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Research
Consistency of species ranking based on functional
leaf traits
Blackwell Science Ltd
E. Garnier1, G. Laurent1, A. Bellmann1, S. Debain1, P. Berthelier1, B. Ducout1, C. Roumet1 and M.-L. Navas1,2
1Centre d’Ecologie Fonctionnelle et Evolutive (CNRS-UPR 9056), 1919, Route de Mende, 34293 Montpellier Cedex 5, France; 2UFR de Biologie et Pathologie
Végétales, ENSA-M, Place Viala, 34060 Montpellier Cedex 2, France
Summary
Author for correspondence:
E. Garnier
Tel: +33 4 67 61 32 42
Fax: +33 4 67 41 21 38
Email: [email protected]
Received: 7 March 2001
Accepted: 18 June 2001
• Specific leaf area (leaf area to dry mass ratio), leaf dry matter content (leaf dry
mass to saturated fresh mass ratio) and leaf nitrogen concentration (LNC) have been
proposed as indicators of plant resource use in data bases of plant functional traits.
• We tested whether species ranking based on these traits was repeatable by
studying spatio-temporal variations in specific leaf area and leaf dry matter content
of water-saturated leaves (SLA SAT and LDMCSAT), as well as in LNC, for 57 herbaceous
and woody species (or subsets thereof) growing under the Mediterranean climate
of southern France.
• Interseason and intersite variations were more pronounced than interannual
variations, but species ranking for a given trait remained mostly consistent in space
and time. Classifications based on LDMCSAT were generally more repeatable across
years and sites, whereas those based on SLASAT were more stable over seasons. LNC
usually gave the least repeatable classifications.
• Species rankings were not completely similar for the three traits. Discussion of
reproducibility, ease of trait measurement, as well as trait–function relationships led
us to propose that measurements of the leaf traits, SLASAT and/or LDMCSAT, were
the most suitable in large screening programmes.
Key words: functional leaf traits, leaf dry matter content, leaf nitrogen concentration,
Mediterranean old fields, plant functional classification, spatio-temporal variability,
specific leaf area, structure-function relationships.
© New Phytologist (2001) 152: 69–83
Introduction
The constitution of a large database of functional traits is
currently gaining high priority in the research agenda of plant
ecology, because it appears as a fundamental step both to
understand and to predict the distribution of species in
present and future environments (Grime et al., 1988; Keddy,
1992; Westoby, 1998), and to relate the functioning of
species to that of ecosystems (Grime, 1997; Chapin et al.,
2000). In the recent debate on which characteristics should
be measured to feed such a database, the inclusion of traits
relevant to the acquisition and use of resources has been
considered of primary importance, and leaf traits have been
proposed to fulfil this aim ( Westoby, 1998; Weiher et al.,
1999).
Three such traits, assumed to affect processes at different
scales have recently been screened: specific leaf area (SLA: the
© New Phytologist (2001) 152: 69 – 83 www.newphytologist.com
ratio of leaf area to leaf dry mass), leaf dry matter content
(LDMC: the ratio of leaf dry mass to saturated fresh mass)
and leaf nitrogen concentration (LNC) (Cunningham et al.,
1999; Reich et al., 1999; Wilson et al., 1999). At the leaf level,
a combination of SLA and LNC has been shown to predict
accurately the maximum photosynthetic rate of a wide range
of species (Reich et al., 1997), and both traits are related to
leaf life-span (Reich et al., 1997), as is the case for LDMC
(Ryser & Urbas, 2000). At the whole-plant level, all three
traits have been found to be involved in a fundamental tradeoff between a rapid production of biomass and an efficient
conservation of nutrients (Grime et al., 1997; Poorter &
Garnier, 1999). Finally, at the ecosystem level, a small amount
of data suggest that SLA (or related leaf traits) and LNC of
component species may have a significant impact on primary productivity and nutrient cycling (Reich et al., 1992;
Cornelissen et al., 1999; Aerts & Chapin, 2000).
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Screening for these traits can be made in experiments
conducted under identical, standardized conditions in the
laboratory (Poorter & Remkes, 1990; Garnier, 1992; Grime
et al., 1997). In this case, a single trait value can be attributed
to a particular species. However, to avoid some of the conceptual pitfalls and technical difficulties of an approach
based on laboratory experiments (Garnier & Freijsen, 1994),
screening procedures may also be carried out in the field
(Díaz & Cabido, 1997; Thompson et al., 1997; McIntyre
et al., 1999), with the consequence that comparisons between
species may be confounded by interactions with the environment. It may, therefore, be asked how traits can be used to
classify species relative to one another in a consistent way, even
if their absolute values vary across environments – that is even
if they are plastic. The aim of this study was to examine this
question for SLA, LDMC and LNC.
All three traits are known to be plastic, but a small amount
of data suggest that species ranking for these traits do not
change substantially in time or across different environments.
For example, Jurik (1986), comparing the SLA of six tree species in two contrasting light situations over a 5-month period,
found only small differences in ranking over time, while the
rank of a single species changed across the two light environments. Similarly, Thompson et al. (1997) collected samples of
six herbaceous species in different sites more than 20 yr apart,
and did not detect any significant effect of site or year of
sampling on LNC values, and thus on species ranking for this
trait. Further evidence is provided by plants growing in the
laboratory and in the field: although the absolute values of
traits may differ substantially across the two environments,
there are usually significant relationships between values
measured on the same species in the field and in the lab
(Poorter & Garnier, 1999). As demonstrated by Abrams et al.
(1994) in a study on 17 temperate tree species, this relative
stability in species ranking for structural traits (SLA and leaf
thickness in particular) translates into a stable functioning
hierarchy (gas exchange in this case) under contrasting environmental conditions.
The main aim of the present study was to test in a more systematic way whether the ranking of species for SLA, LDMC
and LNC remained essentially similar both temporally and
spatially, that is whether species classifications based on each
of these traits are repeatable (sensu Gitay & Noble, 1997). We
used species growing in the Mediterranean region of southern
France to assess how the three traits varied: among seasons at
a given site; between years at a given site; and among years and
sites. The degree of similarity in species rankings given by the
three traits was also compared, that is we tested whether the
classifications obtained were congruent (sensu Gitay & Noble,
1997). To further help select which trait would be most
appropriate for plant classifications (cf. Lavorel, 2001), their
ease of measurement and their reproducibility, estimated by
partitioning their variance at different levels (from replicates
to growth form) were also compared, and their relationships
to different aspects of plant and ecosystem functioning were
discussed.
Materials and Methods
Study sites
The study was conducted between October 1997 and June
1999, at three sites located in southern France (Table 1). At
all sites, the soil is derived from a limestone substrate. The
Table 1 Characteristics of the three study sites
Site
Cazarils (St Martin de
Londres, Hérault)
Camp Redon
(Montpellier, Hérault)
Les Agros
(Bargemon, Var)
Latitude
Longitude
Altitude (min – max) (m)
Average soil pH
43°46′ N
3°42′ E
280 –290
7.1
43°38′ N
3°52′ E
56 –70
8.1
43°25′ N
6°35′ E
400 – 450
8.0
Mean climatic data*
Annual precipitation (mm)
Air temperature (°C)
Minimum air temperature of the coldest month (°C)
Maximum air temperature of the warmest month (°C)
1148
12.8
− 0.8
29.5
785
13.9
0.6
29.9
1041
13.6
− 1.1
31.9
369
509
11.7
12.1
232
352
12.8
12.8
346
332
12.3
12.2
Mean climatic data from January to June**
Precipitation (mm)
Air temperature (°C)
1998
1999
1998
1999
Climatic data were obtained from the nearest meteorological station. *, averaged over 1969 –98 in Cazarils, 1970 –98 in Camp Redon and
1988– 98 in Les Agros. **, calculated for the first six months of 1998 and 1999.
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climate is Mediterranean subhumid (Daget, 1977), with a
marked summer drought, frequent frosts in winter, and
unpredictability of precipitation in timing and amount,
with generally frequent heavy rainfall events in autumn.
Annual rainfall and range in temperature are noticeably
higher in Cazarils and Les Agros than in Camp Redon. Mean
annual temperature is slightly lower in Cazarils than at the
two other sites (Table 1). In Cazarils and Camp Redon,
rainfall was substantially lower between January and June
1998 than over the same time interval of 1999, the two
periods when most measurements were taken (see below); at
all sites, average daily temperatures were comparable in both
years (Table 1).
The main study site, Cazarils, is located 20 km north-west
of Montpellier and 32 km from the Mediterranean coast. It is
typical of the French Mediterranean shrublands on limestone
rocks (i.e. garrigue) (Aronson et al., 1998 for details). Both
interseason and interannual comparisons were conducted at
this site (see below and Table 2). The second site at Camp
Redon, where the CEFE-CNRS experimental station stands,
is located in the northern outskirts of Montpellier, 15 km
from the coast. It consists of a patchwork of old-fields of
different ages (Thébaud et al., 1996 for details). The third site,
Les Agros, is located 220 km east of Montpellier and 27 km
from the coast, on the southern edge of a large limestone plateau.
It consists of a series of south facing terraces formerly cultivated
mainly with olive trees, until the second half of the 19th century. Until c. 20 yr ago, the terraces have been occasionally
grazed by sheep. Since then, they have been regularly cleared.
The vegetation is mostly herbaceous with numerous shrubs,
surrounded by a mixed Pinus halepensis – Quercus ilex woodland. These last two sites – Camp Redon and Les Agros – were
used for the spatio-temporal (i.e. between sites and years)
comparisons (see below and Table 2).
Species and harvests
A maximum of 57 species were selected at Cazarils (Table 2:
May 1998 harvest). These are common species typical of
widespread plant associations found on calcareous soils in
Mediterranean southern France: the Brachypodietum phœnicoidis
(xeric grassland), and a mix of Quercetum galloprovinciale and
Querceto-Buxetum (mixed evergreen-deciduous oak forest)
(Braun-Blanquet et al., 1952). They belong to 25 botanical
families, and span the whole range of life forms described
by Raunkiaer (1934): there were 10 herbaceous annuals
(therophytes), 24 herbaceous perennials (four geophytes
and 20 hemicryptophytes) and 23 woody perennials (eight
chamaephytes and 15 phanerophytes). Subsets of this list were
used to study the variations in leaf traits.
Interseason variation Leaves of 21 species were harvested
four times in Cazarils: in October 1997, January, May and
July 1998. This corresponds, respectively, to the autumn
© New Phytologist (2001) 152: 69 – 83 www.newphytologist.com
period of growth following the summer drought, the period
of cold stress in winter, the peak production period of most
species in spring, and the onset of drought stress in summer
(e.g. Daget, 1977). Phenological patterns differed among
the species studied, with the consequence that leaves were
not present for all species at all dates. The number of
species sampled thus varied from 16 to 21 among harvests
(Table 2).
Interannual variation This was examined at Cazarils on the
whole set of species except Phillyrea latifolia (an evergreen
small tree), which did not produce new leaves at that site in
1999. Harvests were conducted between 19 May and 3 June
in 1998 (‘May 98’ hereafter), and between 11 May and 17 June
in 1999 (‘May 99’ hereafter).
Spatio-temporal variation In Camp Redon and Les Agros,
we selected species previously found in Cazarils in May 1998
(Table 2): there were 28 species in Camp Redon, collected
between 5 May and 15 June 1999, and 18 species in Les
Agros, collected on 25 and 26 May 1999.
The harvest conducted in Cazarils in May 1998 was set as
the ‘reference harvest’ for this study, because it corresponds to
the period of peak production of most species, and the largest
set of species was sampled at that time.
Sampling and measurements of leaf traits
All material was collected from robust, well grown plants. For
herbaceous and small woody species, samples were taken from
plants in full light (i.e. not under tree cover), while for tall
woody species, these were taken from the part of the plant
lit by direct sunlight at the time of sampling. Measurements
of leaf traits were conducted on 10 replicate samples per species. For most species, these corresponded to 10 different
individuals, except for phanerophytes for which two replicates
were taken from each of five individuals. Stems or twigs
bearing between 1 and 30 leaves were severed from a plant,
rapidly wrapped in moist paper, placed in plastic bags and
stored in a cool box until further processing in the laboratory.
As soon as possible – approx. 5–6 h after field collection –
each sample was recut under deionized water to remove
approx. 1 cm of stem or petiole, and placed immediately
into a test-tube filled with deionized water. The tubes
were then stored in a dark, cold room at 4°C for at least
14 h. This whole procedure (recutting under water and
storage in tubes) insured full rehydration of leaves, and
allowed us to determine the water-saturated values of SLA
and LDMC (SLASAT and LDMCSAT hereafter) (Garnier
et al., 2001).
After this period and for each replicate sample, the youngest fully expanded leaves free from herbivore or pathogen
damage were severed from the stem or twig. All subsequent
manipulations were carried out on leaf blades only, that is
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Table 2 List of species studied (nomenclature follows Tutin et al., 1968 –1980; 1993). Life forms according to Raunkiaer (1934) were taken from
Braun-Blanquet et al. (1952), de Bolòs et al. (1993) and completed with personal observations
Site
Cazarils
Species
Family
Life form
Acer monspessulanum
Aegilops geniculata
Anagallis arvensis
Aristolochia rotunda
Avena barbata
Avenula bromoides
Brachypodium distachyon
Brachypodium phoenicoides
Bromus erectus
Bromus lanceolatus
Bupleurum rigidum
Buxus sempervirens
Calamintha nepeta
Carex hallerana
Catananche coerulea
Clematis vitalba
Convolvulus arvensis
Crataegus monogyna
Crepis sancta
Crepis vesicaria
Dactylis glomerata
Daucus carota
Dorycnium hirsutum
Dorycnium pentaphyllum
Echinops ritro
Eryngium campestre
Helianthemum nummularium
Juniperus oxycedrus
Kickxia spuria
Lavandula latifolia
Lonicera etrusca
Lotus corniculatus
Medicago minima
Phillyrea latifolia
Phleum pratense
Pistacia terebinthus
Plantago lanceolata
Potentilla crantzii
Prunus mahaleb
Prunus spinosa
Psoralea bituminosa
Quercus ilex
Quercus pubescens
Rosa micrantha
Rubia peregrina
Rubus sp.
Ruscus aculeatus
Sanguisorba minor
Scabiosa atropurpurea
Stachys officinalis
Teucrium chamaedrys
Thymus vulgaris
Trifolium angustifolium
Urospermum dalechampii
Viburnum tinus
Viola scotophylla
Xeranthemum inapertum
Aceraceae
Gramineae
Primulaceae
Aristolochiaceae
Gramineae
Gramineae
Gramineae
Gramineae
Gramineae
Gramineae
Umbelliferae
Buxaceae
Labiatae
Cyperaceae
Compositae
Ranunculaceae
Convolvulaceae
Rosaceae
Compositae
Compositae
Gramineae
Umbelliferae
Leguminosae
Leguminosae
Compositae
Umbelliferae
Cistaceae
Cupressaceae
Scrophulariaceae
Labiatae
Caprifoliaceae
Leguminosae
Leguminosae
Oleaceae
Gramineae
Anacardiaceae
Plantaginaceae
Rosaceae
Rosaceae
Rosaceae
Leguminosae
Fagaceae
Fagaceae
Rosaceae
Rubiaceae
Rosaceae
Liliaceae
Rosaceae
Dipsacaceae
Labiatae
Labiatae
Labiatae
Leguminosae
Compositae
Caprifoliaceae
Violaceae
Compositae
Ph. (W)
Th. (H)
Th. (H)
Ge. (H)
Th. (H)
He. (H)
Th. (H)
He. (H)
He. (H)
Th. (H)
He. (H)
Ph. (W)
Ch. (W)
He. (H)
He. (H)
Ph. (W)
Ge. (H)
Ph. (W)
Th. (H)
He. (H)
He. (H)
He. (H)
Ch. (W)
Ch. (W)
He. (H)
Ge. (H)
Ch. (W)
Ph. (W)
Th. (H)
Ch. (W)
Ph. (W)
He. (H)
Th. (H)
Ph. (W)
He. (H)
Ph. (W)
He. (H)
He. (H)
Ph. (W)
Ph. (W)
He. (H)
Ph. (W)
Ph. (W)
Ph. (W)
Ch. (W)
Ph. (W)
Ge. (H)
He. (H)
He. (H)
He. (H)
Ch. (W)
Ch. (W)
Th. (H)
He. (H)
Ph. (W)
He. (H)
Th. (H)
Oct 97
Jan 98
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
May 98
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
July 98
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
Camp Redon
Les Agros
May 99
May 99
May 99
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
Therophytes (Th.), geophytes (Ge.) and hemicryptohytes (He.) were grouped into « herbaceous » species (H), while chamaephytes (Ch.) and phanerophytes
(Ph.) were grouped into « woody » species (W). The species harvested at each site and sampling date are given as (X).
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after removal of petioles or rachis in the case of compound
leaves. A sufficient number of leaves (from one in, e.g. trees, to
20–30 in, e.g. Thymus vulgaris) was taken to reach a minimum
cumulated area of 2 cm2 per replicate. Leaf blades were dried
with tissue paper to remove any surface water, and immediately weighed to determine their saturated fresh mass. Their
projected area (one side of the leaves) was determined with an
area meter (Delta-T Devices, Cambridge, UK, model MK2).
Samples were then oven-dried at 60°C for at least 2 d, and dry
mass determined.
For each species, two or three leaf samples were subsequently pooled together to obtain three to five batches
(four in 75% of cases) for nitrogen analyses. These bulked
samples were then ground individually, and their total
nitrogen concentration determined with an elemental
analyser (Carlo Erba Instruments, model EA 1108, Milan, Italy).
Treatment of data
SLASAT and LDMCSAT were transformed to their natural
logarithms before analyses to meet assumptions of the
ANOVA. Differences in SLASAT, LDMCSAT and LNC
among seasons (season), years (year) and sites (site) were tested
with two-way ANOVA, with species and either season, year
or site as main factors, using species common to all modalities
of a given factor (cf. Table 2). Trait plasticity was assessed
using coefficients of variation (CV ): within species, CVINTRA
was calculated using the mean values of traits obtained
for each modality of a given factor; and among species, the
average plasticity of a particular trait for a given factor,
CVINTER, was assessed by averaging the CVINTRA of each species.
Spearman rank correlation coefficients were calculated to
test whether the ranking of species for a given trait was conserved over time and space. Unless otherwise stated, ranking
was always tested against that obtained in Cazarils in May
1998 (reference harvest). Data from that harvest were also
used: to analyse how the variance of each leaf trait was
partitioned among replicates, species, life forms and growth
forms (i.e. herbaceous vs woody), using a nested analysis of
variance; and to test whether species rankings obtained for the
different traits were comparable, calculating Spearman rank
coefficients among traits.
Statistical analyses were performed with the Statgraphics
Plus package (Manugistics, Rockville, MA, USA) for two-way
ANOVAs and rank correlations, and with the Statistical
Analysis System (SAS Institute, Cary, NC, USA) for nested
ANOVAs (NESTED procedure).
Results
Overview of leaf traits for the ‘reference harvest’
SLASAT, LDMCSAT and LNC varied substantially among the
57 species harvested in Cazarils in May 1998 (Appendices
© New Phytologist (2001) 152: 69 – 83 www.newphytologist.com
Table 3 Results of hierarchical ANOVAs for specific leaf area
(SLASAT), leaf dry matter content (LDMCSAT) and leaf nitrogen
concentration (LNC). Results are the percentage of the total variance
accounted for at each level
Trait
Growth form*
Life form**
Species
Replicate
SLASAT
LDMCSAT
LNC
25
28
6
23
6
1
40
57
82
12
9
11
*, growth form refers to herbaceous vs. woody species. **, life form
refers to Raunkiaer’s (1934) classification (cf. Table 2).
1–3). SLASAT varied from 6.0 ± 0.3 to 31.7 ± 1.1 m2 kg−1,
LDMCSAT from 131 ± 3 to 472 ± 13 mg g−1, and LNC from
0.79 ± 0.01 to 2.79 ± 0.10 mmol g−1.
The greatest variance was observed at the species level for
all traits, especially LNC (Table 3). Growth form explained
more than 25% of the variance in SLASAT and LDMCSAT:
woody species had lower SLASAT (13.4 ± 1.2 m2 kg−1) and
higher LDMCSAT (338 ± 16 mg g−1) than herbaceous species
(17.8 ± 1.0 m2 kg−1 and 263 ± 12 mg g−1, respectively). For
SLASAT, a substantial part of the variance was due to life form:
this was mainly due to therophytes having a significantly
higher SLASAT than other species (23.5 ± 1.3 vs 14.5 ±
0.7 m2 kg−1). Replicates accounted less of the variance than
species, and their contribution was slightly higher for SLASAT
and LNC than for LDMCSAT (Table 3).
Since a substantial part of the variance was accounted for
by growth form for two of the traits studied (SLASAT and
LDMCSAT), particular attention will be paid to the difference
between herbaceous and woody species.
Trait variation
Results of two-way ANOVAs testing for the effects of species,
season, year and site on SLASAT, LDMCSAT and LNC are
shown in Fig. 1. The species effect was always significant.
Differences between seasons and sites were also significant
(Fig. 1a,d,g,c,f,i), as well as those between years for SLASAT
and LDMCSAT (Fig. 1b,e), but not for LNC (Fig. 1h ). The
interactions between species and each of the three other
factors were all significant (Fig. 1). These effects will now be
examined successively, combining results shown in Fig. 1 with
data obtained on all individual species, taking the May 1998
harvest conducted in Cazarils as a reference.
Interseason variation Average SLASAT and LNC remained
relatively stable from October to May, and decreased in July
(−24% for SLA and −34% for LNC: Fig. 1a,g). In herbaceous
species, SLASAT and LNC decreased gradually from October
( January for LNC) to July. Both traits were more stable in
woody species, but they nevertheless displayed higher values
in May (Fig. 2a–c,g –i). Average LDMCSAT was lowest in
May (Fig. 1d), especially in woody species (Fig. 2d–f ).
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Fig. 1 Patterns of spatio-temporal variations
in specific leaf area (SLASAT), leaf dry matter
content (LDMCSAT) and leaf nitrogen
concentration (LNC) for species growing in
the Mediterranean region of southern
France. (a, d, g) Interseason variations of
traits for the 12 species harvested at each
of four sampling dates at the Cazarils site:
(b, e, h) interannual variations of traits for the
56 species measured in May 1998 and May
1999 at the Cazarils site; (c, f, i) spatiotemporal variations of traits for the 11
common species collected in Cazarils in May
1998 (Caza 98), in Camp Redon (CRed 99)
and Les Agros (Agro 99) in May 1999. Mean
leaf trait values of each species are
represented by open circles and the average
values across species for a given harvest are
represented by closed circles. F-values of
two-way analyses of variance are given on
panels for main effects and their interactions:
Se, sampling season; Sp, species; Yr, sampling
year; Si, sampling site. All effects and
interactions are significant at the 0.001 level,
except that of sampling year on LNC (not
significant). CVINTER is the average coefficient
of variation of the trait calculated among
species.
Species ranking for all three traits was relatively well
conserved among seasons (Table 4; Fig. 2), either when tests
were performed on the whole set of species, or on each growth
form separately (except for SLASAT in herbaceous species
and LNC in woody species at the beginning of summer).
Although seasonal variations were larger in SLASAT than in
LDMCSAT (compare CVINTER values in Fig. 1a,d and see
Fig. 2), ranking was better conserved for the former (Table 4).
LNC was the most variable trait over seasons (cf. Figure 1a,d,g
and Fig. 2), and that for which the ranking was least conserved
(Table 4).
Interannual variation On average, SLASAT, LDMCSAT
and LNC varied less between years than they did between
seasons (Fig. 1). Averaged over the 56 species measured, SLASAT
was significantly higher (+3%: Fig. 1b) and LDMCSAT was
significantly lower (−1%: Fig. 1e) in 1999 as compared to
1998, while LNC did not differ between years (Fig. 1h).
However, there were differences between growth forms (Fig. 3):
in herbaceous species, SLASAT and LNC (respectively
LDMCSAT) were higher (respectively lower) in 1999 than
in 1998. In woody species, SLASAT and LDMCSAT were very
stable, while LNC was lower in 1999 than in 1998.
For the three traits, species ranking remained similar
between the two years of sampling, even when growth forms
were analysed separately (Fig. 3a–c, Table 4). The ranking of
species was better conserved for LDMCSAT than for SLASAT
or LNC (Table 4), which may be linked to its lower interannual variability (compare CVINTER values on Fig. 1b,e,h,
and see Fig. 3a–c).
Spatio-temporal variation On average, SLASAT and LNC
were highest in Les Agros and lowest in Cazarils (Fig. 1c,f,i: 11
and 8% difference, respectively), with intermediate values
in Camp Redon. In Camp Redon, SLASAT and LNC of
herbaceous species were higher than in Cazarils, while this
was true for species of both growth forms in Les Agros
(Fig. 4a,b,e,f ). Both traits were more variable in herbaceous
(average CVINTRA, 18%) than in woody species (average
CVINTRA, 11%). LDMCSAT was significantly lower in Camp
Redon and Les Agros than in Cazarils (−4% and −8%,
respectively), because of the lower values of herbaceous species
in Camp Redon and of both growth forms in Les Agros
(Fig. 4c,d).
Ranking for all species pooled together did not differ
significantly between Cazarils and either of the other sites for
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Fig. 2 Patterns of interseason variations in
(a – c) specific leaf area (SLASAT) (d– f ) leaf dry
matter content (LDMCSAT) and (g– i) leaf
nitrogen concentration (LNC), for
herbaceous (open circles) and woody (closed
circles) species sampled at the Cazarils site
between October 1997 and July 1998.
Values of traits obtained during the May
1998 harvest were taken as reference values
(X-axes). The dotted line represents the 1 : 1
line. Spearman ranking coefficients for the
various comparisons are given in Table 4. Bars
represent standard error of means (not
shown when smaller than symbol).
Table 4 Spearman ranking coefficients for the leaf traits measured in Cazarils during different seasons (inter-season variation), years
(interannual variation) and sites (spatio-temporal variation): specific leaf area (SLASAT), leaf dry matter content (LDMCSAT) and leaf nitrogen
concentration (LNC). The reference ranking is taken in Cazarils in May 1998. Comparisons were conducted separately for herbaceous (Herb.)
and woody species, and for all species pooled together (all)
Interseason variation
Oct 97
May 99
C. Redon
Growth form
SLASAT
Herb.
Woody
All
0.94*
0.94**
0.89***
0.95*
0.91*
0.89***
0.49n.s.
0.90**
0.87***
0.85***
0.79***
0.86***
0.70**
0.96**
0.87***
0.60n.s.
0.71*
0.65**
LDMCSAT
Herb.
Woody
All
0.89*
0.81*
0.77**
0.87*
0.81*
0.67**
0.94*
0.84**
0.87***
0.89***
0.87***
0.90***
0.91***
0.86**
0.92***
0.71(a)
0.90**
0.88***
LNC
Herb.
Woody
All
0.94*
0.58(a)
0.62*
0.55n.s.
0.69(a)
0.59*
0.94*
0.49n.s.
0.60*
0.78***
0.80***
0.75***
0.70**
0.74*
0.73***
0.77(a)
0.85**
0.80***
n
Herb.
Woody
All
8
9
17(†)
July 98
Spatio-temporal variation
Traits
6
10
16
Jan 98
Interannual
variation
6
11
17
34
22
56
17
11
28
Les Agros
6
12
18
Significance level is indicated as: (a), P < 0.10; *, P < 0.05; **, P < 0.01; ***, P < 0.001; n.s., not significant. (n) is the number of species for each
comparison. (†), n = 17, except for SLASAT where n = 16 (missing data for Brachypodium distachyon).
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76 Research
the three traits (Table 4). However, for herbaceous species, the
ranking was not conserved between Cazarils and Les Agros,
probably a consequence of the low number of common
species (n = 6: cf. Table 2). Species ranking was better conserved among sites for LDMCSAT than for the two other traits
(Table 4). Again, this could be related to the lower among
site variability in LDMCSAT (compare CVINTER values in
Fig. 1c,f,i and see Fig. 4).
When the reference ranking was taken from the May 1999
harvest instead of the May 1998 one (both in Cazarils), results
were qualitatively similar, with improved values of Spearman
coefficients (range: 0.79–0.96 instead of 0.65–0.92).
Comparison of species ranking among traits
To test whether the ranking of species remained similar for
the three traits measured, Spearman ranking coefficients were
calculated among traits for species harvested at Cazarils in
May 1998. Coefficients were all significant when the analysis
was conducted on all species together (Table 5). They were
negative between LDMCSAT and both SLASAT and LNC, and
positive between SLASAT and LNC. The ranking was better
conserved when SLASAT was involved in the comparison. The
same trends were found when species were pooled by growth
form, with higher coefficient values for woody than for
herbaceous species.
Discussion
Inter- vs intraspecific variability in leaf traits
The stability of species ranking for a given trait among
different environments depends on the direction of trait
response to environmental variations and on the relative
magnitude of inter- vs intraspecific variability for this trait.
This can be illustrated for theoretical cases involving two
species growing in two environments (Fig. 5). Species ranking
remains stable when:
• traits are not plastic, or are similarly plastic for all species
(Fig. 5a,b), i.e. when there is no significant difference among
species in trait response to environment;
• traits show differential plasticity in response to changes in
the environment, but:
Fig. 3 Patterns of interannual variations in (a) specific leaf area
(SLASAT) (b) leaf dry matter content (LDMCSAT) and (c) leaf nitrogen
concentration (LNC), for herbaceous (open circles) and woody
(closed circles) species sampled at the Cazarils site in May 1998 and
May 1999. Values of traits obtained during the May 1998 harvest
were taken as reference values (X-axes). The dotted line represents
the 1 : 1 line. Spearman ranking coefficients for the various
comparisons are given in Table 4. Bars represent standard error of
means (not shown when smaller than symbol).
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Fig. 4 Patterns of spatio-temporal variations
in (a,b) specific leaf area (SLASAT) (c,d) leaf
dry matter content (LDMCSAT) and (e,f) leaf
nitrogen concentration (LNC), for
herbaceous (open circles) and woody (closed
circles) species sampled at the Cazarils site in
May 1998, and at the Camp Redon and Les
Agros sites in May 1999. Values of traits
obtained in Cazarils during the May 1998
harvest were taken as reference values
(X-axes). The dotted line represents the 1 : 1
line. Spearman ranking coefficients for the
various comparisons are given in Table 4. Bars
represent standard error of means (not
shown when smaller than symbol).
Table 5 Spearman ranking coefficients calculated among leaf traits for species harvested in Cazarils in May 1998 : specific leaf area (SLA SAT),
leaf dry matter content (LDMCSAT) and leaf nitrogen concentration (LNC). Comparisons were conducted separately for herbaceous and woody
species, and for all species pooled together (all)
Herbaceous (n = 34)
Woody (n = 23)
All (n = 57)
Trait
SLASAT
LDMCSAT
SLASAT
LDMCSAT
SLASAT
LDMCSAT
LDMCSAT
LNC
− 0.32(a)
0.33(a)
−
− 0.36*
− 0.73***
0.62**
−
− 0.60**
− 0.57***
0.51***
−
− 0.47***
Significance level is indicated as: (a), P < 0.10; *, P < 0.05; **, P < 0.01; ***, P < 0.001. The number of species for each comparison is given
between brackets.
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Fig. 5 Hypothetical variations in trait values of two species (each
represented by a single symbol) growing both in different
environmental conditions (A and B). Variations depicted in panels a to
d lead to a similar ranking of species in the two conditions, while those
depicted in e and f lead to a situation where ranking is not maintained.
- the difference in plasticity between species remains lower
than their initial difference, when the direction of trait
response to environment is identical for the two species
(Fig. 5c), or
- the sum of changes in trait values of the two species remains
lower than their initial difference, when the direction of trait
response to environment differs between the two species
(Fig. 5d).
In other cases (Fig. 5e,f ), species ranking is not maintained.
In the present study, intraspecific variability may be due to
genotypic variation and/or to phenotypic plasticity of genotypes. Plants of the same species harvested at different sites are
probably genetically different, but plants harvested at a given
site over seasons or in different years are likely to belong to the
same populations (even to the same genotypes in the case of
tall woody species). Most temporal variation in leaf traits
may then be attributable to phenotypic plasticity, while for
spatial variation, genotypic differences obviously also come
into play.
Whatever the explanation for intraspecific variability, leaf
traits varied more among than within species, but with differ-
ent relative magnitudes of inter- vs intraspecific variability.
Interspecific variability was larger for SLASAT (5.3-fold variation) than for both LDMCSAT and LNC (3.6 and 3.5-fold
variation, respectively) (Fig. 3 and Appendices A-C), as
already found in the few large scale comparative studies where
all three traits have been measured on the same set of species
(Cornelissen et al., 1997; Cunningham et al., 1999; Niinemets,
1999). Here, intraspecific variability was highest for SLASAT
(2.6-fold maximum variation), lowest for LDMCSAT (1.8-fold)
and intermediate for LNC (2.2-fold) (Figs 1–4). The difference between inter- and intraspecific variability was therefore
larger for SLASAT than for LDMCSAT and LNC, as also found
in studies comparing inter- and intraspecific variability of these
traits for more than 10 species. For example, in a study comparing 10 species growing at a range of Mediterranean sites
(N. Díaz Burlinson & P. Roche, unpublished), SLA varied by
a factor of 15 among species, and by a factor of 11 for the most
variable of these species, while these values were 13 and
3.5 for LDMC (traits determined without rehydrating leaves).
Similarly, for 40 temperate species growing in habitats of contrasting productivity, SLASAT varied more among (ninefold
difference) than within (3.5-fold difference) species (Poorter
& de Jong, 1999). By contrast, intraspecific variability in
LNC among sites can be higher than interspecific variability
(Grimshaw & Allen, 1987), in relation to a higher sensitivity
to soil nutrient status compared to SLASAT or LDMCSAT.
Species ranking is thus expected to be better conserved for
SLASAT and LDMCSAT than for LNC.
But what are the causes of intraspecific variability in leaf
traits, and how does it affect species ranking?
Causes of variation in leaf traits and effects on
species ranking
Interseason variation Leaf traits of herbaceous species varied
more than those of woody species, and on average SLASAT
and LNC varied more than LDMCSAT (Figs 1 and 2). For
herbaceous species the decrease in SLASAT observed from
October to July may be the consequence of changes in light
level and air temperature during this period (steady increase
from January to July) (e.g. Ku & Hunt, 1973; Björkman,
1981) or in water availability (e.g. Ehleringer & Cook, 1984),
particularly in spring, or of leaf ageing during periods of
low leaf production (winter and end of spring), as cell wall
and lignin concentrations tend to increase (Wilson, 1976).
The same factors are likely to explain the seasonal variation in
LDMCSAT observed here (Figs 1b and 2d–f ), at least partially
(Pammenter et al., 1986; Gond et al., 1999). For woody
species, the changes in SLASAT and LDMCSAT observed
during the period of rapid leaf production in spring (Fig. 2)
are well documented ( Jurik, 1986; Hevia et al., 1999, for
SLA; Leroy, 1968; Tognetti et al., 2000, for LDMC), and
suggest that leaves sampled in May, although fully expanded,
were probably not completely mature.
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Seasonal variations in LNC were similar to those in
SLASAT. In herbaceous species, the regular decrease observed
from January to July (Fig. 2g–i) may be related to dilution by
stored carbohydrates as light level increases (Linder, 1995)
and/or to nutrient deficiency induced by low water availability, triggering retranslocation of nitrogen towards storage
organs (Harrington et al., 1989). In woody species, LNC
values were highest in May in newly produced leaves, and
tended to stabilize when leaves were mature (from July in the
present study), as found in other studies (Escudero et al.,
1987; Hevia et al., 1999).
To classify species relative to one another, traits should be
measured on mature leaves whose physiological activities
are optimal and stable ( Jurik, 1986; Escudero et al., 1987;
Reich et al., 1992). Here, the largest seasonal variations were
induced by summer drought in herbaceous species and by
processes related to leaf maturation during spring in woody
species. Measurements should thus be conducted in May in
herbaceous species and in July in woody species, by which
time leaves will have reached at least 15–25% of their total
life-span (Reich et al., 1992). This recommendation is valid
when working under most of the Mediterranean climate in
the Northern hemisphere, but should be adapted according to
the particular environmental conditions prevailing at the sites
where species are sampled.
Species ranking was relatively well maintained over the
seasons, with SLASAT giving the most stable hierarchy
(Table 4), as also suggested by other studies ( Jurik, 1986;
Gratani & Crescente, 1997; Poorter & de Jong, 1999) (Spearman coefficient > 0.83; P < 0.05 in all cases). Ranking based
on LDMCSAT was less stable than that based on SLASAT. LNC
gave the least stable ranking over seasons (Table 4), indicating
substantial interactions between species and environmental
conditions and/or phenology.
Interannual variation Interannual changes in leaf traits were
small compared with within years variations (Fig. 1), and may
be the consequence of the higher rainfall observed in Cazarils
in 1999 as compared with 1998 (Table 1). Species occurring
in environments with high water availability have higher
SLA (Dìaz & Cabido, 1997; Cunningham et al., 1999) and
lower LDMC (Cunningham et al., 1999) than those from
dryer sites, whereas differential water availability does not
seem to affect LNC (Foulds, 1993; Cunningham et al., 1999).
The ranking of species was better conserved between years
than among seasons for LDMCSAT and LNC, but not for
SLASAT (Table 4). LDMCSAT gave the most stable ranking
and again, LNC gave the least stable one.
Spatio-temporal variations Significant intersite variations
were found for the three traits studied (Fig. 1c,f,i). Differences
in LNC values suggest that soil fertility was highest in Les
Agros, intermediate in Camp Redon and lowest in Cazarils.
Trends in SLASAT and LDMCSAT agree with this hypothesis,
© New Phytologist (2001) 152: 69 – 83 www.newphytologist.com
since SLASAT is usually higher (Cunningham et al., 1999;
Poorter & de Jong, 1999) and LDMCSAT lower (Cunningham
et al., 1999) in fertile than infertile sites. Other factors (e.g.
rainfall, temperature: see Table 1) may explain some of these
differences between sites as well, but their effect cannot be
assessed properly with the data available.
Species ranking was relatively well conserved across sites,
especially for LDMCSAT (Table 4). To further test whether
species classifications remained stable over space and time, the
ranking of a subset of species harvested in May 1998 at
Cazarils was compared with those obtained from three other
studies. Two were conducted in southern France (Garnier
et al., 1997; Lebreton et al., 1997), while the third one was conducted in Central England ( J. H. C. Cornelissen, K. Thompson
and J. G. Hodgson, unpublished). Within Mediterranean
sites, Spearman ranking coefficients were all significant (Table 6).
Species ranking was very well maintained between Cazarils
and Sheffield for SLASAT and LDMCSAT, in spite of the lower
SLASAT (15.4 ± 1.4 vs 20.2 ± 2.5 m2 kg−1, P < 0.01), and
higher LDMCSAT (315 ± 19 vs 291 ± 26 mg g−1, P = 0.11)
values in Cazarils (Table 6). LNC values were slightly lower in
Cazarils than in Sheffield (1.36 ± 0.11 vs 1.55 ± 0.11 mmol g−1,
P = 0.11), and the ranking based on this trait was only marginally conserved.
Overall, these results further confirm that classifications
based on LDMCSAT and SLASAT are more stable than those
based on LNC.
Table 6 Spearman ranking coefficients calculated from published
data obtained in three different sites and calculated for three leaf
traits: specific leaf area (SLASAT), leaf dry matter content (LDMCSAT)
and leaf nitrogen concentration (LNC). The reference ranking was
taken in Cazarils in May 1998. Sites 1 and 2 are in southern France
(Garnier et al., 1997; Lebreton et al., 1997), site 3 is located in
Central England, in the vicinity of Sheffield (J. H. C. Cornelissen,
K. Thompson and J. G. Hodgson, unpublished)
Site
Leaf traits
1
2
3
SLASAT
LDMCSAT
LNC
n
0.72*
−
0.90*
9
−
−
0.88*
8
0.80***
0.87***
0.56(a)
17, 12(†)
Significance level is indicated as: (a), P < 0.10; *, P < 0.05; ***,
P < 0.001. n indicates the number of species for each comparison.
(†)
: n is 17 for SLASAT and LDMCSAT and 12 for LNC. Species used for
these tests are: Site 1 (SLA determined on non-rehydrated leaves):
A. geniculata, A. barbata, A. bromoides, B. distachyon,
B. phoenicoides, B. erectus, B. lanceolatus, D. glomerata, P. pratense.
Site 2: B. sempervirens, J. oxycedrus, L. etrusca, P. latifolia,
P. terebinthus, P. bituminosa, Q. ilex, V. tinus. Site 3: B. erectus,
B. sempervirens, C. monogyna, D. glomerata, H. nummularium,
L. corniculatus, P. lanceolata, P. spinosa, Q. ilex, R. sp., S. minor,
V. tinus, A. arvensis, C. arvensis, D. carota, P. pratense, S. officinalis.
The LNC of the five latter species was not available.
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80 Research
The choice of leaf traits for plant classifications
Species rankings may differ for the three traits studied,
especially within herbaceous species (Table 5). The classifications obtained are thus not completely congruent. Since in
large screening programmes, it is unlikely that all three traits
will be measured (Westoby, 1998; Lavorel, 2001), we will now
examine which one would be best to retain. The relationships
between leaf traits and functions will be briefly reviewed before
discussing the robustness of species ranking (repeatability of
classification) obtained for the three traits, the reproducibility
of their measurement, and their comparative ease of
measurement.
Trait-function relationships The three leaf traits studied
here were selected on the basis of their assumed or
demonstrated relationships with function at different scales:
• at the leaf level, positive associations are usually found
between SLA, LNC and net photosynthetic rate per unit mass
(Amax: Reich et al., 1997; Garnier et al., 1999) while this
association is negative for LDMC (Garnier et al., 1999;
Niinemets, 1999). SLA and LNC are important in photosynthesis because SLA expresses how much area a leaf displays per unit mass, hence giving an index of light capture,
and LNC is related to the amount of photosynthetic
machiney per unit mass (Evans & Seemann, 1989). The
causal link with LDMC is less straightforward, but may be
due to the fact that the fraction of the leaf volume occupied
by mesophyll – the tissue where CO2 fixation takes place – is
higher in low LDMC leaves (Garnier & Laurent, 1994).
Whatever the underlying causes, in interspecific comparisons,
correlations between SLA and Amax are usually tighter than
those involving LNC (Reich et al., 1997; Garnier et al., 1999)
or LDMC (Garnier et al., 1999);
• at the whole-plant level, all three traits are also correlated
with relative growth rate (RGR: Wright & Westoby, 2001;
Poorter & Garnier, 1999) and are involved in a trade-off in
whole-plant functioning, between a rapid production of
biomass (high RGR, SLA and LNC; low LDMC) and an
efficient conservation of nutrients (low RGR, SLA and LNC;
high LDMC), as low RGR species tend to have long-lived
leaves (Reich, 1998), which increases the time nutrients
remain within the plant (Eckstein et al., 1999; Aerts &
Chapin, 2000). Which of these traits captures best this tradeoff remains to be established, and a combination of at least
two traits related to resource use may prove useful, as is the
case to predict plant strategies (Hodgson et al., 1999: SLA and
LDMC in this particular case);
• at the ecosystem scale, since net primary productivity
(NPP) depends on the RGR of individual species (Chapin,
1993), we may hypothesize that leaf traits related to RGR will
also be related to NPP. A small amount of data suggest that
this is the case, at least for SLA (Reich et al., 1997). Similarly,
the decomposition of leaf litter depends on its chemical
composition and structure (Heal et al., 1997; Aerts &
Chapin, 2000), and whether it can be related to the properties
of living tissues is an area of intensive research (Berendse,
1994; Cornelissen et al., 1999).
Repeatability of classification Across seasons, classifications
based on SLASAT were generally the most repeatable (Table 4).
In interannual and spatio-temporal comparisons, LDMCSAT
usually gave the most repeatable classifications, while in most
cases, LNC gave the least repeatable (Tables 4 and 6).
Classifications based on structural traits thus appear to be
more repeatable than those based on biochemical ones. This
can also be deduced from the study by Hevia et al. (1999),
who showed that SLA varied less than LNC and leaf
phosphorus concentration during the course of a growing
season in three congeneric tree species. This conclusion can
probably be extended to all foliar nutrients, since nitrogen was
the least variable among 10 nutrients measured in the leaves of
15 species growing in different sites (Grimshaw & Allen, 1987).
Reproducibility of measurement Few studies have compared
the partitioning of variance among hierarchical levels for
several leaf traits (Table 3). Comparing the SLASAT and
LDMCSAT of 769 species from Central England, Wilson et al.
(1999) concluded that LDMCSAT should be preferred to
SLASAT as a descriptor of plant resource use, because of the
substantially higher among-replicate variation in the latter
(38% and 18% of variance accounted for at the replicate
level for SLASAT and LDMCSAT, respectively). This was less so
in the present study, where these figures were 12 and 9%,
respectively (Table 3). Working on 34 species of herbaceous
angiosperms, Shipley (1995) even found that the variability
between individuals of a species and between leaves of an
individual was lower for SLASAT than for LDMCSAT. High
between-replicate variance in SLASAT can result from errors
in the measurement of leaf area (Wilson et al., 1999, see
below) or from incomplete rehydration of leaf tissues before
measurement, especially in high SLASAT leaves (Garnier et al.,
2001). Discrepancies between reproducibility of measurement among studies may well result from differences in the
experimental procedures followed to determine SLASAT and
LDMCSAT (rehydration in particular), which thus require
careful standardization (Garnier et al., 2001). Finally, amongreplicate variability in LNC was comparable to that in SLASAT
(Table 3), but it is not possible to assess the generality of
this conclusion from published experiments, since nested
ANOVA have usually not been conducted.
Logistics LDMCSAT is by far the easiest trait to measure
among the three. It requires only a careful preconditioning
of samples for the leaves to reach full turgor (Garnier et al.,
2001), and measurements can be taken with only one piece of
equipment. The determination of SLASAT requires that leaf
area be measured, which is relatively time consuming and
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requires the use of additional equipment. As stressed by
Wilson et al. (1999), measuring the area of a leaf may not be
without problems, since it implies a decision as to which area
should be measured (e.g. in vertical, rolled up leaves or
needles, in succulent species). Finally, for LNC, the processing
of samples after the harvests (grinding and preconditioning
before analysis) and the analytical device required (be it for a
Kjeldahl procedure or an elemental analysis) makes it the
most difficult, time consuming and expensive trait to obtain.
Conclusion
Specific leaf area, leaf dry matter content and leaf nitrogen
concentration all display some variations within species. The
ranking of traits in order of decreasing preference for each of
the three criteria directly examined in the present study is the
following:
• repeatability of classification: SLASAT > LDMCSAT > LNC
(interseason); LDMCSAT > SLASAT > LNC (interannual and
intersite);
• reproducibility of measurement: LDMCSAT > SLASAT = LNC;
• ease of measurement: LDMCSAT > SLASAT > LNC.
Since LNC always ranks last, we suggest that this trait be
left out for classification purposes. LDMCSAT is easier to
measure than SLASAT, its reproducibility appears to be higher,
and once seasonal effects are accounted for, classifications
obtained with LDMCSAT are more repeatable. However, the
connections with functions are less straightforward in the case
of LDMCSAT, and many of them have not been investigated
as yet. The choice of SLASAT and/or LDMCSAT as surrogates
of function to be used in screening programmes will thus
depend on how well these traits finally relate to the function
of interest. Whatever the case, both of them remain stable
enough in time and space to be used in plant classifications.
Acknowledgements
Many thanks to James Aronson and Edouard Le Floc’h for the
setting of the favourable scientific conditions at the Cazarils
site; to Joël and Danièle Garnier for the re-birth of Les Agros
and for allowing us to establish permanent plots and conduct
experiments there; to the technical staff of CEFE and students
for help in data collection; to Christian Collin and Michel
Grandjanny for providing us with the meteorological data of
the Camp Redon site; to Max Debussche for his kindness to
share his knowledge on plant species; to Hans Cornelissen,
Ken Thompson, John Hodgson, Nadia Díaz Burlison and
Philip Roche for providing us with as yet unpublished data.
Hans Cornelissen, Pablo Cruz, Max Debussche, Sandra
Lavorel and Philip Roche provided helpful comments to
improve a former version of this manuscript. This study is
a contribution to the G.C.T.E. Core Research Program
MELODY (Mediterranean landscapes in a changing world:
coupling dynamic and functional analyses).
© New Phytologist (2001) 152: 69 – 83 www.newphytologist.com
Supplementary Material
The following material is available from http://www.blackwellscience.com/products/journals/suppmat/NPH/NPH239/
NPH239sm.htm
Appendix 1 Means and standard error of means (between
brackets) of water-saturated specific leaf area (m2 kg−1) of the
species studied in Cazarils at different dates and years and in
Camp Redon and Les Agros in May 1999
Appendix 2 Means and standard error of means (between
brackets) of water-saturated specific leaf dry matter content
(mg g−1) of the species studied in Cazarils at different dates
and years and in Camp Redon and Les Agros in May 1999
Appendix 3 Means and standard error of means (between
brackets) of water-saturated specific leaf nitrogen concentrarion
(mmol g−1) of the species studied in Cazarils at different dates
and years and in Camp Redon and Les Agros in May 1999
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