Journal of
Journal
of
Plant Ecology
Plant
Ecology
Volume
6, Number 1,
PAGES
1–10
Pages 19–28
doi: 10.1093/jpe/rts011
March 2013
doi:10.1093/jpe/rts011
Advance Access publication
25 April 2012
available online at
www.jpe.oxfordjournals.org
Changing assembly processes
during a primary succession of plant
communities on Mediterranean
roadcuts
Vale´rie Raevel1, Francxois Munoz2,*, Virginie Pons1, Alain Renaux1,
Arnaud Martin1 and John D. Thompson1
1
Universite´ Montpellier 2 and CNRS, Centre d’Ecologie Fonctionnelle et Evolutive, UMR 5175, 1919 route de Mende,
34293 Montpellier Cedex 5, France
2
Universite´ Montpellier 2, botAnique et bioinforMatique de l’Architecture des Plantes, TA A-51/PS2, 34398 Montpellier
Cedex 5, France
*Correspondence address. Université Montpellier 2, AMAP, TA A-51/PS2, 34398 Montpellier Cedex 05, France.
Tel: +334-67-61-49-07; Fax: + 334-67-61-56-68; E-mail: [email protected]
Abstract
Aims
Studying plant ecological succession provides insights into the spatiotemporal processes underlying community assembly and is of
primary importance for restoration ecology. We investigate here
colonization events and local community assembly over an original primary succession occurring on roadcuts after roadwork.
For this, we addressed both the changes in species presence-absence
presence–absence
(incidence data) to highlight pre-establishment filters and in species
relative abundances to further assess the influence of local biotic processes.
Methods
We studied 43 limestone roadcuts in Mediterranean France, covering
five age classes up to an age of 80 years, along with 13 natural cliffs as
a reference, and we counted 14
322 plant individuals on these sites.
14322
We applied a constrained nonsymmetric correspondence analysis of
presence-absence and abundance data to assess
both the incidence (presence–absence)
the variation of these data along the chronosequence.
Important Findings
Along the first 30 years, the initially abundant short-lived species
declined both in terms of incidence and abundance and were
replaced by longer lived herbaceous and woody species. This first
INTRODUCTION
Investigating the ecological processes that drive the assembly
of plant communities is fundamental to our understanding of
variation in species diversity in space and time (Shipley 2010)
and provides relevant information for establishing priorities for
phase was characterized by species that are widespread in the
surrounding scrublands and was comparable to an early secondary
succession there. After 30 years, there were continuing changes in
incidence data with age, but no more significant change in species’
abundances. This second phase was marked by the late colonization
of specialists that did not become dominant. Although colonization
and establishment limitation was thereby apparent for specialist
species, a slow convergence of community composition toward
the situation of natural cliffs could be detected in the older stages
of the chronosequence. These findings convey insights into the
natural dynamics of man-made outcrop plant communities and
may be useful for the ecological management and restoration of such
contexts. It also illustrates the interest of comparing incidence and
abundance data to investigate the relative influence of ecological
determinants on the assembly of plant communities.
Keywords: primary succession d roadcut d colonization
dynamics d assembly rules d Mediterranean
environment d non-symmetric correspondence analysis
Received: 17 November 2011 Revised: 21 February 2012 Accepted:
10 March 2012
the restoration of highly degraded habitats (Walker and del
Moral 2003, 2009). The incidence (presence/absence) and
abundance structures of a local plant community depend on
filters imposed on a pool of incoming species. Three independent filters are involved, including dispersal constraints,
environmental constraints (also named habitat filtering) and
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The Author
Author 2012.
2012. Published
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Presson
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behalfofofthe
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Botany,Chinese
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20
2
internal dynamics (Belyea and Lancaster 1999; Fukami et al.
2005; Lortie et al. 2004). The former filter is dependent upon
physical and ecological barriers, as well as on the contingent
history of the communities, while the two latter are deterministic assembly rules influencing the relative abundances and
the functional structure of the community. After the initial
colonization, a number of factors such as resource limitation,
positive and negative, direct and indirect interactions drive
the internal community dynamics and influences community
composition and relative abundances (Cingolani et al. 2007).
Both the contingent history of dispersal events and the local
assembly rules thereby determine community patterns in
space and time (Holdaway and Sparrow 2006; Lortie et al.
2004).
Primary ecological succession represents the change in species composition and/or structure over time in sites that are
initially devoid of propagules. Variation in species diversity
during the succession provides a context in which to investigate the relative influence through time of the colonization
and establishment processes from the regional species pool
(Gleason 1927) and of the internal dynamics based on local
autecological preferences and biotic interactions (Clements
1916). But a direct investigation of ecological succession
requires long-term observation, which is in practice difficult
if not impossible. Hence it is most often necessary to substitute
space for time, by comparing sites of varying age at a given time
(Cutler 2010; Mori et al. 2008; Pickett 1989). These chronosequences provide an appealing alternative to long-term studies
and, despite various limitations (Johnson and Miyanshi 2008),
the approach has received support from studies indicating
a close correspondence of synchronic and diachronic data
(Foster and Tilman 2000; Walker et al. 2010).
Our purpose here is to analyze plant primary succession
along an age gradient of limestone roadside outcrops (roadcuts) in the Mediterranean region of southern France. Roadcuts represent a particular ecological context by exposing
natural rock and due to their vertical aspect and sparse spatial
distribution in the landscape. Because of the water and nutrient limitation, Larson et al. (2000) argued that assembly rules
in plant cliff communities should be different to those in
surrounding communities that do not suffer such limitations. However, only a few studies have investigated this
issue (Novak and Konvicka 2006; Ursic et al. 1997; Yuan
et al. 2006). In our study area, successive phases of road construction over the last 80 years has produced a large number
of roadcuts, which allowed us to design a stratified sampling
scheme based on 43 sites in five age classes, with an additional
set of 13 natural cliffs as a reference state for the study. We
addressed the following questions. First, is there any variation
in species composition and relative abundance with time, with
evidence of possible convergence toward natural cliff communities? Second, does the comparison of variation in species
abundance and incidence (presence/absence) provide information on the colonization history and the variation of assembly
processes in space and time?
Journal of Plant Ecology
MATERIALS AND METHODS
Site location and selection
The study area is located in the French Mediterranean region
to the west of the Rhône valley (4837#–4358#N, 328#–4E).
The climate is Mediterranean subhumid, with hot and dry
summers, relatively cold winters and considerable interannual
variation in the timing and amount of rainfall. We selected
roadcuts according to the following criteria: (i) hard calcareous
rocks, in order to provide a fairly uniform geochemical substrate, (ii) roadcuts at least 6-m high with an average slope
between 80 and 90, (iii) the overall vegetation cover lesser
than ;20% and (iv) a similar surrounding vegetation of fairly
open Mediterranean scrublands with Quercus ilex. We excluded
sites that were either unstable (evidence of rock falls) or too
close to the road, for safety reasons.
Based on historical maps and information from the local authorities that planned road construction and maintenance, we
designed five age classes and selected within each class several
roadcuts as uniformly spread across the study area as possible:
0–10 years old (n = 8), 10–20 years old (n = 7), 20–30 years old
(n = 10), 30–50 years old (n = 7), 50–80 years old (n = 11). In
each class, the roadcuts were opened within a 10-year interval,
corresponding to a given planning of road development in the
area. The larger limits of older age classes acknowledged some
imprecision in the roadwork dating.
Overall, we sampled 43 roadcuts across a rectangle of 46-km
east–west by 41
km north–south
east-west
41km
north-south (Fig.
(Fig. 1).
1).The
Thesampling
samplingscheme
sceme
was devised to be as robust as possible to spatial variation by
spreading the sites over a large area, in the limits of the history
of road construction. The youngest sites more often occurred
in the south of the study area, due to recent city expansion,
while the older roadcuts were contrastingly found more often
in the north part. But we still devised the scheme so that sites of
contrasting age were generally closer to one another than
roadcuts of similar age. In the same area, we also sampled
13 natural cliffs across the study area, according to similar criteria, to provide a reference state in the same bioclimatic context, so as
al.al.
(2000:
p. 12,
asto
toaddress
addressthe
thehypothesis
hypothesisofofLarson
Larsonet et
(2000:
see also p. 119–123) that ‘man-made cliffs [. . .] because [of]
their flora, fauna and ecology often show striking similarities
with natural cliffs and because ecological factors controlling
these communities are similar’.
Community sampling
For each site, we selected a 25-m-long stretch and divided it
into five 5-m-long and 6-m-high bands. We randomly placed
five 2 by 2-m quadrats in vegetation patches, one in each band
(Fig. 2). We counted and identified all the individuals of vascular plant species occurring in the four 1 by 1-m subplots
within each quadrat. To be as exhaustive as possible, especially
regarding annual species, each quadrat was investigated twice,
at the beginning and at the end of spring 2008 or 2009. We also
repeated the procedure in both 2008 and 2009 for five sites
belonging to different age classes to control for interannual
Raevel et al. al. | Primary
Primary succession on Mediterranean roadcuts21
roadcuts
3
Figure 1: location of the studied limestone roadcuts and natural cliffs in southern France (legends: black squares, 0–10 years old; gray squares,
10–20 years old; black circles, 20–30 years old; gray circles, 30–50 years old; black triangles, 50–80 years old; gray triangles, natural).
variation. For the subsequent statistical analyses, we will
consider site-level data by merging the five quadrats of each
site. We also listed all the species that were present in the
complete 25-m-long stretch but not recorded within the
quadrats (hereafter referred to as ‘extraquadrat’ species),
after visual inspection of the site (using binoculars when
necessary) up to 6-m height. Finally, we visually estimated
the canopy vegetation cover (m2) and the cover (m2) of
woody species in the quadrats. To limit subjectivity, a single
observer (VR) performed this assessment. We identified the
taxa using the flora of Tison and Jauzein (in press) and a taxonomic reference list for resolving synonymies (BDNFF
4.02, Bock 2005).
We further compiled information on life form following the
classification of Raunkiaer (1934), using the most recent synthesis in the study area (Tison and Jauzein, in press). We also
obtained ecophysiological information about desiccationtolerant species (five species, Proctor and Tuba 2002) and Crassulacean acid metabolism species (five species, Sayed 2001),
i.e. stress (drought)-tolerant species (see supplementary
Table S1) from literature. We finally obtained information
on typical vegetation of limestone cliffs from Braun-Blanquet
et al. (1952) and the interpretation manual of European
Union Habitats (Anonymous 2007) to identify other specialist
species (22 species, see supplementary Table S1). This information was used as a marker of the functional changes in community composition along the succession. We therefore tested
their contribution to the changes observed in plant communities along the chronosequence.
Data analysis
We analyzed the site-level community data in the form of siteby-species tables including either abundance (number of individuals) or incidence (presence/absence) information. Our
purpose was to address the variation in community structure
along the chronosequence, that is, its variation across age
classes. Incidence data were used to indicate colonization
and subsequent establishment success, depending on the
available sources of migrants and the species niche requirements (habitat filtering). Abundance data conveyed additional
information on the result of species interactions (internal community dynamics). We performed a constrained multivariate
nonsymmetric correspondence analysis of these tables (NSCA;
Gimaret-Carpentier et al. 1998a; Kroonenberg and Lombardo
1999). NSCA investigates the deviation of the composition of
each site from the average profile of all sites. The constrained
version of the NSCA here incorporated the age classes as the
constraint (using the pcaiv and dudi.nsc functions in R package
22
4
Journal of Plant Ecology
Figure 2: the roadcut sampling scheme (a) and a photographed example (b).
ade4), so as to highlight the part of the deviation that was
explained by changes in composition with age (Pélissier et al.
2003). We tested whether age explained a significant part of
community variation in the constrained NSCA by performing
a Monte Carlo randomization of the age labels (randtest in R
package ade4, 999 permutations and 0.1% resolution). Both
species and sites were sorted along the constrained axes, and
the axes each explained a decreasing proportion of the variation
in community composition with age. To assess the robustness of
the result, we also performed a constrained analysis of principal
coordinates (CAP; Anderson and Wills 2003) on the basis of the
non-Euclidean Bray-Curtis
Bray–Curtis distance of the profiles (using the
capscale function in R package vegan). Finally, we further used
a constrained NSCA and the subsequent randomization procedure to test the interannual variation in species composition and
abundances for the five sites sampled in both 2008 and 2009.
We found no difference between the two dates, thus showing
that there was no bias in our sampling due to any particular
conditions during the sampling period.
We also tested the variation with age in community summary statistics, namely the number of individuals, the site species richness, the vegetation cover, the cover of woody species
and the number of extraquadrat species absent from quadrats,
using one-way analyses of variance (ANOVA). We performed
Box-Cox power transformation whenever the normality of
Shapiro-Wilk test.
the model residuals was rejected after a Shapiro–Wilk
We also tested the difference between roadcuts and natural
cliffs by performing Helmert contrasts (Chambers and Hastie
1992). We performed all the statistical analyses using the R
statistical software (R Development Core Team 2008) and
the ade4 package for multivariate statistical analyses (Dray
and Dufour 2007; Thioulouse et al. 1997).
Raevel et al. al. | Primary
Primary succession on Mediterranean roadcuts23
roadcuts
5
Results
14322
Overall, we detected 14
322 individuals belonging to 221 vascular plant species and 59 families (list in supplementary Table
S1) with an average of 26.2 (standard error [SE] = 0.2) species
per site. The vegetation cover and the percent cover of woody
species increased with age, while the number of individuals
increased in the first 20 years and then decreased and species
richness showed no variation. There was a significant overall
contrast in each of these variables between roadcuts and natural cliffs except for species richness, but the contrast of natural
cliffs with oldest roadcuts (50–80) was only significant for the
cover data (Table 1). The linear models used for ANOVA and
contrast analyses all conformed, after Box Cox transformation,
to the assumptions appropriate for statistical testing.
We found 57 therophytes, 86 hemicryptophytes s.l. (including 14 geophytes and 72 hemicryptophytes), 45 chamaephytes
and 33 phanerophytes. We tested the variation in life-form
composition with time by performing a constrained NSCA
of the life-form counts per site according to the age classes.
The corresponding Monte Carlo randomization test highlighted a significant overall variation in life-form composition
over the five age classes and natural cliffs (Monte Carlo test,
P < 0.001). On roadcuts <30 years old, herbaceous perennials
(hemicryptophytes s.l.) increased in proportion while therophytes decreased, both in abundance and for incidence data
(Fig. 3). The proportion of chamaephyte species increased in
incidence while their relative abundance decreased. On roadcuts >30 years old, both therophytes and hemicryptophytes
s.l. decreased in proportion while chamaephytes increased.
The proportion of phanerophytes was higher in natural cliffs
than in any roadcut age class.
there was not a single prominent trend in variation, and
two dimensions were needed to depict most variation in incidence data with age. The ordination of sites according to the
two first axes showed two branches, one with a sequence from
0 to 30 years, the other with a sequence of the older sites
(Fig. 4A). Furthermore, the ANOVA analysis of the species
scores according to life form was significant for both axes
(ANOVA F = 7.9, P < 0.001 for axis 1 and F = 6.6, P < 0.001
for axis 2, degrees of freedom [df] = 3 and 217), which indicated that the detected successional trends were related to life
form. The branching pattern was consistent with the progressive replacement of therophytes species (e.g. Sonchus oleraceus,
Crepis sancta, Urospermum picroides) by longer lived hemicryptophytes (e.g. Biscutella laevigata, Avenula bromoides) until
30 years, on the first branch. The more specialized species such
as Sedum spp., Lactuca perennis, Phagnalon sordidum, Teucrium
flavum (Braun-Blanquet et al. 1952) and saxicolous ferns
(Ceterach officinarum, Asplenium trichomanes) subsequently
colonized the roadcuts on the second branch (Crassulacean acid
metabolism and desiccation-tolerant vs. other species on NSCA
axis 1, F = 4.4, P < 0.001, df = 1 and 219). Phanerophytes such as
Rhamnus alaternus, Juniperus phoenicea, Pistacia terebinthus and
Prunus mahaleb all appeared associated on axis 1 with older
roadcuts and natural cliffs (Fig. 4C). Plant composition of oldest
roadcuts became more similar to that of natural cliffs, where
a higher frequency of phanerophytes was still found (Fig. 4C),
such as the characteristic specialist J. phoenicea. We also performed the CAP based on Bray-Curtis
Bray–Curtis distances between communities and found the same overall pattern of species and
community ordination, thus indicating that the result was
not dependent upon the nature of the metric used.
Relative abundances
Species incidence
We found significant variation in species’ incidence across age
classes (Monte Carlo permutation test, P < 0.001). The first two
axes of the constrained NSCA accounted for 49.9 and 20% of
the global inertia across age classes, respectively. Therefore,
The ordination of species based on their abundance likewise
showed significant variation among age classes (Monte Carlo
permutation test P < 0.001). As with incidence data, the constrained NSCA showed two prominent axes (first axis, 35.2%,
second axis, 30.7% of variation explained) and a branching
Table 1: vegetation parameters for each age class in the chronosequence of roadcut sites and for the reference natural cliffs
Number of individuals
Species richness
Vegetation cover (m2)
Woody cover (m2)
Extraquadrat species
0–10 (n = 8)
262 6 31.3
24.4 6 2.8
2.1 6 0.2
0.6 6 0.3
5.1 6 0.9
10–20 (n = 7)
377.7 6 136.6
29.1 6 5.7
3.4 6 0.8
1.6 6 0.4
5.1 6 1.2
20–30 (n = 10)
312.3 6 40.8
28.5 6 1.6
3.5 6 0.3
1.5 6 0.2
5.1 6 0.8
273 6 42.4
25 6 2.3
4.1 6 4
2.3 6 0.5
4.9 6 1.5
50–80 (n = 11)
231.8 6 36.9
27.7 6 2.2
3.6 6 0.4
2.2 6 0.5
9.6 6 1.5
Natural (n = 13)
153.7 6 26.4
23.4 6 2.3
5.9 6 0.7
4.9 6 0.7
10.9 6 1.3
3.01*
NS
4.55**
8.94***
5.29***
3.61***
NS
4.35***
6.24***
4.05***
NS
3.00***
3.9***
NS
Age classes (years)
30–50 (n = 7)
F values
Contrast t value, natural vs. all
Contrast t value, natural vs. 50–80
NS
Mean values are given per class along with the SEs. ANOVAs test the effect of age (F values), and the contrasts between roadcuts and natural cliffs
are also provided (t values). Significant levels are denoted as *P < 0.05, **P < 0.01 and ***P < 0.001. Variables were transformed using the Box-Cox
Box–Cox
procedure. For each test, the df is 5 for the effect and 50 for the error term.
24
6
Journal of Plant Ecology
Figure 3: life form (sensu Raunkiaer 1934) composition according to age classes and in natural cliffs for (a) presence absence data (sums of occurrences in quadrats) and (b) abundance data (sums of abundances in quadrats). Hemicryptophytes s.l. (filled circles) includes hemicryptophytes
and geophytes. Other life forms are: therophytes (filled squares), chamaephytes (filled triangles) and phanerophytes (open circles).
ordination of the roadcuts and natural cliffs. The first axis acknowledged the variation with age of roadcuts <30 years old,
while the second axis displayed variation across older classes
(Fig. 4B). Furthermore, the ANOVA analysis of the species
scores according to life form was significant for both axes
(ANOVA F = 3.0, P < 0.05 for axis 1, and F = 3.0, P < 0.05
for axis 2, df = 3 and 217), which indicated that the detected
successional trends were related to life form. As for incidence
data, therophytes dominated in early stages (e.g. C. sancta,
S. oleraceus, etc.) and were progressively replaced by hemicryptophyte grasses (e.g. A. bromoides, Festuca occitanica) and small
chamaephytes (e.g. Thymus vulgaris), which dominated the 20to 30-years old communities (Fig. 4D). However, we did not
find any subsequent sequence in age classes after 30 years
on the second branch associated to constrained axis 2 (30.7%)
(Monte Carlo permutation test P > 0.05). Hence natural cliff
and roadcut communities over 30 years old were dominated
by comparable groups of species (Fig. 4B). Furthermore, the
second branch contrasted specialist species, that is, saxicolous
(e.g. Galium lucidum, Braun-Blanquet et al. 1952) and droughttolerant species (e.g. Sedum spp., saxicolous fern species), with
earlier successional species (Crassulacean acid metabolism and
desiccation-tolerant vs. other species, F = 7.5, P < 0.001, on
1 and 219 df). The specialist species became more frequent
in late successional stages but their contribution to the variation in abundance and incidence was dissimilar, because they
remained at a low level of relative abundance. Herbaceous perennials such as F. occitanica and Brachypodium retusum were
more abundant on younger roadcuts and are highlighted in
the abundance analysis of Fig. 4D. However, they occurred
over a large range of age classes and did not contribute to
the variation in composition of the incidence analysis
(Fig. 4C). On the other hand, the late arrival of phanerophytes
(R. alaternus, J. phoenicea, P. terebinthus, Amelanchier ovalis)
and of specialists such as T. flavum (Braun-Blanquet et al.
1952) was highlighted by the incidence analysis (Fig. 4C).
But these species contributed little to the abundance
analysis, where the smaller and more numerous specialists
such as Sedum spp. most contributed to characterize the older
roadcuts (Fig. 4D).
Extraquadrat species
We detected a mean number of 7.32 (SE = 0.61) extraquadrat
species per site. Among the total of 238 extraquadrat species,
only 17 were never found in quadrats (see supplementary
Table S1). Most extraquadrat species were rarer than the
species in the quadrats but could be found elsewhere or at
another stage of the succession. There was a significant variation
in their richness among age classes (ANOVA F = 5.29, P < 0.001,
on 5 and 50 df), with apparent increase with age. Finally,
although this richness was significantly different between road
outcrops and natural cliffs (Helmert contrast t = 4.052, P <
0.001), the contrast was not significant between natural cliffs
and the older roadcuts of 50–80 (t = 0.8, P > 0.05; Table 1).
DISCUSSION
We found a significant variation in species incidence and relative abundances along the primary succession of outcrop
plant communities, converging toward the situation of natural
cliff communities (Fig. 4A and B). Furthermore, patterns of
variation in species incidence and relative abundance were
similar during the early succession of generalist species and
dissimilar during the late succession of specialist species. The
relative variation in incidence and abundance data conveyed
information on how both the contingent history of colonization
Primary succession on Mediterranean roadcuts25
roadcuts
7
Raevel et al. al. | Primary
Figure 4: NSCA of incidence data (A and C) and of abundance data (B and D), constrained according to age classes. Presentation of the first two
axes, with (A and B) sites positions (points), grouped in age classes (ellipses and labels, legends: filled squares, 0–10 years old; open squares, 10–20
years old; filled circles, 20–30 years old, open circles, 30–50 years old; filled triangles, 50–80 years old; open triangle, natural), (C and D) species
position for species that contribute >0.8% to the variation on one of the first two axes. T (therophyte), H (hemicryptophyte s.l.), C (chamaephyte)
and P (phanerophyte) labels are placed at the barycentres of the corresponding life form (sensu Raunkiaer 1934) groups of species. Abbreviations
for species are provided in supplementary Table S1.
events and the deterministic assembly rules contributed to
community dynamics in space and time (Belyea and Lancaster
1999; Lortie et al. 2004). Dispersal limitation and the selection
of species according to local environmental constraints (habitat filtering) determine which species (according to particular
combinations of trait values) are most likely to establish in particular sites. Subsequent internal dynamics based on species
interactions contribute to variation in relative abundance
and, more specifically, determine which species are most likely
to become dominant in the community (Cingolani et al. 2007;
2007,
Keddy 1992). The consistent changes in species incidence and
relative abundance on roadcuts <30 years old were associated
with a transition in ecological strategies from ruderal species to
more competitive, longer lived species (Grime 2002), which in
26
8
turn came to dominate. In contrast, on roadcuts >30 years old
and natural cliffs, variation in incidence and relative abundance showed dissimilar temporal trends. During late succession, a sequence of specialist species colonized roadcuts at
varying times, causing variation in incidence data across age
classes, but they mostly remained at low relative abundances
so that there was no temporal trend in their relative abundance. This result is consistent with our observation of an increase in the richness of very rare (extraquadrat) species in the
oldest age class roadcuts and on natural cliffs, indicating that
more and more species are sparsely distributed within the sites.
The specialist strategy, which we evaluated on the basis of
information on drought-tolerance and saxicolous preference,
did not contribute significantly to the succession during the
earlier period after roadcut formation. Indeed, between 0 and
30 years, therophyte species were gradually replaced by longer
lived species that are common in the surrounding scrublands,
primarily T. vulgaris, A. bromoides and F. occitanica, and which
are also observed during secondary field succession after agricultural abandonment in our study region (Garnier et al.
2004). As illustrated in secondary succession in the study area,
therophytes are progressively excluded by the growth of longer lived established species through competition for light, water and nutrients (Garnier et al. 2004). Similar rapid changes in
species composition have also been observed in studies of the
colonization of abandoned quarries faces (Yuan et al. 2006). In
contrast, specialized saxicolous species displaying high capacities for water resource capture (root systems), storage (succulent) or drought resistance (e.g. Asplenium ruta-muraria,
C. officinarum, Galium lucidum, Hormatophylla spinosa, Sedum
dasyphyllum) contributed significantly to the community
changes only after 30 years. These specialists are typical of
the Mediterranean limestone cliff environment (BraunBlanquet et al. 1952,
1951, Escudero 1996). The
1952; Davis 1951;
prominent contribution of these species to age classes spanning
30–80 years old is consistent with temporal patterns observed
in the development of vegetation on rock faces in abandoned
quarries (Ursic et al. 1997), which often display plant communities similar in composition to those of natural limestone cliffs
(Larson et al. 2000). The seeds of cliff specialists could arrive
late in the succession due to the limited availability of seed
sources in remote locations, thus illustrating the importance
of contingent dispersal and colonization, as observed in other
primary successions (Jones and del Moral 2009; Novak and
Konvicka 2006). A typical example is provided by T. flavum,
which strongly contributed to the successional sequence of incidence data after 30 years (Fig. 4C) but did not contribute to
the variation after 30 years in the abundance-based analysis
(Fig. 4D). This specialist is scattered in the area on typical limestone natural cliffs and may suffer substantial dispersal limitation. Conversely, therophyte and competitive species were
easily found in the vegetation nearby the roadcuts and could
rapidly colonize during the first 30 years. On the other hand,
Booth and Larson (1998, 2000) provided evidence that the
seeds of cliff specialists can arrive soon on cliff faces but that
Journal of Plant Ecology
the establishment success of the seedlings is limited until an
advanced stage of the succession. Both these processes can explain the pattern observed here. The trend further illustrates
how community composition on roadcuts gradually progresses
towards that of natural limestone cliffs.
Although our chronosequence study provided clear and
consistent successional patterns, some caution should be taken
in the interpretation of the synchronic approach. We sampled
a broad area of 1886 km2 and the sampling necessarily introduced some variation among sites in terms of aspect, heterogeneity, microclimate and neighboring land use (Prach and
Rehounkova 2006), as well as regarding the sources of colonizers. However, all the species at all stages, including the specialists, are widespread all over the study area and we therefore
did not expect significant differences in the availability of
colonizers. Furthermore, regarding environmental variation,
there was no major bioclimatic bias in dominant vegetation
across the study area, where the ‘humid Meso-Mediterranean’
vegetation of limestone scrublands naturally gives way to
evergreen oak forests. Finally, although it is practically impossible to ensure complete homogeneity among replicate roadcuts within age classes, replicating many sites over the study
area allowed us to capture a large range of environmental
variation within each age class, making the results more robust
to criticism of the chronosequence approach (Johnson and
Miyanshi 2008).
Furthermore, the NSCA has proved to be useful for analyzing the variation in community composition with respect
to environmental variables (Gimaret-Carpentier et al. 1998b;
Pélissier et al. 2003;
2003, Pelissier and Couteron 2007; RejouMechain et al. 2008). Nevertheless, ordination techniques
based on linear algebra have been often criticized for the
spurious arch effects they can yield when nonlinear trends
occur. The shape of the ordination should then be discussed
with caution, but the two-branch ordination pattern was still
not central to the present work. More insightful is the fact that
the changes in incidence and abundance data are similar in
early succession, and dissimilar in late succession, which is
a feature independent from any bias in the ordination technique. It is further noticeable that the ordination based on
Bray-Curtis distances (Anderson and Wills 2003) provided
the same two-branch pattern than the NSCA. The pattern
was therefore not an artifact and provided relevant insights
on the ecological succession on roadcuts.
In conclusion, our investigation of species incidence and relative abundances along a succession of roadcut and natural
cliff plant communities in Mediterranean France provides
novel insights into the relative importance of colonization
events and community assembly rules. Although the vertical
aspect and scattered spatial distribution of roadcuts may cause
community dynamics to differ from that in other types of plant
communities (Larson et al. 2000), only a few studies have investigated this possibility (Novak and Konvicka 2006; Ursic
et al. 1997; Yuan et al. 2006), and there has been no detailed
study of the underlying processes. An important fact is that
Raevel et al. al. | Primary
Primary succession on Mediterranean roadcuts27
roadcuts
9
dispersal and/or establishment limitation of outcrop specialists
is likely to explain why the first decades of succession are quite
similar to that of a secondary succession in nearby scrublands,
while the subsequent phase is marked by the dynamics of specialists coming from farther sources.
A perspective would be to further address the patterns of
functional trait diversity during succession, in particular in
terms of resource acquisition and conservation (Caccianiga
et al. 2006; Navas et al. 2010), which would provide further
insights into the nature of the underlying processes. Moreover,
we did not investigate the issue of habitat and community
heterogeneity within road and natural outcrops, and a perspective will be to assess how the local variation in abiotic context
due to microenvironmental heterogeneity (Baasch et al. 2009)
and the differences in soil accumulation and resource availability (Matthes and Larson 2006; Yuan et al. 2006) influence
the gradual differentiation in vegetation composition across
sites but also within sites. In ‘niche construction’ theory
(Chapin et al. 1994; Connell and Slatyer 1977), early species
may facilitate the arrival and coexistence of later more competitive species by improving substrate in local patches
(Novak and Konvicka 2006). Localized disturbances related
to rock falls and shattering of rocks by root development of
establishing dwarf phanerophytes or erosion can further
open new microsites allowing early colonists to persist in
a sort of cyclic process (Escudero 1996). The vertical outcrops
therefore open promising perspectives for investigating complex spatial and temporal aspects of ecological succession
and community dynamics.
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ACKNOWLEDGEMENTS
Fukami T, Martijn Bezemer T, Mortimer SR, et al. (2005) Species divergence and trait convergence in experimental plant community
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Conflict of interest statement. None declared.
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