Journal of

An integrated analysis of the effects of past land use on

Blackwell Publishing Ltd.

Ecology 2003
91, 731742 forest herb colonization at the landscape scale
KRIS VERHEYEN, GLENN R. GUNTENSPERGEN*,
BERNARD BIESBROUCK and MARTIN HER MY
Laboratory for Forest, Nature and Landscape Research, University of Leuven, V. Decosterstraat 102, B-3000 Leuven,
Belgium, and *Patuxent Wildlife Research Center, US Geological Survey, 11530 American Holly Drive, Laurel, MD
20708, USA

Summary
1 A framework that summarizes the direct and indirect effects of past land use on forest
herb recolonization is proposed, and used to analyse the colonization patterns of forest
understorey herbaceous species in a 360-ha mixed forest, grassland and arable land-
scape in the Dijle river valley (central Belgium).
2 Fine-scale distribution maps were constructed for 14 species. The species were
mapped in 15 946 forest plots and outside forests (along parcel margins) in 5188 plots.
Forest stands varied in age between 1 and more than 224 years. Detailed land-use his-
tory data were combined with the species distribution maps to identify species-specific
colonization sources and to calculate colonization distances.
3 The six most frequent species were selected for more detailed statistical analysis.
4 Logistic regression models indicated that species frequency in forest parcels was a
function of secondary forest age, distance from the nearest colonization source and
their interaction. Similar age and distance effects were found within hedgerows.
5 In 199 forest stands, data about soils, canopy structure and the cover of competitive
species were collected. The relative importance of habitat quality and spatio-temporal
isolation for the colonization of the forest herb species was quantified using structural
equation modelling (SEM), within the framework proposed for the effects of past land
use.
6 The results of the SEM indicate that, except for the better colonizing species, the
measured habitat quality variables are of minor importance in explaining colonization
patterns, compared with the combination of secondary forest age and distance from col-
onization sources.
7 Our results suggest the existence of a two-stage colonization process in which
diaspore availability determines the initial pattern, which is affected by environmental
sorting at later stages.
Key-words: Adoxa, Arum, dispersal limitation, forest herbs, Geum, historical ecology,
Lamium, landscape ecology, Primula, Ranunculus, secondary forest succession, structural
equation modelling
Journal of Ecology (2003) 91, 731742

the first to challenge the traditional view of niche-

Introduction
A better understanding of colonization processes is
critical to understanding the general patterns and proc-
esses in plant communities. Grubb (1977) was among
Correspondence: Kris Verheyen, Laboratory for Forest,
Nature and Landscape Research, University of Leuven, V.
2003 British Decosterstraat 102, B-3000 Leuven, Belgium
Ecological Society (e-mail kris.verheyen@agr.kuleuven.ac.be).
assembled plant communities. By elaborating on the
different processes involved in colonization (the pro-
duction of viable diaspores, dispersal in space and time,
germination requirements, establishment of seedlings
and the further development of the immature plant),
Grubb stated that, at the local scale, differential colon-
ization capacities of plant species are of crucial import-
ance for the coexistence of large numbers of species with
similar resource requirements. Twenty years later, a
732
K. Verheyen et al.

Fig. 1 Model hypothesizing the effects of past land use on forest herb species colonization. COLONIZATION (the frequency of
colonizing forest herbs) is a latent variable, while the variables in octagons are statistical composites: LAND USE = land-use
history and spatial isolation, SOIL = soil conditions and CANOPY = canopy structure. Variables shown in boxes are the
measured variables: forest age = secondary forest age; distance = species-specific distances from colonization sources; texture
= soil texture; moisture = soil moisture; pH = soil pH; shrub BA = log-transformed basal area of the shrubs; cover
competitives = the cover of competitive herbs and colonization frequency = ln-transformed frequency of the colonizing forest
herbs. Double-headed arrows represent correlations between independent variables, while single-headed arrows describe
assumed causal relationships.

growing body of literature confirms Grubbs thesis. It
has been demonstrated that dispersal is a key factor in
community assembly. Evidence comes from observa-
tional studies (e.g. Hubbell et al. 1999), experimental
studies (e.g. Turnbull et al. 2000) and mathematical
models (e.g. Tilman 1994).
Most data concern established communities per-
petuated by small-scale, low-intensity disturbances (i.e.
gap-phase dynamics). However, there is no reason to
believe that fundamentally different processes operate
when larger spatial scales and more intensive dis-
turbances are involved (Bazzaz 1996). Although our
understanding of the theoretical framework of succes-
sion has been significantly improved (e.g. Connel &
Slatyer 1977; Huston & Smith 1987), the possibility
that a successional sere could be generated by species
having different dispersal capacities remains largely
unexplored. Recently, however, a simulation study by
Hovestadt et al. (2000) demonstrated that typical suc-
cessional patterns can be generated by differential dis-
persal alone.
Forest herb communities develop slowly in second-
ary forest established on former agricultural land. It
has been demonstrated that some species do not col-
onize secondary forests even after tens to hundreds of
years, while others are able to recolonize quickly (e.g.
Peterken & Game 1984; Motzkin et al. 1996; Wulf
1997; for recent overviews see Hermy et al. 1999 and
Verheyen et al. 2003). A niche-based approach would
suggest that these highly different colonization capa-
cities are mainly a consequence of recruitment being
hampered by the poor habitat quality in young forests.
The relationship observed between habitat quality and
2003 British past land use depends both on the nature and duration
Ecological Society, of the former land use and on processes related to
Journal of Ecology, aggrading forest ecosystems. For instance, following
91, 731742 arable use, levels of mineral nutrients, especially pho-
sphate, generally increase (Koerner et al. 1997; Honnay
et al. 1999). In conjunction with a still open canopy,
these promote the vigorous growth of competitive
species (sensu Grime et al. 1988) such as Urtica (Pigott
1971), which may, in turn, hamper the recruitment of
forest species. More recently, however, both observa-
tional studies (Matlack 1994; Grashof-Bokdam 1997;
Brunet & von Oheimb 1998; Bossuyt et al. 1999;
Butaye et al. 2001; Dzwonko 2001; Singleton et al.
2001; Verheyen & Hermy 2001a,b) and experimental
studies (Ehrln & Eriksson 2000) have demonstrated
that some form of dispersal limitation can also occur
in secondary forest succession.
We propose a model to explain the effects of past
land use on both environmental and canopy variables
and forest herb colonization (Fig. 1). Past land use can
have direct effects on herb colonization (from the phys-
ical removal of the plant species and the subsequent
spatial and temporal isolation from their respective
colonization sources) as well as indirect effects caused
by its impact on habitat quality variables (e.g. on the
cover of competitive species or on soil nutrient levels).
In this study, structural equation modelling (SEM) is
introduced to quantify these direct and indirect effects,
and thus to perform a novel integrated analysis of the
colonization process. Furthermore, our study extends
work at the local scale (i.e. one forest patch), to the
landscape or land mosaic scale (i.e. forest patches
embedded in a non-forested, agricultural matrix).
Three specific questions are addressed. (i) Is spatio-
temporal isolation from diaspore sources a limiting
factor for forest herb colonization at a landscape scale?
(ii) What are the direct and indirect effects of past
agricultural land use on present-day habitat quality of
forests? (iii) What is the relative importance of these
two factors (isolation and quality) for landscape scale
colonization?
733
Land use and forest
herb colonization
Fig. 2 Map of the study area (the 360-ha Doode Bemde
nature reserve) showing the 1999 land use, the location of the
hedgerows (i.e. parcel margins composed of trees and/or
shrubs indicated by bold lines) and the location of sampling
points for environmental and canopy variables (circles). The
scale is approximately 1 : 17000.
Materials and methods
The study was carried out in the 360 ha Doode Bemde
nature reserve (Fig. 2), 20 km east of Brussels in central
Belgium. The whole study area is located in the valley
bottom of the Dijle river, a medium-sized lowland river,
that has cut deep (c. 40 m) into the surrounding plateau
during past glaciations. Large-scale deforestation and
several thousand years of human settlement have led to
river discharge being increasingly influenced by surface
run-off. The gradual deposition of eroded silt sedi-
ments resulted in relatively elevated levees with alluvial
floodplain depressions. The soils in the depressions
are fine textured, base rich, poorly drained Fluvisols,
while levee soils are dryer and relatively coarse textured
Fluvisols (De Becker et al. 1999).
At present, almost half (150 ha) of the study area is
forested and Populus x canadensis (Moench.) is the
dominant canopy species in almost all stands. From the
2003 British
1950s onwards, the tree layer in most of the existing for-
Ecological Society, ests was cut and replanted with poplars, which were
Journal of Ecology, also widely planted on abandoned agricultural land.
91, 731742 However, the wide (10 m 10 m) spacing used allowed
the spontaneous establishment of other tree and shrub
species and hence many forests have a well-developed
subcanopy characterized by Alnus glutinosa, Coryllus
avellena, Fraxinus excelsior and Quercus robur. The
non-forested parts of the valley are almost all grass-
lands and arable land is relatively uncommon (Fig. 2).
The forests on the better drained sites are rich in early
flowering forest species characteristic of mesic, rich
sites, while alder carr develops on the wettest sites.
Nomenclature follows Lambinon et al. (1998).
During April and May 1999, the distribution of 14 typ-
ical forest understorey herbs was mapped. Verheyen &
Hermy (2001a,b) provide more details about the selec-
tion of fast and slow colonizing species. The latter
ancient forest species recolonize forests after agricul-
tural abandonment at very slow rates (cf. Hermy et al.
1999). In the forest parcels, the species were fully
mapped by walking along parallel transects approxi-
mately 10 m apart and scoring every 10 m the presence/
absence of the species in a circular plot of 5 m radius. A
compass was used where the regular planting pattern of
the poplars did not allow alignment of transects. Out-
side the forests, only the parcel margins were mapped,
to include both hedgerows (i.e. margins composed of
trees and/or shrubs) and non-woody margins (fences,
ditches, roadsides). Again, the presence/absence of the
species was scored every 10 m. This resulted in 21 134
plots, of which 15 946 were situated in forest parcels
and 5188 along parcel margins. The location of all
transects was marked on large scale (1 : 2500) land reg-
ister maps in the field and all plots were later digitized
as points using ArcView 3.1 (ESRI 1998). This method
allowed the distribution of plant species in a 360-ha
landscape to be mapped relatively quickly and
accurately.
:
Land use was reconstructed using historical maps
(1775, 1850, 1865, 1891, 1936) and aerial photographs
(1947, 1969, 1980, 1990, 1995), with scales varying
between 1 : 12500 and 1 : 40000, which are all available
from the National Geographic Institute of Belgium.
In addition, the primitive land register (from 1834
onwards) and an historical work (Martens 1994) were
consulted. Large-scale maps of 1665, 1759 and 1769
that covered only parts of the study area were used to
verify the 1775 map. Land use was categorized as forest
or non-forest at each date. Throughout the historical
period, non-forested land was predominantly grass-
land. Land-use changes between 1775 and 1999 are
shown in Fig. 3. Forested area was very low, with a
minimum in the middle of the 19th century, until a
sharp increase following World War II.
We then delineated parcels within which there was a
common land use at each survey date. For each, we
734
K. Verheyen et al.
Fig. 3 Land use changes in the Dijle valley study area
between 1775 and 1999. Areas are expressed in ha. Dia-
monds indicate forest, squares ancient forest and triangles
non-forest.
Fig. 4 Map showing the distribution of forest age classes and
the ancient parcel margins, based on historical maps and
aerial photographs. The scale is approximately 1 : 17000.
calculated the number of years since reforestation,
assuming that any land-use changes occurred midway
between the dates of two maps (cf. Verheyen et al.
1999). Five classes were distinguished, with ages of 1
24 years, 41 years, 58 years, 86 195 years, and more
than 224 years. At present, the extent of the oldest class
2003 British
is only 15 ha (Figs 3 and 4), but as such stands are prob-
Ecological Society, ably much older than 224 years, they are referred to as
Journal of Ecology, ancient forest. To distinguish possible relict popu-
91, 731742 lations from newly colonized populations of forest
Fig. 5 Distribution map of Adoxa moschatellina, indicating
the species-specific colonization sources, the colonized points
and the non-colonized points. The scale is approximately
1 : 17000.
plant species along woody parcel margins, we identified
ancient parcel margins. These were defined as margins
that (i) were present as woody margins on the 1775
map, (ii) were mapped as boundaries on the 1834 land
register, and (iii) still exist today (Fig. 4). This defini-
tion allowed us to account for ancient parcel margins
that are actually part of a forest. Next, we tried to assess
the age of the hedgerows present in 1999. However,
except for 1775, it was very hard to distinguish hedge-
rows on the historical maps. Therefore, only the five
aerial photographs were used to determine the hedge-
row age, classifying them with ages of 124 years,
41 years and more than 58 years.
:
The combination of land-use history data and spe-
cies distribution maps allowed us to identify species-
specific colonization sources (cf. Peterken & Game
1981). These were defined as plots in which a particular
species was present and that were situated either in
ancient forest parcels or within 10 m of an ancient
parcel margin. We refer to Verheyen & Hermy (2001a)
for a more detailed description of the method and the
assumptions involved. Hence, 14 sets of species-specific
colonization sources were obtained (see example in
Fig. 5).
735 Using the ArcView NearFeat extension (Jennes
Land use and forest 2000), the distance from all points (occupied and
herb colonization non-occupied) to the five nearest colonization sources
was calculated for each species. The average of the five
distances was calculated and grouped into six con-
secutive classes: < 100 m, 100199 m, 200299 m, 300 Soil texture
399 m, 400 499 m and > 500 m.
: Cover competitive 62.95
The environmental and canopy data were collected
during July and August 1999 at 503 sampling points
distributed over 199 forest stands at a density of
approximately four points/ha (Fig. 2). Forest stands
were defined as parcels with both a homogeneous land-
use history and canopy structure. The average stand area
was 0.6 ha, with a minimum of 0.1 ha and a maximum
of 5 ha. At each sampling point, data on soil, the canopy
structure and the competitive species were collected.
After removing the litter, 10 5 cm deep soil sam-
ples were taken within a 5-m radius around each
sampling point and bulked per stand. In the laboratory,
the pH (KCl) 1 N, 1 : 5 suspension was determined
after the samples had been air-dried. The canopy was
described using a modified point-centred quarter
method (Bonham 1989). The tree layer was subdivided
in four diameter classes: < 15 cm, 1530 cm, 3045 cm,
and > 45 cm. Four 90 sectors around each sampling
point were established. In each sector and for every
diameter class, the distance to the nearest tree or shrub
was measured. The average diameter of each class
(7.5 cm, 22.5 cm, 37.5 cm and 52.5 cm, respectively),
was used to calculate its basal area (m2 ha1). The
omnipresent homogeneous poplar canopy meant that
only the smallest diameter class showed significant vari-
ation and therefore only this class (the shrubs) was used
for further analysis. Finally, the combined percentage
cover of tall competitive herbs (sensu Grime et al. 1988)
was estimated within a radius of 5 m around the sam-
pling point using the following cover classes: 0%, < 5%,
6 10%, 1115%, 16 20%, 21 40%, 4160%, 6180%, ratios indicate how much more or less likely it is that a
and > 81%. Urtica dioica was by far the most dominant
competitive herbaceous species, but Angelica sylvestris,
Galium aparine, Filipendula ulmaria, Phragmites austra-
lis and Symphytum officinale also occurred frequently.
For all environmental and canopy variables, average
values at the forest stand level were calculated. Informa-
tion about the soil texture and soil moisture regime
was extracted from the digital Belgian Soil Map
(1 : 20 000) for each stand. Soil texture and moisture
were assigned scores on an ordinal scale and an area-
weighted texture and moisture score was calculated for
each stand. Scores for soil texture ranged from 1 to 3
(1 = loamy sand, 2 = loam, 3 = clay) and from 1 to 4 for
2003 British
soil moisture regime (1 = relatively well drained,
Ecological Society, 2 = imperfectly drained, 3 = poorly drained, 4 = very
Journal of Ecology, poorly drained). An overview of the environmental and
91, 731742 canopy variables is given in Table 1.
Table 1 Overview of the environmental and canopy variables.
See text for more details of measurement
Variable Mean Range Transformation
Soil moisture 2.79 1 4 None
2.08 13 None
Soil pH 4.97 3.37.2 None
Basal area 3.04 0 35 Log (x + 0.1)
shrubs (m2 ha1)
3 90 None
herbs (%)
A necessary first step of the statistical analysis was the
assessment of the species association with forests, as
all the subsequent analyses rely on the assumption that
the studied species occur predominantly in forest hab-
itat. Therefore, the fraction of species occurrences in
non-woody parcel margins vs. the occurrences in forest
parcels and hedgerows was calculated. Statistical sig-
nificance was assessed with a 2 statistic and species not
exhibiting a significant positive association with forests
and woody parcel margins were excluded.
For the remainder of the statistical analysis, plots
located in ancient forest parcels and along ancient par-
cel margins were omitted, as they do not provide any
information about the colonization process. In the first
part of the analyses data at the plot level are used,
whereas in the second part data at the forest stand level
are used.
To explore the spatio-temporal colonization pat-
terns, a multiple logistic regression of the individual
species presence/absence scores against secondary for-
est age, average distance from the colonization source
and the agedistance interaction was performed (cf.
Verheyen & Hermy 2001a). Inclusion of the interaction
allowed us to assess whether the importance of dis-
tance from the colonization source decreases with
increasing secondary forest age. The resulting odds
species is present when the respective variables are
increased by one class. Statistical analyses were done
separately for the plots in the forest parcels and along
the hedgerows. Plots along non-woody parcel margins,
where colonization by forest herbs is unlikely, were
excluded. All analyses were performed with SPSS
10.0.
Structural equation modelling (SEM) (e.g. Maruyama
1998) was used to quantify the relative importance
of spatio-temporal isolation and habitat quality for
the colonization of the different forest species. SEM
compares observed covariances among variables with
those expected from hypothesized relationships. Model
fit to the data is assessed with a 2 test between the
expected and observed covariance matrices. Previous
studies of colonization processes led to our hypothes-
ized model (Fig. 1), which includes observed indicator
736
K. Verheyen et al.
Fig. 6 (a) Percentage of the species occurrences in forests and hedgerows vs. non-woody parcel margins. The species marked with an asterisk are not
significantly associated with woody habitats. (b) The proportion of species occurrences situated in ancient forests and ancient parcel margins (i.e. the
colonization sources). Only the species marked with an asterisk were frequent enough in recent forests to use for the remainder of the statistical analyses.
Values adjacent to the bars indicate the absolute number of occurrences.
variables (boxes), composite variables (octagons) and
a latent variable (ellipse). Statistical composites
(Fornell & Cha 1994; Grace & Jutila 1999; Grace et al.
2000) were constructed in order to examine the col-
lective effects of landscape, soil and canopy variables,
using a multistage least squares approach. Each com-
posite was constructed individually so as to maximize
the variance explained for colonization frequency. The
SAS Proc Reg procedure was used to generate a
predictive equation and predicted scores were used for
the composite values. LAND USE represents the
composite effects of the secondary forest age and the
distance to the species-specific colonization sources;
SOIL represents the composite effects of soil moisture,
soil moisture and soil pH and CANOPY represents the
composite effects of the basal area of the shrubs and
the cover of competitive herbs.
The possible intercorrelation between LAND USE
and SOIL is represented in Fig. 1 by double-headed
arrows. The use of the latent variable COLONIZA-
TION is based on the premise that the observed fre-
quency of forest herbs in the secondary forest parcels is
measured with error and provides an imperfect estim-
ate of the underlying variable of conceptual interest.
Following the convention of SEM, latent variables are
presumed to be the underlying causal influence on
observed values, which is the reason that the arrow
points from the latent variable to the indicator. All
SEM analyses were done using LISREL 8.30 (Jreskog
& Srbom 2000).
Results
2003 British
Ecological Society, The typical distribution pattern of the forest under-
Journal of Ecology, storey herbaceous species is represented by Adoxa
91, 731742 moschatellina (Fig. 5). Three species (Aegopodium
podagraria, Ajuga reptans and Stellaria holostea) were
not significantly associated with forests and woody
parcel margins and thus were excluded from further
analysis (Fig. 6a). A large number of the species occur-
rences were relict populations (i.e. situated in ancient
forest or along ancient parcel margins) and only six
species were frequent enough in recent forests and three
species in recent margins to use for the remainder of the
statistical analyses (Fig. 6b).
All logistic regression models were highly signi-
ficant, but the explained variation varied considerably
between species (Table 2). Both age and distance from
the species-specific colonization sources were import-
ant factors explaining the colonization patterns (Table 2
and Fig. 7). In the forest stands, the frequency of all
species, except Geum urbanum, consistently increased
with increasing secondary forest age and decreased
with increasing distance from the colonization source
(Table 2a and Fig. 7a). Nevertheless, it also appears
that there is a large variation in colonization potential
among these species. Some species (e.g. Lamium
galeobdolon) only colonized older forest parcels lying
close to the colonization sources, while others (e.g.
Ranunculus ficaria) also colonized points in the young-
est forest age class and the furthest distance class. Further-
more, most agedistance interactions were significant
(Table 2a), indicating that the distance effect is not
the same for all the age classes. For species with an
interaction odds ratio larger than one (A. moschatel-
lina, L. galeobdolon and, to a lesser extent, G. urbanum),
the distance effects disappeared as the secondary
forest age increased, suggesting a gradual com-
pletion of the colonization process (Fig. 7a). The
opposite pattern, i.e. a species exhibiting only distance
effects in the oldest age classes, was found for R. ficaria,
Primula elatior and, although not significant, Arum
737
Land use and forest
herb colonization

2003 British
Ecological Society,
Fig. 7 The
Journal species frequency (%) in each age and distance class (grey circles) and in each age-distance class combination (open circles). Colonization
of Ecology,
patterns
91, (a) in forest stands and (b) in hedgerows.
731742
738
K. Verheyen et al.

Fig. 7 continued

maculatum (Table 2a and Fig. 7a). Somewhat similar
spatio-temporal colonization patterns are observed in
the hedgerows (Tables 2b and Fig. 7b). For the few species
that colonized hedgerows, frequency also increased
with increasing hedgerow age and decreased with increas-
ing distance from the colonization sources, except for
A. moschatellina.
Most of the environmental and canopy variables had
a relatively wide range (Table 1). Only soil texture and,
to a lesser extent, soil drainage exhibited less variation:
most soils have a loamy texture and are relatively
poorly drained. The results of the SEM analyses are
given in Figs 8 and 9. For each species modelled, non-
significant P-values associated with the 2 tests indicate
that the covariance structure in the data fitted well to
the hypothesized covariance structure (Fig. 8). The
effect of LAND USE on CANOPY was consistently
strong for all species, while the effect of SOIL on CAN-
OPY was weaker or absent (Fig. 8). LAND USE had a
strong effect on the frequency of the colonizing forest
herbs in secondary forest parcels (Figs 8 and 9). How-
ever, this effect was less pronounced for the relatively

Table 2 Multiple logistic regression of the species presence/absence scores on secondary forest age, average distance from the
colonization source and the interaction between these variables. Analyses were done separately for plots located in forests (a) and
for plots along hedgerows (b)

Odds ratios

Species n Nagelkerke R2* Age Distance Distance age

(a) Forests
Adoxa moschatellina 14 220 0.42**** 1.18* 0.09**** 1.75****
Arum maculatum 14 305 0.23**** 2.30**** 0.48*** 0.96 NS
Geum urbanum 14 323 0.09**** 1.50**** 0.73**** 1.07**
Lamium galeobdolon 14 366 0.52**** 2.90**** 0.21**** 1.27**
Primula elatior 14 323 0.21**** 2.09**** 0.61** 0.86*
Ranunculus ficaria 13 840 0.05**** 1.96**** 0.83*** 0.95*
(b) Hedgerows
Adoxa moschatellina 1028 0.14**** 0.45 NS 0.09** 2.64***
2003 British Geum urbanum 1023 0.10**** 3.70 NS 0.68 NS 0.90 NS
Ecological Society, Ranunculus ficaria 1006 0.08**** 2.90** 1.28 NS 0.66*
Journal of Ecology,
91, 731742 * 2 test statistic; Wald test statistic; ****P 0.0001; ***P 0.001; **P 0.01; *P 0.05; (*)P 0.1; NS = not significant.
739 good colonizing species G. urbanum and R. ficaria (cf.
Land use and forest Figs 6b and 7) and SOIL appeared to be equally import-
herb colonization ant for the latter species. CANOPY had minor to no
effect on colonizing forest herbs.
Discussion
We attempted to perform an integrated study of the
factors controlling forest herb colonization during sec-
ondary forest succession in a recently reforested valley
landscape dominated by relatively simple structured
poplar plantations. It has long been recognized that
past agricultural land use can have multiple, but very
often correlated, effects on the recolonization of forest
herbs. However, for the first time, a formalized frame-
work is proposed that quantifies the relative import-
ance of its direct and indirect effects.
-
Verheyen & Hermy (2001a) discuss the assumptions made
in delimiting species-specific colonization sources.
However, as most of the forests in the Dijle valley are
situated on former grasslands, the assumption that
none of the studied species survived in the pre-forest
grasslands needs further consideration. At present, no
populations of the studied species occur in the few rel-
icts of semi-natural grasslands in the Dijle valley. Fur-
thermore, 164 of the 180 recent forest stands were
established after World War II, when intensive farming
practices (e.g. the application of chemical fertilizers)
had already been introduced. Such practices severely
reduce the survival chances of forest herbs in grass-
lands. Finally, none of the studied species forms a per-
sistent seed bank (e.g. Bossuyt & Hermy 2001).
The high number of species occurrences in ancient
forests and ancient margins compared with recent for-
ests (Fig. 6b) indicates the low colonizing capacities of
most species. Large variation in the size of the relict
populations further suggests large differences in colon-
ization source strength among the different species.
Interestingly, some of the source populations occur in
ancient margins, suggesting that they have persisted for
at least 200 years. Since 1775, these populations have
thus survived long-term adjacent agricultural use (pre-
dominantly as grassland), margin management (e.g.
pollarding, coppicing) and, in some cases, even com-
plete hedgerow clearance. These results are consistent
with the findings of Pollard (1973) and Peterken &
Game (1981) in England, who demonstrated long-term
survival of Mercurialis perennis in hedgerows. In North
America, relict populations of forest species also have
been observed in hedgerows (Fritz & Merriam 1993).
Survival chances would probably have been much
2003 British
smaller if intensively farmed arable fields rather than
Ecological Society, grasslands had bordered the margins (Boutin & Jobin
Journal of Ecology, 1998). Indirectly, our results support the assumption
91, 731742 made by Honnay et al. (1999) and Verheyen & Hermy
(2001a), who deduced from the present-day forest
plant species distributions in two forests, that forest
plant species had survived in (woody) margins during
periods of past agricultural use.
Like other authors (e.g. Matlack 1994; Brunet & von
Oheimb 1998; Bossuyt et al. 1999; Singleton et al.
2001), we assume that the observed decline in fre-
quency of species with increasing distance from the
colonization source can be attributed to distance-
restricted seed dispersal. For the forest parcels, it
appears that every species exhibits an age and distance
effect (Tables 2a and 7a). However, distance effects for
species such as G. urbanum and R. ficaria are only
present in the youngest forest parcels and therefore dis-
persal cannot be regarded as a factor limiting colon-
ization. In contrast, limited dispersal is an important
factor in shaping the distribution of the other species
throughout the landscape. In a comparable study in
a 10 10 km landscape elsewhere in central Belgium,
Butaye et al. (2001) found similar dispersal limitation
in A. moschatellina, L. galeobdolon and P. elatior. As in
the present study, no significant distance effects were
found for R. ficaria but, in contrast, the distance-effect
was also significant for G. urbanum. Distance-dependent
colonization at the landscape scale was also found in
the Netherlands by Grashof-Bokdam (1997).
The similar distance-dependent decline of species
frequency in hedgerows suggests that they have a con-
duit corridor function (sensu Corbit et al. 1999) in our
study area. However, as only a few species have signi-
ficantly colonized the margins, we can assume that the
woody parcel margins act as a filter that discrimin-
ates among the species that move along them. These
findings support those of McCollin et al. (2000), who
found that some forest species are less frequent in
hedgerows than in forests. This is not surprising, as
hedgerows represent a rather different habitat (e.g. Fritz
& Merriam 1993, 1996). Furthermore, more or less
the same age-distance effects are observed as with
colonization in forest stands. Corbit et al. (1999) also
observed a distance effect in hedgerows, implying col-
onization from an adjacent attached stand. However,
unlike water dispersal of riparian flora, for example
(e.g. Honnay et al. 2001), it remains to be demonstrated
whether hedgerows are functional corridors for forest
plant species.
Finally, it is noteworthy that the spatio-temporal
colonization patterns presented here are very similar
to the patterns found in a methodologically identical
study covering the same time-scale but a smaller spatial
scale (34 ha; Verheyen & Hermy 2001a). Differences
were mainly found for moderately good colonizing spe-
cies like A. moschatellina that did not exhibit distance
effects at the local scale, but strong distance effects at
the landscape scale. Hence, it can be deduced that in
this case similar diffusion-like processes dominate the
colonization process both at the local and at the land-
scape scale. However, in less forested landscapes than
the Dijle valley (forest covers 42% of the area), this may
740
K. Verheyen et al.
Fig. 8 Models for the six study species showing 2 model fit statistics and standardized partial correlation and regression
coefficients. See Fig. 1 for symbols. Dashed lines refer to relationships that were non-significant. R2-values associated with
COLONIZATION describe the total amount of variance explained.
not be the case and rare long-distance dispersal events
will probably play a more important role in the colon-
ization process.
-
It is interesting to note that the joint age-distance effect
is by far the most important factor that explains the
species colonization patterns (Fig. 9). Our results sug-
gest that dispersal limits the forest plant species distri-
bution at a landscape scale, which confirms the findings
2003 British
of Ehrln & Eriksson (2000) and Butaye et al. (2001).
Ecological Society, As our analysis accounts both for spatial isolation and
Journal of Ecology, for indirect effects of secondary forest age, an effect of
91, 731742 time per se may be to cause slow colonization processes.
Hence, it is likely that the delayed colonization of forest
plants is not only caused by poor diaspore dispersal,
but also by factors such as limited and/or delayed diaspore
production or diaspore predation (cf. Verheyen et al.
2003). Indeed, the colonization patterns of the study
species cannot be explained by taking into account
only their dispersal strategy. For instance, the diaspores
of the good colonizing R. ficaria lack adaptations for
long-distance dispersal, while the slow colonizing A.
maculatum produces bird-dispersed fleshy fruits. How-
ever, A. maculatum only starts producing seeds after 6
years (Sowter 1949), and the seeds do not germinate
easily (personal observation). By contrast, R. ficaria has
already started producing easily germinating, vegetative
bulbils by the second year (Taylor & Markham 1978).
In conclusion, we think that the importance of the
measured environmental and canopy variables in the
741
Land use and forest
herb colonization
Fig. 9 Total effects of the composite variables on the
frequency of colonizing forest herbs. The total effect of a
variable is the sum of all direct and indirect pathways (see
Fig. 8), standardized with a maximum possible of 1.0.
SEM models for G. urbanum and R. ficaria (i.e. species
that exhibit relatively good colonizing abilities), sug-
gests that colonization is a two-stage process in which
diaspore availability determines the initial colonization
pattern and in which the effects of environmental sort-
ing become apparent at later stages. In areas with more
pronounced environmental gradients than in our study
area, the sorting effects will probably become apparent
earlier. To strengthen these ideas, future models should
include other key habitat quality variables, such as soil
nutrient content, canopy composition and litter depth.
For instance, it has already been demonstrated that
litter accumulation can hamper recruitment in non-
mull ecosystems (Staaf 1992; Eriksson 1995).
Acknowledgements
The authors thank Eric van Beek for assistance with
the field work and Bea Bossuyt, Hans Jacquemyn,
George Peterken, Jim Grace and three anonymous
reviewers for their useful comments. The paper was
written while the first author held a grant from the
Flemish Institute for the encouragement of Scientific
and Technological Research (I.W.T.).
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Received 11 December 2002
revision accepted 13 May 2003