Actn Oecologicu 19 (3) (1998) 227-240 / 0 Elsevier, Paris

Identifying functional groups for response to disturbance

in an abandoned pasture
Sandra Lavorel I*, Blaise Touzard ‘, Jean-Dominique Lebreton I, Bernard Clement 2

’ Gntw d’Prolo,yic fonctionnelle rt holutivc; CNRS UPR 9056, 34293 Montpellier cedex 5, France.
’ U.M.R. C.N.R.S. 6553 Kcobio’, univmiti dr Rennes I, rampus de Beaulieu, 35042 Bennes c:edex, France.
* Cwre.sponding author (fax: (3?) 46 7 412 138; e-mail: lu7lorel@ce~~.cnrs-mop./i-)

Received September 26, 1996; revised February 17, 1997; accepted September 26, 1997

Abstract - In an abandoned pasture in Brittany, we compared artificial small-scale disturbances to natural disturbances by wild boar and undis-
turbed vegetation. We developed a multivariate statistical approach which analyses how species biological attributes explain the response of com-
munity composition to disturbances. This technique, which reconciles the inductive and deductive approaches for functional classifications,
identifies groups of species with similar responses to disturbance and characterizes their biological profiles. After 5 months of recolonization, arti-
ficial disturbances had a greater species richness than undisturbed vegetation as a result of recruitment of new species without the exclusion of
pre-existing matrix species. Species morphology, described by canopy structure, canopy height and lateral spread, explained a large part (16 %) of
community response to disturbance. Regeneration strategies, described by life history, seed mass, dispersal agent, dormancy and the existence of
vegetative multiplication, explained a smaller part of community response to disturbance (8 %). Artificial disturbances were characterized by
therophyte and compact rosettes with moderately dormant seeds, including a number of Asteraceue and other early successional species. Natural
disturbances were colonized by leafy guerrilla species without seed dormancy. Few species were tightly related to undisturbed vegetation and
were essentially grasses with a phalanx rosette morphology. The functional classification obtained is consistent with the classification of the com-
munity into fugitives, regenerators and persistors. These groups are structured according to Grubb’s model for temperate grasslands, with regene-
rators and persistors in the matrix and fugitives taking advantage of gaps open by small-scale disturbances. The conjunction of functional diversity
and species diversity within functional groups is the key to resilience to disturbance, an important ecosystem function. 0 Elsevier, Paris

Plant functional group I disturbance I land abandonment I mullivariate statistics

1. INTRODUCTION They are characterized by a set of common biological

attributes that correlate with their behaviour. In pre-
The effects of human-induced changes in distur- vious studies, functional groups for response to distur-
bance regimes are of important concern to recent eco- bance have been identified using more or less
logical research stimulated by several international extensive sets of traits (see [25] for a complete
programmes (Diversitas, Global Change and Terres- review). Overall, life form appears to have the largest
trial Ecosystems; [lo, 381). Land use policies in effect since this trait is correlated with other functio-
western Europe have been leading to the abandonment nally important traits such as plant size. At the scale of
of large areas of previously cultivated or grazed land. particular communities, species tend to belong to a
In some regions, this process has been occurring since limited number of life forms. For example, temperate
the beginning of the century and accelerating since the grasslands are structured as a matrix of perennials
fifties. Such regions offer the opportunity to study the (mostly grasses) with a ‘shifting cloud’ of short-lived
effects of the removal of agricultural pressure on vege- forbs (therophytes and hemicryptophytes) in the inter-
tation dynamics and diversity. To expand results stitial gaps [ 191. Therefore, response to disturbance
obtained from these natural laboratories and to gene- should be defined using a more detailed set of traits in
rate predictions for regions where land abandonment order to identify groups that will allow the prediction
has started only recently (such as north-western of the effects caused by changes in disturbance
Europe), it is essential to identify general rules freed regimes.
from particular species identities and based on their In Brittany, land abandonment started at the begin-
biological characteristics. Relevant traits will relate to ning of the twentieth century. Landscapes were ini-
response to disturbance. tially fine-grained mosaics of pastures and cultivated
Functional groups are defined as groups of species fields separated by a complex network of hedgerows
(taxa) with similar responses to a given factor [15]. [7]. A first phase of agricultural intensification led to
228
the abandonment of less productive and less accessible
fields, and to an increase of the grain of the landscape
with larger plots without hedgerows. Currently, due to
a recent wave of land abandonment, whole blocks of
land are being returned to a dynamics where anthro-
pogenic disturbances have been replaced by soil dis-
turbance by wild mammals (essentially moles, rabbits
and wild boars), browsing of woody species by deer,
and fire. In early successional herbaceous-dominated
communities, soil disturbances by earthworms, moles
and wild boar are frequent and can affect up to 50 % of
a field every year. In this study, we compared artificial
soil disturbances of two different intensities to natural
disturbances by wild boar and intact vegetation in a
pasture abandoned for 3 years. In order to identify
functional groups for response to soil disturbance, the
composition of the recolonized disturbances after one
season were analysed in relation to 8 traits describing
plant morphology and regeneration strategy. A series
of multivariate ordinations were used to quantify
which part of the disturbance effects are due to these
traits, and to identify and characterize the functional
groups.
2. EXPERIMENTAL METHODS
2.1. Study site
The disturbance experiment was carried out in a
c. 2 ha abandoned pasture, in Coetquidan (47”55’ N,
2”15’ E), a military camp located in an abandoned
agricultural area since 1912. The pasture was last cul-
tivated 40 years ago. Since then, it has been managed
as a pasture, with hay making in the spring and
grazing in late summer and autumn.
The climate is temperate, with an annual rainfall of
600 to 800 mm spread over 150 to 185 days. The mean
annual temperature is 10 “C, with mean minimum
temperatures of 1.5 “C in January and mean maximum
temperatures of 23 “C in July. The soil, resting on a
substrate of Brioverian schists, is classified as brown
acidic and organic [ 141. The vegetation is classified as
a Luzulo-Brometum. It is dominated by a matrix of
perennial grasses (Anthoxanthum odoratum, Bromus
commutatus, Dactylis glomerata, Holcus lanatus, Poa
trivialis) and perennial forbs (e.g. Cirsium arvense,
Leucanthemum vulgare, Ranunculus repens, Trifolium
pratense) where annuals recolonize patchy natural dis-
turbances.
2.2. Experimental disturbances
Artificial disturbances were created in April 1995.
Thirty 1 m2 quadrats were placed at random in a
16 x 16 m plot chosen at the centre of the pasture to
avoid edge effects. The plot was fenced in order to
protect the experiment from wild mammals.
S. Lavorel et al.
Systemic herbicide (Glyphosate 5 % solution, Roun-
dup@) was applied in 20 quadrats. Two weeks later, the
litter and all dead plant material were removed. For 10
of these quadrats, the top 3 cm of the soil were dis-
turbed mechanically with a hoe. Treatments were ran-
domly allocated among the thirty quadrats: IO controls
with no disturbance (labelled Control), 10 disturbed
quadrats without superficial soil disturbance (‘litter
disturbance’, henceforth labelled LitterDis) and 10
disturbed quadrats without superficial soil disturbance
(‘soil disturbance’, henceforth labelled SoilDis). An
additional ten 1 m* quadrats were chosen using a Latin
square design in two 5 x 5 m wild boar disturbances
(‘pig disturbances’, henceforth labelled PigDis) loca-
ted around the plot. These disturbances dated from
winter 1994 and affected the top 6 to IO cm of the soil.
Species presence in the quadrats was recorded bi-
weekly from mid-April to early August. Species
composition data analysed for this study included the
total of all species observed in each quadrat over the
period. In the area, the phenological optimum occurs
in mid-June. Species richness in each quadrat and the
cumulated richness over the 10 quadrats for each treat-
ment were recorded on that date. Total vegetation
cover was recorded at its maximum which occurred in
August.
2.3. Species traits
Eight traits were selected to describe plant mor-
phology and regeneration strategy. Morphology of the
established phase was described by three traits cap-
turing the way a plant occupies space: canopy struc-
ture (sensu [ 171) plant height, and lateral spread
(sensu 1171). The regeneration strategy was characte-
rized by the life cycle, three seed traits (seed mass.
seed dispersal mode and the level of dormancy) and
the capacity for vegetative reproduction. Attribute
nomenclature and data for the majority of species were
obtained from Grime et al. [17]. Missing information
on seed characteristics of several species were found
in Guyot et al. [20]. Quantitative and categorical data
were reclassified so as to obtain classes with reaso-
nably balanced representations. The resulting classes
and their designations are presented in table I.
3. STATISTICAL ANALYSES
Vegetation cover and species richness were analysed
using one-way ANOVAs of the effect of disturbance
treatments.
Multivariate ordinations were used to quantify
which part of the disturbance effects is due to these
traits and to identify and characterize the functional
groups.
Functional groups in an abandoned pasture 229

Table I. Species attributes for the identification of functional groups for the response to disturbance.

Trait Levels Categories

Morphology Canopy structure (S&m) 2 1 Rosette Rosette or Semi-rosette

2 Leafy Leafy stems (no basal rosette)
Canopy height (CHei) 3 Hl < 100 mm
H2 101-300 mm
H3 > 300 mm
Lateral spread (LatS) 4 Thero Therophyte (limited extent)
Compact Compact: Perennial < 100 mm)
Phalanx Phalanx: Perennial lo&250 mm
Guerrilla Guerrilla: Perennial > 250 mm

Monocarpic: annual or biennial

Regeneration Life history (Lhis) 2 AnBis
Perennial
Pere
Seed mass (SMas) 3 SMal Very light: < 0.33 mg
SMa2 Light: 0.33-l mg
SMa3 Heavy: l-10 mg
Dispersal agent (ADis) 3 I WIND Anemochorous
2 zooc Zoochorous
3 UNSP Autochorous, barochorous, hydrochorous
Seed dormancy (SDor) 3 SDol None or low dormancy
SD02 Moderate dormancy
SD03 Strong dormancy
Vegetative multiplication (MVeg) 2 I NoVeg No vegetative multiplication
2 MVeg Vegetative multiplication possible

Our data set consisted of three tables:
the sample- species table Y, with presence-absence
(O/l) data for the p species (columns) in the n = 40
samples (rows);
- the treatment table X, with 4 treatment levels
(Control, PigDis, LitterDis, SoilDis) represented as
q = 4 columns for the four categories over n rows (the
y1samples):
- the trait table Z, with 8 traits representing a total of
r = 9 levels (columns) for morphological and 13 levels
for regeneration traits, characterizing the p species
(rows).
Because multivariate relationships between such
tables are not trivial to analyse, we developed a new
method that allows the optimization of the search for
correspondence between species, environmental varia-
bles and species biological traits. Below, we detail the
rationale for that method and the logistic steps
involved (figure I).
A classical approach would have been to obtain
simultaneous ordinations of the rows and columns of
Y, and then to relate the scores of the rows (samples)
to environmental variables (here, the treatments), and
the scores of the columns (species) to traits. Corres-
pondence analysis (CA) is recommended for such an
analysis since it can be viewed as a canonical correla-
tion analysis between the indicator variables of sam-
ples and those of species [16]. As such, and as
indicated in its name, it expresses in an optimal way
the correspondence between samples and species.
The relationship between the sample scores and
environmental variables can be based on a multiple
regression [32]. However, this two-step procedure
(ordination, then regression) is not optimal [33] since
there is no particular reason for CA axes, which reflect
the strongest differences between samples in species
composition, to reflect the differences which are most
strongly related to environmental variables. Canonical
correspondence analysis [39] of Y with respect to X
goes one step further: it looks for ordinations of sam-
ples which are linear combinations of the environ-
mental variables in X. It can be viewed as a canonical
correlation analysis between the indicator variables of
species and the environmental variables weighed by
the distribution of species in samples. As such, it
expresses in the best possible way the correspon-
dence between species and environmental variables. In
mathematical terms, it reduces this correpondence to
the CA of the sample x species table predicted from
the environmental variables by regression, i.e. a pro-
jection, and can be noted as CA(PxY) [S]. Further
links with discriminant analysis are developed by
Lebreton et al. [26].
The same rationale can be used to directly relate
samples to traits. One starts from the transposed table

Vol. 19 (3) 1998

230
samples
Figure 1. Schematic presentation of the steps involved
samples (table Y), environmental variables (envt. var.) characterizing
Y’, in which species appear as rows and samples as
columns. The CCA of Y’ with respect to Z is a cano-
nical correlation analysis between the indicator varia-
bles of samples and the traits. It can be denoted as
CA(PzY’), or as CA(YPz’) because of the symmetry
inherent in CA.
While in the CCA of Y with respect to X, samples
appear as statistical units in which the environmental
variables are measured, in the CCA of Y’ with respect
to Z, species appear as statistical units in which the
traits are measured.
Following Bacou et al. [2], we went one step further
by using CA(P,YP& This analysis is a canonical cor-
relation analysis between environmental variables and
traits weighed by the bivariate sample-species distri-
bution. Algorithmically, it can be obtained from a
standard CCA programme as the analysis CCA(Y’PJ
with respect to Z, or CCA(YPa with respect to X. By
directly linking traits and environmental variables and
by looking for a maximal correlation, it provides a
canonical approach to the problem of the relationship
between biological attributes and the environment.
Effectively, this procedure makes it possible, through
the set of canonical coefficents, to project over a single
multidimensional space the positions of treatments
and those of life history traits.
The total variance of the data set of species compo-
sition Y is measured by the inertia of CA(Y) (hence-
fort denoted CAI). Therefore, the predictive power for
each of the further analyses can be measured by a mul-
tivariate correlation coefficient (MCR [35]) equal to
the ratio of their inertia to that of CA(Y).
A further difficulty was that the number of attributes
(traits by categories) (r) was large relative to the
number of species Go). Different attributes are also
likely to be correlated due to trade-offs among traits. It
was then necessary to reduce the dimensionality of the
trait table and at the same time to take into account the
correlation patterns among attributes. This was done
S. Lavorel et al.
attributes
species m
CA2
I.c.(attributes)
e11vt .var. m
in the multivariate analyses of the relationships among species composition of vegetation
those samples (table X). and species biological attributes (table Z).
by treating the trait table Z by correspondence ana-
lysis. The axes of the analysis represent linear combi-
nations of the r attributes. The first s axes with the
largest variances were retained as new synthetic
attribute variables (SAVs). The resulting matrix U was
used as a substitute for Z. This technique is classical in
regression for improving robustness (see e.g. [40]
p. 138 ff.). The full characterization of the functional
groups in terms of biological attributes required a
return to original attributes. The positions of the ori-
ginal Y attributes on the axes of the analysis
CA(PxYPJ were obtained by substituting in the linear
combinations of the variates of U, which are the first s
axes of CA(Z), the original attributes in Z. This was a
means of obtaining an approximation of CA(P,YPa
robustness against a high number of attributes Y.
Calculations were performed using the software
package Biomeco 4.2 [27]. Further details on the tech-
nical steps within the software can be obtained from
the authors. We thus obtained simultaneous ordina-
tions of the s synthetic attribute variables, and of the (I
environmental variables (treatments), with the highest
possible correlations, in decreasing order. The traits,
species and samples were positioned on the corres-
ponding axes. Since this CA with a double linear
constraint was a special CA, that of PxYP,‘, the stan-
dard graphical approach for the interpretation of CA
could be used. In practice, the projections of the dif-
ferent treatments on the axes of CA(PxYP,‘) were
used to interpret those axes. Species were then allo-
cated to a functional group if their projections along
those axes overlapped with the projection of a given
disturbance treatment. The same method was applied
to associate biological attributes to disturbance treat-
ments. In previous analyses not presented here, this
procedure was tested against a hierarchical classifica-
tion on the correlations of species (and similarity of
traits). Since the results were entirely convergent, we
will present only the graphical interpretations.
Functional groups in an abandoned pasture
Control Pig
disturbance
Litter
disturbance
Soil
disturbance
Figure 2. Effects of disturbance treatments on species richness.
and standard deviation of number of species per quadrat.
4. RESULTS
4.1. Effects of soil disturbance on species richness
In natural undisturbed ovegetation, vegetation cover
is 100 %. Over the growing season, recolonization
achieved 80 % cover for the litter disturbances and
60 % for the soil disturbances. However, there was no
difference between treatments (F(2,30) = 0.285,
P = 0.61) due to the large variance in the disturbed
quadrats, where cover ranged from 20 to 100 %.
A full vegetation list with traits for the 45 species
encountered in the quadrats is presented in the
Appendix. The artificial soil disturbances resulted in a
37 % increase in species richness relative to undis-
turbed vegetation (t(9) = 4.714, P < O.OOl), with soil
disturbances having a higher richness than litter dis-
turbances (t(9) = 3.545, P < 0.01) (figure 2). Natural
disturbances on the other hand did not differ signifi-
cantly from undisturbed quadrats (t(9) = 1.050, n.s.).
Cumulated species richness for ten 1 m2 plots per
treatment increased from the control plots (29 species)
to soil (32 species) and litter disturbances (38 species),
suggesting that artificial disturbances favoured a group
of disturbance-specialists which were added to the
compositional background of undisturbed vegetation.
Pig disturbances had the lowest cumulated richness
with only 20 species.
4.2. Canonical correspondence analysis of the
effects of soil disturbance on species composition
The CA of the table of species composition Y, CA1 ,
estimated a total variance of species composition
Vol. 19 (3) 1998
231
*Control
i LitterDis
.
PbgDis
1
Mean Figure 3. Projection of the different disturbance treatments in the
plane of the first two axes of the CCA of the effects of disturbance
treatments on species composition (CCAl).
among quadrats of 2.183. CCAl of Y with respect to
the treatments (table X) explained 27.6 % of that vari-
ance (table Zr). The first axis of the ordination sepa-
rated the artificial disturbances (soil and litter dis-
turbances) from the undisturbed control vegetation and
the natural pig disturbances, which were separated by
the second axis (figure 3). The first three axes had con-
tributions greater than 10 % to the variance, and were
retained to model species composition according to
treatment effects.
4.3. Canonical analyses of the patterns of
association among species attributes
Attributes of the established phase are known to
often show independent correlation patterns from
regeneration attributes (e.g. [28, 361). As a conse-
quence, it is difficult to identify functional groups
based simultaneously on adult and regeneration traits.
For that reason, the attribute data were split into two
separate tables describing species morphology
(canopy structure, plant height, lateral spread; a total
of 10 variables) and regeneration strategy (life cycle,
seed mass, dispersal mode, dormancy, vegetative
reproduction; a total of 13 variables).
The CA of the table of morphological attributes
(CA2), was strongly influenced by the effect of canopy
structure. The first 2 axes separated rosette plants from
leafy plants (figure 4). Within these groups, the second
axis represented a gradient in height, and more gene-
rally in volume. Five morphological groups were iden-
tified. Within leafy plants, 1) small plants with mod-
232 S. Lavorel et al.

Table II. Results of the multivariate analyses. Changes in species composition depending on disturbance treatment (CCAI); natural patterns of
correlation among morphological (CA2) and regeneration traits (CA3); effects of morphological (CCA2) and regeneration attributes (CCA3) on
community changes due to disturbances.

Analysis Factor i Eigenvalue h, Canonical car. car, 5% inertia

CCA I I 0.347 0.589 57.7

Effects of disturbance 3 0.169 0.41 I 28.1
on composition 3 0.085 0.292 14.2
Z.h, = 0.601
MCR = 0.276

CA 2 I 0.535 0.732 26.8

Morphological traits 2 0.424 0.651 21.2
3 0.342 osxs 17.1
4 0.325 0.570 16.3

CA3 I 0.348 0.590 21.x

Regeneration traits 2 0.304 0.55 I 19.0
3 0.233 0.483 14.6
4 0.215 0.464 13.5

CCA 2 I 0.24x 0.49x 71.0

Effects of morphology 2 0.079 0.7X0 2 .5 s
on disturbance response 3 0.023 0. I so 6.5
n, = 0.349
MCR = 0.160

CCA 3 I 0.143 0.378 83.5

Effects of regeneration 2 0.025 0.159 14.8
biology 3 0.003 0.054 1.7
Zh, = 0. I7 I
MCR = 0.07X

erate lateral spread (phalanx strategists) were opposed
to 2) large species with large lateral spread (guerrilla
strategists) and 3) therophytes with long stems. Within
rosettes, the second axis represented a height gradient
from 4) small compact plants to 5) long-stemmed
therophytes or compact tussocks.
The CA of the table of regeneration attributes
(CA3), was dominated by life cycle effects, vegetative
multiplication and seed mass on the first axis, and seed
mass on the second axis (figure 5). The first two axes
separated 5 regeneration strategies based on subdivi-
sions within seed mass classes: 1) heavy seeded spe-
cies, with a mix of monocarpous and perennial
species; 2) light seeded species with vegetative multi-
plication, separated into 2a) strongly dormant and 2b)
moderately dormant zoochorous seeds; 3) very light-
seeded, anemochorous species, separated into 3a)
annuals and 3b) perennials. As expected, there was
little overlap between these species groups and those
obtained based on morphological attributes.
The first four axes of each correspondence analysis,
representing 81 % and 69 % of the total variance of
vegetative and regeneration traits respectively, were
retained to form the synthetic attribute variables.
4.4. Canonical correspondence analysis of the
effects of species attributes on variation between
treatments
4.4.1. Plant morphology
In the CCA of the effects of morphological attributes
on variation in species composition between treat-
ments (CCA2), species morphological attributes
explained 16 % of the variability among disturbance
treatments (table If). The first two axes separated leafy
plants, associated with natural and artificial soil dis-
turbances, from rosettes, associated with artificial
litter disturbances and controls (figure 6). Soil distur-
bances were colonized by small-statured leafy phalanx
strategists. Natural pig disturbances were strongly
Functional groups in an abandoned pasture 233

Figure 4. Correspondence analysis of the morphological attributes (CAl). Morphological groups were identified by overlaying the projections of
species and attributes (codes as in table fl in the plane formed by the first two axes of the analysis. The two major groups of canopy structure are
delimited by solid lines encompassing the projections of species with leafy vs. rosette canopy structure. Numbered morphological groups listed below
are delimited by dashed lines encompassing the projections of the representative species.

Morphological group Representative species

1 Short phalanx leafy species Bellis perennis, Hypericum humifiisum, Prunella vulgaris, Veronica chamaedrys, Veronica serpillyfolia
2 Guerrilla leafy species Agmstis capillaris, Cirsium arvense, Convolvulus arvensis, Linaria vulgaris, Lotus uliginosum
3 Leafy therophytes Anagallis arvensis, Bromus commutatus, Cerastium glomeratum, Senecio vulgaris, Trifolium dubium, Vicia tetrasperma

4 Compact rosettes
short Hypochoeris radicata, Ox&is europaeum, Poa trivialis
medium Plantago lanceolata, Plantago majo Rumex acetosella
long Malva moschata, Rumex crispus, Taraxacum oficinale
5 Rosette therophytes Crepis capillaris, Crepis vesicaria, Cirsium vulgare, Daucus carota, Kickxia elatine, Sonchus aspec Senecio jacobae,
Viola tricolor

4 Axis 1 J

associated with leafy guerrilla strategists. Litter distur- storey in established vegetation or as part of the reco-
bances favoured the recruitment of rosettes with a lonization of disturbances.
moderate above-ground volume, in particular annual
Asteraceae (Crepis sp. pl., Senecio sp. pl., Sonchus 4.4.2. Regeneration traits
asper). Controls had little specificity, reflecting the
fact that disturbances led more to the recruitment of In the CCA of the effects of regeneration attributes
species absent from intact vegetation than to an actual on variation in species composition between treat-
loss of species. The classification characterized them ments (CCA3), regeneration attributes explained only
as a small group of rosette phalanx species which are 8 % of the variability among disturbance treatments
often dominant in undisturbed vegetation. Overall, the (table ZZ). Therefore, species profiles in relation to
natural groupings identified by CA1 were retained as treatments were less strongly distinguishable than
response groups to disturbance. Leafy therophytes and those for vegetative traits (figure 7). The first axis,
short compact rosettes were the only groups not asso- which represented 83.5 % of the variance, separated
ciated with any of the disturbance treatments, which species with no or low seed dormancy from species
suggests that these small species are a component of with moderate dormancy. The second axis showed a
the vegetation common to all states. They would in seed mass gradient from light, wind-dispersed seeds
fact be species which can survive either as a, under- associated with control quadrats to heavy-seeded spe-

Vol. 19 (3) 1998

234 S. Lavorel et al.

Figure 5. Correspondence analysis of the regeneration attributes (CA2). Regeneration groups were identified by overlaying the projections of species
and attributes (codes as in table I) in the plane formed by the first two axes of the analysis. Three numbered regeneration groups (listed below) based
on seed mass are delimited by solid lines encompassing the projections of species within each class of seed mass. Light-seeded species (group 2) arc
further split into two graphically disjointed dormancy subgroups (2a and 2b) delimited by dashed lines. Within very light-seeded species (group 3).
annual and perennial species overlapped graphically.

Regeneration group

1 Heavy seeded

’ species without vegetative multiplication: ’ non anemochorous

-0.13 0.26 0.64 1.0

Axis 1

ties represented in artificial disturbances. Relation-
ships between treatments and seed mass are to be
considered with care since the second axis represented
only 14.8 % of the variance. Artificial litter and soil
disturbances were not separated by the analysis. They
were positively correlated with axes 1 and 2 and asso-
ciated with moderate dormancy. Within this group,
3 subgroups could be distinguished according to seed
mass. In general, artificial disturbances favoured many
Asteraceae and other species regarded as early succes-
sional. Natural pig disturbances, which were strongly
negatively correlated with axis 1, were associated with
species without dormancy and generally wind-dis-
persed seeds. Finally, undisturbed controls, negatively
positioned along axis 2, were associated with species
having very light anemochorous seeds with moderate
dormancy. Unlike vegetative attributes, the natural
groupings identified by CA2 were not well conserved
by CCA3. Groups based on seed mass (gradient figu-
red in dotted lines onfigure 7> were not relevant to dis-
turbance response and were split between treatments.
In particular, the group of very light seeded species was
Functional groups in an abandoned pasture 235

Figure 6. Ordination of treatments, morphological attributes and species by CCA2. Functional groups were identified by overlaying the projections
of treatments (in bold), morphological attributes (codes as in table r) and species in the plane formed by the first two axes of the analysis. The two
natural groups of canopy structure (leafy and rosette) are separated along axis 1 by a dotted line. Numbered morphological groups listed below are
delimited by solid lines encompassing the projections of the representative species correlating with each disturbance treatment. Within group 3.
species are further split into two graphically disjoint subgroups of lateral spread (3a and 3b) delimited by dashed lines.

Functional group Attributes Representative species

1 Soil disturbance Leafy, phalanx, short Bel/i.s perennis, Hypericum hum$usum, Prune/In vulgcrri.s, ti~roniccr chomaetlrys

2 Pig disturbance Leafy. guerrilla

3 Litter disturbance a Compact rosette

l , .

l Leafy i \ 3a;
:I

\
‘,---’
, ‘\

i -- :,
-1.79 1.10

Axis 1 ~

split between artificial disturbances and controls. Spe- Artificial disturbances (litter and soil) were charac-
cies with light, strongly dormant seeds did not appear terized by therophytic and compact rosettes with mod-
as representative of any of the treatments and would erately dormant seeds, among which a number of
then be common to all as a background component Asteruceae and other early successional species often
with occasional germination and vegetative spread. encountered as agricultural weeds. In the case of natu-
ral disturbances and undisturbed vegetation, species
4.5. A functional classification for response classifications according to morphological vs. regene-
to disturbance? ration traits were somewhat discordant. Some species
Groups of response to artificial and natural distur- associated by morphology with one type of treatment
bances identified either on the basis of morphological appeared associated with the other by regeneration
traits or on the basis of regeneration traits generally strategy. Because the analysis relative to morpholo-
converged towards a classification into three groups gical traits had a stronger explanatory power, we
(tabZe III). Within these broad response groups, par- would favour that classification. Natural pig distur-
ticular species would be allocated to different sub- bances were then associated with leafy guerrilla spe-
groups depending on whether the classification was cies, while control quadrats tended to support phalanx
based on morphological or regeneration traits. rosettes and mostly grasses.

Vol. 19 (3) 1998

236 S. Lavorel et al.

Figure 7. Ordination of treatments, regeneration attributes and species by CCA3. Functional groups were identified by overlaying the projections of
treatments (in bold), regeneration attributes (codes as in ruble r) and species in the plane formed by the first two axes of the analysis. The three natural
groups of seed mass are separated along axis 2 by dotted lines. Numbered regeneration groups listed below are delimited by solid lines encompassing
the projections of the representative species correlating with each disturbance treatment. Within group 1, species are further split into three
graphically disjointed subgroups of seed mass (la, b, c) delimited by dashed lines,

Functional group Attributes Representative species

1 Artificial disturbance Moderate dormancy

Soil disturbance or a very light seeds Achilles millefolium. Cerustium glomeratum, Crepis capillaris, Kickxia &tine,
litter disturbance Senecio jacobae, Senecio w&are, Sonchus asper
b light seeds, zoochory Daucus carom, Anthoxantum odoratum, 0xali.r europeurn, Prunella vulgaris
c heavy seeds Cirsium arvense, M&a moschata, Plantago lunceolato

2 Pig disturbance No dormancy, Cirsium w&are, Lolium perenne, Rumex acetosellu

anemochorous

3 Control Very light, anemochorous seeds, Holcus lam&s, Poa trivialis, Linnrirr wlgaris
moderate dormancy

SDo3’

5. DISCUSSION
This study develops a new method of direct iden-
tification and characterization of functional groups in
terms of biological attributes. This method proposes
a reconciliation of inductive and deductive approa-
ches [42]. The multivariate approach takes into
account patterns of correlation among attributes and
simultaneously derives species classifications that
relate to function by identifying sets of traits which
correlate with species response to environmental fac-
tors. This method makes it possible to go one step
beyond an analysis that imposes patterns of correlation
of attributes identified by CA (inductive classification)
onto further ordinations associated with environmental
variables [37]. The classifications obtained are defi-
nitely deductive as the response groups that we iden-
tified did not entirely overlap with the results of the
inductive classifications.
In our example, the function analysed was commu-
nity response to disturbance. The same approach
would apply to any other function by using relevant
environmental variables in the initial CCA. Appro-
priate trait selection is a prerequisite to the success of
the approach since traits taken into account in the
canonical analysis constrain the final results if they are
strongly correlated with a number of other traits (as is
the case for plant size or seed mass). This selection
needs to be inductive, and thus necessarily subjective,
based on expert knowledge [42]. The number of traits
which can be chosen will however be constrained by
the number of species needed for the analyses to
remain robust [39]. In the example analysed here, the

Acto Oecologica
Functional groups in an abandoned pasture 237

small number of species put limitations on the number
of traits which could be taken into account.
Functional groups based on morphological attributes
were closely related to natural attribute groupings
based on canopy structure. On the other hand, for
regeneration attributes, natural seed mass patterns
were not directly relevant to disturbance response for
which seed dormancy was the functionally meaningful
trait. The response groups identified were generally
consistent between the analysis on morphology and
the analysis on regeneration traits, although sub-
groups based on detailed species biology differed. By
essence, our two classifications and their intersection
into broad response groups could not allocate all spe-
cies into a definite group because multivariate ana-
lyses give prominence to species with contrasted dis-
tribution patterns. Species which are evenly distributed
across treatments, i.e. species indifferent to distur-
bance, would be located near the origin of the axes and
not appear in a classification based on correlations
with those axes. In addition, group limits are neces-
sarily fuzzy because the classification operates on a
double continuum of responses and biological attri-
butes.
The analysis of the recolonization of natural and
artificial disturbances showed that disturbances signi-
ficantly increased species richness by favouring the
recruitment of new species without eliminating origi-
nal species from undisturbed vegetation. Most studies
involving animal or artificial small scale disturbance
have also found greater species richness in disturbed
than in intact vegetation (e.g. [ 1, 21, 241). Species
richness was increased locally by the opening of the
matrix dominated by perennial grasses and forbs (e.g.
Dactylis glomerata, Lolium
repens). Disturbances favoured a group of distur-
bance-specialists (table III group 1) which were added
to indifferent species present in both undisturbed and
Table III. Functional classification of species
disturbed vegetation. The dynamics of these commu-
nities is consistent with the model of a perennial
matrix of dominant species where gaps are needed for
the recruitment of specialized species with poorer
competitive abilities to occur [19].
Species’ response to different disturbances was well
correlated with their morphology, in particular to
canopy structure. Similarly, McIntyre et al. [31] found
that in Australian temperate grasslands, Raunkiaer’s
life forms [34], which overlap with Grime et al.‘s [17]
canopy structure categories used in this study, were
well correlated with response to soil disturbance. In
their study, soil disturbance favoured therophytes and
flat rosette chamaephytes. In our case, soil distur-
bances created artificially or by wild boar were colo-
nized by leafy (or protohemicryptophyte) species,
while therophytes and rosettes were more frequent in
the artificial litter disturbances and the undisturbed
vegetation. Consistent with previous results, soil dis-
turbances were colonized by generally small statured
species [3, 131. In general, morphologies favoured by
disturbances appeared to be those achieving efficient
ground cover and light capture by spreading their
leaves flat on the ground and being quite compact.
The difference in morphological attributes between
artificial soil disturbances and sites where dead bio-
mass was left on the ground suggests that the low stat-
ured leafy phalanx species are unable to compete with
litter. Inhibitory effects by litter are often species-spe-
cific [6, 111, but we are not aware of systematic inves-
tigations of these effects in relation to species
morphology. Bergelson [4] found that the recruitment
of two small leafy annuals (Senecio vulgaris and
Capsella bursa-pastori) was inhibited by grass (Poa
perenne, TrifXum annua) litter. Effects on rosette species can be positive
(Erigeron annuu.s [ 11I), absent (Verbascum thupsus
[6]) or negative (Centaurea nigra, Dipsacus sylvestris
and Hypericum perforatum [6]).
response to disturbance

Functional group Morphological Attributes Regeneration Attributes Representative species

I Artificial disturbances:
Soil disturbance Leafy, phalanx. short Be//is perumis, Hypericum humifusum, Prunellu vulgaris,
Veronicx chamaedrp
Litter disturbance Compact rosette Moderate dormancy Ma/vu moschatct, Plnnfago lanceoiutu, Pluntago majo
Rosette therophyte I Cirsiwn vulpre, Crepis ccrpillaris, Crepis vesicurirr,
Daucus carotu, Kick.& e&tine, Senecio jacobae,
Sonchus usper

2 Pig disturbances Leafy, guerrilla No dormancy Agrostis capillaris, Cirsium arvense, Linaria vulgaris,
Trifolium repens

3 Undisturbed vegetation Rosette, phalanx Very light, Dactylis glomeratu, L&urn perenne, Trifolium pratense
wind dispersed seeds

Vol. 19 (3) 1998

238 S. Lavorel et al.

Canopy gaps and disturbed sites are often associated triggered the recruitment of fugitives, mostly small
with short lived species [3, 13, 19,231. Here, the vege- and short-lived species with moderate dormancy,
tation comprised one third of annual or biennial spe- present in the underlying seed bank. Natural distur-
cies but these were spread evenly across treatments. bances are colonized by persistors, probably essen-
Regeneration niches were not determined by life his- tially vegetatively (guerrilla species) or through long-
tory but primarily by seed dormancy. Artificial distur- distance seed dispersal. These rapidly exclude the
bances favoured species with a quick response seed weakly competitive fugitives.
bank (moderate dormancy) whose germination was This conceptual model associating the dynamics of
triggered by exposure to light. Species with no dor- disturbance response to species biology contributes to
mancy observed in natural disturbances would have understanding one component of the relationship
been dispersed at the end of the 1994 vegetative between biodiversity and ecosystem functioning.
season and germinated in the spring of 1995. Previous Indeed, resilience to disturbance is an important eco-
studies have found that soil disturbances were colo- system function [22]. Our analysis points to two
nized preferentially by light wind-dispersed seeds [5, aspects of old field plant diversity that contribute to
311. Although these species were relatively abundant this resilience. Firstly functional diversity, the exist-
in the germinable seed bank [41], they failed to colo- ence of several functional groups favoured under dif-
nize artificial disturbances. ferent conditions, is the key to the persistence of the
The comparison between artificial disturbances and system in the face of disturbance. The analysis of the
natural disturbances provides insights into the dyna- regeneration traits emphasized the role of the soil seed
mics of recolonization. Differences in species compo- bank which provides a buffer against variability in the
sition can be seen as a result of disturbance age, since frequency of disturbances. Secondly, species diversity
wild boar disturbances were approximately one year within functional groups would be expected to provide
old. Then, disturbances first favour the germination of a second buffer against environmental variability. Dis-
species with good colonizing ability thanks to their flat turbances may occur under a variety of environmental
morphology. These are rapidly displaced by guerrilla conditions (e.g. climatic, microsite) which will favour
strategists colonizing vegetatively from edges and with different individual species. The persistence of the
fast-growing, strongly competitive, seedlings from whole community will then be mediated through lot-
large seeds [30]. Alternatively, Fahrig et al. [12] tery mechanisms with storage effects (sensu [9])
showed that annuals are favoured by intermediate dis- within functional groups.
turbance frequencies, while high disturbance frequen-
cies select for long-distance clonal dispersal. Pig Acknowledgements
disturbances are known to recur at the same locations This study was funded by a grant from the minis&e de I’Enseigne-
for several years and hence, would select for guerrilla ment Superieur et de la Recherche, DPSTS, Action Biodiversite. We
strategists. Finally, natural disturbances were also the thank C. Lacombe for the graphics. The manuscript was improved
most intense in our design and would therefore be thanks to the comments of two anonymous referees.
expected to support lower species diversity than the
less intense artificial disturbances [29].
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240 S. Lavorel et al.

APPENDIX. List of species recorded and biological attributes (from [17]). Codes for traits are those listed in table I.

Morphology traits Regeneration traits Frequency in quadrats

Species Scan CHei LatS LHis SMas ADis SDor Mveg Control LitterD SoilD PigDis
- - - - - -
Achilles millefolia 2 2 4 2 1 I 2 1 0 4 1 0
Agmstis capillaris 1 2 4 2 1 1 3 1 4 0 0 3
Anagallis arvensis 1 2 1 1 2 3 3 1 0 0 9 0
Anthoxantum odoratum 1 2 2 2 2 2 2 I 10 0 0 6
Bellis perennis 1 1 3 2 1 1 1 1 0 0 1 0
Bromus commutatus 1 3 1 1 3 1 1 0 4 0 0 0
Cerastium glomeratum 1 2 1 1 1 1 2 0 2 2 6 9
Cirsium arvense 1 3 4 2 3 1 2 1 4 1 5 0
Cirsium vulgare 2 3 1 1 3 1 1 0 0 9 0 6
Convolvulus arvensis 1 3 4 2 3 3 1 1 7 0 7 0
Crepis capillaris 2 2 1 1 1 1 2 0 3 9 10 4
Crepis vesicaria 2 3 1 1 1 1 1 0 0 4 0 1
Dactylis glomerata 2 3 3 2 2 1 2 0 6 0 1 0
Daucus carota 2 2 1 1 2 2 2 0 2 10 10 7
Festuca rubra 2 2 4 2 2 2 1 1 3 0 0 0
Geranium dissectum 2 3 1 1 3 2 3 0 7 8 10 0
Holcus lanatus 1 3 3 2 1 1 2 1 10 4 0 10
Hypericum humtjkum 1 1 3 2 1 1 3 1 0 3 6 0
Hypochoeris radicata 2 1 2 2 2 1 1 0 3 10 10 7
Kyckxia elatinr 2 2 1 1 1 1 2 0 0 4 7 0
Leucanthemum vu&are 1 3 2 2 1 1 2 1 8 8 10 6
Linaria vulgaris 1 3 4 2 1 1 2 I 2 4 4 0
Lolium perenne 2 2 3 2 3 1 1 0 1 0 0 0
Lotus uliginosum 1 3 4 2 2 3 3 1 0 1 1 0
Malva moschata 2 3 2 2 3 1 2 0 1 3 3 0
Mercurialis annua 1 1 1 1 3 2 3 0 0 4 IO 0
Oxalis europaeum 2 1 2 2 2 2 2 1 0 8 6 0
Plantago lanceolata 2 2 2 2 3 2 2 0 7 10 10 8
Plantago major 2 2 2 2 I 2 3 0 0 4 3 0
Poa trivialis 2 1 2 1 1 1 2 1 6 0 0 6
Prunella vulgaris 1 1 3 2 2 2 2 1 1 0 4 I
Ranunculus repens 2 2 4 2 3 3 3 1 8 10 10 10
Rumex acetosella 2 2 2 2 2 1 1 0 2 2 4 9
Rumex crispus 2 3 2 2 3 2 3 0 2 0 1 0
Senecio jacobae 2 3 1 2 1 1 2 0 0 1 0 0
Senecio vulgaris 1 3 1 1 1 1 2 0 0 2 2 0
Sonchus asper 2 3 1 1 1 1 2 0 0 2 2 0
Tarazacum oflcinale 2 3 2 2 2 1 1 0 8 9 10 1
Trtfolium dubium 1 2 1 1 1 2 3 0 1 0 0 0
Trtfolium pratense 2 2 3 2 3 2 2 0 5 0 0 9
Trifolium repens 1 1 4 2 2 2 3 1 0 9 9 3
Veronica chamaedqw 1 1 3 2 1 3 3 I 2 I 9 1
Veronica serpyllifolia 1 1 3 2 1 1 3 1 1 2 0 0
Vicia tetrasperma 1 2 1 1 3 3 3 0 1 0 0 1
Viola tricolor 2 2 1 2 2 2 3 1 0 0 1 0

Acta Oecologica