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RESEARCH ARTICLE
Legacy effects of past land use on current biodiversity in alow-intensity farming landscape in Transylvania (Romania)
Patrick D. Culbert . Ine Dorresteijn . Jacqueline Loos .
Murray K. Clayton . Joern Fischer . Tobias Kuemmerle
Received: 1 October 2015 / Accepted: 29 August 2016
� Springer Science+Business Media Dordrecht 2016
Abstract
Context Ecological impacts of past land use can
persist for centuries. While present-day land use is
relatively easy to quantify, characterizing historical
land uses and their legacies on biodiversity remains
challenging. Southern Transylvania in Romania is a
biodiversity-rich area which has undergone major
political and socio-economic changes, from the Aus-
tro-Hungarian Empire to two World Wars, communist
dictatorship, capitalist democracy, and EU acces-
sion—all leading to widespread land-use changes.
Objectives We investigated whether present-day
community composition of birds, plants, and butter-
flies was associated with historical land use.
Methods We surveyed birds, plants, and butterflies
at 150 sites and classified those sites as forest, arable
land, or managed grassland for six epochs using
historical maps from the 1870s, 1930s, and 1970s,
satellite imagery from 1985 to 2000, and field visits in
2012. Sites were labelled permanent if they had the
same land use at all epochs and non-permanent
otherwise. We used clustering and PERMANOVA
based on community similarity to test for associations
between community composition and land-use
history.
Results We found significant differences (p = 0.030)
in bird communities between permanent and non-
permanent forest sites, and permanent and non-perma-
nent grassland sites (p = 0.051). No significant associ-
ations were found among plants or butterflies and land-
use history.
Conclusions Bird communities were associated
with historical land use, though plants and butter-
flies were not. Historical land-use change in our
study area was likely not sufficiently intense to
cross relevant ecological thresholds that would lead
to legacy effects in present-day plant and butterfly
communities.
Keywords Agricultural intensification � Birds �Butterflies � Farmland abandonment � Historical
ecology � Land-use change � Legacy effects � Plants
Electronic supplementary material The online version ofthis article (doi:10.1007/s10980-016-0441-3) contains supple-mentary material, which is available to authorized users.
P. D. Culbert (&) � T. Kuemmerle
Geography Department, Humboldt-Universitat zu Berlin,
Unter den Linden 6, 10099 Berlin, Germany
e-mail: [email protected]
I. Dorresteijn � J. Fischer
Faculty of Sustainability, Leuphana University Luneburg,
Rotenbleicher Weg 67, 21335 Luneburg, Germany
J. Loos
Agroecology, Georg August University, Grisebachstrasse
6, 37077 Gottingen, Germany
M. K. Clayton
Department of Statistics, University of Wisconsin-
Madison, 1300 University Avenue, Madison, WI 53706,
USA
123
Landscape Ecol
DOI 10.1007/s10980-016-0441-3
Introduction
Agroecosystems provide important habitat for many
species (Donald et al. 2001; Stoate et al. 2009). Land-
use change is a key driver of biodiversity loss in
agroecosystems, (Foley et al. 2005), with both aban-
donment and intensification threatening species’ per-
sistence (Strohbach et al. 2015). However, present-day
land use is not the only important factor influencing
species richness and community composition. Past
land use, particularly agricultural, may result in
ecosystem changes that persist for decades to centuries
(Dupouey et al. 2002; Foster et al. 2003). Yet, few
studies have successfully reconstructed historical land
use and related it to current biodiversity, and most
existing studies have focused on plants only (e.g.,
Dupouey et al. 2002; Lindborg and Eriksson 2004;
Cousins and Lindborg 2008), while the responses of
other taxa remain poorly understood.
Time delayed effects of past land use can occur due
to a range of factors (Lindborg and Eriksson 2004;
Dullinger et al. 2013; Essl et al. 2015). The local
extinction of species, especially long-lived species,
may be substantially delayed following habitat loss or
degradation (Helm et al. 2006; Kuussaari et al. 2009).
Where such an extinction debt exists, contemporary
community composition may better reflect historical
conditions. For example, in a pan-European study of
remnant grassland fragments, present-day richness of
vascular plants was more closely associated with
historical land use patterns, indicating an extinction
debt over a 40 year time frame (Krauss et al. 2010).
However, short-lived specialist butterfly species
showed no extinction debt over this time frame
(Krauss et al. 2010). Conversely, certain forcing
events, such as conversion of an arable field to semi-
natural grassland, may make an area suitable to a new
group of species, though an immigration lag results in
an immigration credit, a temporary deficit in species
while the area is recolonized (Jackson and Sax 2010).
Aside from these time lag effects, other factors may
contribute to a persistent legacy of historical land use
(Foster et al. 2003). Differences in soil characteristics
and plant species composition (Dupouey et al. 2002)
as well as phosphorus levels, pH and seed bank
richness (Plue et al. 2008) were measureable up to
1600–2000 years after cultivation. Past landscape
composition and configuration may also influence
present-day communities. In remnant semi-natural
grasslands in Sweden, herbaceous plant richness at a
given location had a small but significant positive
association with the amount of surrounding grassland
in 1800 (Reitalu et al. 2012), and remnant grassland
species diversity is strongly related to habitat connec-
tivity from 50 to 100 years ago (Lindborg and
Eriksson 2004).
Such legacy effects due to past land use should be
particularly widespread in regions with a long land-
use history. Agriculture has been a dominant driver of
land-use change for centuries in Europe (Ellis and
Ramankutty 2008; Jepsen et al. 2015). Over the past
50 years, Europe as a whole has experienced intensi-
fication of agricultural practices, including increased
applications of fertilizer and pesticides, reduced crop
diversity, increasing mechanization, increasing field
size, and the removal of hedgerows and edge habitat
(Chamberlain et al. 2000; Benton et al. 2003;
Tscharntke et al. 2005; Stoate et al. 2009; Geiger
et al. 2010). This intensification has been associated
with a sharp decline in farmland biodiversity (Cham-
berlain et al. 2000; Donald et al. 2001; Kleijn et al.
2009; Stoate et al. 2009). Along with intensification,
Europe is also experiencing large-scale abandonment
of agricultural land, largely in less profitable locations
(Ceausu et al. 2015; Estel et al. 2015). While
abandonment may benefit some species, it threatens
species dependent on low-intensity agricultural man-
agement (Plieninger et al. 2014; Queiroz et al. 2014).
Eastern Europe is an especially important area in
which to study the relationship between biodiversity
and agricultural land-use change, for two reasons.
First, the level of agricultural intensification has not
yet reached that of Western Europe, and the tradi-
tional farming landscapes that are still widespread in
Eastern Europe continue to support high biodiversity
(Tscharntke et al. 2005; Fischer et al. 2012; Sutcliffe
et al. 2014). However, following EU accession and
EU Common Agricultural Policy, these landscapes
are increasingly threatened by agricultural intensifi-
cation and land abandonment, which may have
severe negative consequences on many species
(Donald et al. 2001, 2002; Loos et al. 2014a, 2015;
Dorresteijn et al. 2015b). Second, Eastern Europe has
experienced several dramatic changes in government
and political systems in the past two centuries,
driving pronounced land-use changes (Lerman et al.
2004; Hostert et al. 2011; Munteanu et al. 2014).
Landscape Ecol
123
These changes can be grouped into several time
periods (Munteanu et al. 2014; Jepsen et al. 2015).
During the 1800s (the Austro-Hungarian Empire),
there was a general trend away from feudalism to land
ownership by peasants, along with the introduction of
new crops and technologies such as the steel plow
(Jepsen et al. 2015). After World War I, agricultural
practices further intensified with new machinery, the
introduction of natural mineral fertilizer, and a shift
from subsistence agriculture to market-oriented pro-
duction (Jepsen et al. 2015). After World War II, under
Soviet influence, most countries in Eastern Europe
experienced dramatic agricultural intensification
through collectivization of agricultural land with an
increase in farm and field sizes, further mechanization,
and increased use of agrochemicals (Jepsen et al.
2015). After the fall of Eastern European socialism in
1989–1991, state farms dissolved and privatized,
resulting in widespread agricultural abandonment
with remaining agricultural production occurring in
large, private, industrial farms or small subsistence
farms (Lerman et al. 2004; Hartvigsen 2014; Estel
et al. 2015). Most recently, as Eastern European
countries have acceded to the European Union, there
has been a mix of agricultural abandonment in
marginal areas, intensification, and some re-cultiva-
tion of formerly abandoned land (Estel et al. 2015).
While land-use change in this region has been
primarily agricultural, forested areas have also under-
gone changes including harvesting, clearing of forest
land, and the planting of timber plantations. Consid-
ering the large magnitude and timespan of land-use
change in Eastern Europe, in order to best develop
biodiversity conservation strategies, it is important to
understand how current biodiversity and species
abundance patterns relate to both present and histor-
ical land use.
Focusing on Transylvania in central Romania as a
case study, the overarching goal of our study was to
determine whether there was a relationship between
present day bird, plant, and butterfly community
composition and the legacy of land use from the
Austro-Hungarian Empire (founded in 1867) to the
present. We hypothesized the following:
1. Present-day land use is the strongest driver of bird,
plant, and butterfly community composition.
2. Historical land use also affects bird, plant, and
butterfly community composition. Specifically,
sites with a single, permanent land use will have
different community compositions than sites that
have changed land use at least once.
3. The association between community composition
and historical land use will be strongest for plants,
because they are most directly affected by phys-
ical changes resulting from land use (e.g., nitrogen
enrichment of soil from fertilizer application, or
changes in physical soil structure from plowing).
Butterfly and bird communities will be less
strongly associated with land-use history because
they are further removed from these primary
effects, although they are still affected by sec-
ondary effects, such as differing vegetation struc-
ture between primary and secondary forests. In
addition, butterflies, and to a greater extent, birds,
have better dispersal ability than plants and may
therefore be able to more quickly recolonize an
area after it has returned to a species’ preferred
land-use type (e.g., re-colonization by grassland
birds of an arable field that transitions to
grassland).
Methods
Study area
The study area covered 7440 km2 in southern Tran-
sylvania, Romania (Fig. 1). The study area included
village catchments within a roughly 50 km radius of
Sighisoara. Mountainous villages were excluded,
leaving a study area characterized by undulating
terrain and a mosaic of agricultural land, grasslands,
and forest. The cities of Sighisoara and Medias were
excluded from consideration. The area is in the
foothills of the Carpathian Mountains with elevation
ranging from 230 to 1100 m above sea level. Romania
in general and Transylvania in particular have very
high biodiversity (Fischer et al. 2012; Wilson et al.
2012; Hanspach et al. 2014). Several species that are
rare or declining in the rest of Europe are common in
Transylvania, such as the corncrake Crex crex (Dor-
resteijn et al. 2015b), European brown bear Ursus
arctos (Roellig et al. 2014), yellow-bellied toad
Bombina variegata (Hartel et al. 2010) and several
butterfly species, such as Lycaena dispar, Phengaris
arion, and Euphydryas aurinia (Loos et al. 2014a).
Landscape Ecol
123
The land use and culture of the region still show
heavy influence from the Saxons, who arrived in the
area in the twelfth century (Akeroyd and Page 2006;
Fischer et al. 2012). The Saxon communities were
highly organized, with communal ownership of forest
and pasture, and private ownership of arable land
(Sutcliffe et al. 2013; Hartel et al. 2014). Following
World War II, roughly 30,000 Saxons were deported,
and other waves of Saxon emigration occurred prior
to, and immediately after the 1989 revolution
(Gundisch 1998). Today, residents of the study area
are primarily Romanian, Hungarian, or Roma, but
Saxon legacies remain, such as communal ownership
of wood pastures (Hartel et al. 2014). Present-day
agricultural practices in the study area are generally of
low intensity, with small-scale cultivation, mixed use
of livestock, low chemical inputs, low mechanization
(horse-drawn plows are common), and production
Fig. 1 Study area
composed of non-
mountainous village
catchments within roughly
50 km of Sighisoara,
Romania. The village
catchments randomly
selected for study are
outlined in black. The cities
of Sighisoara and Medias
were excluded from
consideration
Landscape Ecol
123
mainly for subsistence or local markets (Fischer et al.
2012; Hanspach et al. 2014). Land cover is a mosaic of
forest (28 %), managed grassland (24 %), and arable
land (37 %) (EEA Corine land cover 2006). Agricul-
tural field sizes are small and patches of semi-natural
vegetation are common throughout the landscape
(Loos et al. 2014a).
Study site selection
The study area was delineated into 448 villages and
their surrounding land. In order to obtain a represen-
tative sample of the landscape, villages were stratified
according to terrain ruggedness and protection status
under the EU Birds and Habitats Directives, and 30
villages were randomly selected, covering all combi-
nations of ruggedness and protection status (see Loos
et al. 2014a for further detail). These villages were
selected for use in multiple studies, (e.g., Hanspach
et al. 2014; Loos et al. 2014a; Dorresteijn et al. 2015a),
though ruggedness and protection status were not
considered as covariates in our study. Within each
selected village, each hectare was assigned a woody
vegetation cover category (low: 0–5 %, medium:
5–15 %, high: [15 %) derived from a classification
of 10 m resolution SPOT imagery, as well as a spectral
heterogeneity class (low, medium, or high, defined as
the lower, middle, or upper one-third quantiles of the
standard deviation calculated from SPOT 2.5 m
resolution panchromatic data). Study sites were ran-
domly selected from each woody vegetation—hetero-
geneity combination, such that 60 grassland and 59
arable sites were selected, with an average of four sites
in each of the 30 village catchments (see Loos et al.
2014a for further detail). In addition, 30 forested study
sites were randomly selected, with an average of one
site per village catchment.
Community composition data
Abundance of breeding birds was sampled three times at
30 forest, 58 grassland, and 53 arable sites between mid-
April and mid-June, 2012, using a 10 min point count
including visual and auditory observations from the plot
center. Point counts were conducted in suitable weather
conditions by one of four experienced observers between
5:30 and 11:00 a.m., and all birds heard or seen within the
1 ha site (i.e. within a 56 m circle) were recorded (see
Dorresteijn 2015 for further detail). Plants were surveyed
in eight 1 m2 plots in each of 23 forest, 57 grassland, and
59 arable study sites between May 26 and August 26,
2012. Within the 1 ha circular study sites, plots were
distributed every 45� at stratified random distances from
the plot center, with possible distances alternating
between\40 m and[40 m in order to equally sample
the inner and outer 0.5 ha of each site. All vascular plants
were identified and recorded by percent cover (see Loos
et al. 2015 for further detail). Abundance of butterflies
and burnet moths (which are ecologically similar to
butterflies) was sampled in 59 arable, 60 grassland, and
15 forest sites by walking four 50 m transects in the
cardinal directions, starting 6 m from the plot center.
Butterflies observed within 2.5 m of the transect line and
5 m in front of the observer were identified and recorded.
Surveys were repeated four times in each site between
May and August 2012 by four different trained observers
(see Loos et al. 2014a for further detail).
Land-use history
We used historical maps, classified and raw satellite
imagery, and field visits to classify each study site as
arable, managed grassland, or forest for six epochs:
1870, 1930s, 1970s, 1985, 2000, and 2012s. These
epochs represent five distinct periods: The Austro-
Hungarian Empire (1870), interwar period (1930s),
Socialism (1970s, 1985), transition to Capitalism
(2000), and accession to the EU (2012). Historical
maps were used to classify the first three epochs. The
initial epoch was classified from maps produced by the
2nd and 3rd Military Mapping Surveys of the Austrian
Empire (Fig. 2a, b). Both surveys mapped Transylva-
nia around 1870, and thus we consulted both map sets
simultaneously. Unfortunately, it was not possible to
distinguish arable land from grassland with these
maps, so at this epoch, each study site was classified as
forest or non-forest. For the 1930s and 1970s epochs,
each study site was classified based on topographic
maps from those time periods (Fig. 2c, d). Land cover
for 1985 and 2000 was based on an existing classifi-
cation derived from all available Landsat imagery in
the time window considered (Griffiths et al. 2013),
with the classification of each study site then visually
verified with raw Landsat imagery (and corrected
when necessary). Finally, the present land cover of
each site was verified during field work in 2012.
After classifying land use at each epoch, study sites
were assigned to one of six land-use history classes:
Landscape Ecol
123
permanent forest, non-permanent forest, permanent
grassland, non-permanent grassland, permanent ara-
ble, and non-permanent arable. We used a strict
definition of permanent. For example, a site that was
forest in all epochs would be considered permanent
forest, while a site that was forest in 2012, but non-
forest in any earlier epoch, would be non-permanent
forest. Because the 1870 epoch was classified as forest
or non-forest, sites that were non-forest in 1870 and
grassland in all other epochs were considered perma-
nent grassland, and likewise, sites that were non-forest
in 1870 and arable in all subsequent epochs were
labelled permanent arable.
Statistical approach
We calculated species richness for each taxon as the
total (i.e. pooled) number of species observed across
Fig. 2 Example of historical maps used for land-cover classification in area of Drauseni, Romania. a 2nd Austrian Military Survey, ca.
1870. b 3rd Austrian Military Survey, ca. 1870. c Interwar period, ca. 1930s. d Socialist period, ca. 1970s
Landscape Ecol
123
all point counts, transects, or plots at each study site,
and for each present-day land use, we tested for
difference in richness between permanent and non-
permanent sites using two-tailed, two-sample t-tests.
We also produced tornado plots for each combination
of taxon and present-day land use to visually compare
the abundance of each species between permanent and
non-permanent sites.
To quantify the similarity of plant, butterfly, and bird
communities among permanent and non-permanent
study sites, we used the Yue-Clayton community
similarity index (Yue and Clayton 2005). The Yue-
Clayton community similarity index is a measure of
similarity of two communities ranging from 0 (least
similar) to 1 (most similar). It is related to the Jaccard
index, however it considers species proportions of both
shared and non-shared species (Yue and Clayton 2005).
For each taxon, we calculated the similarity index for all
pairs of sites using the observed total abundances of
each species. We converted the measures from similar-
ity to dissimilarity by subtracting each from 1.
We performed Ward clustering to group the study
sites based on the dissimilarity matrices for each taxon
and present-day land use and displayed the results as
dendrograms. We annotated the dendrograms with
land-use history, woody vegetation level, and hetero-
geneity level and visually examined them for indica-
tions of which factors were driving the observed
clustering. Because dendrograms are not amenable to
quantitative interpretation, we also used PERMA-
NOVA (permutational multivariate analysis of vari-
ance), a statistical method that partitions sources of
variation within distance (i.e. dissimilarity) matrices
(Anderson 2001). We tested for differences in com-
munity composition based on present-day land use and
land-use history. For arable and grassland sites, we
also tested for an effect of land-use history after
accounting for differences in woody vegetation and
heterogeneity, because these are considered major
drivers of contemporary farmland biodiversity (Dor-
resteijn et al. 2015a).
Results
Land-use history
Classification of study sites by land-use history, based
on land use during the six epochs considered, showed
25 permanent and five non-permanent forest sites, 26
permanent and 34 non-permanent grassland sites, and
44 permanent and 15 non-permanent arable sites.
There were slightly more sites classified as forest in
early epochs (Fig. 3). Through time, there was a
noticeable increase of grassland sites and a decrease of
arable sites, with both leveling off in later epochs.
Richness and community composition
In forest sites, species richness of all three taxa was
higher in permanent than non-permanent sites, but the
opposite was true in grassland and arable sites
(Table 1). However, the differences in species rich-
ness were only significant for plants in permanent
versus non-permanent arable sites (p = 0.030, two-
tailed two-sample t test).
Plant communities showed very high dissimilar-
ity among sites, while bird communities had high
dissimilarity within arable and grassland sites and
much lower dissimilarity in forest sites (Supplement
S1). Butterfly communities showed less dissimilar-
ity among study sites than birds or plants (Supple-
ment S1). Examination of tornado plots gave no
evidence of the existence of indicator species that
were strongly associated with permanent or non-
permanent sites (Supplement S2), and there were no
apparent generalizable patterns (e.g., related to
functional groups) regarding differences in commu-
nity composition.
Clustering and PERMANOVA
Clustering indicated a relationship between forest
land-use history and bird communities—in the den-
drogram displaying the clustering of forest sites by
similarity of bird community composition, all non-
permanent sites were in the same cluster at the initial
split (Fig. 4). For the other combinations of taxa and
present-day land use, dendrograms showed some
evidence of clustering related to current land use,
heterogeneity, and woody vegetation, but no cluster-
ing related to land-use history was visually evident
(Supplement S3).
Community composition for all three taxa was
significantly associated with present-day land use, as
confirmed by PERMANOVA results (Table 2). Fur-
thermore, in non-forest sites, community composition
of birds was significantly associated with woody
Landscape Ecol
123
vegetation level, but this was not the case for plants or
butterflies (Table 3). The level of heterogeneity was
only significantly associated with bird communities in
arable sites (Table 4). With regard to land-use history,
a significant difference in bird community
composition was found between permanent and non-
permanent forest sites (p = 0.030), although the
sample size was low for non-permanent forest
(n = 5), and a borderline significant difference
between permanent and non-permanent grassland
Fig. 3 The number of study
sites classified by each land-
use category in each epoch.
The number of sites
classified as forest increased
slightly in the earlier epochs
but were otherwise stable.
Agricultural study sites
showed a steady increase in
the number of grassland
sites at the expense of arable
sites, with land-use
stabilizing in the most recent
epochs
Table 1 Mean and
standard error of species
richness by land use and
taxon
H0 lPerm = lNon-Perm, HA
lPerm = lNon-Perm
p-values are from a two-
sample two-tailed t-test.
Asterisks denote
significance level
(* p\ 0.1, ** p\ 0.05,
*** p\ 0.01)
Taxon Land use Mean species richness p-value
Permanent Non-permanent
Birds Forest 11.0 ± 0.6 (n = 25) 8.8 ± 0.4 (n = 5) 0.123
Birds Grassland 5.4 ± 0.5 (n = 24) 5.5 ± 0.5 (n = 34) 0.831
Birds Arable 5.3 ± 0.6 (n = 42) 6.3 ± 1.2 (n = 15) 0.400
Butterflies Forest 4.8 ± 0.8 (n = 13) 4.5 ± 0.5 (n = 2) 0.900
Butterflies Grassland 20.4 ± 1.4 (n = 26) 21.1 ± 1.5 (n = 34) 0.749
Butterflies Arable 18.1 ± 1.1 (n = 44) 21.7 ± 1.9 (n = 15) 0.111
Plants Forest 16.4 ± 1.9 (n = 19) 14.3 ± 2.9 (n = 4) 0.634
Plants Grassland 55.8 ± 3.1 (n = 23) 61.1 ± 2.2 (n = 32) 0.157
Plants Arable 31.3 ± 2.5 (n = 40) 41.8 ± 3.7 (n = 15) 0.030**
Landscape Ecol
123
(p = 0.051) (Table 5). Land-use history was not
significant for other taxa and land uses.
Because grassland sites had diverse characteristics,
we also used PERMANOVA to verify that the effect
of land-use history remained significant after
accounting for the level of heterogeneity and woody
vegetation at each site. In grassland sites, we found no
significant association (p = 0.847) between bird com-
munities and heterogeneity (Table 4). Woody vegeta-
tion was significantly associated (p = 0.00001) with
Fig. 4 Dendrogram showing Ward clustering based on bird community similarity in forest sites. Study site labels show land use in each
epoch (N non-forest, F forest). The initial split clusters all non-permanent forest sites in the same branch of the tree
Table 2 PERMANOVA results comparing community composition among present-day land use classes
Taxon Current land cover Comparison groups R2 Pr ([F)
Plants All Arable, forest, grassland 0.155 0.00001***
Plants All Forest, non-forest 0.055 0.00001***
Plants Non-forest Arable, grassland 0.128 0.00001***
Birds All Arable, forest, grassland 0.146 0.00001***
Birds All Forest, non-forest 0.128 0.00001***
Birds Non-forest Arable, grassland 0.024 0.00198***
Butterflies All Arable, grassland, forest 0.149 0.00001***
Butterflies All Forest, non-forest 0.126 0.00001***
Butterflies Non-forest Arable, grassland 0.030 0.00411***
Bold indicates the significance of values in Pr ([F) column
For all three taxa, community composition was significantly associated with present-day land use
Asterisks visually indicate the level of significance (* p\ 0.1, ** p\ 0.05, *** p\ 0.01)
Landscape Ecol
123
Table 3 PERMANOVA results comparing community composition among different levels of woody vegetation in non-forest study
sites
Taxon Current land cover Comparison groups R2 Pr ([F)
Plants Grassland Woody vegetation (low, med., high) 0.012 0.79773
Plants Arable Woody vegetation (low, med., high) 0.021 0.25636
Plants Non-forest Woody vegetation (low, med., high) 0.009 0.48851
Birds Grassland Woody vegetation (low, med., high) 0.070 0.00001***
Birds Arable Woody vegetation (low, med., high) 0.124 0.00001***
Birds Non-forest Woody vegetation (low, med., high) 0.080 0.00001***
Butterflies Grassland Woody vegetation (low, med., high) 0.016 0.41370
Butterflies Arable Woody vegetation (low, med., high) 0.014 0.56659
Butterflies Non-forest Woody vegetation (low, med., high) 0.007 0.51049
Bold indicates the significance of values in Pr ([F) column
A significant association exists for birds but not plants or butterflies
Asterisks visually indicate the level of significance (* p\ 0.1, ** p\ 0.05, *** p\ 0.01)
Table 4 PERMANOVA results comparing community composition among different levels of heterogeneity
Taxon Current land cover Comparison groups R2 Pr ([F)
Plants Grassland Heterogeneity (low, med., high) 0.016 0.57511
Plants Arable Heterogeneity (low, med., high) 0.016 0.59402
Plants Non-forest Heterogeneity (low, med., high) 0.007 0.80306
Birds Grassland Heterogeneity (low, med., high) 0.012 0.84707
Birds Arable Heterogeneity (low, med., high) 0.040 0.02016**
Birds Non-forest Heterogeneity (low, med., high) 0.014 0.07347
Butterflies Grassland Heterogeneity (low, med., high) 0.019 0.31252
Butterflies Arable Heterogeneity (low, med., high) 0.013 0.63036
Butterflies Non-forest Heterogeneity (low, med., high) 0.008 0.43984
Bold indicates the significance of values in Pr ([F) column
Only for birds in arable sites was the association significant
Asterisks visually indicate the level of significance (* p\ 0.1, ** p\ 0.05, *** p\ 0.01)
Table 5 PERMANOVA
results comparing
community composition
between sites with
permanent and non-
permanent land-use history
Bold indicates the
significance of values in
Pr ([F) column
Asterisks visually indicate
the level of significance
(* p\ 0.1, ** p\ 0.05,
*** p\ 0.01)
Taxon Current land cover Comparison groups R2 Pr ([F)
Plants Forest Perm. forest, non-perm. forest 0.029 0.921
Plants Grassland Perm. grassland, non-perm. grassland 0.024 0.208
Plants Arable Perm. arable, non-perm. arable 0.024 0.143
Birds Forest Perm. forest, non-perm. forest 0.068 0.030**
Birds Grassland Perm. grassland, non-perm. grassland 0.029 0.051*
Birds Arable Perm. arable, non-perm. arable 0.020 0.400
Butterflies Forest Perm. forest, non-perm. forest 0.055 0.676
Butterflies Grassland Perm. grassland, non-perm. grassland 0.009 0.762
Butterflies Arable Perm. arable, non-perm. arable 0.011 0.709
Landscape Ecol
123
bird community composition in grasslands, and after
accounting for this relationship, the association
between bird community composition and land-use
history was more significant than without accounting
for woody vegetation (p = 0.033) (Table 6).
Discussion
Understanding how past land use influences contem-
porary biodiversity is important for designing effec-
tive conservation policies. Our study sites showed a
steady transition from arable to managed grassland,
stabilizing between 1985 and 2012. Even through
periods of dramatic political and social change, land
use in the study area has changed remarkably grad-
ually over nearly two centuries. Southern Transylva-
nia thus appears to have been less affected by
collectivization and restitution than other parts of
Romania (Kuemmerle et al. 2008). Yet, even with less
dramatic land-use change than expected, we found
evidence of legacy effects, with statistically significant
differences in bird community composition between
permanent and non-permanent forest and between
permanent and non-permanent grasslands.
We found mixed support for our hypotheses. Our
first hypothesis, that present-day land use was the
strongest driver of community composition, was true in
nearly all cases, with a significant relationship between
community composition and land use and a stronger
association (higher R2 value) than with land-use
history, woody vegetation, or heterogeneity. The sole
exception was birds in grassland and arable sites,
where the association between community composi-
tion with woody vegetation (R2 = 0.08, p = 0.00001)
was stronger than the association with land use
(R2 = 0.024, p = 0.002). We found only partial
confirmation of our second hypothesis, that
community composition of birds, plants, and butter-
flies would be associated with land-use history. Bird
communities had a significant association with land-
use history in forest and grassland sites, but not in
arable sites. Surprisingly, no association was found
between land-use history and plant or butterfly com-
munities. This also directly contradicted our third
hypothesis, that the association between land-use
history and community composition would be stron-
gest for plants and weaker for birds and butterflies.
The unexpected lack of a relationship between
land-use history and plant or butterfly community
composition may be related to post-war agricultural
practices in the study area. Agricultural practices in
the study area presently utilize low levels of agro-
chemical inputs, low mechanization, and high labor-
intensity (Fischer et al. 2012; Hanspach et al. 2014).
Agricultural intensification may have been relatively
low in comparison to other areas of Romania, or
Europe in general; moreover, after the collapse of
communism, agricultural practices may have returned
to previous low-intensity levels (Fischer et al. 2012;
Mikulcak et al. 2013). For example, the average
agricultural use of inorganic fertilizer was only 16 kg/
ha in 2013 in the four counties including our study area
(INS—Institutul National de Statistica (Romanian
National Institute of Statistics) 2015), while the
average use in 2009 was 28 kg/ha in Romania and
76 kg/ha for the entire European Union (Eurostat
2012). Likewise, a pan-EU study of agricultural
intensity (Levers et al. 2015) found relatively low
agricultural land-use intensity in our study area (and
Romania as a whole) compared to the rest of the EU.
Low-intensity agricultural fields are more likely to
return to a natural state after abandonment than high-
intensity fields, with a threshold effect between
intensity level and lasting impacts on the biotic
community (Cramer et al. 2008). Perhaps in our study
Table 6 Sequential PERMANOVA table testing association of bird community composition in grassland sites with land-use history,
given woody vegetation
Df Sum of squares Mean square F R2 Pr ([F)
Woody vegetation class 1 1.53 1.53 4.25 0.070 0.00001***
Land-use history 1 0.64 0.64 1.77 0.029 0.033**
Residuals 55 19.83 0.36 0.901
Total 57 22.00 1.000
The effect of land-use history is slightly more significant after accounting for woody vegetation class
Asterisks denote significance level (* p\ 0.1, ** p\ 0.05, *** p\ 0.01)
Landscape Ecol
123
area, the level of intensity in arable fields throughout
socialism was low enough that no thresholds were
exceeded, and fields that transitioned from arable to
grassland were thus able to transition back to a state
similar to that of permanent grasslands.
Plant communities have been shown to be associ-
ated with past land use elsewhere (Dupouey et al.
2002; Lindborg and Eriksson 2004; Standish et al.
2008). In a study site in France, Dupouey et al. (2002)
found that 200 years of agriculture during Roman
times changed soil chemical and physical structure in a
manner still measurable today, which was reflected by
current vegetation. In semi-natural grasslands in
Sweden, present-day plant species diversity was more
strongly associated with landscape configuration
50–100 years ago than with present-day configuration
(Lindborg and Eriksson 2004). In a review of land-use
legacy studies, Foster et al. (2003) concluded that the
major drivers of agricultural land-use legacy effects
relate to changes in the soil (e.g., pH, carbon,
nitrogen). Similarly, Cramer et al. (2008) speculated
that recovery of former agricultural fields was strongly
related to the intensity and duration of agricultural
activity. Evidently, agricultural intensity in our study
area remained low enough such that soil characteris-
tics did not exceed critical ecological thresholds.
After agricultural abandonment (or in our case, the
conversion from arable to grassland) the availability of
seed banks and required dispersal distances influence
recovery of native vegetation (Cramer et al. 2008).
Remnant patches of native vegetation in an agricultural
matrix function as sources of grassland plant species
when former arable fields are converted to managed
grassland, with the influence diminishing with increas-
ing distance (Cousins and Lindborg 2008). Our study
area is notable for small field sizes and a heterogeneous
landscape of forest, grassland, and arable land (Loos
et al. 2014a), potentially reducing the dispersal dis-
tances required for re-colonization of native vegetation
during conversion from arable land to grassland.
Similarly, abundant field margins and roadside vege-
tation (Loos et al. 2014a) may have provided refugia for
plant species extirpated from arable fields. The bulk of
the conversion from arable to grassland in our study
area occurred by our 1985 epoch (Fig. 3), so, assuming
soil characteristics were not dramatically altered by
agriculture, it is possible that the three decades between
that time point and the biodiversity sampling was
sufficient time for these communities in non-permanent
sites to recover to a state similar to that in permanent
sites (i.e., to overcome an immigration credit).
Butterfly community composition is strongly asso-
ciated with plant community composition (Futuyma
1976), and in our study, roughly one-third of species
observed are specialists utilizing a single plant species
for food (Hanspach et al. 2015). Because no significant
differences in plant communities were found between
permanent and non-permanent sites, it is unsurprising
that no significant differences in butterfly communi-
ties were found. Butterfly communities were also more
homogeneous overall than bird or plant communities
(Supplement S1.1), and a previous study using these
butterfly data found significant overlap in community
composition between arable and grassland sites (Loos
et al. 2014a). With limited differences in butterfly
communities among different land uses, it is not
unexpected that no strong community differences
were found between permanent and non-permanent
sites in the same land-use class.
We were surprised to find significant associations
between land-use history and bird community compo-
sition since we did not find associations for plants or
butterflies. The strongest association was between
birds and land-use history in forest sites (R2 = 0.068,
p = 0.030). Though we did not measure forest tree
species composition or stand structure at our study
sites, these attributes are influenced by land-use history
(Rhemtulla et al. 2009), and vegetation structure in
particular can influence bird communities (Culbert
et al. 2013). Similarly, because trees grow slowly (e.g.,
compared to grassland plants), a forest site that was
formerly arable land or grassland may retain, for a long
period of time, floristic and structural attributes that
differ from those in permanent forest. In the Carpathian
Mountains, areas of non-permanent forest were more
likely to be logged in recent times than permanent
forest, even after accounting for other covariates (e.g.,
elevation, distance to roads) (Munteanu et al. 2015).
This could lead to perpetuating differences in forest
structure between non-permanent and permanent
forests. In the case of grasslands, large scattered trees
are an important habitat component for birds (Hartel
et al. 2013). It is possible that grasslands that were once
arable fields would be less likely to include these large
old trees than permanent grasslands.
Aside from ecological explanations for our unex-
pected results, there are potential sources of error in the
analysis. First, sample sizes of sites with non-
Landscape Ecol
123
permanent land-use histories were low for forest
(n = 5) and arable sites (n = 15), potentially limiting
statistical power. Historical land-use classification
may have been influenced by mapping errors during
the surveying and production of the original maps or
during our visual interpretation of land use from these
maps. Forest boundaries in historical maps were easily
identifiable and closely aligned with contemporary
boundaries. However, grassland and arable land were
more difficult to distinguish in the historical maps,
possibly resulting in misclassification. To examine this
possibility, we re-ran the PERMANOVA analysis for
arable and grassland sites with a lax definition of
permanent land-use (i.e., the same land use in at least
five of six epochs). The association between bird
community composition and land-use history in
grassland sites remained significant (p = 0.020 vs.
p = 0.051 for the strict definition), and the association
between plant communities and land-use history in
arable land was closer to significant (p = 0.083 vs.
p = 0.209). There were otherwise no notable changes
in results. It is also possible that sites classified as
permanent may have transitioned to a different land use
and then back to the original one during the period in
between our epochs, although this appears unlikely.
Another potential error source is the biodiversity
sampling. Although our sampling plan was carefully
determined following a pilot study that evaluated
different levels of survey effort (Loos et al. 2014b),
bias due to differences in detectability among species is
still possible in mobile species such as birds (Boulinier
et al. 1998) and butterflies, as well as for sedentary
species like plants (Chen et al. 2009). Lastly, historical
landscape configuration (in addition to composition) is
known to influence biotic communities (Lindborg and
Eriksson 2004; Reitalu et al. 2012). While we were
confident in assigning land use to our study sites from
the historical maps, identifying the precise boundaries
among cover types from the historical maps proved
difficult, and we do not believe the accuracy would
have been adequate for making inference about
landscape measures. It is therefore possible that we
missed effects of landscape pattern in the analysis.
Conclusion
Through the use of historical maps, satellite imagery,
and field visits, we reconstructed historical land use for
150 field sites in southern Transylvania at six epochs
spanning 142 years, and related these land-use histo-
ries to present-day plant, bird, and butterfly commu-
nity compositions. Bird communities in forest and
managed grassland sites were significantly associated
with land-use history, though we found no significant
associations between land-use history and plant or
butterfly community composition. Our land-use his-
tory classification showed that the study area under-
went gradual land-use changes rather than dramatic
transitions, and apparently critical ecological thresh-
olds were not transgressed, even during Socialism. We
suggest that similar analyses be carried out in other
areas of Romania or Eastern Europe that experienced
more dramatic agricultural intensification during the
post-war agricultural collectivization period, and de-
intensification or abandonment in the post-socialist
period since the early 1990s. Many of these areas
harbor high biodiversity that is under threat due to both
agricultural intensification and abandonment.
Although previous studies mainly focused on the
legacy effects of historical land use on plants, our
study showed that land-use legacy can also be
significant for other taxa (e.g., birds). Conservation
planning efforts in particular must be aware that
present-day ecosystems are not solely driven by
present-day conditions, but also historical conditions.
Studies of plant and animal distributions and commu-
nity composition, particularly in areas that have
undergone land-use change, will benefit from consid-
eration of land-use legacies.
Acknowledgments We thank Anne-Catherine Klein, Cosmin
Moga, Elek Telek, Jorg Steiner, Joszef Pal Frink, Kimberley
Pope, Laura Sutcliffe, Laurie Jackson, Paul Kirkland, Pavel Dan
Turtureanu and Remi Bigonneau for their tremendous efforts in
the field. Catalina Munteanu provide helpful translation
assistance for the historical maps. JF was funded through a
Sofja Kovalevskaja Award by the Alexander von Humboldt
Foundation. PC and TK gratefully acknowledge funding by the
European Commission (projects VOLANTE, No. 265104 and
HERCULES, No. 603447) and by the Einstein Foundation,
Berlin.
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