60 (0·14)
Q10 is the multiple by which Ra (µmol m–2 s–1) increases in
response to a 10 °C increase in temperature, obtained by
fitting Equation 2 (see Materials and methods); r 2 is the
coefficient of determination of the fitted model. Values are
means from temperature responses of two to four leaves per
species (±1 SD).
method (Allen et al. 1974). SLA was used to convert
mass-based nutrient concentrations (Nm, Pm; mg g–1)
to an area basis (Na, Pa; g m–2) and to calculate the massbased respiration rate (Rm, nmol m–2 s–1) from Ra.
 
An exponential model was fitted to the temperature
response data. This type of model is frequently used to
represent the temperature response in respiration (e.g.
Amthor 1989; Bolstad et al. 1999; Landsberg 1986),
and was chosen to facilitate comparison with other
studies, although the relationship is almost linear over
small temperature ranges. The model used was:
Ra = R0 ekT
eqn 2
where T is temperature in °C, R0 is Ra at 0 °C and k is
the temperature sensitivity in Ra. The relative rate at
which Ra increases with an increase in temperature
of 10 °C is termed the Q10 (Q10 = e10k ). Respiration,
leaf-nutrient concentration and SLA values were
compared using single and multiple linear regression
analyses. To make an appropriate comparison with
area-based leaf nutrient concentrations, SLA (cm2 g–1)
was converted into its reciprocal, leaf mass per area
(LMA; g m–2). As an area-based description of leaf
nutrient content (g m–2) comprises LMA and the massbased value of that nutrient concentration (g g–1),
multiple linear regression analysis (using a stepwise
procedure) was restricted to the combination of LMA
and mass-based nutrient concentrations. Differences
between sites or species were tested using t-tests.
Statistical analyses were done using SPSS v.6.
Results
Ten species in each canopy were sampled (Table 2),
including individuals from the dominant families of
each forest. The list includes species with suspected
arbuscular mycorrhizal associations, but none with
ectomycorrhizal associations.
Leaf temperatures during dark respiration measurement ranged from 21–25 °C at Jarú and 19–24 °C at
Mbalmayo, dropping during the night by up to 4 °C at
the top of the canopy and by up to 2 °C near the
ground. The fitted exponential model explained 47 – 87%
of the variance in Ra with temperature, and yielded
Q10 values between 1·5 and 4·1 for individual species,
with a mean for each forest close to 2 (Table 3). Ra
was corrected to 25 °C using the individual species
temperature-response functions where available, or
by applying the mean Q10 for each forest for species
where a temperature-response function was not
available. All measured respiration rates, whether Ra
or Rm, are reported here corrected to 25 °C.
    
     

© 2001 British
Ecological
Society,
Fig.
1. Changes
in leaf respiration (Ra or Rm at 25 °C) and SLA with height, at Jarú (d) and
Mbalmayo
(s). Error bars are ±1 SD for all leaves measured per level, one to four species
Functional Ecology,
per
level,
n per species = 2 – 4. (a) Ra, µmol m–2 s–1; (b) Rm, nmol g–1 s–1; (c) SLA, cm2 g–1.
15, 378
– 387
Overall Ra (µmol m–2 s–1) was significantly smaller at
Jarú than at Mbalmayo (t56 = 5·3, P < 0·001; Fig. 1a),
and Ra was significantly larger in the upper canopy
(above 25 m) than near the ground (below 5 m) in both
forests (t6 = –5·4, P < 0·01 at Jaru; t6 = –3·1, P < 0·01 at
Mbalmayo; Table 2). Ra by species and height (Table 2)
ranged from 0·78 (upper canopy) to 0·11 µmol m–2 s–1
(1 m) at Jarú; at Mbalmayo Ra ranged from 1·19 (upper
canopy) to 0·22 µmol m–2 s–1 (1 m). Mass-based respiration, Rm (nmol g–1 s–1), did not vary with height in either
FEC534.fm Page 382 Friday, May 4, 2001 3:00 PM
non-palms at the same height (t5 = – 2·0, P > 0·05).
Although SLA was slightly larger at Jarú, it decreased
with height in both forests from ≈200 cm2 g–1 at 1 m to
≈90 cm2 g–1 at the top of the canopy (Fig. 1c).
382
P. Meir et al.
   ,
  ,    
   
Fig. 2. Specific leaf area (SLA), leaf mass per unit area (LMA), nutrient
concentrations and respiration rate: Jarú (d) and Mbalmayo (s). (a–c) Variation in Na
(g m–2), Pa (g m–2) and Ra at 25 °C (µmol m–2 s–1) with LMA (g m–2); (d–f ) variation in
Nm (mg g–1), Pm (mg g–1) and Rm at 25 °C (nmol g–1 s–1) with SLA (cm2 g–1). Also plotted
in (d) are data from Reich et al. (1998) for a rainforest in Venezuela (crosses) and a
relationship (solid line) reported by Schulze et al. (1994), where Nm = 0·157 SLA. Also
plotted in (f ) (solid line) is an Rm–SLA relationship reported by Reich et al. (1998).
Values for p and r 2 in each graph refer to regression results for each data set.
forest (Fig. 1b), though Rm was also smaller at Jarú
(t56 = 6·41, P < 0·001). Differences among species were
mostly confounded by position in the canopy, though
a climber, Strychnos amazonicus, had a significantly
higher rate relative to nearby tree species (t2 = 4·8,
P < 0·05; Table 2); and a palm, Maximilliana maripa,
had a (non-significantly) lower respiration rate than
For Mbalmayo, significant regressions (P < 0·001) were
obtained for Na and Pa on LMA, and for Nm and Pm on
SLA (Fig. 2). At Jarú the same relationships were either
non-significant (Na on LMA; P = 0·26) or less significant
than at Mbalmayo (P < 0·05 for all other regressions;
Fig. 2). Pa and Pm were significantly smaller at Jarú than
at Mbalmayo (Pa: t56 = 12·1; P < 0·001; Pm: t56 = 9·6;
P < 0·001; mean Pm was 0·44 mg g–1 at Jarú and
0·71 mg g–1 at Mbalmayo), but leaf nitrogen concentrations, on the other hand, were similar at both sites,
with Na between 0·9 and 3·0 g m–2 and Nm between 10
and 40 mg g–1 (Fig. 2).
Respiration (Ra ) was significantly associated with
LMA at both forests (P < 0·05 for Jarú, P < 0·01 for
Mbalmayo; Fig. 2c; Table 4), but the slopes of the
regressions were not significantly different from each
other [slopes: Jarú = 0·004 (±0·002 SE), Mbalmayo =
0·008 (±0·002 SE)]. In contrast, Rm was not related to
SLA at either site (P > 0·2; Fig. 2f). Significant regressions for Ra on Na and Pa were obtained for both sites
(P < 0·01; Fig. 3a,b). For Rm (Fig. 3c,d) there was no
significant relationship with Nm or Pm at Mbalmayo,
but at Jarú there was, with Pm explaining more of the
variance in Rm than Nm (Fig. 3c,d).
LMA alone explained 20% of the variance in Ra for
the leaves at Jarú (Table 4). In a stepwise multiple
regression for the Jarú data, incorporating LMA, Nm
and Pm as variables, Nm was less significant than Pm
in combination with LMA alone, and became nonsignificant when combined with LMA and Pm (Table 4).
For Mbalmayo, LMA explained 70% the variance in
Table 4. Regression results for stepwise multiple linear regressions of Ra (µmol m–2 s–1) on LMA, Pm and Nm for Jarú (J) and
Mbalmayo (M), where Ra = a + bLMA + cNm + dPm
© 2001 British
Ecological Society,
Functional Ecology,
15, 378 – 387
Site
Intercept
a
LMA
b
J
J
J
J
M
M
M
M
J+M
J+M
J+M
J+M
0·074
– 0·479*
– 0·413**
– 0·496**
0·031
0·043
– 0·014
0·017
– 0·002
– 0·523**
– 0·355***
– 0·526
0·004*
0·006***
0·006***
0·006***
0·008***
0·008***
0·008***
0·008***
0·007***
0·009***
0·008***
0·009***
Nm
c
Pm
d
0·014**
0·004
0·773***
0·629*
– 0·0004
– 0·001
0·026
0·036
0·014**
0·007
0·324***
0·292***
n
r2
P (overall regression)
30
30
30
30
28
28
28
28
58
58
58
58
0·20
0·42
0·53
0·52
0·70
0·68
0·68
0·67
0·35
0·42
0·60
0·60
0·01
<0·0001
<0·0001
<0·0001
<0·0001
<0·0001
<0·0001
<0·0001
<0·0001
<0·0001
<0·0001
<0·0001
LMA (g m–2 ), Pm (mg g–1) and Nm (mg g–1) are regression variables; *, ** and *** indicate significance of variable where
P < 0·05, 0·01 and 0·001, respectively; n is the number of leaves measured; r 2 is adjusted for multiple regressions.
FEC534.fm Page 383 Friday, May 4, 2001 3:00 PM
may reflect true species differences, as similar variation
in k has been found elsewhere in temperate forest and
grassland species (Amthor 1989; Bolstad et al. 1999;
Ryan 1991). It is also possible that the measurements
included an unquantified component of respiration in
addition to the true ‘maintenance’ value, such as that
required for biochemical export processes, although
this is unlikely because non-senescing leaves were selected
(McCree 1970; Thornley & Cannell 2000). Consistent
with this view, our data are exceeded by maintenance
respiration rates reported for the leaves of crops and
grasses (2–16 versus 7–30 nmol g–1 s–1 at 25 °C; Amthor
1989), but with the exception of the slowest rates they
are similar to those found for temperate hardwood
trees (4–13 nmol g–1 s–1 at 25 °C; Mitchell et al. 1999).
383
Leaf respiration in
tropical forests
     
 
Fig. 3. Leaf nutrient concentration and respiration: Jarú (d) and Mbalmayo (s). (a,b)
Ra (µmol m–2 s–1), Na (g m–2) and Pa (g m–2); (c,d) Rm (nmol g–1 s–1), Nm (mg g–1) and Pm
(mg g–1). Also plotted in (c) (solid line) is an Rm–Nm relationship from Reich et al.
(1998). Regression equations for each data set are specified in each graph.
Ra, but the addition of Nm and Pm into the regression
did not improve the fit: Nm and Pm were non-significant
variables in all formulations (Table 4). Overall, respiration was best predicted on an area basis (Ra ), using
LMA alone at Mbalmayo (r 2 = 0·70) and LMA and Pm
together at Jarú (r 2 = 0·53), and also for the combined
data set of both forests (r 2 = 0·60; Table 4).
Discussion
       

© 2001 British
Ecological Society,
Functional Ecology,
15, 378 – 387
Few published data exist for dark respiration of leaves
in tropical forests, although Reich et al. (1998) reported
values for a terra firme rainforest in Venezuela of
0·7–1·2 µmol m–2 s–1 (at 25 °C), a narrower range than
presented here (0·1–1·2 µmol m–2 s–1), with a higher
minimum.
The mean Q10 for respiration was close to 2 at Jarú
and Mbalmayo, although interspecific variation was
noticeable (Table 3). This variation may have resulted
from uncertainty in fitting the temperature-response
parameter (k) over a small temperature range, but it
Nitrogen concentration and respiration (Nm and Ra )
were significantly related to the changes in SLA and
LMA accompanying the light gradient within both
canopies (Fig. 2). Although the high species diversity
at each site made it difficult to determine how representative each sample was of the canopies as a whole,
the outcome is strongly consistent with other studies of
N and Amax in other temperate and tropical broadleaf
canopies (e.g. Carswell et al. 2000; Ellsworth & Reich
1993). Unlike Ra, Rm did not scale with SLA at either
forest, and was significantly related to Nm only at Jarú
(Fig. 3). These results contrast with a global data set
(Reich et al. 1998) where Rm was strongly correlated
with Nm. However, Reich et al. (1998) reported on sun
leaves only, and where a vertical canopy profile has
been sampled elsewhere, only a weak Rm–Nm relationship has been observed (Mitchell et al. 1999). Some
Rm : Nm ratios from (canopy-top) sun leaves at Jarú
and Mbalmayo are close to those predicted by Reich
et al. (1998), but lower in the vertical profile, large variation in SLA disrupts any relationship that may exist
between Nm and Rm (Figs 2f, 3c). Strong Rm–Nm correlations have been found among subalpine and boreal trees
and shrubs (e.g. Ryan 1995), and an additional explanation for the difference in outcomes may be that such
multistand studies incorporate a wider range of species
groupings (conifer, broadleaf, etc.), and hence of LMA
and Nm, than is usually found in a single canopy
(Mitchell et al. 1999). The use of a simple Rm–Nm (or
an Amax–Nm ) relationship based only on measurements
of sun leaves may therefore overestimate respiration (or
photosynthesis) in the middle and lower canopy of a
forest.
The significant relationship at Jarú and Mbalmayo
between SLA and Nm (Fig. 2d) agrees closely with a
global correlation reported by Schulze et al. (1994), and
with data from the Venezuelan rainforest reported by
Reich et al. (1998). The conservation of this relationship
among canopies and widely differing species contrasts
with the weaker Rm–Nm relationships described above,
FEC534.fm Page 384 Friday, May 4, 2001 3:00 PM
384
P. Meir et al.
Fig. 4. The mass- and area-based relationships between photosynthetic capacity, Amax,
from McWilliam et al. (1996) and Meir (1996), and mean respiration rate. Data points
from both sites are mean values for individual species at the same height; Jarú (d) and
Mbalmayo (s). Values for P and r 2 in each graph refer to regression results for
combined-site data sets.
Table 5. Mean leaf nitrogen (Nm, mg g–1) and phosphorus (Pm, mg g–1) concentrations
from different individual rainforest sites (*) and the range in Nm and Pm for three classes
of rainforest, grouped by soil type (†)
Individual forest site*
or forest class†,
grouped by soil type
Nm
Pm
Reference
*SW Amazon
*Central Cameroon
*Central Amazon
*Central Amazon
*Central Amazon
25·0
25·7
27·9
18·0
15
0·44
1·15
0·7
0·54
0·51
*Venezuela
*Venezuela
*Venezuela
†‘Moderately fertile’
†‘Infertile’ (oxisol /ultisol)
†‘Very infertile’
(podsol /psamment)
14·5
11·6
12·7
24·5–25·4
12·7–19·3
7·4 –1·11
0·7
0·73
0·60
1·2–1·5
0·5 – 0·6
0·4 –1·2
This study
This study
Carswell et al. (2000)
Furch et al. (1989)
Ferraz et al.
(personal communication)
Reich et al. (1994)
Medina & Cuevas (1989)
Medina & Cuevas (1989)
Vitousek & Sanford (1986)
Vitousek & Sanford (1986)
Vitousek & Sanford (1986)
Vegetation was classified as ‘tall’ in the original references, with the exception of the
‘very infertile’ group of sites given by Vitousek & Sandford (1986), which was classified
as ‘low’.
© 2001 British
Ecological Society,
Functional Ecology,
15, 378 – 387
and indicates a general structural requirement for nitrogen. In some stands nitrogen may be allocated to structural compounds such as lignin in response to differential
within-canopy water stress (Niinements & Kull 1988).
However, leaves with larger SLA also had a larger Nm
(Fig. 2d); investment in epidermal thickening of canopytop leaves may increase leaf mass per unit area at a small
nitrogen cost. Alternatively, high nitrogen investment at
low respiratory cost may reflect the presence of nonstructural nitrogen stored in those leaves with large
Nm and SLA values. This has been proposed for some
species (e.g. Cromer et al. 1993; Field & Mooney
1986), and possible storage sites include defence
compounds and Rubisco (Amthor 1989; Millard 1988;
Stitt & Schuze 1994).
The two forests differed in the variables that best
predicted leaf respiration. Although Na and Pa were
significantly related to Ra (Fig. 3), the discussion is
restricted here to the components of these variables,
LMA, Nm and Pm. At Mbalmayo, LMA explained 70%
of the variation in Ra, with nutrient concentration
contributing no additional predictive power to the
regression. In contrast, at Jarú Pm was most strongly
related to respiration, explaining the most variation
in Ra (33%); LMA improved the coefficient of determination by a further 20%, but Nm was non-significant
(Table 4). The small Pm at Jarú may explain the lower
Ra values at that site: Pm significantly below 0·7–
1·0 mg g–1, as found at Jarú but not at Mbalmayo,
limits leaf photosynthesis and respiration in tropical
trees and herbs (Cromer et al. 1993; Marschner 1995,
Zech & Drechsel 1992). Small Pm or Ra at Jarú was not,
however, associated with low SLA or LMA, relative to
Mbalmayo (Fig. 2). Consequently, whilst Pm may have
acted as a key constraint on the absolute respiration
rate at Jarú, the relative distribution of Ra within the
vertical canopy profile in both forests was most
strongly influenced by LMA.
It is likely that the low Ra at Jarú also reflected a
smaller photosynthetic capacity (Amthor 1989). Mean
Amax values from McWilliam et al. (1996) and Meir
(1996) show significant linear relationships between
Amax and R for individual species at Mbalmayo and
Jarú (Fig. 4). Respiration was 8–10% of Amax, and the
data imply a range in the ratio of Amax : leaf phosphorus
between 2 and 5 mmol CO2 mol–1 P s–1. This phosphorususe efficiency exceeds that for Pinus (Reich & Shoettle
1988), but is not exceptionally high in comparison
with other tropical species (3–8 mmol CO2 mol–1 P s–1;
Raaimakers et al. 1995). The corresponding nitrogen-use
efficiency is relatively low for both sites (20–70 µmol
CO2 mol–1 N s–1), in keeping with the notion that nitrogen
is relatively abundant in tropical forests in comparison
with temperate forests (Martinelli et al. 1999). Although
nitrogen-fixing species were present in both forests
(the Leguminoseae is a dominant family at both sites),
ectomycorrhizal species were not found amongst
the sampled species, perhaps also indicating a relative
abundance of nitrogen (Buscot et al. 2000).
Leaf phosphorus and nitrogen stoichiometry therefore appear to be relatively well conserved at both sites,
even where Pm is low. However, why Pm should be higher
at Mbalmayo is unclear, as both sites have low soil
phosphorus concentrations and a similar number of
species considered to host arbuscular mycorrhizal (AM)
associations (Table 2). Although the presence of AM
species may imply adaptation to low phosphorus availability (Moyersoen et al. 1998), those species with AM
did not have significantly larger Ra or Pm (paired t-test
for AM species at the same height at both sites Ra:
t3 = –0·60, P = 0·59; Pm: t3 = 0·03, P = 0·97). On the
other hand, the slightly larger soil phosphorus concentration at Mbalmayo (Table 1) conceivably reflects
higher phosphorus availability, as the previous disturbances at Mbalmayo (Lawson 1995) could have
led to a slow release of available nutrients through the
decomposition of organic matter (cf. Lloyd et al. 2001).
FEC534.fm Page 385 Friday, May 4, 2001 3:00 PM
385
Leaf respiration in
tropical forests
Compared with other tropical forests in the Amazon
region and elsewhere, the Pm values at Jarú appear to
be especially small, particularly for high forest (Table 5).
Whether or not those species at Jarú with small respiration rates and small Pm are capable of responding to
higher phosphorus availability is unclear (Veenendaal
et al. 1996), but with mean Pm < 0·5 mg g–1, the leaves
are probably close to being critically low in phosphorus
(Cromer et al. 1993; Zech & Drechsel 1992) and may
represent an extreme point on the spectrum of leaf
metabolic capacity in tall lowland rainforests.
Conclusions
Changes in LMA associated with the vertical radiation
gradient in both forest canopies strongly influenced
the relative response in leaf respiration rate to changes
in leaf nutrient concentration. Leaf stoichiometry and
respiratory metabolism at both sites were fairly well
conserved in terms of phosphorus-use efficiency or
temperature response in comparison to other studies.
However, exceptionally low Pm at Jarú appeared to
constrain respiration more strongly than Nm, and is
probably responsible for the low absolute rates of
respiration at Jarú relative to Mbalmayo, where Pm was
higher. Nitrogen was relatively abundant in leaves at
both sites and was not the best predictor of respiration
for either canopy.
Acknowledgements
We are grateful to two research programmes for financial
and infrastructural support in Brazil and Cameroon: the
Brazil–UK ABRACOS project, supported by the UK
Overseas Development Administration (now DFID)/
Agencia Brasileira Cooperação, and the UK NERC
programme ‘Terrestrial Initiative for Global Environment Research’, TIGER (grant no. GST/02/065). We
gratefully acknowledge the support and help of local
collaborating institutions, including INCRA in Brazil
and ONADEF in Cameroon. We would also like to thank
L. Kruuk, L. Gormley, J. Lloyd, A. Gray, Y. Malhi and
F. Carswell for providing technical support or comments
on the manuscript, and to I. Alexander for providing
information on mycorrhizal associations of different
species.
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Received 20 December 2000; accepted 8 February 2000