Potential effects of climate change on plant communities in

three montane nature reserves in Scotland, UK

Mandar R. Trivedi
a,b,
*
, Michael D. Morecroft
c
, Pamela M. Berry
a
, Terence P. Dawson
d
a
Environmental Change Institute, Oxford University Centre for the Environment, South Parks Road, Oxford OX1 3QY, United Kingdom
b
Centre for Ecology and Hydrology, Lancaster Environment Centre, Library Avenue, Bailrigg, Lancaster LA1 4AP, United Kingdom
c
Centre for Ecology and Hydrology, Maclean Building, Crowmarsh Gifford, Wallingford OX10 8BB, United Kingdom
d
School of Geography, University of Southampton, Higheld, Southampton SO17 1BJ, United Kingdom
A R T I C L E I N F O
Article history:
Received 21 June 2007
Received in revised form
27 March 2008
Accepted 7 April 2008
Available online 27 May 2008
Keywords:
Arctic-alpine plants
Classication tree
Grampian highlands
Mountains
Natura 2000
Special area of conservation
Species distribution models
Topography
A B S T R A C T
Mountain ecosystems are often identied as being particularly sensitive to climate change,
however this has rarely been investigated at the scale of individual mountain ranges using
local relationships between plants and climate. This study uses ne resolution data to
assess the potential changes to internationally important Arctic-alpine plant communities
in three national nature reserves in the Scottish Highlands, United Kingdom. Distribution
models were created for 31 species, representing a range of community types. A relation-
ship between distribution and temperature was found for all species. These models were
aggregated to explore potential future changes to each community under two Intergovern-
mental Panel on Climate Change warming scenarios for the 2080s. The results indicate that
Arctic-alpine communities in these reserves could undergo substantial species turnover,
even under the lower climate change scenario. For example, Racomitrium-Carex moss-
heath, a distinctive community type of the British uplands, could lose suitable climate
space as other communities spread uphill. These ndings highlight the need to maintain
these communities in an optimal condition in which they can be most resilient to such
change, to monitor them for signals of change and to develop more exible conservation
policies which account for future changes in mountain protected areas.
2008 Elsevier Ltd. All rights reserved.
1. Introduction
Human activities during the Industrial period have warmed
the climate and could lead to an increase in global average
surface temperature of 1.16.4 C by 2100, compared with an
increase of around 0.76 C over the last century (IPCC, 2007).
The warming trend has affected ecosystems worldwide (Par-
mesan, 2006) and mountain ecosystems are considered to
be particularly sensitive due to the rapid change in climate
with altitude and species close adaptations to the cold envi-
ronment (Ko rner, 1999). For example, plants and animals have
shifted to higher altitudes across Europes mountains (Grabh-
err, 1994; Klanderud and Birks, 2003; Pen uelas and Boada,
2003; Walther et al., 2005; Wilson et al., 2005; Pauli et al., 2007).
Due to the limited knowledge of species dynamic re-
sponses to a changing environment, the potential effects of
climate change are commonly projected using distribution
models which are based on correlations between current dis-
tributions and climate (Guisan and Zimmermann, 2000). Most
studies use coarse resolution (e.g. 50 km 50 km) data and are
0006-3207/$ - see front matter 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2008.04.008
* Corresponding author: Present address: Global Canopy Programme, John Krebs Field Station, University of Oxford, Wytham OX2 3QJ,
United Kingdom. Tel.: +44 1865 724555.
E-mail addresses: mandar.trivedi@gmail.com (M.R. Trivedi), mdm@ceh.ac.uk (M.D. Morecroft), pam.berry@eci.ox.ac.uk (P.M. Berry),
t.p.dawson@soton.ac.uk (T.P. Dawson).
B I O L O G I C A L C O N S E R VAT I O N 1 4 1 ( 2 0 0 8 ) 1 6 6 5 1 6 7 5
avai l abl e at www. sci encedi r ect . com
j our nal homepage: www. el sevi er . com/ l ocat e/ bi ocon
useful for highlighting vulnerable regions or taxa (e.g. Bakk-
enes et al., 2002; Berry et al., 2002; Thomas et al., 2004; Thuil-
ler et al., 2005). However, coarse models may not be
appropriate for mountains, where local climates diverge from
that of the region. Furthermore, the prediction of biotic im-
pacts at ne scales is seen as one of the key scientic chal-
lenges for the development of conservation plans in
response to climate change (Brooker et al., 2007). The pattern
of vegetation change with altitude, resulting from the com-
pression of climatic zones in mountain terrain (Barry, 1992),
presents researchers with a valuable opportunity to study
the potential impacts of climate change using a space-for-
time approach (Ko rner, 1999). In Europe, a small number of
studies mainly in the Alps have projected climate change
impacts using ne resolution species, climate and topo-
graphic data (e.g. Zimmermann and Kienast, 1999; Guisan
and Theurillat, 2000; Dirnbo ck et al., 2003; Dullinger et al.,
2004). The results suggest that climate warming will have sig-
nicant negative impacts on high-altitude species in the Alps.
This paper presents the rst application of such ne scale
models to montane plants within the British Isles.
Upland climates of the British Isles are dominated by the
inuence of the Atlantic Ocean, resulting in a distinctly oce-
anic character to the vegetation (Averis et al., 2004). Several
vegetation types, such as wet heaths and Racomitrium moss-
heaths, are more common in these uplands than elsewhere
in Europe (Averis et al., 2004). The mountains are small in a
European context (up to 1344 m), but there are large changes
in climatic conditions with moderate increases in altitude
(Manley, 1952; Pepin, 1995). Consequently, Arctic-alpine vege-
tation exists in a relatively narrow zone above about 750 m
a.s.l. (Nagy, 2003), with limited potential to track suitable cli-
mate space by migration to higher altitudes.
While there have been investigations of climate change
impacts on nature reserve networks (Dockerty et al., 2003;
Arau jo et al., 2004), little attention has been paid to specic
conservation sites. Under the European Communitys Habi-
tats Directive (92/43/EEC), each member state is obliged to
designate, monitor and maintain Special Areas of Conserva-
tion (SAC) to contribute to the pan-European Natura 2000 re-
serve network. This study focused on three neighbouring
Scottish national nature reserves, which were designated as
SACs for their internationally important high-altitude plant
communities. For example, they have the most extensive
development of alpine and subalpine calcareous grasslands
in the United Kingdom, as well as siliceous alpine and boreal
grassland and sub-Arctic Salix spp. scrub (Jackson and McLe-
od, 2000). The study aimed to test the sensitivity of plant spe-
cies and communities to two warming scenarios low and
high corresponding to the B1 and A1FI greenhouse gas
emissions scenarios proposed by the Intergovernmental Pa-
nel on Climate Change (IPCC) (Nakicenovic and Swart, 2000).
The rst stage of the SAC designation process involves
vegetation mapping surveys of all candidate SACs to allow
land managers to assess the extent and status of each target
plant community. Here we used these baseline survey data for
the common species found in each community type to model
plant species distributions in relation to topography and soils.
The projections of the individual species models were subse-
quently amalgamated into species assemblages, for current
climate and the two potential future climates. This predict
rst, assemble later approach (Ferrier and Guisan, 2006) al-
lows individualistic species responses to climate change,
which are supported by evidence from both palaeoecological
(Huntley, 1991; Hewitt, 1999) and experimental (Bruelheide,
2003) research. There are few examples of such an approach
to projecting climate change impacts on community compo-
sition (e.g. Guisan and Theurillat, 2000; Peppler-Lisbach and
Schro der, 2004; Thomas et al., 2004), but it has the advantage
of providing information on both species of interest and spe-
cies assemblages (Peppler-Lisbach and Schro der, 2004). This
strategy produces projections of future vegetation changes
at specic survey locations within the nature reserves, which
can be compared with future monitoring data or eld
experiments.
2. Methods
2.1. Study site
The study area covers the Breadalbane range in the south of
the Grampian Highlands of Scotland, UK (lat: 5630
0
to
5634
0
and long: 413
0
to 419
0
, Fig. 1), including three nature
reserves (Ben Lawers, Ben Heasgarnich and Meall na Samhna)
covering a total area of 9690 ha. The main axis of the moun-
tains is aligned in a roughly south-west/north-east direction.
Summits vary between 1000 and 1214 m a.s.l. Unusually for
the mainly acidic Scottish Highlands, the geology consists of
soft Dalradian calcareous mica schists which give rise to basic
soils supporting a rich Arctic-alpine ora (Lusby and Wright,
2001). Below the alpine zone there are more acidic glacial
drifts. The annual maximum temperature is 11.6 C, mini-
mum temperature 4.7 C and precipitation 1252 mm per an-
num at 130 m a.s.l. at Ardtalnaig (Fig. 1). There is a
precipitation gradient across the site, increasing by about
20 mm per annum per kilometre westwards, favouring great-
er peat formation in the west (Poore, 1993). Due to the cool,
moist climate the soils are continually leached, giving rise
to podsolic soils even where the underlying bedrocks are
nutrient-rich schists. Large areas of podsols underlie much
of the Nardus stricta grasslands and heaths of the area. Floris-
tically richer vegetation is found where the soil is enriched
through deposits of weathered rock (e.g. at cliff bases) or
ushing with water which has run through or over the bed-
rock (Poore, 1993).
2.2. Botanical data
Aeld survey, following the UKNational Vegetation Classica-
tion (NVC) protocol (Rodwell, 2006), was carried out between
2002 and 2004 (Smith et al., 2003; Cornish and Dayton, 2005;
Dayton and Cornish, 2005) to map out the three nature re-
serves vegetation communities in accordance with their SAC
designation. Cover estimates of all species (including bryo-
phytes and lichens) were recorded in 282 2 m 2 m quadrats,
stratied by community type and covering the full range of
topographical/environmental conditions. The survey design
was based on sampling representative vegetation rather than
random sampling, resulting in some quadrats being close to-
gether. To reduce the impact of spatial autocorrelation on the
1666 B I O L O G I C A L C O N S E R VAT I O N 1 4 1 ( 2 0 0 8 ) 1 6 6 5 1 6 7 5
subsequent models (Guisan and Zimmermann, 2000), quad-
rats were removed from the data set at random so that no
twowere closer than200 m, leaving 213 for the analysis. Distri-
bution models were only constructed for species occurring in
more than ca. 10% of the plots to avoid problems associated
with modelling species with low prevalence (McPherson
et al., 2004; Liu et al., 2005; Jime nez-Valverde and Lobo, 2006).
The surveyors classied each quadrat by NVCcommunity type
and this information was used in interpreting the results.
Nomenclature follows Stace (1997) for vascular plants and
Smith (2004) for bryophytes.
2.3. Environmental data
The Geographical Positioning System (GPS) location, altitude,
slope and aspect of each quadrat were recorded. Missing ter-
rain data were lled in from a 10 m digital elevation model
(DEM, Ordnance Survey/EDINA). Further topographic vari-
ables solar radiation, planform and prole curvature and a
wetness index were derived from the DEM using ArcGIS
and ArcInfo (Environmental Science Research Institute, Red-
lands, California). Potential solar radiation on the equinoxes
and summer solstice was estimated using the shortwave
routine (Kumar et al., 1997; Zimmermann, 2001). The three
estimates were aggregated into one srad variable using prin-
cipal components analysis (PCA) in SPSS 14.0. Site wetness
was estimated using a compound topographic index, which
combines the catchment area draining into a grid cell with
the ability of water to drain away from that cell, based on
the FD8 multiple ow dispersion algorithm (Kirkby, 1975;
Moore et al., 1993).
Recent investigations of the potential impacts of climate
change on United Kingdoms wildlife have used the climate
of the 19611990 periodas a baseline against whichto compare
future scenarios (e.g. Berry et al., 2005). Hence, monthly tem-
perature averages for 19611990 were obtained for the Ardtal-
naig Met Ofce station, at 130 m a.s.l. approximately 10 km
east of the study site. Since there are fewhigh-altitudeweather
stations in Britain, obtaining altitudinal lapse rates of temper-
ature is difcult. We derived monthly lapse rates from high-
quality climate grids (Perry and Hollis, 2005) using the method
of Zimmermann and Kienast (1999). The annual mean of
6.3 C km
1
was similar to previous published rates (Harding,
1978). The monthly lapse rates were applied to the Ardtalnaig
monthly averages to calculate the expected annual mean tem-
perature, T
mean
, at each survey location.
Temperature changes were added to the baseline T
mean
to
project climate change impacts for the 2080s. Two future sce-
narios were investigated in which global greenhouse gas
emissions over the coming decades are either low or high
(B1 and A1FI scenarios, respectively, of the IPCC, Nakicenovic
and Swart, 2000). The scenarios data were from a high-resolu-
tion (ca. 50 km) regional model of the European atmosphere
(HadRM3, Hulme et al., 2002), which has a 20-year history of
development and has been used in a number of climate im-
pact studies in the UK (e.g. Berry et al., 2005; McEvoy et al.,
2006). The study site is predominantly located within two of
HadRM3s grid cells. So the projected average temperature in-
creases of these two cells were used, averaging: low = 1.7 C,
high = 3.3 C.
Soil type was assigned to each quadrat from soil maps at
1:63,360 and 1:50,000 scale (Macaulay Institute for Soil Re-
search, 1982, 1985). Soils were categorised according to major
soil sub-group: (i) gleys, (ii) peats, (iii) leached soils, or (iv) rock
and scree.
2.4. Data analysis
2.4.1. Species distribution modelling
All analyses were carried out using the R statistical environ-
ment (version 2.4.1, R Development Core Team, 2005). Logistic
regression (Hosmer and Lemeshow, 1989) was used to model
the presence/absence of each species in response to the
environmental variables. The regressions were tted using
Fig. 1 The study area of the Breadalbane range, south Scottish Highlands. Circles represent the location of survey quadrats
across three Special Areas of Conservation: Ben Heasgarnich, Ben Lawers and Meall na Samhna.
B I O L O G I C A L C O N S E R VAT I O N 1 4 1 ( 2 0 0 8 ) 1 6 6 5 1 6 7 5 1667
generalizedadditivemodels (GAM, HastieandTibshirani, 1990)
with a binomial probability distribution and a logistic link
function. GAMs are the non-parametric counterparts of gener-
alized linear models (GLM) and are commonly used to model
species distributions (e.g. Arau jo et al., 2005; Wintle et al.,
2005). Initially, univariate GAMs with smoothing splines with
approximately four degrees of freedom were used to investi-
gate the importance of each continuous independent variable.
Variables showing signicant relationships with the presence/
absence of the species were then entered into a multivariate
model selectionprocess, using appropriate degrees of freedom
based on examination of the univariate plots. Variable selec-
tion and model simplication were based upon Akaikes Infor-
mation Criterion (AIC, Akaike, 1973; Wintle et al., 2005).
Models were evaluated using the area under the curve
(AUC) of the Receiver Operating Characteristic (ROC, Swets,
1988) and Millers calibration statistics, both estimated using
a resampling method (Ferrier and Watson, 1997; Wintle et al.,
2005). The predictions from the GAMs were converted from
decimal fraction suitability to binomial presence/absence
using a threshold value which minimised the difference be-
tween the sensitivity and specicity of the predictions (Bonn
and Schro der, 2001). Models were constructed for 60 species,
but due to lowprevalence among many montane species, ade-
quately tting models (AUC P0.6) were found for only 31,
which represented a range of biome associations (Table 1).
These models were used to project the potentially suitable
quadrats under a future climate by changing T
mean
according
to the two scenarios. The potential change in quadrat occu-
pancy was then calculated for each species.
2.4.2. Assessing change in species composition
The results from the individual species models were aggre-
gated to predict the species assemblage at each quadrat. The
observed and predicted species assemblages were compared
using ordination techniques described in detail by Peppler-Lis-
bach and Schro der (2004). Detrended correspondence analysis
(DCA, Hill, 1979; Jongman et al., 1995) was applied to both pre-
dicted and observed species site matrices to evaluate the
effect of species modelling on the predicted community struc-
ture and species-environment relationships. Observed and
predicted ordination axes were compared using Spearmans
correlation, as in Guisan and Theurillat (2000). The observed
and predicted ordination patterns were compared using
Table 1 Results of generalized additive models based on occurrence data for 31 species, ordered according to magnitude
of projected change in quadrat occupancy under low and high climate change scenarios
Species Code Distribution
a
AUC
b
Change in occupancy (%)
c
Low High
Narthecium ossifragum (L.) Huds. naross Oceanic Boreo-temperate 0.69 120 178
Dicranum scoparium dicsco 0.63 112 265
Tricophorum cespitosum (L.) Hartm. trices Circumpolar Boreal-montane 0.74 108 176
Erica tetralix L. eritet Suboceanic temperate 0.67 93 166
Molinia caerulea (L.) Moench molcae Eurosiberian Boreo-temperate 0.69 78 230
Calluna vulgaris (L.) Hull calvul European Boreo-temperate 0.78 58 111
Sphagnum capillifolium sphcap 0.64 51 95
Eriophorum vaginatum L. erivag Circumpolar Boreo-Arctic montane 0.84 41 114
Potentilla erecta (L.) Raeusch. potere Eurosiberian Boreo-temperate 0.74 31 58
Festuca rubra L. fesrub Circumpolar wide-boreal 0.67 26 21
Viola riviniana Rchb. vioriv European temperate 0.62 22 0
Thymus polytrichus A. Kern. Ex Borbas thypol European Boreo-temperate 0.70 18 8
Carex pulicaris L. carpul Suboceanic temperate 0.66 17 59
Juncus squarrosus L. junsqu Suboceanic temperate 0.66 6 7
Eriophorum angustifolium Honck. eriang Circumpolar wide-boreal 0.68 0 2
Carex paniculata L. carpan European Boreo-temperate 0.67 0 47
Anthoxanthum odoratum L. antodo Circumpolar wide-temperate 0.69 1 24
Empetrum nigrum L. empnig Circumpolar Boreo-Arctic montane 0.70 8 4
Nardus stricta narstr European Boreo-temperate 0.59 11 41
Vaccinium vitis-idaea L. vacvit Circumpolar Boreo-Arctic Montane 0.61 20 40
Carex nigra (L.) Reichard carnig Eurosiberian Boreo-temperate 0.61 26 64
Festuca vivipara (L.) Sm. fesviv Circumpolar Boreo-Arctic montane 0.64 40 74
Alchemilla alpina L. alcalp European Arctic-montane 0.81 44 74
Deschampsia cespitosa (L.) P. Beauv. desces Circumpolar Wide-boreal 0.71 57 81
Salix herbacea L. salher European Arctic-montane 0.82 83 100
Racomitrium lanuginosum raclan 0.75 85 100
Carex bigelowii Torr. carbig Circumpolar Arctic-montane 0.90 88 98
Silene acaulis (L.) Jacq. silaca European Arctic-montane 0.69 89 100
Cladonia arbuscula claarb 0.61 96 100
Cladonia uncialis claunc 0.69 97 100
Polytrichum alpinum polalp 0.86 100 100
a Hill et al. (1992), Preston et al. (2002).
b AUC is the Area Under the Curve of the Receiver Operating Characteristic (ROC), which is a measure of model accuracy.
c Projected change in quadrat occupancy (n = 213) is the modelled change in climatic suitability of the quadrats.
1668 B I O L O G I C A L C O N S E R VAT I O N 1 4 1 ( 2 0 0 8 ) 1 6 6 5 1 6 7 5
Mantel tests (Manly, 1997; McCune and Grace, 2002) and Pro-
crustes rotation (Peres-Neto and Jackson, 2001). Next, the
quadrats were classied into community types based upon
their similarity. The aim was to assess the potential impact
of climate change on species composition by seeing if all com-
munities would still occur in the future. The method of Guisan
and Theurillat (2000) was followed:
1. The quadrats were assigned to groups sharing similar sub-
sets of observed species using k-means non-hierarchical
cluster analysis, which partitioned the data around k med-
oids, selected on the basis of average silhouette width, an
index of cluster separation. A dissimilarity matrix of the
standardized binary occurrence data was input to the clus-
tering algorithm (Legendre and Gallagher, 2001).
2. A classication tree was tted to the clusters by using the
observed species occurrences as explanatory variables.
The tree was pruned to improve parsimony using 10-fold
cross-validation (Death and Fabricius, 2000).
3. The tree was used to predict cluster membership of each
quadrat based on the predicted species distributions from
the binomial models.
4. Step three was repeated using the projected species occur-
rences under the two climate change scenarios.
The classication tree was evaluated by using a confusion
matrix of observed and predicted cluster memberships to cal-
culate the misclassication rate and kappa (Cohen, 1960), the
latter measure being less sensitive to the prevalence of the
community type (Manel et al., 2001). The effect on cluster
membership of substituting the observed species occurrences
with those predicted by the binomial models was also tested
in this way. Similarly, the potential effect of climate change
on species composition was examined by means of confusion
matrices.
3. Results
3.1. Species models
According to the classication of Swets (1988), the generalized
additive models for the 31 species ranged from low to use-
ful accuracy, with a mean area under the curve (AUC) of 0.7
(range: 0.60.9; Table 1). The best models (AUC > 0.8) tended
to be for Arctic-montane species such as Alchemilla alpina, Car-
ex bigelowii and Salix herbacea. Models for some temperate and
boreo-temperate species, such as Juncus squarrosus, Viola rivin-
iana, Carex nigra and Nardus stricta had much lower AUC val-
ues. On average, the models explained 28% (range: 1455%)
of the deviance in the data. Temperature was a signicant
predictor for all species (100%), followed by slope (81% of spe-
cies models), wetness (77%), curvature (52%), solar radiation
(42%) and soil type (29%). Thus, considering species individu-
ally, all variables appear to play a role in structuring the com-
munity, with temperature (as determined by altitude) the
most important.
Higher average temperatures under climate change were
projected to result in a decline in climatically suitable habitat
for montane and Arctic-alpine species, such as C. bigelowii,
Racomitrium lanuginosum and A. alpina (Table 1). The magni-
tude of the projected change was large with some species pro-
jected to be absent from all quadrats under the high
scenario. Low-altitude species, such as Calluna vulgaris, Erica
tetralix, Molinia caerulea and Potentilla erecta were projected to
gain suitable climate space (Table 1).
3.2. Community models
The ordination plots show that the observed pattern of com-
munity composition and its environmental correlates (Fig. 2a)
-3 -2 -1 0 1 2 3
-
2
-
1
0
1
2
3
Axis 1
alt
slope
wet
srad
alcalp
sphcap
calvul
carpan
naross
desces
claunc
vioriv
vacvit
fesrub
molcae
empnig
eritet
erivag
claarb
silaca
A
x
i
s

2
-2 -1 0 1 2 3
-
2
-
1
0
1
2
3
Axis 1
alt
slope
plan
prof
wet
srad
narstr
fesviv
alcalp
sphcap
calvul
eriang
naross
desces
claunc
dicsco
vacvit
molcae
empnig
erivag
claarb
silaca
eritet
Fig. 2 Distribution of species on the rst two DCA axes, with signicant environmental variables tted. (a) Observed species
and (b) model predicted species distributions.
Table 2 Mantel test correlation statistics for the
relationship between the similarity structures of
observed and predicted species assemblages projected in
ordination space
r
DCA sample scores axes 12 0.56
DCA sample scores axes 14 0.52
DCA species scores axes 12 0.79
DCA species scores axes 14 0.73
All correlations signicant at the 99% level, based on 1000
permutations.
B I O L O G I C A L C O N S E R VAT I O N 1 4 1 ( 2 0 0 8 ) 1 6 6 5 1 6 7 5 1669
was recreated by the aggregated species distribution models
(Fig. 2b). Procrustes rotation of the observed and predicted
species assemblages in ordination space showed that they
were strongly correlated (r = 0.69, P < 0.001, based upon
1000 permutations). Mantel tests conrmed the correlation
between the similarity structures of the observed and pre-
dicted DCA scores (Table 2). The correlation was stronger
between the observed and predicted data for axes 1 and 2
than for all four DCA axes together. This is supported by
examination of Spearmans rank correlations between the
observed and predicted DCA axes (Table 3). The primary
and secondary oristic axes were well recreated by the pre-
dicted assemblages. As illustrated in Fig. 2, these two axes
were correlated with temperature/wetness (driven by alti-
tude) and slope/solar radiation, respectively. In the case of
the predicted data, the second axis was also correlated with
topographic curvature, reecting the importance of these
variables in the individual species models. The predicted
third and fourth axes were less well correlated with the
observations (Table 3).
Non-hierarchical cluster analysis partitioned the observed
quadrats into six reasonably homogeneous vegetation clus-
ters. A classication tree with 12 terminal nodes was tted
to these clusters using the observed species distributions as
predictor variables (See Electronic Appendix for description
of the vegetation clusters). The tree explained nearly three-
quarters of the deviance in the clusters (D
2
= 0.71). Based upon
a confusion matrix, the agreement between the tted and ob-
served clusters was good (kappa = 0.77), with a misclassi-
cation rate of 18% (Fig. 3a).
Table 3 Spearmans correlation between observed and
predicted DCA sample scores
Predicted
Axis 1 Axis 2 Axis 3 Axis 4
Observed Axis 1 0.79
*
0.07 0.02 0.25
*
Axis 2 0.07 0.56
*
0.00 0.18
*
Axis 3 0.27
*
0.25
*
0.27
*
0.27
*
Axis 4 0.03 0.12 0.33
*
0.21
*
Bold = strongest correlations,
*
denotes signicance at 99% level.
The primary observed vegetation axis correlates with altitude-
driven temperature and wetness. The second axis correlates with
slope and solar radiation.
Fig. 3 Confusion matrices from classication tree predictions of vegetation clusters. The size of each box represents the
agreement between: (a) observed (ordinate axis) and tted (abscissa) vegetation clusters; (b) observed and predicted clusters
from individual species models; and observed versus projected clusters under low (c) and high (d) climate change scenarios,
respectively. Note that under the high-climate change scenario (d), vegetation clusters 3 and 6 are no longer predicted to
occur.
1670 B I O L O G I C A L C O N S E R VAT I O N 1 4 1 ( 2 0 0 8 ) 1 6 6 5 1 6 7 5
Cluster memberships were then assigned using the pre-
dicted species assemblages as input to the classication tree,
as opposed to using the observed species data. The predic-
tions had a lower level of agreement with observed clusters
than the original tted tree (kappa = 0.3, misclassication
rate = 51%, Fig. 3b). The reduced predictive ability was mainly
due to the misclassication of quadrats belonging to both
clusters 1 and 6, which were confused for other vegetation
types, particularly cluster 5 (Fig. 3b).
These species-level projections were aggregated into
changes in the species composition of the quadrats. Under a
low climate change scenario, quadrats which currently sup-
port vegetation clusters 1, 3 and 4 become less suitable for
these communities (Fig. 3c). Locations currently supporting
clusters 1 and4 become more suitable for cluster 5, while those
of cluster 3 become suitable for cluster 4. In contrast, cluster 5
maintains its currently suitable quadrats. The pattern is simi-
lar under a high-climate change scenario (Fig. 3d). In this
instance, noneof thequadrats aresuitablefor thehigh-altitude
vegetation of cluster 3. Those which are currently occupied by
cluster 3 become fairly evenly divided between clusters 1, 2, 4
and 5.
4. Discussion
4.1. Species and community models
Models were tted for 60 species, but only models for 31 spe-
cies showed adequate discriminatory power (AUC P0.6) and
were therefore considered further. Such variable model suc-
cess has been found in previous studies of alpine plants (Gui-
san and Theurillat, 2000; Guisan and Zimmermann, 2000) and
is likely to be caused, in part, by the low prevalence of many
species. Unmeasured variables, such as disturbance, soil
properties and water resurgence, which were not part of the
eld survey, may also have limited model power (Guisan
and Theurillat, 2000). While potentially explanatory variables
were missing, the models still allowed projection of climate
change impacts based upon the primary role of temperature
in governing species distributions. Model inaccuracies may
also have resulted from discrepancies between the resolution
of the species data (2 m 2 m) and that of predictors calcu-
lated from the DEM (10 m 10 m) or the soil maps. Further-
more, at smaller scales, biotic interactions and dispersal
may have a more prominent effect on species distributions,
tending to make models less reliable (Pearson and Dawson,
2003).
Temperature was a signicant term in all 31 species distri-
bution models and was correlated with the primary axis of
the ordination (Fig. 2b). Slope angle, wetness index, curvature
and solar radiation were all also found to be signicant in be-
tween 42% and 81% of the models. Previous studies have
found these variables to be important predictors of montane
species distribution (e.g. Guisan et al., 1998; Dirnbo ck et al.,
2003). Plants, particularly alpine plants, experience surface
microclimates which integrate the effects of ne-grained
topographic variations. In this study, the topographic vari-
ables acted as proxies for this true microclimate and better-
calibrated models, leading to more accurate predictions,
might be achieved through an emphasis on the measurement
of such surface microclimates (e.g. Gottfried et al., 1999; Lo f-
er, 2007).
The classication tree tted the observed vegetation clus-
ters well (kappa = 0.77, Fig. 3a). But there was lower agreement
between predicted and observed cluster membership when
the predictions were made using the species distribution mod-
els (kappa = 0.3, Fig. 3b). Thus caution is required in interpret-
ing the projections of future change incommunity type of each
quadrat. In a study of potential climate change impacts on
grasslands inthe Swiss Alps, Guisanand Theurillat (2000) clas-
sied 205 quadrats into eight clusters using data for approxi-
mately twice the number of species used in our analysis,
reecting the higher species richness of their site. They
achieved similar agreement between tted and observed clus-
ter memberships (kappa = 0.77), but had more success when
using modelledspecies distributionto predict cluster member-
ship (kappa = 0.45). Their use of a larger species set allowed
better discriminationof communities andcounteractedthe er-
rors associated with individual species models.
Reecting the variation in discriminatory power of the indi-
vidual species models, predictive accuracy varied among clus-
ters. The mire and heath communities of clusters 1 and 6 were
poorly predicted by the model, often being misclassied as
belonging to the wet heaths of cluster 5. This confusion may
have arisen due to the reliance of the classication tree on
the indicator species Sphagnumcapillifoliumto discriminate be-
tween wet and dry communities. This species model had rel-
atively low discriminatory power (AUC = 0.64) even though it
had a moderate prevalence (26%). This indicates that the topo-
graphic wetness index may not have given accurate estimates
of soil moisture. Clusters 3 and 4 (high-altitude heaths and up-
land grasslands) were better predicted since the artic-mon-
tane species indicating these clusters tended to be modelled
with greater accuracy (Carex bigelowii and Racomitrium lanugi-
nosum, AUC = 0.9 and 0.75, respectively). Thus, the models for
higher altitude communities were better calibrated.
4.2. Climate change projections
Under both warming scenarios, low-altitude grass and
heather species characteristic of boreo-temperate biomes
were projected to gain suitable climate space, while high-alti-
tude Arctic-montane species lost space (Table 1). Under the
low and high-scenarios, Arctic-montane species were pro-
jected to lose 78% and 93%, respectively, of currently suitable
quadrats (Table 1). The main consequence of this in terms of
NVC communities would be a transition from snow bed com-
munities U10 Carex bigelowiiRacomitrium lanuginosum moss-
heath and U7 Nardus strictaCarex bigelowii grass-heath to-
wards species-rich calcareous grasslands CG11 Festuca ovi-
naAgrostis capillarisAlchemilla alpina grass-heath and CG12
Festuca ovinaAlchemilla alpinaSilene acaulis dwarf-herb. The
sites Carex-Racomitrium moss-heath and species-rich upland
calcareous grasslands have an abundance of Arctic-alpine
species such as Bartsia alpina, Cerastium alpinum, Minuartia
sedoides, Persicaria vivipara, Silene acaulis and Thalictrum alpi-
num (Anon, 2006). But since the individual species models
suggest that the Arctic-alpine component may become
diminished (Table 1), these communities may be transitional
towards upland grasslands such as U5 Nardus stricta-Galium
B I O L O G I C A L C O N S E R VAT I O N 1 4 1 ( 2 0 0 8 ) 1 6 6 5 1 6 7 5 1671
saxatile and U6 Juncus squarrosus-Festuca ovina. While it is dif-
cult to completely separate the effects of inter-related envi-
ronmental variables on vegetation composition, the analysis
found soil type to be the least important explanatory variable.
However, a study of Atlantic calcareous grasslands has high-
lighted the important role of soil in structuring the plant com-
munity (Duckworth et al., 2000). Thus, the basic soils of the
Breadalbane range might provide some favourable locations
for calcicolous Arctic-alpines in the future, especially at
high-altitudes where newly arriving thermophilous species
will require the ability to establish on thin soils and scree
(Kazakis et al., 2007).
The current sites of U5 and U6 upland grasslands would
become suitable for moorland species from the lower alti-
tudes. There would be a transition from U5 and U6 towards
moorland communities such as M15 Trichophorum cespito-
sum-Erica tetralix wet heath. These moorland communities,
which currently occupy large areas of the uplands (Averis
et al., 2004), are projected to expand their potentially suitable
area to higher altitudes. It is however possible that they will in
turn be invaded by other species from lower altitudes. Blanket
mires such as M19 Calluna vulgaris-Eriophorum vaginatum are
an internationally important habitat but were poorly pre-
dicted by the model, possibly due to the topographic wetness
index employed.
The communities projected to lose suitable climate space
(U10 Carex-Racomitrium moss-heath, U7 Nardus-Carex grass-
heath, CG11 Festuca-Agrostis-Alchemilla grass-heath and CG12
Festuca-Alchemilla-Silene dwarf-herb) are part of two habitats
listed under Annex 1 of the European Habitats Directive.
These are siliceous alpine and boreal grasslands and alpine
and subalpine calcareous grasslands, and they qualify the re-
serves for Natura 2000 designation. As the climate changes
and montane vegetation responds, it will become increasingly
difcult to comply with the Directives requirement to main-
tain these habitats at a favourable conservation status
(European Communities, 1992). As suggested by previous
authors (Peters, 1992; Stersdal et al., 1998; Price and Neville,
2003), in order to limit the potential for future deterioration of
these habitats, it is important that current management
activities continue to reduce the existing anthropogenic stres-
ses. However, a more exible approach to conservation desig-
nation may ultimately be required, which accepts the climate
change-induced loss of species and habitats from some sites
(Brooker et al., 2007; Normand et al., 2007).
4.3. Future research needs
As with all climate change impact assessments there are a
number of uncertainties to this modelling exercise, not least
of which is the uncertainty in the future course of climate
change (Arau jo and New, 2007). The assumptions and uncer-
tainties inherent in species distribution modelling have been
discussed in detail by previous authors (Pearson and Dawson,
2003; Hampe, 2004; Pearson and Dawson, 2004; Arau jo and
Guisan, 2006; Guisan et al., 2006; Botkin et al., 2007). In partic-
ular, such equilibrium models normally assume that species
will disperse and track suitable climate space and that their
biotic interactions will not change. However, many marginal
upland plants reproduce vegetatively and grow slowly; conse-
quently they are likely to take a long time to disperse into new
climatically suitable areas (Dullinger et al., 2004). Also, the
type of plantplant interactions may change from facilitative
to more competitive as the climate warms (Brooker, 2006). An-
other important biotic interaction is herbivory, which acts as
an environmental lter, selecting specic groups of plant spe-
cies (De Bello et al., 2005; Louault et al., 2005; Pierce et al.,
2007). Centuries of intensive sheep grazing in the Breadalbane
hills have led to the development of extensive grasslands
(Averis et al., 2004). Therefore, future responses of montane
plant communities to climate change will depend to some ex-
tent on the grazing regime adopted by land managers. Such
local biotic effects might have resulted in relatively poor mod-
el t for some species. Given the importance of investigating
climate change impacts on mountain vegetation at scales rel-
evant to the climates experienced by plants, the challenge
now is to integrate such processes into ne scale distribution
models (e.g. Dullinger et al., 2004).
It is also essential to monitor changes in communities as
they occur in order to determine actual changes and to test
and rene models. This will also require site-based monitor-
ing of climate (especially in mountain areas) and other poten-
tial causes of change, such as grazing management and air
pollution. Existing monitoring of designated sites in the UK
(Common Standards Monitoring, JNCC, 2006) does not provide
for this, nor for detailed quadrat-based recording. A number
of reports have identied the need for this sort of additional
monitoring of UK conservation sites (e.g. Ferris, 2006; Mitchell
et al., 2007) and proposals have been developed (Morecroft
et al., 2006). A wider international approach to monitoring
and modelling change in Europes mountains would also be
valuable (e.g. Nagy et al., 2003).
5. Conclusion
Predicting climate change-driven shifts in species distribu-
tions has been dominated by large-scale studies in recent
years, although landscape to regional scale applications
would be of particular utility to conservation. This is espe-
cially relevant for mountainous terrain where the micro-
and meso-climates may strongly deviate from the macro-cli-
mate. Previous landscape-level ne resolution modelling
studies in Europe have mainly focused on southern European
mountains such as the Alps (e.g. Zimmermann and Kienast,
1999; Guisan and Theurillat, 2000; Dirnbo ck et al., 2003),
which are thought to be most sensitive to climate change
(Thuiller et al., 2005). However, our results indicate that signif-
icant impacts could also occur in the maritime uplands of
Scotland, even under a low warming scenario (B1 of the
IPCC; Nakicenovic and Swart, 2000). While the models can
be rened in terms of including processes such as dispersal
and species interactions, the results highlight the need to
continue to maintain these important high-altitude plant
communities in a condition in which they can be most resil-
ient to climate change. Furthermore, monitoring is needed to
detect and attribute future changes to the correct causal fac-
tors and to test model predictions (Guisan and Theurillat,
2005). Such information is critical for the development of
more exible conservation policies in the face of climate
change.
1672 B I O L O G I C A L C O N S E R VAT I O N 1 4 1 ( 2 0 0 8 ) 1 6 6 5 1 6 7 5
Acknowledgements
We thank a number of agencies for providing datasets: Scot-
tish Natural Heritage for botanical databases; the British
Atmospheric Data Centre and the United Kingdom Climate
Impacts Programme for climate data; and Allan Lilley of the
Macaulay Institute for soil maps and information. David Mar-
don and the staff of the National Trust for Scotland, Killin,
provided advice and institutional support to MT, who was
funded by a NERC studentship. Antoine Guisan and two anon-
ymous reviewers gave valuable comments on the manuscript.
Appendix A. Supplementary data
Supplementary data associated with this article can be found,
in the online version, at doi:10.1016/j.biocon.2008.04.008.
R E F E R E N C E S
Akaike, H., 1973. Information theory as an extension of the
maximum likelihood principle. In: Petrov, B.N., Csaksi, F. (Eds.),
2nd International Symposium on Information Theory.
Akademiai Kiado Budapest, Hungary, pp. 267281.
Anon, 2006. Special Areas of Conservation.
Arau jo, M.B., Guisan, A., 2006. Five (or so) challenges for species
distribution modelling. Journal of Biogeography 33, 16771688.
Arau jo, M.B., New, M., 2007. Ensemble forecasting of species
distributions. Trends in Ecology and Evolution 22, 4247.
Arau jo, M.B., Cabeza, M., Thuiller, W., Hannah, L., Williams, P.H.,
2004. Would climate change drive species out of reserves? An
assessment of existing reserve-selection methods. Global
Change Biology 10, 16181626.
Arau jo, M.B., Thuiller, W., Williams, P.H., Reginster, I., 2005.
Downscaling European species atlas distributions to a ner
resolution: implications for conservation planning. Global
Ecology and Biogeography 14, 1730.
Averis, A., Averis, B., Birks, J., Horseld, D., Thompson, D., Yeo, M.,
2004. An Illustrated Guide to British Upland Vegetation.
Bakkenes, M., Alkemade, J.R.M., Ihle, F., Leemans, R., Latour, J.B.,
2002. Assessing effects of forecasted climate change on the
diversity and distribution of European higher plants for 2050.
Global Change Biology 8, 390407.
Barry, R.G., 1992. Mountain climatology and past and potential
future climatic changes in mountain regions a review.
Mountain Research and Development 12, 7186.
Berry, P.M., Dawson, T.P., Harrison, P.A., Pearson, R.G., 2002.
Modelling potential impacts of climate change on the
bioclimatic envelope of species in Britain and Ireland. Global
Ecology and Biogeography 11, 453462.
Berry, P.M., Harrison, P.A., Dawson, T.P., Walmsley, C.A., 2005.
Monarch 2: modelling natural resource responses to climate
change. United Kingdom Climate Impacts Programme, Oxford.
Bonn, A., Schro der, B., 2001. Habitat models and their transfer for
single and multi-species groups: a case study of carabids in an
alluvial forest. Ecography 24, 483496.
Botkin, D.B., Saxe, H., Araujo, M.B., Betts, R., Bradshaw, R.H.W.,
Cedhagen, T., Chesson, P., Dawson, T.P., Etterson, J.R., Faith,
D.P., Ferrier, S., Guisan, A., Hansen, A.S., Hilbert, D.W., Loehle,
C., Margules, C., New, M., Sobel, M.J., Stockwell, D.R.B., 2007.
Forecasting the effects of global warming on biodiversity.
Bioscience 57, 227236.
Brooker, R.W., 2006. Plantplant interactions and environmental
change. New Phytologist 171, 271284.
Brooker, R., Young, J.C., Watt, A.D., 2007. Climate change and
biodiversity: impacts and policy development challenges a
European case study. International Journal of Biodiversity
Science and Management 3, 1230.
Bruelheide, H., 2003. Translocation of a montane meadow to
simulate the potential impact of climate change. Applied
Vegetation Science 6, 2334.
Cohen, J., 1960. A coefcient of agreement for nominal scales.
Educational and Psychological Measurement 20, 3746.
Cornish, C., Dayton, N., 2005. NVC survey of Beinn Heasgarnich
SSSI and cSAC (Stirling). Quadrat Scotland, Argyll, UK, pp. 131.
Council of the European Communities, 1992. Council Directive 92/
43/EEC of 21 May 1992 on the conservation of natural habitats
and of wild fauna and ora. In: Ofcial Journal of the European
Communities, Series L, 206, pp. 750.
Dayton, N., Cornish, C., 2005. NVC survey of Meall na Samnha
SSSI and cSAC (Stirling). Quadrat Scotland, Argyll, UK, 137 pp.
Death, G., Fabricius, K.E., 2000. Classication and regression
trees: a powerful yet simple technique for ecological data
analysis. Ecology 81, 31783192.
De Bello, F., Leps, J., Sebastia, M.T., 2005. Predictive value of plant
traits to grazing along a climatic gradient in the
Mediterranean. Journal of Applied Ecology 42, 824833.
Dirnbo ck, T., Dullinger, S., Grabherr, G., 2003. A regional impact
assessment of climate and land-use change on alpine
vegetation. Journal of Biogeography 30, 401417.
Dockerty, T., Lovett, A., Watkinson, A., 2003. Climate change and
nature reserves: examining the potential impacts, with
examples from Great Britain. Global Environmental Change
13, 125135.
Duckworth, J.C., Bunce, R.G.H., Malloch, A.J.C., 2000. Modelling the
potential effects of climate change on calcareous grasslands in
Atlantic Europe. Journal of Biogeography 27, 347358.
Dullinger, S., Dirnbock, T., Grabherr, G., 2004. Modelling climate
change-driven treeline shifts: relative effects of temperature
increase, dispersal and invasibility. Journal of Ecology 92, 241
252.
Ferrier, S., Guisan, A., 2006. Spatial modelling of biodiversity at
the community level. Journal of Applied Ecology 43, 393404.
Ferrier, S., Watson, G., 1997. An evaluation of the effectiveness of
environmental surrogates and modelling techniques in
predicting the distribution of biological diversity. In:
Environment Australia, Canberra. <http://www.ea.gov.au/
biodiversity/publications/technical/surrogates/pubs/
surrogates.pdf>.
Ferris, R., 2006. Research priorities: climate change and
adaptation. 35 pp. The UK Biodiversity Research Advisory
Group. <http://www.jncc.gov.uk/page-3997>.
Gottfried, M., Pauli, H., Reiter, K., Grabherr, G., 1999. A ne-scaled
predictive model for changes in species distribution patterns
of high mountain plants induced by climate warming. Global
Change Biology 5, 241251.
Grabherr, G., 1994. Climate effects on mountain plants. Nature
369, 448.
Guisan, A., Theurillat, J.-P., 2000. Equilibrium modeling of alpine
plant distribution: how far can we go? Phytocoenologia 30,
353384.
Guisan, A., Theurillat, J.-P., 2005. Appropriate monitoring networks
are required for testing model-based scenarios of climate
change impact on mountain plant distribution. In: Huber, U.M.,
Bugmann, H., Reasoner, M.A. (Eds.), Global Change and
Mountain Regions: An Overview of Current Knowledge.
Springer, Dordrecht, The Netherlands, pp. 467476.
Guisan, A., Zimmermann, N.E., 2000. Predictivehabitat distribution
models in ecology. Ecological Modelling 135, 147186.
Guisan, A., Theurillat, J.-P., Kienast, F., 1998. Predicting the
potential distribution of plant species in an alpine
environment. Journal of Vegetation Science 9, 6574.
B I O L O G I C A L C O N S E R VAT I O N 1 4 1 ( 2 0 0 8 ) 1 6 6 5 1 6 7 5 1673
Guisan, A., Lehmann, A., Ferrier, S., Austin, M., Overton, J.M.C.,
Aspinall, R., Hastie, T., 2006. Making better biogeographical
predictions of species distributions. Journal of Applied
Ecology 43, 386392.
Hampe, A., 2004. Bioclimate envelope models: what they detect
and what they hide. Global Ecology and Biogeography 13,
469471.
Harding, R.J., 1978. The variation of the altitudinal gradient of
temperature within the British Isles. Geograska Annaler 60,
4349.
Hastie, T., Tibshirani, R., 1990. Generalized Additive Models.
Chapman and Hall, London.
Hewitt, G.M., 1999. Post-glacial re-colonization of European biota.
Biological Journal of the Linnean Society 68, 87112.
Hill, M.O., 1979. Decorana a Fortran program for detrended
correspondence analysis and reciprocal averaging. In:
Department of Ecology and Systematics. Cornell University,
Ithaca.
Hill, M.O., Preston, C.D., Smith, A.J.E., 1992. Atlas of the
Bryophytes of Britain and Ireland. Harley Books, Colchester,
UK.
Hosmer, D.W., Lemeshow, S., 1989. Applied Logistic Regression.
Wiley, New York.
Hulme, M., Jenkins, G.J., Lu, X., Turnpenny, J.R., Mitchell, T.D.,
Jones, R.G., Lowe, J., Murphy, J.M., Hassell, D., Boorman, P.,
Mcdonald, R., Hill, S., 2002. Climate change scenarios for the
United Kingdom: the UKCIP02 scientic report. Tyndall Centre
for Climate Change Research, School of Environmental
Sciences, University of East Anglia, Norwich, UK.
Huntley, B., 1991. How plants respond to climate change
migration rates, individualism and the consequences for
plant-communities. Annals of Botany 67, 1522.
IPCC, 2007. Summary for Policymakers Climate change 2007:
the physical science basis. In: Solomon, S.D., Qin, M.,
Manning, Z., Chen, M., Marquis, K.B., Averyt, M.T., Miller,
H.L. (Eds.), Contribution of Working Group I to the Fourth
Assessment Report of the Intergovernmental Panel on
Climate Change, Cambridge University Press, Cambridge,
UK, p. 18.
Jackson, D.L., McLeod, C.R., 2000. Handbook on the UK status of
EC Habitats Directive interest features: provisional data on the
UK distribution and extent of Annex I habitats and the UK
distribution and population size of Annex II species, Revised
2002 edition. JNCC Report 312.
Jime nez-Valverde, A., Lobo, J.M., 2006. The ghost of unbalanced
species distribution data in geographical model predictions.
Diversity and Distributions 12, 521524.
JNCC, 2006. Common Standards Monitoring Guidance for Upland
Habitats. In: Joint Nature Conservation Committee,
Peterborough, Version October 2006, pp. 2237. ISSN 1743-8160.
<http://www.jncc.gov.uk/>.
Jongman, R.H.G., Ter Braak, C.J.F., Van Tongeren, O.F.R., 1995. Data
analysis in community and landscape ecology, 2nd ed.
Cambridge University Press, Cambridge.
Kazakis, G., Ghosn, D., Vogiatzakis, I., Papanastasis, V., 2007.
Vascular plant diversity and climate change in the alpine zone
of the Lefka Ori, Crete. Biodiversity and Conservation.
doi:10.1007/s10531-006-9021-1.
Kirkby, M., 1975. Hydrograph modelling strategies. In: Peel, R.,
Chisholm, M., Haggett, P. (Eds.), Processes in Physical and
Human Geography. Heinemann, London, pp. 6990.
Klanderud, K., Birks, H.J.B., 2003. Recent increases in species
richness and shifts in altitudinal distributions of Norwegian
mountain plants. Holocene 13, 16.
Ko rner, C., 1999. Alpine plant life: functional plant ecology of high
mountain ecosystems. Springer-Verlag, Berlin.
Kumar, L., Skidmore, A.K., Knowles, E., 1997. Modelling
topographic variation in solar radiation in a GIS environment.
International Journal of Geographical Information Science 11,
475497.
Legendre, P., Gallagher, E.D., 2001. Ecologically meaningful
transformations for ordination of species data. Oecologia 129,
271280.
Liu, C.R., Berry, P.M., Dawson, T.P., Pearson, R.G., 2005. Selecting
thresholds of occurrence in the prediction of species
distributions. Ecography 28, 385393.
Lo fer, J., 2007. The inuence of micro-climate, snow cover, and
soil moisture on ecosystem functioning in high mountains.
Journal of Geographical Sciences 17, 319.
Louault, F., Pillar, V.D., Aufrere, J., Garnier, E., Soussana, J.F., 2005.
Plant traits and functional types in response to reduced
disturbance in a semi-natural grassland. Journal of Vegetation
Science 16, 151160.
Lusby, P., Wright, J.P., 2001. Scottish Wild Plants, 2nd ed. Mercat
Press, Edinburgh.
Macaulay Institute for Soil Research, 1982. Soil Survey of
Scotland, Sheet 47: Crieff. In: Craigiebuckler, Aberdeen, UK.
Macaulay Institute for Soil Research, 1985. Soil Survey of
Scotland, Sheet 51: Loch Tay. In: Craigiebuckler, Aberdeen, UK.
Manel, S., Williams, H.C., Ormerod, S.J., 2001. Evaluating
presenceabsence models in ecology: the need to account for
prevalence. Journal of Applied Ecology 38, 921931.
Manley, G., 1952. Climate and the British Scene. Collins, London.
Manly, B.F.J., 1997. Randomization, bootstrap and Monte Carlo,
2nd ed. Chapman and Hall, London.
McCune, B., Grace, J.B., 2002. Analysis of ecological communities.
MjM Software Design, Gleneden Beach, OR.
McEvoy, D., Handley, J.F., Cavan, G., Aylen, J., Lindley, S.,
McMorrow, J., Glynn, S., 2006. Climate change and the visitor
economy: the challenges and opportunities for Englands
northwest. In: Sustainability Northwest (Manchester) and
UKCIP (Oxford), UK.
McPherson, J.M., Jetz, W., Rogers, D.J., 2004. The effects of species
range sizes on the accuracy of distribution models: ecological
phenomenon or statistical artefact? Journal of Applied Ecology
41, 811823.
Mitchell, R.J., Morecroft, M.D., Acreman, M., Crick, H.Q.P., Frost,
M., Harley, M., MacLean, I.M.D., Mountford, O., Piper, J., Parr,
T.W., Pontier, H., Rehsch, M.M., Ross, L.C., Smithers, R.J.,
Stott, A., Walmsley, C.A., Watt, A.D., Watts, O., Wilson, E., 2007.
England biodiversity strategy towards adaptation to climate
change. Centre for Ecology and Hydrology. Final report to
Defra for contract CRO327. p. 177.
Moore, I.D., Norton, T.W., Williams, J.E., 1993. Modelling
environmental heterogeneity in forested landscapes. Journal
of Hydrology 150, 717747.
Morecroft, M.D., Sier, A.R.J., Elston, D.A., Nevison, I.M., Hall, J.R.,
Rennie, S.C., Parr, T.W., Crick, H.Q.P., 2006. Targeted Monitoring
of Air Pollution and Climate Change Impacts on Biodiversity.
Final report to Department for Environment, Food and Rural
Affairs, Countryside Council for Wales and English Nature
(CR0322). p. 78.
Nagy, L., 2003. The high mountain vegetation of Scotland. In:
Nagy, L., Grabherr, G., Ko rner, C., Thompson, D.B.A. (Eds.),
Alpine Biodiversity in Europe. Springer-Verlag, Berlin, pp. 39
46.
Nagy, L., Grabherr, G., Ko rner, C., Thompson, D.B.A., 2003. Alpine
biodiversity in space and time. In: Nagy, L., Grabherr, G.,
Ko rner, C., Thompson, D.B.A. (Eds.), Alpine Biodiversity in
Europe. Springer-Verlag, Berlin, pp. 453464.
Nakicenovic, N., Swart, R., 2000. Special Report on Emissions
Scenarios. Cambridge University Press, Cambridge, UK.
Normand, S., Svenning, J.C., Skov, F., 2007. National and European
perspectives on climate change sensitivity of the habitats
directive characteristic plant species. Journal for Nature
Conservation 15, 4153.
1674 B I O L O G I C A L C O N S E R VAT I O N 1 4 1 ( 2 0 0 8 ) 1 6 6 5 1 6 7 5
Parmesan, C., 2006. Ecological and evolutionary responses to
recent climate change. Annual Review of Ecology Evolution
and Systematics 37, 637669.
Pauli, H., Gottfried, M., Reiter, K., Klettner, C., Grabherr, G., 2007.
Signals of range expansions and contractions of vascular
plants in the high Alps: observations (19942004) at the
GLORIA
*
master site Schrankogel, Tyrol, Austria. Global
Change Biology 13, 147156.
Pearson, R.G., Dawson, T.P., 2003. Predicting the impacts of
climate change on the distribution of species: are bioclimate
envelope models useful? Global Ecology and Biogeography 12,
361371.
Pearson, R.G., Dawson, T.P., 2004. Bioclimate envelope models:
what they detect and what they hide. Global Ecology and
Biogeography 13, 471473.
Pen uelas, J., Boada, M., 2003. A global change-induced biome shift
in the Montseny mountains (NE Spain). Global Change Biology
9, 131140.
Pepin, N.C., 1995. The use of GCM scenario output to model
effects of future climatic change on the thermal climate of
marginal maritime uplands. Geograska Annaler Series a-
Physical Geography 77A, 167185.
Peppler-Lisbach, C., Schro der, B., 2004. Predicting the species
composition of Nardus stricta communities by logistic
regression modelling. Journal of Vegetation Science 15, 623
634.
Peres-Neto, P., Jackson, D., 2001. How well do multivariate data
sets match? The advantages of a Procrustean superimposition
approach over the Mantel test. Oecologia 129, 169178.
Perry, M., Hollis, D., 2005. The generation of monthly gridded
datasets for a range of climatic variables over the UK.
International Journal of Climatology 25, 10411054.
Peters, R.L., 1992. Conservation of biological diversity in the face
of climate change. In: Peters, R.L., Lovejoy, T.E. (Eds.), Global
warming and biological diversity. Yale University Press,
Newhaven and London, pp. 1530.
Pierce, S., Luzzaro, A., Caccianiga, M., Ceriani, R.M., Cerabolini, B.,
2007. Disturbance is the principal a-scale lter determining
niche differentiation, coexistence and biodiversity in an alpine
community. Journal of Ecology 95, 698706.
Poore, M.D., 1993. The alpine ora and Ben Lawers. In: Mardon,
D.K. (Ed.), Ben Lawers. National Trust for Scotland, Edinburgh.
Preston, C.D., Pearman, D.A., Dines, T.D., 2002. New Atlas of the
British and Irish Flora. Oxford University Press.
Price, M.F., Neville, G.R., 2003. Designing strategies to increase the
resilience of alpine/montane systems to climate change. In:
Hansen, L.J., Biringer, J.L., Hoffman, J.R. (Eds.), Buying Time: A
Users Manual for Building Resistance and Resilience to
Climate Change in Natural Systems, WWF. <http://
assets.panda.org/downloads/buyingtime.pdf>.
R Development Core Team, 2005. R: a language and environment
for statistical computing. R Foundation for Statistical
Computing, Vienna, Austria.
Rodwell, J.S., 2006. NVC Users Handbook. Joint Nature
Conservation Committee, Peterborough.
Stersdal, M., Birks, H.J.B., Peglar, S.M., 1998. Predicting changes
in Fennoscandian vascular-plant species richness as a result
of future climatic change. Journal of Biogeography 25, 111122.
Smith, A.J.E., 2004. The Moss ora of Britain and Ireland, 2nd ed.
Cambridge University Press, Cambridge.
Smith, S., Gray, D., Booth, A.B., 2003. Ben Lawers SSSI NVC Survey
2003. Central Environmental Surveys, Dunblane, Perthshire.
Stace, C.A., 1997. New Flora of the British Isles, 2nd ed. Cambridge
University Press, Cambridge.
Swets, J.A., 1988. Measuring the accuracy of diagnostic systems.
Science 240, 12851293.
Thomas, C.D., Cameron, A., Green, R.E., Bakkenes, M., Beaumont,
L.J., Collingham, Y.C., Erasmus, B.F.N., De Siqueira, M.F.,
Grainger, A., Hannah, L., Hughes, L., Huntley, B., Van Jaarsveld,
A.S., Midgley, G.F., Miles, L., Ortega-Huerta, M.A., Peterson,
A.T., Phillips, O.L., Williams, S.E., 2004. Extinction risk from
climate change. Nature 427, 145148.
Thuiller, W., Lavorel, S., Arau jo, M.B., Sykes, M.T., Prentice, I.C.,
2005. Climate change threats to plant diversity in Europe.
Proceedings of the National Academy of Sciences of the United
States of America 102, 82458250.
Walther, G.R., Beissner, S., Burga, C.A., 2005. Trends in the upward
shift of alpine plants. Journal of Vegetation Science 16, 541
548.
Wilson, R.J., Gutierrez, D., Gutierrez, J., Martinez, D., Agudo, R.,
Monserrat, V.J., 2005. Changes to the elevational limits and
extent of species ranges associated with climate change.
Ecology Letters 8, 11381146.
Wintle, B.A., Elith, J., Potts, J.M., 2005. Fauna habitat modelling and
mapping: A review and case study in the Lower Hunter Central
Coast region of NSW. Austral Ecology 30, 719738.
Zimmermann, N., 2001. Tools for analyzing, summarizing, and
mapping of biophysical variables. <http://www.wsl.ch/staff/
niklaus.zimmermann/progs.html> (Accessed on 1.04.2005).
Zimmermann, N.E., Kienast, F., 1999. Predictive mapping of alpine
grasslands in Switzerland: species versus community
approach. Journal of Vegetation Science 10, 469482.
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