Applied Vegetation Science 20 (2017) 74–83

Interactive effects of land-use history, tree

encroachment and distance to edge on species
richness in an unmanaged heathland
Sebastian Kepfer-Rojas, Christian Damgaard, Torben Riis-Nielsen & Inger Kappel Schmidt

Keywords
Functional groups; Heathland diversity; Land-
use history; Multivariate control; Natural
succession; Structural equation model
Nomenclature
Tutin et al. (1964–1993)
Received 8 February 2016
Accepted 5 August 2016
Co-ordinating Editor: Angelika Schwabe-
Kratochwil
Kepfer-Rojas, S. (corresponding author,
skro@ign.ku.dk )1,
Damgaard, C. (cfd@bios.au.dk)2,
Riis-Nielsen, T. (trni@ign.ku.dk)1,
Schmidt, I.K. (iks@ign.ku.dk)1
1
Department of Geosciences and Natural
Resource Management, University of
Copenhagen, Rolighedsvej 23, 1958
Frederiksberg C, Denmark;
2
Department of Bioscience, Aarhus University,
Vejlsøvej 25, 8600 Silkeborg, Denmark
Abstract
Questions: How do land-use legacies, tree encroachment and distance to the
edge interact to determine species richness patterns in the ground vegetation of
an unmanaged heathland? What are the direct and indirect effects of these fac-
tors? Do different functional groups respond differently to these factors?
Location: Nørholm heathland, southwest Denmark.
Methods: We recorded the overstorey and ground vegetation along with envi-
ronmental variables in 129 plots on a 350 ha heathland where management
ceased more than 100 yrs ago. We used structural equation models (SEM) to
examine the relationship between species richness of functional groups (herbs,
dwarf shrubs and tree seedlings) and ground vegetation cover, overstorey devel-
opment, distance to the edge and nutrient availability.
Results: The relative importance of the driving factors differed between func-
tional groups. Herb richness increased with increasing nutrient availability from
previous land use and decreased with overstorey development. Dwarf shrub
richness responded negatively to overstorey development and herb cover. In
contrast, species richness of tree seedlings responded strongly and positively to
overstorey development but not to environmental variables or ground vegeta-
tion. In general, the effect of nutrient availability and distance to the edge were
of similar magnitude and were largely mediated by the overstorey and ground
vegetation.
Conclusions: Land-use legacies and tree encroachment can have differential
effects on the species richness of different functional groups. Typical heathland
dwarf shrubs were able to withstand moderate levels of increased nutrient avail-
ability and tree colonization. However, the combination of these factors poses a
serious threat, as dwarf shrub richness decreased due to an increase in the cover
of herbaceous species and light limitation. The absence of management did not
lead to a rapid loss of typical heathland species.

lower intensity compared to current agricultural systems,

Introduction
Land-use change is a major driver of species richness at
local, regional and global scales (Sala et al. 2000). Changes
in land use have led to profound changes in terrestrial veg-
etation communities (Foley et al. 2005). In Northwest
Europe the area covered by heathlands has severely
decreased over the last 200 yrs (Fag
undez 2013). Together
with increased N deposition, abandonment of traditional
agricultural practices have been the main reason for this
decline (Webb 1998). Even though these practices were of
the effects on the chemical and physical structure of the
soil can last long after the abandonment of agriculture
(Von Oheimb et al. 2008). In heathlands, a common con-
sequence of land abandonment is the increased nutrient
availability in the soil, which can promote encroachment
by grasses and trees (Mitchell et al. 1997).
Alteration in the availability of resources can have direct
and indirect effects on plant diversity. As resource avail-
ability increases, a higher number of species can meet their
requirements, increasing species richness directly (Grime

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S. Kepfer-Rojas et al.
1973). Indirect effects often involve the relationship
between factors that limit productivity (Grace & Keeley
2006; Grace et al. 2011). According to the species–energy
hypothesis, areas with higher energy potential can support
a higher number of individuals or biomass and thus pro-
mote species richness through different mechanisms
(reviewed in Evans et al. 2005). However, higher produc-
tivity may also result in a decline in species richness
through mediation of competitive interactions. Higher pro-
ductivity often results in declines in species richness due to
increased biomass and height of fast-growing species and
ultimately higher competition for light (Roem & Berendse
2000; Hautier et al. 2009).
Besides the effect of biotic and abiotic factors mentioned
above, stochastic events are also important forces structur-
ing communities. Many studies have demonstrated that
the distance to seed sources is a key factor determining col-
onization of reforested areas due to dispersal limitation
(Verheyen et al. 2003; Bartha et al. 2009). This can lead to
increases in species richness when areas are closer to colo-
nization sources (Matsumura & Takeda 2010; Knappov

et al. 2011). Furthermore, the distance to the edges can
also have indirect effects on species richness, depending on
the landscape context and the proximity to forests or agri-
cultural fields, for example, due to a spillover of nutrients,
which in turn increases productivity (Piessens et al. 2006).
It is clear that these biotic, abiotic and stochastic factors
are not necessarily independent of each other. For
instance, forest development is usually faster in abandoned
fields with higher nutrient concentrations and/or closer to
forest remnants (Matlack & Jul 1994; Bartha et al. 2009).
Alternatively, if nutrient availability promotes other com-
petitive species, forest development can be hindered (Man-
ning et al. 2004; Chauchard et al. 2007; Kepfer-Rojas
et al. 2015).
Furthermore, different responses of functional groups to
drivers of change can obscure the mechanisms that affect
the number of species occurring in an area (Pausas 1994;
L€obel et al. 2006; Oberle et al. 2009). Studies classifying
the vegetation in life forms or functional groups have
revealed differential responses to different mechanisms,
not only in magnitude but also in relative importance
(L€obel et al. 2006; Oberle et al. 2009; Saure et al. 2013).
This differentiation is highly relevant for heathlands,
which are usually dominated by sclerophyllous ericoid
‘dwarf shrubs’, intermixed with grasses and forbs. These
functional groups possess contrasting strategies that allow
them to co-exist but at the same time can be decisive for
the balance of intraspecific competition (Aerts 1990). The
dwarf shrubs possess life history traits of a ‘resource con-
servation’ strategy. In combination with their association
to ericoid mychorrizhae, these strategies can confer advan-
tages at the lower end of a nutrient gradient (Aerts & Peijl
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Species richness patterns on abandoned heathland
1993). In contrast, grasses and forbs possess traits allowing
them fast resource acquisition, giving them the advantage
when nutrient availability is high (Aerts 1990). Further-
more, these life history traits of different functional groups
can have a reciprocal effect on soil properties due to plant–
soil feedbacks (van der Putten et al. 2013). Slowly decom-
posing litter in dwarf shrubs can lead to low N-cycling
rates, compared to faster rates at sites dominated by grasses
with faster decomposing litter, and thus affect nutrient
availability (Berendse 1998).
Because these complex mechanisms can lead to con-
trasting diversity patterns, accounting for the interrelation-
ships between factors and functional groups can lead to a
better understanding of the determinants of species diver-
sity.
Here, we examine the impact of nutrient availability,
tree encroachment, distance to the edge and ground vege-
tation cover (vegetation structure) on patterns of species
richness of different functional groups in a successional
heathland abandoned in the late 1890s. Most of the studies
a addressing these issues have focused on these factors indi-
vidually or without considering how they affect each
other. To explore these interacting multivariate mecha-
nisms, we use structural equation models (SEM) to address
the following questions: (1) does nutrient availability and
distance to the edge influence vegetation structure (over-
storey development and ground vegetation composition);
(2) is there a direct relationship between nutrients, over-
storey development and distance to the edge on species
richness; (3) do nutrients affect species richness through
direct effects on the vegetation; and (4) are there differ-
ences in relative importance of these factors among func-
tional groups?
A priori model development
Structural equation modelling (SEM) is an advanced and
robust statistical framework that allows hypothesis test-
ing of complex multivariate networks. By studying path
relationships in a system of variables, SEM emphasizes
the estimation of relationships between variables in com-
plex systems (Grace et al. 2010). Appealing features of
SEM include (1) the possibility of incorporating theoreti-
cal constructs by using latent variables to unite phenom-
ena under a single term, and (2) the possibility of
identifying direct and indirect effects between interacting
variables.
An important step in SEM is the development of an a
priori conceptual model to guide the formulation of statistic
models (Grace et al. 2010). Our a priori model (Fig. 1) is
based on previous models of other ecosystems (e.g. Weiher
et al. 2004; Laughlin et al. 2007; Grace et al. 2011; Veld-
man et al. 2014) adapted to the particular characteristics of
75
Species richness patterns on abandoned heathland
Fig. 1. A priori model for the hypothesized direct and indirect relationships between land-use legacies, distance to edge, overstorey and vegetation cover
and richness of tree seedlings, herbs and dwarf shrubs. Arrows indicate the direction of influence. Signs in parenthesis indicate whether the effect is
expected to be positive (+), negative (
), absent (0) or unknown (?). When several signs are present the response is dependent on functional group (herb/
dwarf shrub/tree seedling). Dashed arrows are reciprocal relationships. A theoretical justification for these hypotheses can be found in Appendix S1.
heathlands and our ecological understanding of the study
area. Our main interest lies in understanding how land-
use history influences species richness patterns either
directly or indirectly through changes in the overstorey
and ground vegetation structure. A theoretical justification
for the specific hypotheses proposed between the variables
in the a priori model can be found in Appendix S1.
In addition to land-use history and forest development,
our model includes the distance to edge as an exogenous
factor. The rationale for this is that distance to external
seed sources is the main determinant of tree colonization
rates in this heathland (Kepfer-Rojas et al. 2014), and sev-
eral studies have demonstrated that distance to edge is a
good proxy for colonization rates, an important determi-
nant of vegetation structure (Bartha et al. 2009; Mat-
sumura & Takeda 2010; Knappov
a et al. 2011). This also
allows examining whether this factor is directly affecting
species richness patterns independently of effects on vege-
tation structure, for example, if colonization rates are
higher in the edges of the heathland.
Finally, our model includes reciprocal relationships to
assess positive plant–soil feedbacks and competitive inter-
actions between functional groups. Such feedbacks were
assessed through fitting a non-recursive SEM (e.g. Grace
et al. 2007; Laughlin et al. 2015). This technique presents
an analytical tool to examine direct reciprocal relationships
between two variables. Importantly, interpretation of
these models requires the assumption that the processes
being measured occur simultaneously and that the current
state of the feedback process summarizes a time sequence
of events. Thus the results obtained represent an equilib-
rium state between the observed feedback processes (Grace
et al. 2007).
76
S. Kepfer-Rojas et al.
We hypothesized that (1) land-use history and distance
to the edge can influence vegetation structure (i.e. cover of
the different functional types); (2) vegetation structure can
have reciprocal effects on nutrient availability; (3) the
overstorey can have effects on both functional types of the
ground vegetation (dwarf shrubs and herbs); and (4) all of
these factors are associated with patterns of species rich-
ness.
Methods
Study site
This study was conducted at the 350-ha heathland of
Nørholm (NH) in southwest Denmark. In contrast to the
majority of heathlands in Europe, this area has been kept
unmanaged for over a century following agricultural
abandonment in 1867. The area consists of previously
cultivated ‘infields’ and uncultivated ‘outfields’. Cur-
rently, approximately 30% is covered by forest of differ-
ent successional stages. Tree colonization has been
indirectly and negatively affected by land-use legacies,
resulting in higher encroachment rates in the former out-
fields where soil nutrients are lower (Kepfer-Rojas et al.
2014, 2015). The ground vegetation (defined here as veg-
etation <2-m tall) is dominated by ericoid dwarf shrub
species (mainly Empetrum nigrum and Calluna vulgaris) on
the outfields and grasses (Deschampsia flexuosa and Molinia
caerulea) on the infields. This heathland has been the sub-
ject of different ecological studies and a more detailed
description of the site’s history, topography and vegeta-
tion dynamics can be found elsewhere (Riis-Nielsen et al.
2005; Kepfer-Rojas et al. 2014, 2015; Ransijn et al.
2015).
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S. Kepfer-Rojas et al.
Data collection
As a detailed description of the sampling methodology
can be found in Kepfer-Rojas et al. (2015), we only
summarize it here. The vegetation was sampled using
129 randomly placed plots between July and August
from 2009 to 2012. Each plot consisted of two concen-
tric circles of 5- and 10-m radius. Within the 5-m radius
circle, the identity (species), DBH and height of all indi-
vidual trees and shrubs was recorded. On the 10-m
radius plot, only stems with DBH >3 cm or height
>50 cm were recorded. We define seedlings as tree and
shrub individuals of height <50 cm and stem diameter
(3–5 cm above ground) <3 cm. Ground vegetation
(vascular plants) was recorded using 12 0.1-m2 circles
(subplots) within each plot. Cover of all species was
visually estimated within each subplot. At each subplot,
canopy cover was measured using a spherical densito-
meter placed in the centre of a plot at approximately
1 m from the ground. Finally, four soil cores were
taken at 5 m from the centre of each plot at every car-
dinal direction.
Statistical analysis
Recent studies of species richness patterns have demon-
strated that multifactorial hypotheses increase the predic-
tive power of models when compared with univariate
hypotheses (e.g. Weiher et al. 2004; Grace et al. 2011).
Prior to evaluating multivariate models, bivariate relation-
ships between richness and the other variables in the
model were assessed (Appendix S2). We examined bivari-
ate plots for the presence of outliers, evidence of skewness
or kurtosis, and for non-linear relations (Laughlin et al.
2007). Some variables were transformed to achieve nor-
mality. All transformations are summarized in
Appendix S3, Table S1.
Development of SEM
Following the structure specified in the a priori model, dif-
ferent observed indicators were used to specify the rele-
vant theoretical constructs in the system. Two latent
variables were specified using two indicators: (1) ‘nutrient
availability’ using the total concentrations of P and the N:C
ratio (using the reciprocal of the C:N ratio makes the indi-
cators positively correlated); and (2) ‘overstorey’ using
stem density (stems >2-m tall) and percentage canopy
cover. Inclusion of latent variables is a common practice in
modern SEM and is used to define variables representing
unobservable theoretical constructs (Grace et al. 2010).
Observed variables that provide some information on these
constructs are then used as indicators. In this case we use
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Species richness patterns on abandoned heathland
the P concentration and the reciprocal C:N ratio to repre-
sent ‘nutrient availability’ because land-use legacies usu-
ally increase the content of P and reduce C from the soil
(Flinn & Marks 2007; De Schrijver et al. 2012). Tree den-
sity and canopy cover were used to represent the effects of
the overstorey, as these represent crowding and light limi-
tation effects occurring as the forest develops.
Other observed variables included in the model were:
‘distance to edge’, as the distance from the centre of each
plot to the closest edge of the heathland; ‘herb cover’ and
‘dwarf shrub cover’ as the average percentage cover of
herbs (i.e. grasses and forbs) and dwarf shrubs per subplot
(n = 12) within a plot; and ‘dwarf shrub richness’, ‘herb
richness’ and ‘seedling richness’, as the average number
of dwarf shrubs, herbs and tree seedlings per subplot
within each plot. To account for possible correlations
between species richness of the different functional
groups we allowed their residual variances to be corre-
lated.
A model was then fitted with the hypothesized rela-
tionships in the a priori model in Fig. 1. Modification
indices and residual covariances were used to identify
possible missing paths and/or non-significant links,
while maintaining the overall initial relationships. Paths
with non-significant P-values (>0.05) were omitted
from the a priori model. The final model was compared
to the a priori model based on Chi-square tests. Overall
model fit was evaluated with the Chi-square statistic
and P-values. Models with P-values >0.05 indicate that
the null hypotheses of no difference between the
observed and the hypothesized correlation structures
cannot be rejected and the model is considered ade-
quate (Grace et al. 2010). In this sense, ‘good-fitting’
SEMs do not demonstrate causality but rather confirm
that the proposed structure in the relationship among
the variables in the system is not inconsistent with a
theoretical causal interpretation (Grace 2006). Direct
and indirect standardized effects were calculated to aid
interpretation of the final model.
Finally, we examined whether spatial autocorrelation
was present in our data and the extent to which it could
affect our results. To do so, we extracted the residuals of
the model and tested for spatial autocorrelation using
Moran0 s I tests, using the matrix of the inverse of the geo-
graphic distances between points as weights. All calcula-
tions and model fitting were done using the lavaan
package (v0.5-15; Rosseel 2012) in the R software (R
Foundation for Statistical Computing, Vienna, AT).
Results
We found 59 species in the ground vegetation layer (dwarf
shrubs = 9, grasses = 19, forbs = 21, tree seedlings = 10).
77
Species richness patterns on abandoned heathland
Average total species richness per subplot (0.1 m2) ranged
from 0.75 to 6.83, with a mean value of 1.62  0.32
(SD). Species richness for the different groups was corre-
lated to all explanatory variables, except for tree seedling
richness, which did not show a significant correlation with
soil parameters (Fig. 2; Appendix S2, Figure S1). Notably,
dwarf shrub richness and herb richness showed opposite
patterns in the response to the explanatory variables,
except for canopy cover, which had a negative effect on
both groups. Bivariate plots for the relationship between
environmental and vegetation structure variables are
shown in Appendix S2, Figure S2.
The overall structure of the a priori model had a good fit
to the data (v = 21.52, df = 17, P = 0.20). However, there
were eight non-significant paths: ‘nutrient availability’ on
‘dwarf shrub cover’ or ‘herb cover’; ‘dwarf shrub cover’ on
‘herb cover’; ‘herb cover’ and ‘dwarf shrub cover’ on ‘seed-
ling richness’; ‘overstorey’ on ‘dwarf shrub richness’; and
‘dwarf shrub cover’ on ‘herb cover’ or ‘herb richness’.
Comparing these models revealed that including these
paths did not significantly improve model fit (D v2 = 6.53,
D df = 7, P = 0.48). Thus, the model without those paths
was accepted. This final model (Fig. 3) showed an ade-
quate fit to the data (v = 28.04, df = 24, P = 0.26).
Moran0 s I tests showed significant spatial autocorrelation
for all the variables in the final model, except for P
Fig. 2. Correlations between indicator, exogenous and endogenous variables. Positive correlations are shown in red, negative correlations in blue.
Numbers indicate Pearson’s correlation coefficients. Significant correlations are denoted with a star (P < 0.05).
78
S. Kepfer-Rojas et al.
concentration and tree seedling richness (Table 1,
Appendix S3). Because positive spatial autocorrelation
reduces the effective sample size we used the degree of spa-
tial autocorrelation to estimate a new effective sample size:
1
q
n0 ¼ n
1þq
where n is the sample size, n0 is the new effective sam-
ple size and q is the correlation coefficient obtained from
the Moran’s I test (Dale & Fortin 2014). We used the
new effective sample size to calculate corrected SE for
the parameters in our model and tested whether these
were different from zero using a t-test. All the parame-
ters estimated in our model remained significant after
accounting for spatial autocorrelation (Appendix S4,
Table S2).
The effects of environmental and vegetation structure
variables on species richness were complex and depended
on the functional groups. The model explained 71%, 72%
and 47% of the variation of the richness of dwarf shrubs,
herbs and seedlings. ‘Dwarf shrub richness’ responded
only through effects on vegetation and was negatively
affected by ‘overstorey’ and, to a larger extent, by ‘herb
cover’, whereas ‘dwarf shrub cover’ had a strong positive
effect. ‘Herb richness’ responded to environmental factors
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S. Kepfer-Rojas et al. Species richness patterns on abandoned heathland

Fig. 3. Final structural equation model (v = 28.04, df = 24, P = 0.26) for the hypothesized direct and indirect relationships between land-use legacies,
distance to edge, overstorey and ground vegetation (herbs and dwarf shrubs), vegetation structure and richness of tree seedlings, herb and dwarf shrubs
at Nørholm heathland. Circles are latent variables used to represent two theoretical constructs: (1) ‘nutrient availability’, using P concentration and the
reciprocal C:N; and (2) ‘overstorey’, using percentage canopy cover (canopy) and the density of trees >2-m tall (density). Variables in square boxes pointing
from the latent variables are the indicators. Arrows indicate the direction of influence, with the size of the arrow proportional to its standardized effect
(numbers accompanying arrows). For clarity, black lines are positive and dashed grey lines are negative effects. DS = dwarf shrub.

Table 1. Direct, indirect and total standardized effects of environmental and vegetation structure, decreasing with ‘overstorey’ and
factors (nutrient availability and distance to edge) and vegetation structure ‘distance to the edge’, and increasing with ‘herb cover’ and
(overstorey and ground vegetation cover) on species richness of functional
‘nutrient availability’. ‘Seedling richness’ responded
groups. DS = Dwarf shrub.
strongly and positively to ‘overstorey’ but not to the other
Richness environmental variables or ground vegetation (Fig. 2).
DS Herb Seedling
Direct, indirect and total effects of the predictors on spe-
cies richness varied widely among functional groups
Nutrient Availability
(Table 1). The total effect of ‘nutrient availability’ was pos-
Direct 0 0.24*** 0
itive for herbs, negative for seedlings and not significant
Indirect 0.09n.s. 0.06***
0.32***
Total 0.09n.s. 0.30***
0.32*** for dwarf shrubs. For herbs, both direct and indirect effects
Distance to Edge were positive. For seedlings, the effect was only indirect
Direct 0
0.15** 0 through vegetation because lower overstorey development
Indirect 0.40***
0.06n.s.
0.29*** led to a lower number of tree seedling species.
Total 0.40***
0.21**
0.29*** Distance to the edge had only indirect effects on seedling
Overstorey
and dwarf shrub richness as the moderator of vegetation
Direct 0
0.21** 0.68***
structure. However, these effects differed in direction,
Indirect
0.15n.s.
0.13* n.a.
Total
0.15n.s.
0.34** 0.68*** being positive for dwarf shrubs and negative for tree seed-
Herb Cover lings. For herbs, the total effect of ‘distance to the edge’
Direct
0.25*** 0.61*** 0 was negative due to a direct negative effect and indirect
Indirect
0.46*** n.a. n.a. decrease in ‘herb cover’.
Total
0.72*** 0.61*** n.a. Similar to the effect of distance to the edge, the effect of
DS Cover
‘overstorey’ on ‘dwarf shrub richness’ was only indirect.
Direct 0.66*** 0 0
For herbs, the total effect of the ‘overstorey’ was negative,
Indirect
0.03n.s.
0.02n.s. 0.12*
Total 0.63***
0.02n.s. 0.12* due to a direct effect and a decrease in ‘herb cover’. The
total effect on seedlings was strong and positive, and not
*P < 0.05; **P < 0.01; ***P < 0.001; n.s.
= not significant; n.a. = not
mediated by the ground vegetation.
applicable.

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Species richness patterns on abandoned heathland
‘Dwarf shrub cover’ had an indirect positive effect on
tree seedling richness, due to a negative effect on ‘over-
storey’ mediated by a decrease in nutrient availability.
Discussion
Nutrient enrichment and tree encroachment are important
drivers of diversity patterns in European heathlands. Appli-
cation of an SEM framework disclosed direct and indirect
relationships between these interacting factors and how
they can ultimately affect species richness patterns. Results
of this analysis revealed complex interactions between
these factors and support the growing body of evidence for
multivariate control of species richness patterns (Weiher
et al. 2004; Grace & Keeley 2006; Grace et al. 2011).
Although the general structure of our model agrees with
models applied in other systems, there were important dif-
ferences in the direction of some relationships. In many
systems land-use legacies typically result in soils depleted
of organic matter and with high nutrient concentrations
and pH (Flinn & Marks 2007). However, the magnitude
and persistence of land-use legacies is dependent on the
type, intensity and duration of agriculture and the pre-
existing biophysical conditions. In Nørholm heathland, the
current differences in soil nutrients are moderate, mainly
because traditional agricultural practices were not as inten-
sive as modern agriculture and because these practices
ceased more than 100 yrs ago.
Despite these moderate changes, higher nutrient avail-
ability was related to lower levels of tree encroachment.
Studies in heathlands and other systems have shown that
tree colonization benefits from increased nutrient avail-
ability (Manning et al. 2004). However, previous work on
this heathland attributed this negative effect to suppression
of tree colonization by increased grass cover (particularly
Deschampsia flexuosa), mediated by nutrient availability
(Kepfer-Rojas et al. 2014, 2015), which highlights the
importance of the abiotic environment in regulating biotic
interactions.
On the other hand, nutrient availability was not related
to the cover of dwarf shrubs or herbs, instead we found a
negative effect of dwarf shrub cover on nutrient availabil-
ity. A possible explanation for the lack of an effect of nutri-
ent availability on dwarf shrub species can be found in
their adaptations and functional strategies. Ericoid dwarf
shrubs are characterized by physiological and anatomical
adaptations, allowing them to minimize nutrient loss (e.g.
thick evergreen leaves with low nutrient levels, slow
growth rates and slow decomposing litter). In addition,
their association with ericoid mycorrhizae allows them to
access nutrients even at low concentrations and from com-
plex organic sources and thus attain a high cover indepen-
dently of the availability of nutrients (Aerts & Heil 1993).
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S. Kepfer-Rojas et al.
Areas dominated by dwarf shrubs accumulate slow decom-
posing litter and can maintain the soil at low nutrient
levels, which in turn can result in spatially aggregated
nutrient patterns, as observed with the positive spatial
autocorrelation found for soil nutrients in this heathland.
The lack of an effect of nutrient availability and the low
explanatory power found for herb cover suggest that other
factors could be in play. For instance, disturbances follow-
ing abandonment of agriculture, fires and heather beetle
attacks could create colonization opportunities for fast-dis-
persing herb species (Riis-Nielsen et al. 2005). The long-
term observations in this heathland support this notion as
disturbances were more strongly related to vegetation pat-
terns than soil conditions (Ransijn et al. 2015).
Studies dealing with ecological succession suggest that
the importance of abiotic and biotic factors relative to dis-
persal limitation should increase during the course of vege-
tation development (Baasch et al. 2009). Here we found
that even after ca. 120 yrs of free succession, the effects of
dispersal limitation are still important. First, the positive
residual spatial autocorrelation in vegetation variables
(canopy cover, tree density and the cover and richness of
herbs and dwarf shrubs) indicates that the vegetation is spa-
tially structured likely due to dispersal. Second, distance to
the edge was an important determinant of vegetation struc-
ture patterns, with slightly stronger effects than nutrient
availability. The strong effect on the development of the
overstorey confirms previous studies in the area and high-
lights the importance of the proximity to external sources
for forest development (Kepfer-Rojas et al. 2014). Distance
to the edge can be a proxy for colonization, indicating that
colonization pressure is higher in areas closer to external
sources. However, this proxy is likely to be associated with
other processes, such as higher disturbance levels in the
edges and proximity to other habitats. Clarifying the mech-
anisms behind this relationship will require future work.
Analysing diversity patterns of different functional
groups provided valuable insights into plausible mechanis-
tic drivers of diversity patterns in this heathland. Although
the general structure of the model proved to be appropriate
for the different functional groups, there were important
differences in the relative importance of the factors and
mechanisms that control species richness for the particular
functional groups.
The effect or nutrient availability and distance to the edge
were largely mediated by the overstorey and ground vegeta-
tion, except for herb richness, which was also affected
directly, albeit weakly, by these factors. Ground vegetation
was an important and strong link between abiotic factors
and species richness, supporting the hypothesis of a causal
relationship between productivity and plant diversity
(Grime 1973). Although this relationship is widely recog-
nized, the functional shape of this relationship has been a
Applied Vegetation Science
S. Kepfer-Rojas et al.
matter of contention (e.g. Adler et al. 2011; Fridley et al.
2012). In the case of herb richness, we observed a linear
positive relationship with no indication of a decrease at the
higher end of the nutrient gradient, as is expected when
competitive exclusion is operating (Grime 1973). It is likely
that the increase in nutrient availability was not sufficiently
high to promote competitive exclusion within this func-
tional group. On the other hand, increases in herb cover
had a strong total negative effect on dwarf shrub richness. A
decrease in one functional group at the expense of another
suggests that competitive interactions are possibly operating
(Rosenzweig & Abramsky 1993) and are being mediated by
increased nutrient availability. However, recent studies have
demonstrated that the changes in diversity with increased
nutrient availability are mostly a result of increased compe-
tition for light (Hautier et al. 2009; Borer et al. 2014),
favouring taller species. Our results seem to contradict this
hypothesis, since dwarf shrubs can attain taller statures than
most herbs and forbs in this area. However, in this case the
appearance of bare ground areas following land-use aban-
donment could provide establishment opportunities for fast-
growing species like grasses (Grubb 1977). Increased pro-
ductivity of these grasses can then prevent seedlings of
dwarf shrubs and trees from establishing, because of compe-
tition for light and higher litter production.
The development of the overstorey had a large impact in
this community. Light limitation led to a decrease in the
number of herb and dwarf shrub species, mainly due to
the reduced ground vegetation cover. On the other hand,
species richness of seedlings was exclusively determined
by the overstorey and only indirectly by the effects of
dwarf shrub cover, nutrient availability and distance to the
edge. The same effect was found in a successional study of
this area, demonstrating that species richness and composi-
tion of trees were not in equilibrium with soil conditions
(Kepfer-Rojas et al. 2014). We cannot rule out, however,
that this could be an effect mediated by the grass cover. As
mentioned previously, increased grass cover suppresses
seedling colonization in high nutrient areas, and possibly
because seedlings fail to access these areas, the effects on
diversity are not evident. We could not test this explicitly
because this effect is expected to act on seedlings at the
time of establishment and not on adult trees.
Although the indirect effects were the determinant for
the patterns of species richness, nutrient availability and
overstorey had direct effects on herb richness. The fact that
species richness responded to nutrient and light availability
independently of cover suggests a filtering effect, whereby
species lacking particular life history traits are excluded
from lower extremes of this gradient (Gough et al. 1994;
Grace & Keeley 2006). Although this is a plausible mecha-
nism partly explaining the species richness patterns of
herbs, species richness of seedlings and dwarf shrubs were
Applied Vegetation Science
Doi: 10.1111/avsc.12270 © 2016 International Association for Vegetation Science
Species richness patterns on abandoned heathland
not determined directly by higher nutrient availability or
distance to the edge. A possible explanation for this is that
the life history traits of these groups allow them to be suc-
cessful at lower nutrient availability. For instance, associa-
tions of trees and dwarf shrubs with ectomychorrhizae and
ericoid mycorrhizae, respectively, makes them more effi-
cient at foraging for organic sources of N in the soil (Read
et al. 2004; Collier & Bidartondo 2009), and thus to sur-
vive in areas with low resource availability. Furthermore,
higher shade tolerance of some tree species, combined
with increased seed output as the forest develops, can
result in a higher number of seedling species.
This study revealed how intricate relationships between
land-use legacies and tree colonization have contributed to
determine the diversity patterns of this heathland. Although
at Nørholm heathland traditional management has been
abandoned for over a century, typical heathland vegetation
has been remarkably stable (Ransijn et al. 2015). In other
similar areas, conversion into grasslands and forest occurs
within a few decades. In this case, the effects of land-use
legacies on grass invasion and on tree encroachment have
so far allowed persistence of ericoid vegetation. Although
the increase in nutrient availability promoted grass invasion,
dwarf shrubs are able to attain high levels of cover and rich-
ness. Similarly, dwarf shrub vegetation seems to cope with
light limitation to a certain extent. However, the combina-
tion of these factors poses a serious threat, as dwarf shrubs
are not likely to persist in areas with high nutrient availabil-
ity and low light, because of the effect that these factors will
have on productivity of herbaceous species and biotic inter-
actions. Nevertheless, the general impoverishment of spe-
cies as the forest develops can be a temporary effect due to a
delay in colonization of typical forest herb species, provided
that these species are present in the remaining forest
patches outside the heathland.
Acknowledgements
We are grateful to Allan O. Nielsen, Xhevat Haliti, Jane
Kongstad, Geshere Abdisa, Annelies Van der Craats and
Karen Sverrild for assisting with fieldwork. We owe special
thanks to Karl and Martha Nielsen, the owners of Nørholm
Heath, for welcoming the research. The research was sup-
ported by the participating institutes. We thank Angelika
Schwabe-Kratochwil and three anonymous reviewers for
commenting on a previous version of this manuscript.
References
Adler, P.B., Seabloom, E.W., Borer, E.T., Hillebrand, H., Hautier,
Y., Hector, A., Harpole, W.S., O’Halloran, L.R., Grace, J.B.,
(. . .) & Yang, L.H. 2011. Productivity is a poor predictor of
plant species richness. Science 333: 1750–1753.
81
Species richness patterns on abandoned heathland
Aerts, R. 1990. Nutrient use efficiency in evergreen and decidu-
ous species from heathlands. Oecologia 84: 391–397.
Aerts, R. & Heil, G.W. 1993. Heathlands: Patterns and Processes in a
Changing Environment. Kluwer Academic, Dordrecht, NL.
Aerts, R. & Peijl, M.J. Van Der. 1993. A simple model to explain
the dominance of low productive perennials in nutient-poor
environments. Oikos 66: 144–147.
Baasch, A., Tischew, S. & Bruelheide, H. 2009. Insights into suc-
cession processes using temporally repeated habitat models:
results from a long-term study in a post-mining landscape.
Journal of Vegetation Science 20: 629–638.
Bartha, S., Scott, M.J., Steward, T.A. & Cadenasso, M.L. 2009.
Plant colonization windows in a mesic old field succession.
Applied Vegetation Science 6: 205–212.
Berendse, F. 1998. Effects of dominant plant species on soils dur-
ing sucession in nutrient-poor ecosystems. Biogeochemistry
42: 73–88.
Borer, E.T., Seabloom, E.W., Gruner, D.S., Harpole, W.S., Hille-
brand, H., Lind, E.M., Adler, P.B., Alberti, J., Anderson,
T.M., (. . .) & Yang, L.H. 2014. Herbivores and nutrients con-
trol grassland plant diversity via light limitation. Nature 508:
517–520.
Chauchard, S., Carcaillet, C. & Guibal, F. 2007. Patterns of land-
use abandonment control tree-recruitment and forest
dynamics in Mediterranean Mountains. Ecosystems 10: 936–
948.
Collier, F.A. & Bidartondo, M.I. 2009. Waiting for fungi: the
ectomycorrhizal invasion of lowland heathlands. Journal of
Ecology 97: 950–963.
Dale, M.R.T. & Fortin, M. 2014. Spatial Analyis: A Guide for Ecolo-
gists, Cambridge University Press, Cambridge, UK.
Evans, K.L., Warren, P.H. & Gaston, K.J. 2005. Species–energy
relationships at the macroecological scale: a review of the
mechanisms. Biological Reviews of the Cambridge Philosophical
Society 80: 1–25.
Fag
undez, J. 2013. Heathlands confronting global change: dri-
vers of biodiversity loss from past to future scenarios. Annals
of Botany 111: 151–172.
Flinn, K.M. & Marks, P.L. 2007. Agricultural legacies in forest
environments: tree communities, soil properties, and light
availability. Ecological Applications 17: 452–463.
Foley, J.A., Defries, R., Asner, G.P., Barford, C., Bonan, G., Car-
penter, S.R., Chapin, F.S., Coe, M.T., Daily, G.C., (. . .) & Sny-
der, P.K. 2005. Global consequences of land use. Science 309:
570–574.
Fridley, J.D., Grime, J.P., Huston, M.A., Pierce, S., Smart, S.M.,
Thompson, K., B€ orger, L., Brooker, R.W., Cerabolini, B.E.L.,
(. . .) & Le Bagousse-Pinguet, Y. 2012. Comment on “Produc-
tivity is a poor predictor of plant species richness”. Science
335: 1441.
Gough, L., Grace, J.B. & Taylor, K.L. 1994. The relationship
between species richness and community biomass: the
importance of environmental variables. Oikos 70: 271–279.
Grace, J.B. 2006. Structural Equation Modeling and Natural Systems.
Cambridge University Press, Cambridge, UK.
82 Doi: 10.1111/avsc.12270 © 2016 International Association for Vegetation Science
S. Kepfer-Rojas et al.
Grace, J.B., Michael Anderson, T., Smith, M.D., Seabloom, E.,
Andelman, S.J., Meche, G., Weiher, E., Allain, L.K., Jutila,
H., (. . .) & Willig, M.R. 2007. Does species diversity limit pro-
ductivity in natural grassland communities? Ecology Letters
10: 680–9.
Grace, J.B., Anderson, M.T., Olff, H. & Scheiner, S.M. 2010. On
the specification of structural equation models for ecological
systems. Ecological Monographs 80: 67–87.
Grace, J.B., Harrison, S. & Damschen, E.I. 2011. Local richness
along gradients in the Siskiyou herb flora: RH Whittaker
revisited. Ecology 92: 108–120.
Grace, J.B. & Keeley, J.E. 2006. A structural equation model
analysis of postfire plant diversity in California shrublands.
Ecological Applications 16: 503–514.
Grime, J.P. 1973. Competitive exclusion in herbaceous vegeta-
tion. Nature 242: 344–347.
Grubb, P.J. 1977. the Maintenance of Species-Richness in Plant
Communities: the Importance of the Regeneration Niche.
Biological Reviews 52: 107–145.
Hautier, Y., Niklaus, P.A. & Hector, A. 2009. Competition for
light causes plant biodiversity loss after eutrophication.
Science 324: 636–638.
Kepfer-Rojas, S., Schmidt, I.K., Ransijn, J., Riis-Nielsen, T. &
Verheyen, K. 2014. Distance to seed sources and land-use
history affect forest development over a long-term heathland
to forest succession. Journal of Vegetation Science 25: 1493–
1503.
Kepfer-Rojas, S., Verheyen, K., Johannsen, V.K. & Schmidt, I.K.
2015. Indirect effects of land-use legacies determine tree col-
onization patterns in abandoned heathland. Applied Vegeta-
tion Science 18: 456–466.
Knappov
a, J., Hemrov
a, L. & M€
unzbergov
a, Z. 2011. Coloniza-
tion of central European abandoned fields by dry grassland
species depends on the species richness of the source habi-
tats: a new approach for measuring habitat isolation. Land-
scape Ecology 27: 97–108.
Laughlin, D.C., Abella, S.R., Covington, W.W. & Grace, J.B.
2007. Species richness and soil properties in Pinus ponderosa
forests : a structural equation modeling analysis. Journal of
Vegetation Science 18: 231–242.
Laughlin, D.C., Richardson, S.J., Wright, E.F. & Bellingham,
P.J. 2015. Environmental Filtering and Positive Plant Lit-
ter Feedback Simultaneously Explain Correlations
Between Leaf Traits and Soil Fertility. Ecosystems 18:
1269–1280.
L€
obel, S., Dengler, J. & Hobohm, C. 2006. Species richness of
vascular plants, bryophytes and lichens in dry grasslands: the
effects of environment, landscape structure and competition.
Folia Geobotanica 41: 377–393.
Manning, P., Putwain, P.D. & Webb, N.R. 2004. Identifying and
modelling the determinants of woody plant invasion of low-
land heath. Journal of Ecology 92: 868–881.
Matlack, G.R. & Jul, N. 1994. Plant species migration in a mixed-
history forest landscape in eastern North America. Ecology
75: 1491–1502.
Applied Vegetation Science
S. Kepfer-Rojas et al.
Matsumura, T. & Takeda, Y. 2010. Relationship between species
richness and spatial and temporal distance from seed source
in semi-natural grassland. Applied Vegetation Science 13: 336–
345.
Mitchell, R.H., Marrs, R.H., Duc, M.G.L. & Auld, M.H.D. 1997. A
study of succession on lowland heaths in Dorset, Southern
England: changes in vegetation and soil chemical properties.
Journal of Applied Ecology 34: 1426–1444.
Oberle, B., Grace, J.B. & Chase, J.M. 2009. Beneath the veil:
plant growth form influences the strength of species rich-
ness–productivity relationships in forests. Global Ecology and
Biogeography 18: 416–425.
Pausas, J.G. 1994. Species Richness Patterns in the Understorey
of Pyrenean Pinus sylvestris. Journal of Vegetation Science 5:
517–524.
Piessens, K., Honnay, O., Devlaeminck, R. & Hermy, M. 2006.
Biotic and abiotic edge effects in highly fragmented heath-
lands adjacent to cropland and forest. Agriculture, Ecosystems
& Environment 114: 335–342.
Ransijn, J., Kepfer-Rojas, S., Verheyen, K., Riis-Nielsen, T. &
Schmidt, I.K. 2015. Hints for alternative stable states from
long-term vegetation dynamics in an unmanaged heathland.
Journal of Vegetation Science 26: 254–266.
Read, D.J., Leake, J.R. & Perez-moreno, J. 2004. Mycorrhizal
fungi as drivers of ecosystem processes in heathland and bor-
eal forest biomes. Canadian Journal of Botany 1263: 1243–
1263.
Riis-Nielsen, T., Schmidt, I.K., Frandsen, B. & Binding, T. 2005.
Nørholm Hede: en langtidsundersøgelse af hedens vegetationsud-
vikling og tilgroning. Skov & Landskab, Copenhagen, DE.
Roem, W.J. & Berendse, F. 2000. Soil acidity and nutrient supply
ratio as possible factors determining changes in plant species
diversity in grassland and heathland communities. Biological
Conservation 92: 151–161.
Rosenzweig, M.L. & Abramsky, Z. 1993. How are diversity and
productivity related? In: Ricklefs, R.E. & Schluter, D. (eds.)
Species Diversity in Ecological Communities: Historical and Geo-
graphical Perspectives, pp. 52–65. University of Chicago Press,
Chicago, IL, US.
Rosseel, Y. 2012. lavaan: an R package for structural equa-
tion modeling. Journal of Statistical Software 48: 1–36.
Sala, O.E., Chapin, F.S., Armesto, J.J., Berlow, E., Bloomfield, J.,
Dirzo, R., Huber-Sanwald, E., Huenneke, L.F., Jackson, R.B.,
(. . .) & Wall, D.H. 2000. Global biodiversity scenarios for the
year 2100. Science 287: 1770–1774.
Saure, H.I., Vandvik, V., Hassel, K. & Vetaas, O.R. 2013. Do vas-
cular plants and bryophytes respond differently to coniferous
invasion of coastal heathlands? Biological Invasions 16: 775–
791.
Applied Vegetation Science
Doi: 10.1111/avsc.12270 © 2016 International Association for Vegetation Science
Species richness patterns on abandoned heathland
De Schrijver, A., Vesterdal, L., Hansen, K., De Frenne, P.,
Augusto, L., Achat, D.L., Staelens, J., Baeten, L., De Keers-
maeker, L., De Neve, S. & Verheyen, K. 2012. Four decades
of post-agricultural forest development have caused major
redistributions of soil phosphorus fractions. Oecologia 169:
221–34.
Tutin, T.G., Heywood, V.H., Burges, N.A., Moore, D.M., Valen-
tine, D.H., Walters, S.M. & Webb, D.A. (eds.) 1964–1993.
Flora Europaea,Vols. 1–5. Cambridge University Press, Cam-
bridge, UK.
van der Putten, W.H., Bardgett, R.D., Bever, J.D., Bezemer,
T.M., Casper, B.B., Fukami, T., Kardol, P., Klironomos, J.N.,
Kulmatiski, A., Schweitzer, J.A., Suding, K.N., Van de
Voorde, T.F.J. & Wardle, D.A. 2013. Plant–soil feedbacks: the
past, the present and future challenges. Journal of Ecology
101: 265–276.
Veldman, J.W., Brudvig, L.A., Damschen, E.I., Orrock, J.L., Mat-
tingly, W.B. & Walker, J.L. 2014. Fire frequency, agricultural
history and the multivariate control of pine savanna under-
storey plant diversity. Journal of Vegetation Science 25: 1438–
1449.
Verheyen, K., Guntenspergen, G.R., Biesbrouck, B. & Hermy,
M. 2003. An integrated analysis of the effects of past land use
on forest herb colonization at the landscape scale. Journal of
Ecology 91: 731–742.
Von Oheimb, G., H€ ardtle, W., Naumann, P.S., Westphal, C., Ass-
mann, T. & Meyer, H. 2008. Long-term effects of historical
heathland farming on soil properties of forest ecosystems.
Forest Ecology and Management 255: 1984–1993.
Webb, N.R. 1998. The traditional management of European
heathlands. Journal of Applied Ecology 35: 987–990.
Weiher, E., Forbes, S., Schauwecker, T. & Grace, J.B. 2004. Mul-
tivariate control of plant species richness and community
biomass in blackland prairie. Oikos 106: 151–157.
Zobel, M. 2014. Plant species coexistence: the role of historical,
evolutionary and ecological factors. Oikos 65: 314–320.
Supporting Information
Additional Supporting Information may be found in the
online version of this article:
Appendix S1. Theoretical justifications for a priori model.
Appendix S2. Bivariate relationships between factors in
the system.
Appendix S3. List of variable ranges and transformations.
Appendix S4. Spatial autocorrelation analyses.
83