Content uploaded by Damien Bonal
Author content
All content in this area was uploaded by Damien Bonal on Nov 20, 2014
Content may be subject to copyright.
Abstract The interspecific variability of sunlit leaf car-
bon isotope composition (δ
13
C), an indicator of leaf in-
trinsic water-use efficiency (WUE, CO
2
assimilation
rate/leaf conductance for water vapour), was investigated
in canopy trees of three lowland rainforest stands in
French Guiana, differing in floristic composition and in
soil drainage characteristics, but subjected to similar cli-
matic conditions. We sampled leaves with a rifle from
406 trees in total, representing 102 species. Eighteen spe-
cies were common to the three stands. Mean species δ
13
C
varied over a 6.0‰ range within each stand, correspond-
ing to WUE varying over about a threefold range. Species
occurring in at least two stands displayed remarkably sta-
ble δ
13
C values, suggesting a close genetic control of spe-
cies δ
13
C. Marked differences in species δ
13
C values
were found with respect to: (1) the leaf phenology pattern
(average δ
13
C=–29.7‰ and –31.0‰ in deciduous-leaved
and evergreen-leaved species, respectively), and (2) dif-
ferent types of shade tolerance defined by features re-
flecting the plasticity of growth dynamics with respect to
contrasting light conditions. Heliophilic species exhibited
more negative δ
13
C values (average δ
13
C=–30.5‰) (i.e.
lower WUE) than hemitolerant species (–29.3‰). How-
ever, tolerant species (–31.4‰) displayed even more neg-
ative δ
13
C values than heliophilic ones. We could not pro-
vide a straightforward ecophysiological interpretation of
this result. The negative relationship found between spe-
cies δ
13
C and midday leaf water potential (Ψ
wm
) suggests
that low δ
13
C is associated with high whole tree leaf spe-
cific hydraulic conductance. Canopy carbon isotope dis-
crimination (∆
A
) calculated from the basal area-weighed
integral of the species δ
13
C values was similar in the
three stands (average ∆
A
=23.1‰), despite differences in
stand species composition and soil drainage type, reflect-
ing the similar proportions of the three different shade-
tolerance types among stands.
Key words Tropical rainforest ·
13
C · Interspecific
diversity · Functional grouping · Canopy carbon isotope
discrimination
Introduction
Tropical rainforests are characterised by the co-existence
of a multitude of tree species. More than 1300 tree spe-
cies with a diameter at breast height (DBH) higher than
10 cm have been identified by botanists in French
Guiana (Riéra et al. 1989; Sabatier and Prévost 1990; D.
Sabatier and M.F. Prévost, unpublished data). Studies on
the ecophysiological diversity of tropical rainforest tree
species remain scarce and have concentrated only on a
small number of species, which were mostly chosen
based on light adaptation features (Bazzaz and Picket
1980; Doley et al. 1988; Huc and Guehl 1989; Roberts
et al. 1990; Alexandre 1991; Meinzer et al. 1993; Huc
et al. 1994; Koch et al. 1994; Hogan et al. 1995; Guehl
et al. 1998; Bonal et al., in press).
Plant carbon isotope composition (δ
13
C) measures al-
low the assessment of ecophysiological traits and their
differences among tree species. Leaf δ
13
C is related to
the time-integrated intrinsic water-use efficiency (WUE),
defined as the ratio of leaf area based rate of CO
2
assimi-
lation (A) to stomatal conductance for water vapour (g
s
)
(Farquhar et al. 1982). Even though leaf δ
13
C is greatly
affected by environmental factors, namely light penetra-
tion in the canopy and vertical gradients of canopy air
δ
13
C (Medina and Minchin 1980; Sternberg et al. 1989;
Van der Merwe and Medina 1989; Buchmann et al.
D. Bonal
Silvolab Guyane, Ecophysiologie Forestière, INRA Kourou, BP 709,
97387 Kourou Cedex, French Guiana
D. Sabatier
Institut de Recherche pour le Développement,
Unité de Recherche ORFHE, Cirad-Forêt,
Campus de Baillarguet, BP 5035,
34032 Montpellier Cedex 1, France
P. Montpied · D. Tremeaux · J.M. Guehl (
✉
)
Unité Ecophysiologie Forestière, INRA Nancy,
54280 Champenoux, France
e-mail: guehl@nancy.inra.fr
Fax: +33-3-83394069
Oecologia (2000) 124:454–468 © Springer-Verlag 2000
D. Bonal · D. Sabatier · P. Montpied · D. Tremeaux
J.M. Guehl
Interspecific variability of δ
13
C among trees in rainforests
of French Guiana: functional groups and canopy integration
Received: 30 November 1999 / Accepted: 23 March 2000
1997), species effects have been found among tropical
rainforest trees (Huc et al. 1994; Buchmann et al. 1997;
Guehl et al. 1998; Martinelli et al. 1998). The δ
13
C ap-
proach is therefore ideal for addressing functional diver-
sity in complex forest ecosystems, and for distinguishing
functional groups of species (Brooks et al. 1997).
Huc et al. (1994) used the δ
13
C approach to compare
the ecophysiological characteristics of pioneer species
and late-stage forest species growing under similar con-
ditions in plantations. They found that pioneer species
had lower δ
13
C values than late-stage ones, i.e. lower
WUE. Pioneer species also presented higher A, g
s
, leaf
transpiration rate, midday leaf water potential (Ψ
wm
) and
hydraulic conductance than late-stage species. More re-
cently, however, in a study including 18 species in a
rainforest of French Guiana, Guehl et al. (1998) found
that some very abundant shade-tolerant canopy late-stage
species presented lower δ
13
C values than pioneer spe-
cies. This does not conform with the simple paradigm of
pioneer/late stage or heliophilic/shade-tolerant dichoto-
my. Validation of this result over a larger number of spe-
cies is necessary.
Leaf phenology (deciduous-leaved vs evergreen-
leaved) is another trait that has been found to be associ-
ated with contrasting species leaf δ
13
C values in forest
ecosystems. In dry tropical conditions, shallow-rooted
deciduous-leaved species displayed less negative δ
13
C
than the deeply rooted evergreen-leaved ones (Sobrado
and Ehleringer 1997). In contrast, in a Mediterranean
macchia ecosystem, Valentini et al. (1992) found most
negative δ
13
C values for the deeply rooted deciduous-
leaved species. Such an assessment has not been carried
out for tropical rainforests so far, even though the pattern
of leaf phenology of major species is known (for French
Guiana, see Loubry 1994; D. Sabatier, personal commu-
nication). In tropical rainforests, numerous deciduous-
leaved species occur. However, they display distinct sea-
sonal patterns of leaf fall, the drought-deciduous one be-
ing only a particular case. Species occurring in lowland
rainforests in French Guiana are also characterised by
differences in their geographical range of distribution,
from French Guiana exclusively to a wide distribution in
the wet and dry neotropical zone, as shown by the data
compiled in the floras (Flora of the Guianas; Flora Neo-
tropica). Whether such differences in geographical distri-
bution are associated with differences in δ
13
C is an im-
portant question.
Functional grouping of species based on ecophysio-
logical characteristics (Chapin et al. 1996; Brooks et al.
1997) has become a necessary step to the understanding
and modelling of the functioning of complex ecosystems
such as the tropical rainforest (Lloyd and Farquhar 1994;
Lacroix and Abbadie 1998). The knowledge of whole
canopy carbon isotope discrimination (∆
A
) – defined
roughly as the difference between atmospheric δ
13
C and
the CO
2
assimilation weighted average leaf δ
13
C of the
different species in the canopy (Lloyd and Farquhar
1994) – is critical for our understanding of the global
carbon budget and our ability to model carbon fluxes at
the earth scale. Lloyd and Farquhar (1994) attempted to
model the role of the different ecosystems on the earth in
the global carbon cycle on the basis of ∆
A
estimates for
these ecosystems. For the tropical rainforest ecosystem,
the ∆
A
value used in the model was derived from leaf gas
exchange studies performed on a reduced number of spe-
cies, which did not take into account the interspecific
δ
13
C diversity of this ecosystem (Guehl et al. 1998;
Martinelli et al. 1998). Furthermore, tropical rainforests
are characterised by spatial gradients of floristic compo-
sition and soil characteristics (Lescure and Boulet 1985;
Sabatier and Prévost 1990; Sabatier et al. 1997). We
wonder if these factors affect ∆
A
.
The objectives of this study were:
1. To assess the variability of sunlit leaf δ
13
C for a large
number of canopy tree species. Is leaf δ
13
C for a giv-
en species stable over sites differing in overall stand
floristic composition or in soil conditions? Only sites
under similar climatic conditions were considered.
2. To assess whether interspecific differences in δ
13
C are
associated: (1) with traits like shade tolerance or the
leaf phenology pattern, (2) with the type of distribu-
tion of the species in South America (e.g. extension
towards the dry tropics), and/or (3) merely with the
taxonomic position of the species. Based on these
characteristics, is it possible to define a simple group-
ing of species (Tilman 1988) taking account of the
variability of δ
13
C among species?
3. To provide an ecophysiological interpretation of the
variability in species δ
13
C. Does the variability in
δ
13
C among species, and also among possible func-
tional groups of species, relate to differences in hy-
draulic traits assessed by predawn (Ψ
wp
) and midday
(Ψ
wm
) leaf water potential measurements?
4. To estimate canopy carbon isotope discrimination
(∆
A
) by the integration of leaf δ
13
C values over the
different species constituting the canopy. Do spatial
gradients in stand floristic composition or in soil
drainage characteristics modulate ∆
A
under similar
climatic conditions?
Species were selected as representative: (1) of the cano-
py of three lowland forest stands differing in floristic
composition and in soil drainage characteristics, includ-
ing also a large number of rare species, (2) of the differ-
ent light adaptation strategies, (3) of the different leaf
phenology patterns. Since our aim was also to spatially
integrate the tree δ
13
C values, we sampled intensively
the three stands and recorded all tree co-ordinates.
Materials and methods
Sampling sites
This study was carried out in the tropical rainforest of French
Guiana in two areas differing in floristic composition. The St-Elie
site is located in the ECEREX research zone (Sarrailh 1984)
(5°18′N; 53°30′W); the Paracou site is located in the experimental
forest zone of Paracou described by Bariteau and Geoffroy (1989),
455
456
on the concession of “CIRAD-forêt” (5°20′N, 52°50′W). Soils in
both sites are oxisols with a ferralitic cover developed over a Pre-
cambrian metamorphic rock (Boulet 1990). The climate is charac-
terised by a long dry season from mid-August to the end of No-
vember and a short dry season in February/March. Mean annual
rainfall (1986–1993) is 2.9 and 3.0 m in Paracou and St-Elie, re-
spectively. Average annual temperature is 25.8°C. Leaf area index
is close to 8 in both forests (A. Granier, personal communication)
and average canopy height is 30 m.
In St-Elie, two untouched 1-ha stands differing in soil drainage
characteristics were chosen among the stands described by
Sabatier et al. (1997). Stand St-Elie DVD is characterised by a
deep vertical soil drainage, down to several meters depth. Stand
St-Elie SLD has mainly a superficial lateral soil drainage, with
apparition of a “dry to the touch” character at a depth of less than
1.2 m (Guehl 1984). Sabatier et al. (1997) found that such differ-
ences in soil features have a strong influence on the forest commu-
nity. In Paracou, one untouched 1.25-ha stand with mostly deep
vertical soil drainage characteristics was studied.
In each stand, all trees with a DBH higher than 10 cm were in-
ventoried, identified, and named following the Checklist of the
Plants of the Guianas (Boggan et al. 1997). Three main families
(out of a total of 38 in Paracou and 50 in St-Elie) represent about
50.0% of the trees in each stand. In Paracou, the Lecythidaceae,
the Caesalpiniaceae and the Chrysobalanaceae families represent
18.5, 13.2 and 10.1%, respectively (D. Sabatier and J.F. Molineau,
unpublished data). For both stands in St-Elie, the first two families
are the Lecythidaceae (28.5% for St-Elie DVD and 30.6% for
St-Elie SLD) and the Caesalpiniaceae (9.6% for St-Elie DVD and
17.0% for St-Elie SLD), but the next family is the Euphorbiaceae
in St-Elie DVD (6.4%) and the Chrysobalanaceae in St-Elie SLD
(7.1%).
Trees were selected according to the three following criteria:
1. Relative abundance in the stand. At least 3 – and up to 11 –
trees per species were selected for the 20 main species in each
stand. Furthermore, one or two trees per species were selected
for sparse species.
2. Social status of the trees in the canopy. Mainly trees reaching
the top of the canopy were considered. Additionally, few trees
per stands belonging to the sub-canopy, but growing in large
canopy gaps, and thus having sunlit leaves, were selected.
3. To cover a wide range of taxa with consideration of species
present in the three stands.
The second criterion was strictly respected, since it has been dem-
onstrated that vertical gradients in leaf δ
13
C will occur due to light
attenuation and gradients in canopy air carbon isotope composi-
tion (δ
13
C
air
) (Medina and Minchin 1980; Medina et al. 1991;
Buchmann et al. 1997).
We sampled 187 trees representing 64 species in Paracou, 106
trees representing 46 species in St-Elie DVD and 115 trees repre-
senting 54 species in St-Elie SLD (Appendix 1, Fig. 1). One hun-
dred and two species were sampled in total. Twenty-eight species
were common to St-Elie DVD and St-Elie SLD; 18 species were
common to the 3 stands. The species considered in our sampling
procedure represented 81.2, 67.7, and 83.3% of the total stand bas-
al area in Paracou, St-Elie DVD and St-Elie SLD, respectively.
Tree height was measured in Paracou using a laser dendrometer
(Ledha Geo, Jenoptik laser, Jena, Germany). The DBH of each
tree was recorded in the three stands.
Leaf sampling, elemental and isotopic analyses
Leaves were sampled in 1998 in the short dry season in Paracou
and in the long dry season in St-Elie. Ten to fifteen fully expand-
ed, sunlit leaves per selected tree were shot down using a rifle.
Leaves were oven-dried at 70°C for 48 h and finely ground. A
sub-sample of 1 mg of leaf powdered material was combusted and
analysed for C and N elemental concentration and for
13
C compo-
sition using an isotope ratio mass spectrometer (Delta S, Finnigan
MAT, Bremen, Germany) at the stable isotope facility of INRA
Nancy. Carbon isotope composition (δ
13
C) was calculated as:
where R
sa
and R
st
are the
13
C/
12
C ratio in the sample and in the
conventional Pee Dee Belemnite standard, respectively. Since only
sunlit leaves were sampled, atmospheric CO
2
concentration (C
a
)
and carbon isotope composition (δ
13
C
a
) can be considered as con-
stant (Buchmann et al. 1997) (C
a
=358 ppm; δ
13
C
a
=–7.85‰: Buch-
mann et al. 1997). Therefore, leaf δ
13
C is negatively and linearly
related to the time-integrated ratio of intercellular to ambient CO
2
concentration (C
i
/C
a
) and positively related to the time-integrated
leaf intrinsic water-use efficiency (WUE=A/g
s
) (Farquhar et al.
1982):
Leaf water potential
Leaf water potential was measured using a pressure bomb (PMS
Instruments Model 1000, Corvallis, Ore.) (Scholander et al. 1965)
in the two St-Elie stands in the 1998 long dry season and in
the 1999 long wet season. Predawn (Ψ
wp
) and midday (Ψ
wm
,
1100–1330 hours) leaf water potentials were measured on two ful-
ly expanded, sunlit leaves per tree that were shot down on one to
three trees per species. All leaf water potential measurements were
conducted on bright days. Species were selected based on previ-
ous studies (Guehl et al. 1998; D. Bonal and J.M. Guehl, unpub-
lished data) in order to cover a wide range of leaf δ
13
C values. All
selected trees occupied a dominant position in the canopy. Leaf
water potential measurements were performed on the same trees in
the wet and the dry season on 27 species in St-Elie DVD and on
18 species in St-Elie SLD, 8 species being common to the 2
stands.
Integration of δ
13
C at canopy level
To estimate canopy carbon isotope discrimination (∆
A
) in the three
stands, we were not able to assess the CO
2
assimilation weighted
average leaf δ
13
C of the different species in the canopy (Lloyd and
Farquhar 1994). We assumed a proportional relationship between
basal area and CO
2
assimilation of the different species and calcu-
lated a basal area weighted ∆
A
as:
where n is the number of species in the stand considered in this
study, δ
13
C
i
is the average δ
13
C value of species i in the stand, and
BA
i
is the basal area of species i in the stand. Assuming the assim-
ilation of the understorey trees to be negligible in the canopy as-
similation, we only considered trees with DBH >20 cm for the ∆
A
calculation.
Species characteristics
Species were grouped according to their light adaptation features
assessed on the basis of growth dynamics observations made in
Paracou on established trees, either in the pristine cover or in re-
sponse to microclimatic changes induced by thinning of various
intensities (Favrichon 1994). Within one group, species are char-
acterised by similar growth response patterns to light conditions in
δ
13
1000C‰
RR
R
() ,=
−
sa st
st
δδ
13 13
CCaba
C
C
≈−+−
a
i
a
()
δ
13
1
16
Caba
WUE
C
=−+−−
a
a
()(
.
).
∆
A
air
13
ii
i=l
n
i
i=l
n
13
ii
i=l
n
i
i=l
n
C
CBA
BA
1000+
CBA
BA
=
−
(
)
∑
∑
(
)
∑
∑
δ
δ
δ
13
1000,
457
the sub-adult and adult stage. More precisely, this classification is
based on the following characteristics of trees with DBH>10 cm:
(1) species mean DBH, (2) absolute radial growth rate in the dif-
ferent diameter classes both in control undisturbed plots and in
thinned plots in Paracou, (3) mortality, and (4) recruitment (i.e. ac-
cession rate to the 10-cm DBH class) in the control and thinned
plots. According to these criteria, three groups were distinguished:
1. Species reaching the upper canopy, but able to establish and re-
produce under shade, with low growth rates in all DBH class-
es. These species were interpreted by Favrichon (1994) as
shade-tolerant (T) species.
2. Species able to tolerate low light levels for seedling establish-
ment but needing high light levels to reproduce once in the can-
opy. These species are characterised by high growth rates; they
display higher growth rates in the higher DBH classes and were
interpreted as hemitolerant (HT) species. Hemitolerance de-
notes here shade tolerance at the juvenile state and absence of
tolerance in mature trees. Many species within this group are
potentially emergent (i.e. with tree crowns above the canopy).
3. Species needing openings in the forest to establish and repro-
duce, with high growth rates and displaying higher growth rates
in lower diameter classes, interpreted as heliophilic (H) species.
Fig. 1 Carbon isotope composition (δ
13
C) of fully sunlit leaves of a range of species growing in the three studied stands. The species were ordered
according to the δ
13
C values (average species values ±1 SE) observed within each stand. The 18 species common to the 3 stands are indicated in bold
Species not studied by Favrichon (1994) were classified
according to Bena (1960). It must be emphasised that only trees
that had access to full sun were considered in this study. Short-
lived heliophilics, as well as lower canopy and understory shade-
tolerant species, were not included. Species were also grouped ac-
cording to their pattern of leaf phenology (deciduous-leaved/ever-
green-leaved) (Loubry 1994; D. Sabatier, unpublished data) or to
their range of distribution in tropical South America (1 Guianas;
2 Guianas+northeastern Amazonia; 3 Guianas+Amazon; 4 Ama-
zon to Panama; 5 Tropical South America) (Flora Neotropica)
(Appendix 1).
Statistical analysis
Statistical analyses were performed using SAS/STAT procedures
(SAS Institute 1989). Analyses of variance were used to detect
any effect of species, shade-tolerance characteristics, area of dis-
tribution or leaf phenology characteristics on δ
13
C. These analyses
were followed by a Duncan test (P<0.05) to compare the mean
δ
13
C values among the different groups. A regression was per-
formed to detect any relationship between leaf δ
13
C and tree diam-
eter, leaf nitrogen concentration or midday or predawn leaf water
potential. In order to disentangle the intrinsic species effect from
the diameter effect on δ
13
C, a covariance analysis was performed.
Finally, a Pearson’s correlation analysis among the stands on leaf
δ
13
C values corrected for unique nil diameter obtained from the
covariance analysis was performed, in order to compare the rank-
ing of the 18 species which were common to the 3 stands, or the
ranking of the 28 species which were common to the 2 stands in
St-Elie. These corrected values were calculated only for the pur-
pose of the covariance analysis.
Results
Interspecific differences in leaf δ
13
C and relationships
with tree diameter
In each stand, a high interspecific variability in species
leaf δ
13
C values was observed (P<0.001) (Appendix 1,
Fig. 1). Mean δ
13
C values ranged from –33.2 to –27.6‰
in Paracou, from –34.8 to –28.2‰ in St-Elie DVD and
from –33.4 to –27.5‰ in St-Elie SLD, with continuous
values between the extremes (Fig. 1). Mean species diam-
eter ranged from 12.4 to 54.0 cm in Paracou, from 14.2 to
97.0 cm in St-Elie DVD and from 10.7 to 105.0 cm in
St-Elie SLD (data not shown).
In the three stands, leaf δ
13
C values were positively
related to tree diameter (P<0.001), even though the R
2
values were quite low (0.20, 0.23, and 0.20 for Paracou,
St-Elie DVD and St-Elie SLD, respectively). The covari-
ance analysis performed to disentangle the intrinsic spe-
cies effect from the diameter effect on δ
13
C yielded dis-
tinct results among the stands (Table 1). In the two
St-Elie stands, the variability of δ
13
C was accounted for
by the species effect only, whereas in Paracou, both fac-
tors affected δ
13
C independently, even though the slope
of the δ
13
C versus diameter was low (0.039‰ cm
–1
). To
account for this slight diameter effect in Paracou, esti-
mated Y-axis intercepts were considered for comparing
species. These calculated values were related to the mea-
sured ones by a close linear relationship (δ
13
C
corrected
=
0.82 δ
13
C
measured
–6.48; R
2
=0.82, P<0.001), the variation
span of the Y-axis intercepts (data not shown) being sim-
458
ilar to that of the measured ones (i.e. 5.6‰). In Paracou
(no measurements made in St-Elie) species δ
13
C values
were significantly correlated with tree height (R
2
=0.23,
P<0.001).
The range of species leaf N concentration values was
similar in the three stands (7–31 mg g
–1
) (Appendix 1).
Within legumes, there was no significant difference in
leaf N concentration between N-fixing species and non-
fixing species. Mean species leaf δ
13
C values were
slightly related to leaf N concentration values in St-Elie
DVD stand (R
2
=0.22; P=0.03), whereas no significant
relationship was found between these variables in the
two other stands (data not shown).
In the three stands, δ
13
C values and tree diameter
were significantly different among the three groups of
shade tolerance (Table 2). Hemitolerant species dis-
played less negative leaf δ
13
C values than heliophilic and
shade-tolerant species in the three stands. Heliophilic
species were characterised by less negative δ
13
C values
than shade-tolerant species in Paracou and St-Elie DVD
stand, but not in St-Elie SLD stand. Mean tree diameter
of tolerant species was similar to that of the heliophilic
species and was smaller than that of hemitolerant species
(Table 2). The mean diameter differed between helio-
philic and hemitolerant species in St-Elie DVD only.
Leaf δ
13
C was more negative in evergreen-leaved than in
deciduous-leaved species in the three stands (average
difference=1.3‰) (Table 2). There was no significant
difference in δ
13
C among the five different geographic
groups of species distribution (Table 2). In the three
stands, δ
13
C values differed significantly among families
(P=0.001).
Ranking of species δ
13
C among stands
Eighteen species were common to the three stands (Ap-
pendix 1, Fig. 1). The average species δ
13
C values were
significantly correlated among the three stands (Table 3),
reflecting a consistent overall ranking of species. Fur-
åTable 1 Degrees of freedom (df), coefficient of correlation (R
2
)
and significance levels (P-value) from covariance analysis be-
tween leaf δ
13
C and tree diameter or species in canopy tree species
growing in three natural stands in French Guiana. The two stands
in St-Elie differ in soil drainage type: DVD deep vertical drainage;
SLD superficial lateral drainage (Sabatier et al. 1997)
Stand Source of df R
2
P-value
variation
St-Elie DVD 0.76
Diameter 1 0.55
Species 45 <0.001
St-Elie SLD 0.78
Diameter 1 0.27
Species 53 <0.001
Paracou 0.72
Diameter 1 <0.001
Species 63 <0.001
Table 2 Mean leaf δ
13
C values (±1 SE) of canopy tree species
growing in three natural stands in French Guiana. The two stands
in St-Elie differ in soil drainage type: DVD deep vertical drainage;
SLD superficial lateral drainage. Species were grouped according
to their tolerance to shade (tolerant, hemitolerant, heliophilic), or
to their range of distribution in South America (1 Guianas; 2 Guia-
nas+northeastern Amazon; 3 Guianas+Amazon; 4 Amazon to Pan-
ama; 5 Tropical South America), or to their pattern of leaf phenol-
ogy (deciduous-leaved; evergreen-leaved). Additionally, mean tree
DBH (±1 SE) for each shade-tolerance group in the three stands is
represented. For each group and in each stand, an ANOVA was
performed to test the group effect on δ
13
C or DBH (P-value). For
each group and in each stand, mean values not sharing common
letters are significantly different (Duncan’s Multiple Range test,
P<0.05)
Paracou St-Elie DVD St-Elie SLD
Leaf carbon isotope composition (δ
13
C)
Shade tolerance P<0.001 P<0.001 P<0.001
Tolerant –31.6±0.1
c
–31.4±0.2
c
–30.9±0.2
b
Hemitolerant –29.7±0.2
a
–29.3±0.2
a
–29.0±0.2
a
Heliophilic –30.6±0.3
b
–30.7±0.4
b
–30.3±0.2
b
Area of distribution P=0.12 P=0.12 P=0.49
1 –31.1±0.2 –30.4±0.3 –30.4±0.4
2 –31.0±0.2 –30.9±0.2 –30.1±0.3
3 –31.4±0.4 –30.4±0.4 –29.7±0.6
4 –30.8±0.4 –29.1±0.7 –30.7±0.4
5 –30.2±0.3 –30.8±0.5 –29.8±0.2
Leaf phenology P<0.001 P<0.001 P<0.001
Deciduous –30.3±0.2
a
–29.7±0.2
a
–29.0±0.2
a
Evergreen –31.2±0.1
b
–31.1±0.2
b
–30.6±0.2
b
Tree diameter
Shade tolerance P<0.001 P<0.001 P<0.001
Tolerant 28.1±1.2
b
33.4±1.7
b
34.4±1.8
b
Hemitolerant 36.9±2.4
a
55.7±4.5
a
50.3±4.0
a
Heliophilic 31.6±2.5
ab
40.5±6.2
b
43.5±4.6
ab
459
thermore, the species δ
13
C values did not significantly
differ among the three stands, except in Carapa procera
(Appendix 1). Among the nine species that were repre-
sented in two stands with at least two trees sampled by
stand, only Chrysophyllum sanguinolentum displayed
δ
13
C values that differed significantly between stands
(Appendix 1). There was no overall significant effect of
the type of drainage on δ
13
C for the 28 species which
were common to the St-Elie DVD and St-Elie SLD
stands (Table 3).
Relationships between leaf δ
13
C and leaf water potential
Within each stand, there was a close relationship be-
tween the midday leaf water potential (Ψ
wm
) values ob-
served in the different species in the wet and in the dry
seasons (R
2
=0.62 and 0.78 in St-Elie DVD and St-Elie
SLD, respectively). There was no significant seasonal ef-
fect on Ψ
wm
. Therefore, we pooled the data from the dry
and wet seasons within each species (Fig. 2). Average
species Ψ
wm
ranged from –0.4 to –3.2 MPa in St-Elie
DVD and from –0.4 to –2.8 MPa in St-Elie SLD (Fig. 2).
There was a close relationship between Ψ
wm
values mea-
sured in the two stands (eight species only). Predawn
leaf water potential values ranged from –0.2 to –0.7 MPa
for both seasons (data not shown). Extremely high Ψ
wm
values were found in the three species belonging to the
Myristicaceae (Fig. 2, Appendix 1). Additional Ψ
wm
measurements performed on other Myristicaceae species
occurring in French Guiana (Virola sebifera, V. surina-
mensis, Ostephloem platyspermum) yielded values all
higher than –0.4 MPa (data not shown).
In both stands, a negative relationship (P=0.001) was
found between leaf δ
13
C and Ψ
wm
, even though the data
displayed an important scatter (Fig. 2), mainly due to the
distinct position of the hemitolerant and tolerant species
in the overall relationship. For those species common to
the two stands, the position of the data in the δ
13
C versus
Ψ
wm
relationship was similar. Predawn water potential
values (St-Elie DVD) were not related to δ
13
C (data not
shown).
δ
13
C distribution and carbon isotope discrimination
at canopy level (∆
A
)
The distributions of the frequency of species by δ
13
C
classes were roughly monomodal (modal δ
13
C=-31.0‰)
(Fig. 3a-c). The distribution of total basal area (all sam-
pled species pooled) by δ
13
C classes in Paracou was also
monomodal (modal δ
13
C=-31.0‰). In contrast, the distri-
butions were bimodal in both St-Elie stands (Fig. 3d-f): a
first mode corresponded to that of Paracou and a second
mode was displayed at –29.0‰. This second mode, as
well as the basal area corresponding to δ
13
C values higher
than –30.0‰ in Paracou, was composed mostly of hemi-
tolerant species (Fig. 3d-f), which represent a high basal
area with only a small number of species (Appendix 1,
Table 3 Pearson correlation coefficients (R) and significance lev-
els (P-value) from a correlation analysis performed on the leaf
δ
13
C values of 18 species common to 3 natural stands in French
Guiana, and on 28 species common to the 2 St-Elie stands. The
two stands in St-Elie differ in soil drainage type: DVD deep verti-
cal drainage; SLD superficial lateral drainage. Correlation analysis
was performed on estimated leaf δ
13
C values corresponding to the
Y-axis intercepts for the diameter effect in the covariance analysis
presented in Table 1
St-Elie DVD St-Elie SLD Paracou
18 common species
St-Elie DVD R 1.00
P-value 0.00
St-Elie SLD R 0.63 1.00
P-value <0.01 0.00
Paracou R 0.65 0.80 1.00
P-value <0.01 <0.01 0.00
28 common species
St-Elie DVD R 1.00
P-value 0.00
St-Elie SLD R 0.62 1.00
P-value <0.01 0.00
460
Fig. 3a-c). The first mode of the basal area distribution
was almost entirely constituted by the numerous tolerant
species. Heliophilic species represented only a small pro-
portion of the total basal area, despite the large number of
species.
The calculated ∆
A
values were 23.6, 23.0 and 22.6 ‰
in Paracou, St-Elie DVD and St-Elie SLD, respectively.
Discussion
Interspecific variability in leaf δ
13
C
We found a high variability of sunlit leaf δ
13
C among
tropical rainforest canopy tree species. Mean species
δ
13
C values varied over a ca. 6‰ range within each
stand and over a 7.3‰ range (–34.8 to –27.5‰) when
pooling the three stands. This variability is higher than
the range found in a previous study in French Guiana in-
cluding only 18 species (4.5‰) (Guehl et al. 1998).
Martinelli et al. (1998) assessed the interspecific vari-
ability of tree leaves δ
13
C in an Amazonian rainforest in
Rondônia (Brazil), considering both upper and lower
canopy trees. They found an overall range of variability
of 7.1‰ for the average species δ
13
C values. Consider-
ing only upper canopy trees (total height>25 m), this
range was 5.5‰ (from –34.3 to –28.8‰), which is re-
markably consistent with our results.
Even though we only sampled mature, sunlit leaves
in order to minimise canopy effects (Buchmann et al.
1997; Martinelli et al. 1998), leaf δ
13
C was related
Fig. 2 Relationships between midday leaf water potential (Ψ
wm
)
and sunlit leaf (δ
13
C) for the season average species values
(±1 SE) in the two St-Elie stands. The regression lines correspond
to significant correlation (P<0.01). The types of shade tolerance of
the different species (Favrichon 1994) have been represented. The
eight species common to the two stands are indicated in bold
Fig. 3 Frequency distributions of the number of species (a-c) and
the corresponding basal area values (d–f) by δ
13
C classes. The
shade tolerance types of the different species are distinguished ac-
cording to Favrichon (1994)
461
to tree diameter (Table 1). In the two St-Elie stands,
this relationship was entirely accounted for by the
species effect, whereas in Paracou a slight diameter ef-
fect was expressed, independently of the species effect
(Table 1). This intrinsic diameter effect observed in
Paracou, which was also associated with a tree height
effect, might reflect a microclimatic effect on leaf gas
exchange (C
i
/C
a
) and thus on leaf δ
13
C. Trees of the
low-diameter classes were more abundant in Paracou
than in the two St-Elie stands. This led us to sample
more trees in the 15- to 35-cm-diameter classes in Par-
acou as compared to St-Elie (Table 2). These trees
might be subject to more lateral shading from the sur-
rounding taller trees in the morning and in the after-
noon, even though they are fully sunlit at midday. Tak-
ing account of this diameter effect resulted in negligible
effects on the ranking of the species for the δ
13
C values
in Paracou.
Despite differences in topography and soil conditions,
and differences in background floristic composition
among the three stands, species occurring in at least two
stands displayed remarkably stable δ
13
C values (Table 3,
Appendix 1). These results suggest a predominant genetic
control of species δ
13
C under the similar climatic condi-
tions prevailing in the three stands. The absence of modu-
lation of species δ
13
C by the soil characteristics in St-Elie,
together with the fact that stand species composition was
affected (Sabatier et al. 1997), suggest that effects of ex-
treme and rare climatic conditions (e.g. severe drought) –
rather than average conditions – play a predominant role
in community adjustments to soil conditions through dif-
ferential species mortality and/or recruitment.
Functional grouping of species
Marked differences in species δ
13
C values were found
with respect to the different types of shade tolerance
(Table 2). However, the ranking of the δ
13
C values for
these different types was not consistent with the gradi-
ent of shade tolerance. Heliophilic species indeed exhib-
ited more negative δ
13
C values (i.e. lower intrinsic wa-
ter-use efficiency) than hemitolerant species, which is in
agreement with the “gambler” (i.e. resource waster)
ecological strategy proposed by Oldeman and van Dijk
(1991), leading to the ability of heliophilics to rapidly
dominate neighbours. However, tolerant species dis-
played even more negative δ
13
C values than heliophilic
species, confirming our expectations and first results
obtained on a reduced set of species in Paracou (Guehl
et al. 1998). Clearly, there are two distinct groups
among the late-stage species (heliophilic ones excluded)
based on the δ
13
C values, in remarkable correspondence
with Favrichon’s hemitolerant and tolerant groups
(Fig. 3). Tolerant species are able to grow in understory
conditions where light is the main limiting factor. It
might be suggested that the extremely negative δ
13
C
found in this group is associated with high g
s
(Bonal
et al., in press), allowing maximised carbon assimilation
under low light (Givnish 1988). Low light-saturated A
values may also explain the low leaf δ
13
C. It is note-
worthy that this trait was maintained for trees reach-
ing the upper canopy. The hemitolerant group encom-
passes most emergent species – and is characterised on
average by higher DBH values than the tolerant group
(Table 2) – whereas emergent species are not included
in the tolerant group (Favrichon 1994). High WUE in
the former group may be considered as an adaptive trait
to the high evaporative demand prevailing in the emerg-
ing tree crowns.
Evergreen-leaved species displayed more negative
δ
13
C values than deciduous-leaved ones. Sobrado and
Ehleringer (1997) found similar results in a tropical dry
forest. Because, in wet tropical conditions, the drought-de-
ciduous type is only one among different deciduous pat-
terns (Loubry 1994), differences in phenology can not yet
be clearly interpreted from an ecological or ecophysiolog-
ical point of view. The association found here between
δ
13
C and phenology patterns remains to be elucidated.
However, we found to some extent an association between
shade-tolerance types and phenology patterns: most hemi-
tolerant species are deciduous (11 out of 17), whereas he-
liophilic or tolerant species are mainly evergreen (14 out
of 18 and 37 out of 53, respectively). Our results clearly
point to the absence of association between the gradients
in δ
13
C values and the area of distribution of the species.
Particularly, there was no peculiar δ
13
C characteristic for
those species extending towards the dry tropics.
Interestingly, differences among species in δ
13
C, and
their shade-tolerance type, were associated with their
taxonomic situation, at least for the four main families
represented in the study stands: Caesalpiniaceae (average
δ
13
C=–29.5‰) mainly encompass hemitolerant species
with least negative δ
13
C; Chrysobalanaceae (–31.8‰),
Euphorbiaceae (–31.4‰) and Lecythidaceae (–31.2‰)
mainly encompass shade-tolerant species with low δ
13
C.
Heliophilic species are included in numerous families
which are less represented and displayed mostly interme-
diate δ
13
C.
Ecophysiological interpretation of the interspecific
variability in δ
13
C
According to the classical two-step model of carbon
isotope discrimination during photosynthesis (Farquhar
et al. 1982), the range of about 6.0‰ we observed be-
tween species would correspond to a difference of
85 µmol mol
–1
in average C
i
and to A/g
s
ranging from 28
to 82 µmol mol
–1
.
Leaf N concentrations varied over a fourfold range
among species (Appendix 1), highest values being
observed in legumes (Caesalpiniaceae, Fabaceae, Mimo-
saceae), as already found by Roggy et al. (1999). How-
ever, neither the ability for symbiotic nitrogen fixation,
nor leaf N concentration were clearly related to leaf
δ
13
C, confirming previous studies made in Paracou
(Guehl et al. 1998).
462
Midday leaf water potential differed markedly
among the species with consistency over the two sites
(Fig. 2) and the two seasons. One major result of this
study consists of the negative relationships found be-
tween average species leaf δ
13
C values and Ψ
wm
(Fig. 2). These results confirm previous observations
made on a reduced number of species growing in
monospecific plantations near Paracou (Huc et al.
1994; Bonal et al., in press). To our knowledge, such
relationships have not been described in other wet trop-
ical forests so far. Ehleringer et al. (1991) found a neg-
ative relationship between δ
13
C and Ψ
wm
among desert
species, which they attributed to differences in the ac-
cess to summer rains. In a tropical dry forest in Venezu-
ela, Sobrado and Ehleringer (1997) found a negative re-
lationship between δ
13
C and Ψ
wm
, which they attributed
to differences in the depth of the rooting system. In our
study, Ψ
wp
values remained high (>–0.7 MPa) in all
species, even though soil water depletion occurred in
the upper soil layer in the dry season (Guehl 1984;
Bonal et al., in press). This might explain the lack of
relationship between δ
13
C and Ψ
wp
. Since there was no
pronounced difference in Ψ
wm
between the dry and the
wet season in either stand, the low Ψ
wm
values found in
some species, and the high differences in Ψ
wm
among
species, were not induced by differential species re-
sponses to soil drought. Furthermore, Ψ
wm
values of
species growing in St-Elie stands and in a nearby 15-
year-old plantation were similar, and in this plantation,
the range of Ψ
wm
values for 21 tropical rainforest cano-
py tree species was similar to that in the natural forest
(–2.8 to –0.3 MPa) (Bonal et al., in press; D. Bonal and
J.M. Guehl, unpublished data). Therefore, the observed
Ψ
wm
values can be considered as reflecting intrinsic
species characteristics.
A theoretical background to analyse interspecific dif-
ferences in δ
13
C and in Ψ
wm
is provided by the study by
Panek (1996). According to Panek’s equations, the nega-
tive relationship we found between δ
13
C and Ψ
wm
can
only be accounted for by a positive relationship between
δ
13
C and A/K
L
, where K
L
denotes the whole tree leaf
specific hydraulic conductance (i.e. the whole tree hy-
draulic conductance divided by the tree leaf area). In-
deed, results available from ecophysiological studies
performed on seven heliophilic or hemitolerant species
in French Guiana differing in leaf δ
13
C values clearly
show that low δ
13
C values are associated with high A
and very high g
s
and calculated K
L
(Huc et al. 1994;
Bonal et al., in press). For a given range of Ψ
wm
values,
shade-tolerant species clearly displayed lower δ
13
C val-
ues than hemitolerant species (Fig. 2). Whether this re-
flects lower A – or higher K
L
– in the former group is
still unclear.
Canopy carbon isotope discrimination (∆
A
)
The rainforest in French Guiana is characterised by impor-
tant geographic gradients in floristic composition due to
soil, climatic and historical factors (Lescure and
Boulet 1985; Sabatier and Prévost 1990; Charles-
Dominique et al. 1998). We analysed here the effects of
such gradients on ∆
A
under common climatic conditions
by: (1) comparing stands differing in the most represented
families, and (2) comparing two stands with different soil
water drainage types. Sabatier et al. (1997) have shown
that forest communities are affected by the latter factor for
the abundance of major species. Despite the large differ-
ences in floristic composition among the stands (see basal
areas in Appendix 1) and the high interspecific variability
in δ
13
C, ∆
A
values were similar in the three stands. This
result is to be associated with the similar distribution of
the different shade-tolerance groups, which correspond to
distinct δ
13
C values, in the three stands. This shows that in
these highly diverse communities, the substitutions among
species occur in such a way as to maintain the relative im-
portance of the different δ
13
C-contrasted groups and ulti-
mately to maintain ∆
A
almost stable. Whether the stability
of ∆
A
found here for three stands 30 km apart holds in the
more contrasting climatic conditions and floristic gradi-
ents encountered at larger scale (Guiana, Amazonia, dry
tropical forests) is an important question. Schulze et al.
(1998) found a stability of community average carbon iso-
tope discrimination in forests along rainfall gradient in
northern Australia. The mechanisms underlying such ad-
justments and their ecological implications (niche differ-
entiation for the capture of resources, response to pertur-
bations?) remain unknown.
Our calculated ∆
A
values (on average 23.1‰) were
about 5.0‰ higher than the values estimated by Lloyd
and Farquhar (1994) for tropical rainforests inferred from
gas exchange data of a reduced number of species. Hemi-
tolerant and tolerant species constitute the predominant
groups in the studied stands (Fig. 3). The high ∆
A
found
in our study can clearly be attributed to the importance of
the tolerant group comprising species with extremely
negative δ
13
C. Direct and careful estimations of ∆
A
made
in the different types of ecosystems at the surface of the
globe will improve the relevance of bottom-up approach-
es of the global carbon cycle based on the integration of
∆
A
values over the different vegetation types (Lloyd and
Farquhar 1994). However, ∆
A
refers only to the canopy
component of the whole ecosystem carbon isotope dis-
crimination and does not incorporate the contribution of
plant and soil respiration. The model of ecosystem carbon
isotope discrimination (∆
e
) proposed by Buchmann et al.
(1997) includes all these components. Buchmann et al.
(1997) provided an estimate of 20.4‰ for ∆
e
in the Par-
acou forest. The difference between the two approaches
(∆
A
–∆
e
=2.7‰) shows the necessity of further researches
aimed at assessing the factors influencing both estimates,
as discussed in detail by Buchmann et al. (1997).
In conclusion, we found an extremely high interspecif-
ic variability in sunlit leaf δ
13
C among canopy trees, the
range of variations being similar to that found over broad
climatic gradients (Schulze et al. 1998) or among distinct
life forms within communities (Brooks et al. 1997), in
other types of forests. Even though this variability seems
463
to be at least party driven by differences in hydraulic fea-
tures among species, its precise ecophysiological basis, as
well as its ecological implications (e.g. niche differentia-
tion for water acquisition) largely remain to be elucidat-
ed. We found an interesting association between species
δ
13
C, a trait related to leaf gas exchange regulation, and
features reflecting the plasticity of growth dynamics with
respect to contrasting light conditions. To our knowledge,
this association constitutes a first validation, for rainfor-
ests, of the concept of functional types of species (Grime
1977; Tilman 1988), stating a unique grouping of species
with respect to various functional traits. We could provide
here a clear confirmation of the existence of two distinct
groups within the non-heliophilic late-stage species
(Favrichon 1994), as well as elements for the functional
characterisation of these groups. An expression of the as-
sociation between species δ
13
C and the type of shade tol-
erance, at the integrated canopy level, consisted in the
fact that, despite the differences in species composition,
similar proportions of the different shade-tolerance types
among stands were accompanied by similar ∆
A
values.
Acknowledgements We are grateful to “CIRAD-Forêts” in
Kourou for authorisation to sample trees in Paracou. The wise
contribution by Jean-Pierre Pascal (CNRS Lyon) on the discussion
on light adaptation strategies of species is acknowledged. Pascal
Imbert, Dumaine Duchant and Pascal Giraudeau were of great
help in leaf sampling. The excellent technical collaboration of
Claude Bréchet for isotopic measurements is acknowledged. Lau-
rent Tellier (ONF) and Têté Barigah (INRA Kourou) were of great
help in species determination in Paracou. D. Bonal was supported
by a grant from INRA and GIS-Silvolab, French Guiana.
FAMILY Basal area (m
2
ha
–1
) δ
13
C (‰) Leaf N concentration (mg g
–1
)
Species Shade Phenol- Area Paracou St-Elie St-Elie Paracou St-Elie St-Elie P Paracou St-Elie St-Elie P
tole- ogy DVD SLD DVD SLD DVD SLD
rance
ANACARDIACEAE
Thyrsodium – E 1 – 0.37 – - –30.2 – – – 12 – –
guianense
ANNONACEAE
Xylopia sp. H E 2 0.05 – – –32.5 – – – 14 – – –
APOCYNACEAE
Couma T D 2 0.05 – 0.23 – – –28.9 – – – 15 –
guianensis
ARALIACEAE
Schefflera H E 2 – 0.02 0.28 – – –30.2 – – – 8 –
decaphylla
BIGNONIACEAE
Jacaranda H E 5 0.08 0.10 0.11 –31.6 – – – 18 – – –
copaia
BOMBACACEAE
Catostemma T D 2 0.06 0.04 – –30.4 –31.4 – ns 12 15 – *
fragrans
BORAGINACEAE
Cordia sp. – – 1 0.03 – 0.02 –33.1 – – – 18 – – –
BURSERACEAE
Dacryodes – E 1 – 0.17 0.05 – – –31.7 – – – 11 –
nitens
Protium sp. – E – 0.09 0.04 0.01 –31.7 – – – 11 – – –
Protium T E 2 – 0.21 – – –31.1 – – – 13 – –
subserratum
Tetragastris T E 4 – 0.18 0.03 – –28.7 – – – 10 – –
panamensis
Appendix 1
Shade-tolerance characteristics (H heliophilic; HT hemitolerant;
T tolerant) according to Favrichon (1994), leaf phenology pattern (D
deciduous-leaved; E evergreen-leaved) (Loubry 1994; D. Sabatier,
personal communication) and area of distribution in tropical
South America (1 Guianas; 2 Guianas+northeastern Amazon;
3 Guianas+Amazon; 4 Amazon to Panama; 5 Tropical South Ameri-
ca) (Flora Neotropica) of tree species growing in three stands
(Paracou, St-Elie DVD, St-Elie SLD) in the tropical rainforest of
French Guiana. The two stands in St-Elie differ in soil drainage type:
DVD deep vertical drainage; SLD superficial lateral drainage
(Sabatier et al. 1997). Species total basal area (m
2
ha
-1
) is reported. For
each sampled species and in each stand, leaf δ
13
C values (‰) and ni-
trogen concentration (mg g
–1
) are reported. Average species values
(±1 SEM) within sites were 0.50‰ for δ
13
C and 1.5 mg g
–1
for N con-
centration. For each species, leaf δ
13
C or nitrogen concentrations of
species common to at least two stands were compared. The number of
trees sampled per species and per stand ranged from 1 to 11
(F symbiotic nitrogen fixation; Guehl et al. 1998; Roggy et al. 1999)
464
CAESALPINIACEAE
Bocoa T E 1 0.33 0.22 0.11 –31.8 –29.7 –30.7 ns 25 20 22 ns
prouacensis
Dicorynia HT D 2 0.94 0.60 1.16 –29.0 –28.6 –28.0 ns 20 18 21 ns
guianensis
Eperua HT D 2 0.66 1.50 5.42 –28.5 –28.6 –28.3 ns 16 20 18 *
falcata
E. grandiflora HT E 1 1.33 1.46 2.58 –28.9 –29.5 –28.9 ns 12 12 15 ns
Peltogyne HT D 3 – 2.90 0.37 – –29.7 –27.9 ns – 16 17 ns
venosa
Recordoxylon HT D 1 1.23 – – –28.0 – – – 20 – – –
2 venosa
Sclerolobium H E 1 – 0.55 – – –30.0 – – – 29 – –
albiflorum
F
S. melinonii
F
H E – 0.33 0.44 0.21 –30.0 –28.6 –30.1 ns 25 23 31 ns
Swartzia HT D 4 0.04 1.39 – –29.2 –28.4 – – 27 22 – –
polyphylla
F
Vouacapoua T D 2 1.66 0.33 0.80 –32.4 –30.7 –31.1 ns 21 21 23 ns
americana
CARYOCARACEAE
Caryocar HT D 5 0.52 – 0.12 –29.4 – –29.4 ns 11 – 20 ns
glabrum
CELASTRACEAE
Goupia glabra H E 4 0.50 – 0.62 –29.9 – –30.0 ns 17 – 14 ns
CHRYSOBALANACEAE
Couepia T E – – 0.20 0.05 – –30.7 –29.6 – – 17 15 –
caryophylloides
C. guianensis HT E – – – 0.17 – – –31.7 – – – 13 –
Licania alba T E 1 0.40 0.79 1.24 –32.1 –31.6 –31.5 ns 12(1) 7(2) 11 ns
L. glabriflora T – 4 – – 0.09 – – –32.1 – – – 14 –
L. granvillei T E 4 – – 0.14 – – –31.0 – – – 6 –
L. membran- T E 3 0.38 0.30 0.01 –32.0 –32.0 –33.4 ns 11 17 13 *
acea
L. ovalifolia T E 1 0.16 – 0.01 –31.8 – – – 11 – – –
Licania sp. 1 T – 2 0.25 – – –30.6 – – – 12 – – –
Licania sp. 2 T – 2 0.42 – – –32.5 – – – 12 – – –
Parinari H E 3 – – 0.57 – – –30.8 – – – 12 –
excelsa
P. montana H E 5 0.23 – – –29.8 – – – 15 – – –
Parinari sp. H E 5 0.25 – – –31.5 – – – 14 – – –
Undetermined – – – 3.31 – – –31.8 – – – 12 – – –
CLUSIACEAE
Moronobea HT D 1 0.29 0.84 – –30.8 –30.3 – ns 12 14 – ns
coccinea
Platonia HT D 2 – – 0.87 – – –28.0 – – – 10 –
insignis
Symphonia sp. HT E 5 0.96 0.47 0.28 –30.1 –30.2 –30.4 ns 14 15 15 ns
Tovomita sp. T E – 0.52 0.04 0.01 –32.5 – – – 16 – – –
ELAEOCARPACEAE
Sloanea sp. T D – 0.05 0.18 0.01 –27.9 – – – 28 – – –
EUPHORBIACEAE
Amanoa – E 2 – – 0.49 – – –28.4 – – – 11 –
congesta
Chaetocarpus T E 1 0.73 0.02 0.27 –31.3 –33.8 –31.9 ns 10 11 9 *
schomburg.
Drypetes T E 2 0.12 – 0.02 –31.0 – – – 26 – – –
variabilis
Glycydendron – D 2 – 0.05 0.03 – –30.8 – – – 21 – –
amazoni.
Hevea T D 2 – – 0.03 – – –29.2 – – – 23 –
guianensis
Appendix (continued)
FAMILY Basal area (m
2
ha
–1
) δ
13
C (‰) Leaf N concentration (mg g
–1
)
Species Shade Phenol- Area Paracou St-Elie St-Elie Paracou St-Elie St-Elie P Paracou St-Elie St-Elie P
tole- ogy DVD SLD DVD SLD DVD SLD
rance
465
FABACEAE
Andira HT D 1 0.03 – – –30.8 – – – 18 – – –
coriacea
F
Diplotropis H E 2 0.15 0.03 – –30.7 –31.2 – ns 19 20 – ns
purpurea
F
FLACOURTIACEAE
Laetia procera H E 4 – – 0.27 – – –31.3 – – – 19 –
HUGONIACEAE
Hebepetalum T E 2 0.03 0.15 0.02 –31.8 – – – 17 – – –
humiriifoli.
HUMIRIACEAE
Humiriastrum – E – – 0.03 0.20 – –34.8 –32.7 – – 9 10 –
subcrenat.
Vantanea – E – – 0.23 0.10 – –30.1 –31.3 – – 10 9 –
parviflora
ICACINACEAE
Dendrobangia T E – 0.08 0.04 0.07 –31.1 –31.5 –31.3 – 16 13 15 –
boliviana
Poraqueiba – E – – 0.08 – – –32.9 – – – 11 – –
guianensis
LAURACEAE
Ocotea rubra HT E 2 0.22 0.01 – –31.9 –29.1 – ns 14 18 – ns
LECYTHIDACEAE
Couratari T D 4 0.13 – – –30.9 – – – 19 – – –
guianensis
Eschweilera T E 4 – – 0.04 – – –31.1 – – – 20 –
coriacea
E. decolorans T E 3 – 0.06 0.37 – –31.1 –29.8 ns – 21 22 ns
E. micrantha T E 2 – 2.34 1.02 – –31.8 –31.3 ns – 22 17 *
E. parviflora T E 1 – 1.78 0.02 – –30.7 –33.2 ns – 20 18 ns
E. sagotiana T E 2 – 0.10 0.87 – –32.2 –31.3 – – 15 15 –
Eschweilera sp. T E - 2.17 – – –31.0 – – – 17 – – –
Gustavia T E 3 0.25 0.02 0.01 –32.0 – – – 21 – – –
hexapetala
Lecythis T – 2 0.47 – – –30.8 – – – 23 – – –
c hartacea
L. zabucajo T D 2 0.23 – – –27.7 – – – 15 – – –
L. idatimon T D 2 1.77 1.87 1.97 –31.5 –31.4 –32.0 ns 18 15 13 ns
L. persistens T E 2 – 0.25 1.19 – –30.7 –32.1 – – 17 14 –
MELASTOMATACEAE
Mouriri T E 2 0.65 0.16 0.25 –30.9 –29.4 –30.9 ns 13 10 4 ns
crassifolia
MELIACEAE
Carapa procera H E 5 0.47 0.07 0.22 –29.2 –31.1 –29.3 * 14 15 14 ns
Trichilia sp. – E – 0.12 – – –30.8 – – – 17 – – –
MIMOSACEAE
Abarema – D – – 0.34 – – –29.2 – – – 24 – –
curvicarpa
A. jupunba
F
– D 5 0.23 0.06 0.13 –29.4 –29.4 –29.1 – 18 20 19 –
Balizia – D – 0.28 0.11 0.86 –29.5 –28.3 –27.5 ns 23 24 18 ns
pedicellaris
F
Inga alba
F
H D 3 0.13 – – –32.4 – – – 21 – – –
I. paraensis
F
H – – – 0.18 – – –28.3 – – – 29 – –
I. thibau- H S 3 0.08 – – –29.7 – – – 23 – – –
diana
F
Parkia nitida H D 4 0.12 0.01 0.28 –31.5 – –31.3 – 18 – 20 –
Pseudopipta- – D – – 0.77 – – –29.0 – – – 30 – –
denia suaveol.
Appendix (continued)
FAMILY Basal area (m
2
ha
–1
) δ
13
C (‰) Leaf N concentration (mg g
–1
)
Species Shade Phenol- Area Paracou St-Elie St-Elie Paracou St-Elie St-Elie P Paracou St-Elie St-Elie P
tole- ogy DVD SLD DVD SLD DVD SLD
rance
*P<0.05; ns not significant
a
Subsp. duckeana
b
Subsp. guianensis
466
MORACEAE
Brosimum T D 2 0.19 – – –31.6 – – – 18 – – –
acutifolium
B. guianense T E 5 – 0.13 0.01 – –29.6 – – – 11 – –
B. rubescens T E 5 0.12 – 0.05 –31.1 – – – 12 – – –
Helicostylis T E – 0.07 0.05 – –30.3 – – – 14 – – –
pedonculata
MYRISTICACEAE
Iryanthera T E 2 0.09 – 0.03 –32.4 – –32.0 ns 20 – 15 *
hostmanii
I. sagotiana T E 2 0.39 0.37 0.30 –33.2 –32.6 –32.2 ns 16 12 14 ns
Virola michelii H E 2 – 0.83 0.36 – –31.7 –31.2 ns – 20 12 ns
OLACACEAE
Minquartia – E 5 0.75 – 0.08 –32.4 – –29.2 – 18 – 22 –
guianensis
RUBIACEAE
Posoqueria T E – 0.05 0.25 0.04 –32.7 –32.7 –28.9 ns 12 12 12 ns
latifolia
SAPOTACEAE
Chrysophyllum T D 5 0.16 0.15 –29.7 – –30.0 ns 19 – 19 ns
prieurii
C. sanguino. T E 3 0.57 0.38 –30.3 – –29.4 * 12 – 11 ns
Ecclinusa – – 3 – 0.96 0.13 – –29.9 – – – 14 – –
guianensis
Micropholis T E 4 0.08 – 0.26 –31.4 – –29.4 ns 14 – 16 ns
guianensisa
M. guianensisb T E 4 – – 0.52 – – –32.4 – – – 15 –
M. obscura T E 4 0.58 0.48 – –30.8 –31.0 – ns 13 13 – ns
M. venulosa T E 5 – – 0.43 – – –30.6 – – – 14 –
Pouteria T E 3 – – 0.86 – – –28.8 – – – 8 –
eugeniifolia
P. grandis T E 1 – – 0.18 – – –30.4 – – – 13 –
P. guianensis T E 5 – 0.26 – – –32.8 – – – 15 – –
P. melanopoda HT E 1 – – 0.08 – – –29.1 – – – 21 –
Pradosia T D 2 1.03 – – –30.6 – – – 14 – – –
cochlearia
SIMAROUBACEAE
Simaba cedron T E – 0.14 – – –31.6 – – – 21 – – –
STERCULIACEAE
Sterculia sp. H – 2 0.21 – 0.04 –30.8 – – – 15 – – –
TILIACEAE
Lueheopsis HT D 1 0.03 – – –32.7 – – – 15 – – –
rugosa
VOCHYSIACEAE
Ruizterania HT D 2 0.11 – 0.80 –28.9 – –28.2 14 – 14 –
albiflora
Appendix (continued)
FAMILY Basal area (m
2
ha
–1
) δ
13
C (‰) Leaf N concentration (mg g
–1
)
Species Shade Phenol- Area Paracou St-Elie St-Elie Paracou St-Elie St-Elie P Paracou St-Elie St-Elie P
tole- ogy DVD SLD DVD SLD DVD SLD
rance
467
References
Alexandre DH (1991) Comportement hydrique au cours de la sai-
son sèche et place dans la succession de trois arbres guyanais:
Trema micrantha, Goupia glabra et Eperua grandiflora. Ann
Sci For 48:101–112
Bariteau M, Geoffroy J (1989) Sylviculture et regénération nature-
lle en forêt guyanaise. Rev For Fr 41:309–323
Bazzaz FA, Picket STA (1980) Physiological ecology of a tropical
succession: a comparative review. Annu Rev Ecol Syst 11:
287–310
Bena P (1960) Essences Forestières de Guyane. Imprimerie Na-
tionale, Paris
Boggan J, Funk V, Kelloff C, Hoff M, Cremers G, Feuillet C
(1997) Checklist of the plants of the Guianas: Guiana, Suri-
nam, French Guiana. Guyana, Georgetown
Bonal D, Barigah TS, Granier A, Guehl JM (in press) Late stage
canopy tree species with extremely low δ
13
C and high stoma-
tal sensitivity to seasonal soil drought in the tropical rainforest
of French Guiana. Plant Cell Environ
Boulet R (1990) Organisation des couvertures pédologiques des
bassins versants ECEREX. Hypothèses sur leur dynamique.
Mise en valeur de l’écosystème forestier guyanais. INRA-
CTFT, Paris
Brooks JR, Flanagan LB, Buchmann N, Ehleringer JR (1997) Car-
bon isotope composition of boreal plants: functional grouping
of life forms. Oecologia 110:301–311
Buchmann N, Guehl JM, Barigah TS, Ehleringer JR (1997) Inter-
seasonal comparison of CO
2
concentration, isotopic composi-
tion, and carbon dynamics in an Amazonian rainforest (French
Guiana). Oecologia 110:110–120
Chapin FS III, Bret-Harte MS, Hobbie SE, Zhong H (1996) Plant
functional types as predictors of transient responses of arctic
vegetation to global change. J Veget Sci 7:347–358
Charles-Dominique P, Blanc P, Larpin D, Ledru MP, Riéra B,
Sarthou C, Servant M, Tardy C (1998) Forest perturbations
and biodiversity during the last ten thousand years in French
Guiana. Acta Oecologica 19:295–302
Doley D, Unwin GL, Yates DJ (1988) Spatial and temporal distri-
bution of photosynthesis and transpiration by single leaves in a
rainforest tree, Argyrodendron peralatum. Aust J Plant Physiol
15:317–326
Ehleringer JR, Phillips SL, Schuster WSF, Sandquist DR (1991)
Differential utilisation of summer rains by desert plants. Oeco-
logia 88:430–434
Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship
between carbon isotope discrimination and the intercellular
carbon dioxide concentration in leaves. Aust J Plant Physiol
9:121–137
Favrichon V (1994) Classification des espèces arborées en group-
es fonctionnels en vue de la réalisation d’un modèle de dy-
namique de peuplement en forêt Guyanaise. Rev Ecol 49:
379–403
Givnish TJ (1988) Adaptation to sun and shade: a whole plant per-
spective. Aust J Plant Physiol 15:63–92
Grime JP (1977) Evidence for the existence of three primary strat-
egies in plants and its relevance to ecological and evolutionary
theory. Am Nat 111:1169–1194
Guehl JM (1984) Dynamique de l’eau dans le sol en forêt tropic-
ale humide guyanaise. Influence de la couverture pédologique.
Ann Sci For 41:195–236
Guehl JM, Domenach AM, Béreau M, Barigah TS, Casabianca H,
Ferhi A, Garbaye J (1998) Functional diversity in an Amazon-
ian rainforest of French Guiana. A dual isotope approach
(δ
15
N and δ
13
C). Oecologia 116:316–330
Hogan KP, Smith AP, Samaniego M (1995) Gas exchange in six
tropical semi-deciduous forest canopy tree species during the
wet and dry seasons. Biotropica 27:324–333
Huc R, Guehl JM (1989) Environmental control of CO
2
assimila-
tion rate and leaf conductance in two species of the tropical
rain forest of French Guiana (Jacaranda copaia D. Don and
Eperua falcata Aubl.). Ann Sci For 46s:443–447
Huc R, Ferhi A, Guehl JM (1994) Pioneer and late stage tropical
rainforest tree species (French Guiana) growing under com-
mon conditions differ in leaf gas exchange regulation, carbon
isotope discrimination and leaf water potential. Oecologia
99:297–305
Koch GW, Amthor JS, Goulden ML (1994) Diurnal patterns of
leaf photosynthesis, conductance and water potential at the top
of a lowland rain forest canopy in Cameroun: measurements
from the Radeau des Cimes. Tree Physiol 14:347–360
Lacroix G, Abbadie L (1998) Linking biodiversity and ecosystem
function: an introduction. Acta Oecologica 19:189–193
Lescure JP, Boulet R (1985) Relationships between soil and vege-
tation in a tropical rain forest in French Guiana. Biotropica
17:155–164
Lloyd J, Farquhar GD (1994)
13
C discrimination during CO
2
as-
similation by the terrestrial biosphere. Oecologia 99:201–215
Loubry D (1994) Déterminisme du comportement phénologique
des arbres en forêt tropicale humide de Guyane française (5°
lat. N.). PhD Thesis, University of Paris
Martinelli LA, Almeida S, Brown IF, Moreira MZ, Victoria RL,
Sternberg LSL, Ferreira CAC, Thomas WW (1998) Stable car-
bon isotope ratio of tree leaves, boles, and fine litter in a tropi-
cal forest in Rondônia, Brazil. Oecologia 114:170–179
Medina E, Minchin P (1980) Stratification of δ
13
C values of
leaves in Amazonian rainforests. Oecologia 45:377–378
Medina E, Sternberg LSL, Cuevas E (1991) Vertical stratification
of δ
13
C values in closed natural and plantation forests in the
Luquillo mountains, Puerto Rico. Oecologia 87:369–372
Meinzer FC, Goldstein G, Holbrook NM, Jackson P, Cavelier J
(1993) Stomatal and environmental control of transpiration in
a lowland tropical forest tree. Plant Cell Environ 16:429–436
Oldeman RAA, Dijk JV van (1991) Diagnosis of the temperament
of tropical rain forest trees. In: Gomez-Pompa A, Whitmore
TC, Hadley M (eds) Rain forest regeneration and manage-
ment. MAB UNESCO, Parthenon, Oxford, pp 22–64
Panek JA (1996) Correlation between stable carbon-isotope abun-
dance and hydraulic conductivity in douglas-fir across a cli-
mate gradient in Oregon, USA. Tree Physiol 16:747–755
Riéra B, Puig H, Lescure JP (1989) La dynamique de la forêt na-
turelle. Bois For Trop 219:69–78
Roberts J, Cabral OMR, Ferreira De Aguiar L (1990) Stomatal
and boundary-layer conductance in an Amazonian Terra Firme
rainforest. J Appl Ecol 27:336–357
Roggy JC, Prévost MF, Gourbière F, Casabianca H, Garbaye J,
Domenach AM (1999) Leaf natural
15
N abundance and total N
concentration as potential indicators of plant N nutrition in le-
gumes and pioneer species in a rainforest of French Guiana.
Oecologia 120:171–182
Sabatier D, Prévost MF (1990) Quelques données sur la composi-
tion floristique et la diversité des peuplements forestiers de
Guyane Française. Bois For Trop 219:31–55
Sabatier D, Grimaldi M, Prévost MF, Guillaume J, Godron M,
Doso M, Curmi P (1997) The influence of soil cover organisa-
tion on the floristic and structural heterogeneity of a guianan
rainforest. Plant Ecol 131:81–108
Sarrailh JM (1984) Mise en valeur de l’écosystème forestier
guyanais. Opération ECEREX: résumé des premiers résultats.
Bois For Trop 206:13–32
SAS Institute (1989) SAS/STAT user’s guide. release 6.11 edn.
SAS Institute, Cary
Scholander PF, Hammel HT, Bradstreet ED, Hemmingsen EA
(1965) Sap pressure in vascular plants. Science 148:339–
346
Schulze E-D, Williams RJ, Farquhar GD, Schulze W, Landgridge
J, Miller JM, Walker BH (1998) Carbon and nitrogen isotope
discrimination and nitrogen nutrition of trees along a rainfall
gradient in Northern Australia. Aust J Plant Physiol 25:
413–425
Sobrado MA, Ehleringer JR (1997) Leaf carbon isotope ratios
from a tropical dry forest in Venezuela. Flora 192:121–124
Sternberg L, Mulkey SS, Wright SJ (1989) Ecological interpreta-
tion of leaf carbon isotope ratios: influence of respired carbon
dioxide. Ecology 70:1317–1324
Tilman D (1988) Plant strategies and the dynamics and function of
plant communities. Princeton University Press, Princeton
Valentini R, Scarascia Mugnozza GE, Ehleringer JR (1992) Hy-
drogen and carbon isotope ratios of selected species of a Med-
iterranean macchia ecosystem. Funct Ecol 6:627–631
Van Der Merwe NJ, Medina E (1989) Photosynthesis and
13
C/
12
C
ratios in Amazonian rain forests. Geochim Cosmochim Acta
53:1091–1094
468
