Journal of Animal Ecology 2008, 77, 145–155
doi: 10.1111/j.1365-2656.2007.01303.x
Combined effects of climate and biotic interactions on
the elevational range of a phytophagous insect
Blackwell Publishing Ltd
Richard M. Merrill*§, David Gutiérrez†, Owen T. Lewis*, Javier Gutiérrez†, Sonia B. Díez† and
Robert J. Wilson†‡
*Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK; †Área de Biodiversidad
y Conservación, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos,
Tulipán s/n, Móstoles, E-28933 Madrid, Spain; and ‡Centre for Ecology and Conservation, University of Exeter,
Cornwall Campus, Penryn TR10 9EZ, UK
Summary
1. The ranges of many species have expanded in cool regions but contracted at warm margins in
response to recent climate warming, but the mechanisms behind such changes remain unclear.
Particular debate concerns the roles of direct climatic limitation vs. the effects of interacting species
in explaining the location of low latitude or low elevation range margins.
2. The mountains of the Sierra de Guadarrama (central Spain) include both cool and warm range
margins for the black-veined white butterfly, Aporia crataegi, which has disappeared from low
elevations since the 1970s without colonizing the highest elevations.
3. We found that the current upper elevation limit to A. crataegi’s distribution coincided
closely with that of its host plants, but that the species was absent from elevations below 900 m,
even where host plants were present. The density of A. crataegi per host plant increased with elevation, but overall abundance of the species declined at high elevations where host plants were rare.
4. The flight period of A. crataegi was later at higher elevations, meaning that butterflies in higher
populations flew at hotter times of year; nevertheless, daytime temperatures for the month of peak
flight decreased by 6·2 °C per 1 km increase in elevation.
5. At higher elevations A. crataegi eggs were laid on the south side of host plants (expected to
correspond to hotter microclimates), whereas at lower sites the (cooler) north side of plants was
selected. Field transplant experiments showed that egg survival increased with elevation.
6. Climatic limitation is the most likely explanation for the low elevation range margin of A. crataegi, whereas the absence of host plants from high elevations sets the upper limit. This contrasts
with the frequent assumption that biotic interactions typically determine warm range margins, and
thermal limitation cool margins.
7. Studies that have modelled distribution changes in response to climate change may have underestimated declines for many specialist species, because range contractions will be exacerbated by
mismatch between the future distribution of suitable climate space and the availability of resources
such as host plants.
Key-words: altitude, biotic interactions, climate change, phenology, range shifts.
Introduction
Correspondence: Owen T. Lewis, Department of Zoology,
University of Oxford, South Parks Road, Oxford OX1 3PS, UK.
Tel: + 44 0 1865 271162; Fax: + 44 0 1865 310447;
E-mail: owen.lewis@zoo.ox.ac.uk
§Present address: Department of Zoology, University of Cambridge,
Downing Street, Cambridge CB2 3EJ, UK.
The ranges of many species have expanded at high latitudes
and elevations but contracted at their warm margins in
response to recent climate change (Walther et al. 2002;
Thomas, Franco & Hill 2006). Changes to the distribution of
‘habitable climate space’ may lead to extinctions if future
ranges are too small or isolated from current ranges, and consequently the impact of climate change on biodiversity is of
increasing concern (Thomas et al. 2004). The mechanisms
© 2007 The Authors. Journal compilation © 2007 British Ecological Society
146
R. M. Merrill et al.
that determine geographical range margins remain poorly
understood, limiting our ability to predict future species
distributions and to model the effects of climate change on
biodiversity (Pearson & Dawson 2003; Ibáñez et al. 2006).
Climate can limit distributions directly by influencing survival and fecundity, or indirectly through its effects on interacting species, including food sources, natural enemies and
competitors (Gaston 2003). The prevailing view that climate
limits distributions directly at cool, upper latitude range
margins is supported by considerable empirical evidence
(see references in Gaston 2003). An increasing number of
examples show how climate warming has allowed range
expansions at high latitudes by reducing mortality (Crozier
2004; Walther, Berger & Sykes 2005) or increasing fecundity
(Davies et al. 2006). In contrast, there is little evidence for
direct climate limitation at warm margins, where biotic interactions are believed to be more important (MacArthur 1972;
Brown, Stevens & Kaufman 1996; Parmesan et al. 2005).
Considering that the first symptoms of biodiversity loss are
expected at lower elevational and latitudinal boundaries,
empirical evidence for the mechanisms that limit species
distributions in these areas is of particular importance for
modelling future species ranges and for adapting biodiversity
conservation to climate change (Hampe & Petit 2005).
Phytophagous insects and their host plants are useful
model systems for testing the effects of climate and biotic
interactions on species distributions (Hodkinson 1999; Bale
et al. 2002), and have provided some of the first evidence for
the climatic mechanisms behind population extinctions at
warm range margins (Parmesan 1996, 2005; McLaughlin
et al. 2002). The progressive restriction of phytophagous
insects to warmer microhabitats is a well-documented explanation for the locations of cool range boundaries (Thomas 1993;
Thomas et al. 1999), but evidence for the reverse pattern at
warm margins is lacking. In this study we determine the
relative roles of climate and larval host plants in determining
distribution and abundance for an oligophagous butterfly
across a naturally occurring thermal gradient incorporating both warm (low elevation) and cool (upper elevation)
range limits. We first determine changes to the elevational
range of the black-veined white Aporia crataegi L. after
30 years of climate warming, and test for differences between
the current range of the species and its larval host plants. We
then investigate how climatic effects on the phenology, habitat
associations and survival of A. crataegi could cause its elevational range to be narrower than that of its host plant. In
contrast to prevailing explanations for range margins, we
find stronger evidence for direct climate limitation at the
warm margin of the species distribution and for host plant
limitation at the cool margin.
Methods
STUDY SYSTEM
The black-veined white A. crataegi L. is a widespread Palearctic butterfly, distributed from north-west Africa and western Europe to east
Asia (40 –70° N) and Japan (Tolman & Lewington 1997). In
Europe, the species has expanded its range in Scandinavia but has
also suffered serious declines, including extinctions from the United
Kingdom in the 1920s and recently from the Czech Republic and
the Netherlands (Asher et al. 2001). At its south-western range margin,
in central and southern Spain and in North Africa, A. crataegi is
restricted to high elevations in mountains (García-Barros et al .
2004; personal communication, J. Tennent, 2007).
A. crataegi has one annual flight period, and females lay batches
of up to c. 100 eggs on the leaves of both wild and cultivated Rosaceae
(Emmet & Heath 1989). In particular, the species uses Crataegus spp.
(hawthorn) and Prunus spinosa L. (blackthorn). Eggs hatch after
approximately 2 weeks, and larvae live gregariously in a silken web
from which they emerge to feed. The web is converted into a nest,
constructed from leaves and silk, in which larvae over-winter in the
second instar. In spring, larvae continue feeding in groups on the host
plant before dispersing and pupating alone (Emmet & Heath 1989).
The study location was the Sierra de Guadarrama (central Spain),
a 100 × 30 km mountain range located at c. 40°45′ N 4°00′ W, that
rises to a maximum elevation of 2428 m from plains of ≥ 700 m to the
north and ≥ 535 m to the south (Fig. 1). The main host plants for
A. crataegi in the region are C. monogyna Jacq. and P. spinosa,
although eggs have also been observed rarely on Rosa spp. (D.
Gutiérrez, personal observation). Mean annual temperature in the
region increased by 1·3 °C between 1967–1973 and 1997–2003
(equivalent to an uphill shift in isotherms of c. 225 m), and over the
same time-period the lower elevational limits of 16 butterfly species
with herbaceous host plants shifted uphill by an average of 212 m
(Wilson et al. 2005).
ELEVATIONAL RANGE OF A. CRATAEGI
The elevational range of A. crataegi was recorded in 1967–73 and
2004– 06 at grassland, scrub and woodland sites that were visited
repeatedly to record regional butterfly distributions. Data for
1967–73 (Monserrat 1976) are butterfly counts at 38 sites that
were each visited five or more times in total, including at least once
during the flight period of A. crataegi (mid-May to late July). In
2006, A. crataegi was counted every 2 weeks at 43 sites, stratified by
elevation, of which 20 had also been sampled in 2004 and 2005.
From May to August, butterflies were counted on standardized
500 m long × 5 m wide transects (Pollard & Yates 1993). The overall
elevational range of sites was 640–1860 m asl in 1967–73, and 550–
2240 m in 2006. A. crataegi was considered to be present in either
time-period at locations where two or more individuals were
counted, and absent where no individuals were observed. Sites
where only one individual was recorded were excluded from analyses, because sampled butterflies might be vagrants, rather than
representatives of a local breeding population.
To test the relation between the elevational range of A. crataegi
and its larval host species, the abundance of host plants was estimated at each of the 43 transect sites in 2006. The route of the 500 m
transect was followed in August–September 2006 (before leaf fall)
and the number of plants of C. monogyna, P. spinosa and Rosa spp.
that occurred in the 5 m wide butterfly transect was recorded, to
give a density of each species per 0·25 ha (500 × 5 m). If any of the
plant species was not present in the 5 m wide transect, then the
transect was repeated with increasing widths of 10 m, 20 m, and up
to a maximum of 50 m width (i.e. 25 m on either side of the
recorder): host plant density per 0·25 ha was then estimated based
on the increased transect width. Host plant species are considered
present at a site if they were found in transects of ≤ 50 m wide. When
© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 145–155
Host and climate constraints at range margins 147
Fig. 1. Sample distribution for A. crataegi
and its host plants in 1967–73 and 2006.
Triangles show 1967–73 sites. Transect sites in
2006 are squares (C. monogyna and/or P.
spinosa present) and circles (host plants
absent). Filled symbols show sites where A.
crataegi was observed, open symbols where
absent.
host plant species were not found in ≤ 50 m wide transects, further
searches up to 100 m away from the transect route revealed plants at
only one site (one individual of C. monogyna with abundant eggs, larvae
and pupal cases of A. crataegi). In this case, we include C. monogyna as
‘present’ at the site (given its evident importance for the local population of A. crataegi), and estimate its density as 0·1 per 0·25 ha (i.e.
as if the one plant had been included in a 50 m wide transect).
Universal Transverse Mercator (UTM) coordinates were recorded
at least every 100 m along each transect using a handheld Garmin
GPS unit. The coordinates were used to plot each transect in
ArcView geographic information system (GIS) (ESRI 1996), and the
average elevation of 100 m grid squares intercepted by the transect
was determined using a digital elevation model (NASA/JPL-Caltech
2004). To determine the elevational associations of A. crataegi and
its host plants, binary logistic regressions were carried out for presence (1) and absence (0) of each species against elevation (km) and
elevation2. To test the validity of results based on logistic regression
models, species’ elevational distributions were also fitted to Huisman–
Olff–Fresco (HOF) models (Oksanen & Minchin 2002) (see Supplementary material, Appendix S1). For A. crataegi, logistic regression
models were also fitted with the additional variables of host plant
abundance and its interaction with elevation. For this analysis, host
plant abundance included the total transect count of the two main
hosts C. monogyna and P. spinosa, with Rosa spp. as a separate variable.
Linear regression was used to test for the effects of elevation on
the density of A. crataegi and its host plants at sites where the
respective species were present. The dependent variables were logtransformed counts of each species per 500 × 5 m transect. Normal
rather than Poisson error structures were used because the data were
highly over-dispersed. For A. crataegi, we used the sum of annual
transect counts and included elevation, the density of larval host
plants and their interaction as independent variables. As a further
analysis, we calculated the density of A. crataegi per host plant (i.e.
A. crataegi total count divided by the total count of C. monogyna and
P. spinosa per 0·25 ha), and regressed this variable against elevation.
We tested the validity of results based on the 43 intensive transects
in 2006 by repeating analyses using data from the 20 transects that
had also been walked every 2 weeks in 2004 and 2005.
ELEVATIONAL TRENDS IN PHENOLOGY
The flight period of A. crataegi was summarized by calculating
mean flight date and first appearance date at each transect (each
measured as the number of days since 1 April). Mean flight date was
© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 145–155
148
R. M. Merrill et al.
calculated as the weighted mean date of transect counts (Stefanescu,
Peñuelas & Filella 2003). Linear regressions for flight date were fitted
with elevation (km) as an explanatory variable.
To estimate the temperatures experienced by A. crataegi during its flight period (that could affect habitat associations), Hobo
dataloggers were located at transect sites in 2006, and the temperature
was recorded every hour from the beginning of May onwards. Dataloggers were placed in semishaded locations 1·5 m above the ground,
corresponding to typical A. crataegi egg-laying sites on shrubs.
Daytime temperature for the entire flight period was calculated as
mean temperature (°C) for the 12-hourly intervals of 07.00–18.00 h
GMT, over the 2 months from 15 May to 14 July (encompassing
all A. crataegi observations in 2006). Daytime temperature during the
peak flight period was estimated as the mean for the 29 days
centred on the mean flight date at each occupied site.
EGG-SITE LOCATION
Host plants were searched for eggs and larval webs at sites across and
beyond the elevational range of A. crataegi. Twenty-three sites ranging in elevation from 580 m to 1780 m (14 of which corresponded to
butterfly transect locations) were visited between 23 June and 12 July
2006. Repeated searching at elevations above 1800 m revealed no C.
monogyna or P. spinosa, and no eggs were found on Rosa spp. at any
sites. At each location the first 25 C. monogyna and P. spinosa plants
encountered were searched for A. crataegi egg batches and larval webs.
Where fewer than 25 plants were encountered, all available host
plants were searched. The larval web is almost always on the same or
an adjacent leaf to the oviposition site, and so is an acceptable measure
of egg-site location. The height above the ground (H) and side of the
host plant (S ) were recorded for each egg batch or larval web. In the
field S was recorded as the cardinal and ordinal points (i.e. north,
north-east, east, etc.); data were converted to degrees from north for
subsequent analyses (so that north = 0, both north-east and northwest = 45, both east and west = 90, etc.). The side of the leaf on
which eggs were located (upperside or underside) was recorded for
egg batches.
We hypothesized that at higher elevations eggs would be laid in
warmer microhabitats: on the south side of plants, closer to the
ground, and on the upper surface of leaves. Because egg batches
from the same site are not statistically independent, summary values
for each site were used in analyses. Dependent variables were mean
values of S and H, and the proportion of egg batches on the upperside of the leaf (L). Generalized linear models were constructed for
side of host plant (S) and height above ground (H, log-transformed)
using elevation as a predictor variable. The proportion of egg
batches laid on the leaf upperside (L) was tested using analysis of
deviance, including both elevation and elevation2 to test for a possible
curvilinear effect of elevation. Because the data were over-dispersed,
the model for L was tested using quasi-binomial error structure and
F-tests (Crawley 2002). To test whether the inclusion of sites with
summary values based on few data had a large effect, analyses were
repeated excluding sites where fewer than five egg batches/larval
webs were recorded.
EGG AND LARVAL SURVIVORSHIP
Trends in egg and young larval survivorship were investigated by
transplanting egg batches onto host plants at different elevations.
Ten female A. crataegi were caught at 1450 m and maintained in
captivity outside at 1300 m elevation, where they were provided
with semishaded C. monogyna plants for egg-laying. The number of
eggs in each batch was recorded. Within 3 days of being laid, egg
batches were transplanted to nine sites at approximately 100 m
intervals between 900 m and 1700 m, corresponding to the elevational range of A. crataegi, and to a further location at 580 m,
below the current low elevation limit. Leaf fragments with egg
batches were attached using a drop of UHU® solvent-based glue
to the upper surface of C. monogyna leaves, with two batches in
shaded microhabitats and two in unshaded microhabitats on each
tree. This was repeated for two trees at each site (resulting in eight
experimental batches at each elevation) except at 580 m, where only
one tree (four egg batches) was used because of a shortage of egg
batches. In total, 76 experimental egg batches were established
between 22 and 28 June 2006. The location of each egg batch was
marked so that it could be relocated and identified.
The experimental sites were visited on 17 or 18 July to record
mortality of eggs and young larvae. The criterion for egg batch
survival was that living larvae were present. Sites with unhatched
egg batches were revisited on 27 July in case larvae had not had time
to emerge by the earlier visit. Egg batches were excluded from subsequent analyses if the leaf onto which they had been transplanted
could not be recovered.
Survivorship of egg batches in shaded and unshaded treatments
was compared using a paired t-test. Generalized linear models with
binomial error structure were then used to test the effects of elevation
on survivorship. The proportion of surviving batches at each experimental site was the dependent variable, with elevation as the predictor.
The analysis was repeated excluding data for the 580 m site, which
is outside the current elevational range of A. crataegi.
To determine whether Rosa spp. were potential hosts for A. crataegi
in the region, 10 egg batches were collected from C. monogyna in the
field on 5 July 2006. Half of these were transplanted onto the leaves
of Rosa spp. and the remaining control batches onto C. monogyna.
These egg batches were all placed within 100 m of each other with
the same elevation (c. 1350 m) and aspect (south). Egg batches were
attached to leaves on the south side of trees at approximately 1 m
above ground and were revisited on 17 July.
Results
ELEVATIONAL RANGE OF A. CRATAEGI
In 1967–73, A. crataegi was present at 17 sample locations
(based on observations of two or more adults) and absent from
19 locations. The lowest elevation population was at 640 m
(with a maximum count of 37 in one visit), and the highest at
1800 m (with a maximum of 6). In 2006, A. crataegi was
observed at 26 of 43 transect sites; of these, four were excluded
from analysis because only one individual was recorded. Sites
with two or more adults ranged in elevation from 930 to
1765 m. The elevational range appeared to have shifted
uphill from 1967–73 to 2006, with the loss of populations
below 900 m (Fig. 2a).
The three potential host plants (C. monogyna, P. spinosa
and Rosa spp.) were present, respectively, at 25, 17 and 38 of
the transect sites. The distributions of the two main host
plants extended to lower elevations than that of A. crataegi but
were absent from high elevations: transects with C. monogyna
ranged from 550 to 1535 m, and of P. spinosa from 840 to 1525 m
(Fig. 2b). Additional field searches encountered C. monogyna up
to elevations of 1792 m, and P. spinosa as low down as 580 m.
© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 145–155
Host and climate constraints at range margins 149
Fig. 2. Proportion of occupied sites in 250 m elevation bands for A.
crataegi and its host plants. (a) A. crataegi in 1967–73 (black) and
2006 (white); (b) C. monogyna (black) and P. spinosa (white) in the 43
transect sites in 2006. Number of samples per elevation band shown
above each bar [in (a), n for 1967–73 and 2006 separated by hyphens].
Asterisks show 250 m bands where C. monogyna or P. spinosa were
found, but not at transect sites.
Rosa spp. occurred at both higher and lower elevations than
A. crataegi (elevational range 590–2040 m; see Supplementary material, Fig. S1).
The probability of occurrence of A. crataegi was not significantly related to elevation in 1967–73. In 2006, probability
of occurrence of A. crataegi and of the three plant species
peaked at mid-elevations, with significant positive effects of
elevation (km) and negative effects of elevation2 in logistic
regressions (Table 1). Logistic regressions for A. crataegi
occurrence in 2004 and 2005 also showed significant positive
effects of elevation and negative effects of elevation2 (results
not shown). HOF models showed unimodal relationships of
probability of occurrence with elevation for A. crataegi, P.
spinosa and Rosa spp., but the best model for C. monogyna
was a plateau with a probability of occurrence of > 75% up to
1600 m, which rapidly declined at higher elevations (see Supplementary material, Table S1).
Despite the differences between the distributions of A. crataegi and its host plants, the best-fitting logistic regression
model for A. crataegi occurrence in 2006 included a positive
significant effect of host plant count (C. monogyna + P.
spinosa). The coefficient for host plant count was not significant (P = 0·27) but the removal of the term produced a significant change in log likelihood (P = 0·006) (overall model:
logit probability of occurrence = –33·02 (± SE 12·68) + 50·12
elevation (km) (± 18·75) – 17·88 elevation2 (± 6·65) + 0·08 host
plant density (± 0·07); –2 log likelihood = 19·94, R2 = 0·77,
χ2 = 33·49, P < 0·001).
The mean annual count of A. crataegi at occupied transects
ranged from 14·8 to 16·1 in 2004–06, with maxima per site
ranging from 38 in 2004 to 72 in 2006. Linear regressions for
A. crataegi counts at occupied sites showed significant effects
of elevation (positive) and elevation2 (negative) (Table 2a;
Fig. 3a). Counts of host plants (C. monogyna + P. spinosa) in
sites where they occurred had a marginally non-significant unimodal relationship with elevation (Table 2a, Fig. 3b). Rosa spp.
abundance also increased from low to mid-elevations, before
decreasing at high elevations (see Supplementary material, Fig.
S1). The density of A. crataegi per host plant increased significantly with elevation in 2004 and 2006 (Fig. 3c), but the
relationship was marginally non-significant in 2005
(Table 2b).
ELEVATIONAL TRENDS IN PHENOLOGY
In 2006, the flight period of A. crataegi was later at higher
locations (Fig. 4), whether analysed using mean flight or first
appearance date. Data from the smaller sample of transects in
2004 –05 confirmed this elevational delay, although mean flight
date was not significantly related to elevation in 2005
(Table 3). Flight was approximately 30 –40 days later per
1 km increase in elevation in 2006, whereas in 2004–05 the
delay was 10–30 days per 1 km.
Table 1. Logistic regression models for the elevational range of Aporia crataegi, its main host plants and Rosa spp. Models for logit (probability
of occurrence), showing number of presences (NP) and absences (NA); coefficients for elevation and elevation2; and summary statistics, with R2
based on Nagelkerke (1991)
Species
NP
NA
Elevation (km)
(coefficient)
A. crataegi
C. monogyna
P. spinosa
Rosa spp.
22
25
17
38
17
18
26
5
45·25**
18·60*
59·60*
34·42***
Elevation2
(coefficient)
–16·84**
–8·72**
–25·87*
–13·56***
Intercept
–27·66**
–7·81+
–32·46*
–14·97***
–2 LL
R2
χ2
P
25·50
34·48
30·17
11·10
0·69
0·58
0·64
0·72
27·92
24·00
27·55
19·82
< 0·001
< 0·001
< 0·001
< 0·001
Significance for terms in logistic regression models: ***P < 0·001, **P < 0·01, *P < 0·05, +P < 0·1.
© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 145–155
150
R. M. Merrill et al.
Table 2. Linear regressions for the density of Aporia crataegi, its main host plants and Rosa spp. at occupied sites against elevation, showing
coefficients (± 1 SE). Elevation in km above sea level
Species
N
Elevation
(coefficient)
(a) Models for log10 counts at occupied sites
A. crataegi (2004)
10
11·34 (± 3·71)*
A. crataegi (2005)
11
8·46 (± 3·43)*
A. crataegi (2006)
22
12·21 (± 3·34)*
C. monogyna + P. spinosa
27
10·71 (± 4·83)*
Rosa spp.
38
8·91 (± 1·70)***
(b) Models for log10 A. crataegi density per host plant
Year
2004
9
3·72 (± 1·46)*
2005
10
2·86 (± 1·28)†
2006
19
2·90 (± 1·04)*
Elevation2
(coefficient)
Intercept
R2
F
P
– 4·10 (± 1·35)*
–3·13 (± 1·20)*
– 4·78 (± 1·26)**
–5·18 (± 2·20)*
–3·44 (± 0·64)***
–6·62 (± 2·52)*
– 4·54 (± 2·40)†
–6·54 (± 2·17)**
– 4·27 (± 2·55)NS
– 4·39 (± 1·07)***
0·57
0·49
0·45
0·20
0·46
4·7
3·8
7·9
3·1
14·6
0·051
0·070
0·003
0·065
< 0·001
–5·16 (± 1·92)*
–3·99 (± 1·67)*
–3·47 (± 1·32)*
0·48
0·38
0·31
6·55
4·97
7·84
0·038
0·056
0·012
Significance for terms in models: ***P < 0·001, **P < 0·01, *P < 0·05, †P < 0·1, NSP > 0·1.
Fig. 4. The relationship of A. crataegi mean flight date with
elevation. Mean flight date (no. days since 1 April) on butterfly
transects in 2006 is plotted against elevation (km) (regression
equation shown in Table 3).
Fig. 3. Changes in the abundance of A. crataegi and its host plants
with elevation. (a) A. crataegi annual abundance. (b) C. monogyna and
P. spinosa density per 0·25 ha (c) A. crataegi density per host plant.
Regression lines plotted based on the equations for 2006 in Table 2.
Using data from 17 temperature data-loggers at transect
sites where A. crataegi and its host plants were recorded,
mean daytime temperature (from 07.00 to 18.00 GMT) over
the 2 months of the entire regional flight period in 2006
decreased by 8·9 °C per 1 km increase in elevation (mean
temperature = 33·1 °C (± SE 2·7)–8·9 × elevation (km) (± SE
2·1); R2 = 0·54; F1,15 = 17·4, P = 0·001). Mean daytime temperature for the month of peak flight at each site had a less
pronounced decline of 6·2 °C per 1 km increase in elevation
(mean = 28·8 °C (± SE 2·4)–6·2 × elevation (km) (± SE 1·9);
R2 = 0·41; F1,15 = 10·3, P = 0·006), because of the phenological delay with increasing elevation. Data from a smaller
number of dataloggers in 2004 –05 also showed steeper
declines in temperature with elevation for the 2 months
encompassing the entire flight period than for the local month
of peak flight (results not shown).
© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 145–155
Host and climate constraints at range margins 151
Table 3. Linear regressions for Aporia crataegi mean flight date and first appearance date with elevation (km), showing coefficients (± SE). Date
measured as number of days since 1 April
(a) Mean date
2004
2005
2006
(b) Appearance date
2004
2005
2006
N
Elevation (km)
(coefficient)
Intercept
R2
F
P
10
11
22
24·6 (± 7·0)**
9·2 (± 6·7)NS
33·1 (± 6·6)***
52·5 (± 9·6)**
64·9 (± 9·2)***
30·0 (± 8·7)**
0·61
0·17
0·56
12·6
1·9
25·2
0·008
0·204
< 0·001
10
11
22
28·5 (± 5·3)**
16·2 (± 4·6)**
42·7 (± 7·1)***
39·0 (± 7·3)**
43·9 (± 6·3)***
7·8 (± 9·4)NS
0·78
0·58
0·64
28·8
12·5
36·2
0·001
0·006
< 0·001
Significance for terms in models: ***P < 0·001, **P < 0·01, NSP > 0·1.
EGG-SITE LOCATION
In total, 351 host plants were searched, and data were recorded
for 236 egg batches and 63 larval webs. Egg batches were not
located randomly among host plants: the distribution of egg
batches/larval webs among trees differed significantly from
that expected under a Poisson distribution (χ2-test: observations grouped ≥ 4 egg batches/larval webs per host plant;
χ2 = 237·98, d.f. = 3, P < 0·0001), indicating a clumped distribution of egg batches on relatively few host plants. No egg
batches or larval webs were found below 900 m.
For sites with at least five egg batches, the side of the tree on
which eggs were laid (degrees difference from north) was positively related to elevation (S° = 104·9 (± SE 18·1) × elevation
(km) – 30·6 (± SE 23·9); R2 = 0·72, F1,13 = 33·66, P < 0·001),
indicating that eggs were located on the north side of plants
at lower elevations, and on the south side of plants at higher
elevations (Fig. 5a). Height above ground of egg-sites was not
related to elevation. The proportion of eggs laid on the upper
surface of leaves (L) showed evidence of a curvilinear relationship with elevation, peaking at middle elevations (Fig. 5b).
However, the relationship was not significant in the analysis
of sites with five egg batches or more, where only one site
below 1100 m was included (because most eggs had already
hatched into larvae by the time of egg searches at low elevations).
EGG AND LARVAL SURVIVORSHIP
There was no significant difference in the proportion of egg
batches surviving to form larval webs in shaded and unshaded
environments (paired t-test, t = 0·20, d.f. = 8, P = 0·847).
Data for shaded and unshaded locations were therefore
pooled for subsequent analyses. Elevation was a highly significant predictor of the proportion of egg batches surviving
to form larval webs at experimental sites (generalized linear
model with quasi-binomial error structure to correct for
overdispersion: F1,8 = 11·61, P = 0·009; Fig. 6), and also after
excluding data from the 580 m site (F1,7 = 8·91, P = 0·020).
The parameter estimates for elevation were positive, showing
that mortality decreases with elevation.
Fig. 5. The relationship of egg-site microhabitat with elevation.
(a) Side of host plant (°difference from north: higher values represent
the south-facing side of trees). (b) Proportion of egg batches on the
leaf upperside. Solid symbols show sites with ≥ 5 egg batches or larval
webs (trend line shown in a); open symbols show sites with < 5 egg
batches or larval webs.
© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 145–155
152
R. M. Merrill et al.
Fig. 6. Proportion survival of A. crataegi egg batches as a function
of elevation (km). Solid symbols show locations within the range of
A. crataegi (n = 8 batches transplanted per site); open symbol shows
one location outside the elevational range (n = 4 batches).
upper elevation limit has not increased, and seems to be determined by the distribution of C. monogyna and P. spinosa. The
main host plants are rare above 1500 m and were not found
above 1792 m despite extensive searching. The few transect
locations without host plants where A. crataegi was observed
(all of them at 1400 m elevation or above) were within 2·5 km
of the nearest known C. monogyna plant, and had annual
counts of four or fewer A. crataegi.
At occupied sites, the population density of A. crataegi
increased from low to mid-elevations before declining above
1500 m (Fig. 3). The decline in population density at high
elevations appears to be related to a concurrent decline in
host plant density. There was an indication that the density
of A. crataegi relative to that of its host plants increased linearly with elevation (Fig. 3c). One possible explanation for
such a pattern is that the proportion of host plants that was
suitable (e.g. for egg-laying or larval survival) increased with
elevation.
EGG AND LARVAL SURVIVORSHIP
None of the eggs transplanted onto Rosa spp. survived
as larvae. Living larvae were found at three of five control
manipulations on C. monogyna.
Discussion
We present evidence for a shift in the elevational range of
the butterfly A. crataegi in central Spain between 1967–73
and 2006. The butterfly has apparently disappeared from
low elevations where its larval host plants remain, while its
ability to expand its distribution above its upper elevation
limit has been constrained by the absence of host plants at
higher elevations. We propose increasing temperatures as
a causal factor for the retraction of A. crataegi from low
elevations, based on evidence that larval survivorship
increases with elevation. Information on population density, phenology and habitat use support the importance of
temperature in influencing the population dynamics and
elevational range of A. crataegi.
ELEVATIONAL RANGE OF A. CRATAEGI
The elevational range of A. crataegi retracted uphill between
1967–73 and 2006, with the species disappearing from elevations below 900 m. In 1967–73 the butterfly’s range coincided closely with that of its host plants (assuming that host
plant distribution did not change markedly between 1967–73
and 2006), with large populations recorded as low down as
640 m and up to 1800 m. By 2006, A. crataegi was absent from
sites below 900 m, in spite of the presence of host plants.
The loss of A. crataegi from 600 to 900 m elevations almost
certainly results from local population extinctions rather than
adult dispersal, as the nearest known extant populations of
the species are 25 km or further from the lowest elevation
locations where it was recorded in 1967–73. In contrast, the
Field transplant experiments across and below A. crataegi’s
current range revealed a significant effect of elevation on the
survivorship of egg batches and young larvae. Direct temperature effects seem to be the most likely explanation for the
trends in A. crataegi survival (for effects of high temperatures
on egg and larval survival in other Lepidoptera see Bryant,
Thomas & Bale 1997; Alonso 1999). Differences in rates of
leaf maturation or senescence at different elevations (e.g. Weiss
et al. 1988; Bale et al. 2002) are unlikely to explain differences
in mortality of young A. crataegi larvae, as leaves are fully mature
at all elevations at dates of egg hatch (June–July). In addition,
mortality often occurred before the emergence of larvae, with
no evidence of larval webs for nine of the 14 experimental egg
batches that did not survive at sites below 1200 m.
Insects may escape their natural enemies at higher elevations
or latitudes by entering predator-free space (Randall 1982;
Hodkinson 1999), representing another possible explanation
for elevational trends in A. crataegi survivorship. We observed
no evidence that parasitoids or predators were responsible for
the pattern observed, and in most cases the unhatched eggs
remained intact on the leaves. Nevertheless, it would be necessary to extend the experimental manipulation (e.g. Crozier
2004; Hill & Hodkinson 1995) to determine the contributions to A. crataegi mortality of direct climatic effects, and of
effects mediated by other trophic levels, that potentially
reflect the indirect effects of climate. Whichever mechanism
is responsible, the effects of the elevational gradient on egg
batch and young larval survivorship will have a negative effect
on the viability of A. crataegi populations at low elevations,
with the potential to limit the distribution of this species.
CAUSES AND CONSEQUENCES OF PHENOLOGICAL
VARIATION
Elevation was a significant predictor of both mean and first
flight date, consistent with previous studies reporting later
© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 145–155
Host and climate constraints at range margins 153
emergence dates for insects at higher elevations (Fielding
et al. 1999; Crozier 2004; Hodkinson 2005). Elevation affects
mean temperature, potentially influencing the date of diapause cessation and rates of larval and pupal development
after hibernation. The differences in phenology in 2006 were
pronounced, with butterflies flying 30– 40 days later per 1 km
increase in elevation (Fig. 4).
Climate-driven changes to species phenology could affect
survival or fecundity, by shifting key stages of life cycles to
cooler or warmer times of the year (Wilson, Davies & Thomas
2007) or by disrupting biotic interactions (Ibáñez et al.
2006). Because A. crataegi butterflies fly later at higher elevations, the temperatures experienced by adults do not
decrease with altitude as sharply as might be predicted, all
else being equal. However, results from temperature dataloggers at transect sites show that mean daytime temperature during the local peak month of A. crataegi flight (i.e. the
temperatures experienced by egg-laying females, eggs and
young larvae) still decreased by 6·2 °C per 1 km increase in
elevation.
EGG-SITE LOCATION
At high elevations eggs were laid on the south side of host
plants, corresponding to hotter microclimates, whereas at
low elevations they were found on the north side of plants
(Fig. 5a), suggesting that egg-laying site may depend on
ambient temperature (Davies et al. 2006). Based on our
results for survivorship, the pattern could result from
selection on female oviposition behaviour for sites whose
microclimate favours the development and survival of
larvae (Gilbert & Singer 1977). Further experiments are
needed to confirm whether egg-site location in A. crataegi is
directly related to temperature during oviposition, or
whether egg-site choice and larval survival differ among
populations from different elevations, representing possible
local adaptation.
Further work is also required to determine whether additional
climatic variables influence egg-site selection. For example,
exposure to ultraviolet-B radiation (UV-B) can increase by
c. 20% per 1 km elevation (Blumthaler, Ambach & Ellinger
1997). UV-B can cause tissue damage in insect larvae
(Caldwell et al. 1998), and high levels of UV-B are avoided by
some insects (Mazza et al. 2002). In A. crataegi, there was an
indication that the proportion of egg batches laid on the
leaf upperside peaked at middle elevations (Fig. 5b), a pattern that could result if host plant leaves protect eggs from
UV-B. At low elevations, exposure both to UV-B and high
ambient temperatures might be reduced for eggs on the leaf
underside. Reduced ambient temperatures at increasing
elevations could then favour the upperside, but at the
highest elevations UV-B exposure may be so high that the
leaf underside is again favoured. Research is needed to
determine whether the effects of UV-B radiation on insect
development and survival could limit species’ ability to
track climate change, by preventing range shifts towards
higher elevations.
IMPLICATIONS OF CLIMATE CHANGE FOR SPECIALIST
SPECIES
Increasing temperatures are likely to drive the warm range
margin of A. crataegi away from low elevations, and the future
distribution of the species in the region will depend on its
ability to colonize high elevation sites. However, suitable host
plants might be unlikely to shift their distributions as quickly
in response to climate change. Recent research shows that a
broadening of host plant use by butterflies can increase rates
of range expansion at a landscape scale (Thomas et al. 2001).
The ability to exploit alternative host plants such as Rosa
spp., which have a much wider elevational range (see Supplementary material, Fig. S1), could greatly increase A. crataegi’s
ability to colonize high elevations. However, A. crataegi has
rarely been observed laying eggs on Rosa spp. in the region,
and our experimental transplants showed no evidence that
larvae are able to develop on these plants. Unless A. crataegi
can broaden its host plant use at higher elevations, it seems
inevitable that the species will experience an increasingly
restricted elevational range as the climate warms.
Bioclimate envelope models have been used to predict
future species distributions, based either on the geographical
range of suitable climate space or its overlap with currently
suitable conditions (e.g. Pearson & Dawson 2003; Thomas
et al. 2004). Our research emphasizes how, for specialist species such as many phytophagous insects, observed retractions
in potential or realized distributions are likely to be much
greater than previously estimated, because of reduced overlap
between host species and suitable climate (see Andrew &
Hughes 2004, 2005). Realistic models of future species
ranges should include the effects both of species’ physiological requirements and climatic associations, as well as those
of their key interacting species (Hodkinson 1999; Araújo &
Guisan 2006) or habitats (Franco et al. 2006).
Our work suggests that temperature is the most likely factor
determining the low elevation limit to A. crataegi’s distribution, whereas interacting species are responsible for its upper
elevation margin. This result contrasts with the prevailing
theory that species interactions determine warm limits to
species distributions, while direct climatic limitation imposes
the cool boundaries to species ranges (MacArthur 1972; Brown
et al. 1996; Parmesan et al. 2005). The clearest change to the
distribution of A. crataegi was the loss of populations from
elevations of 600–900 m, despite the continuing presence of
larval host plants. This distribution change is unlikely to
reflect the effects of adult resources, since during A. crataegi’s
June flight period the density of flowers does not increase with
elevation, and many nectar sources are available in the habitats sampled below 900 m (S. B. Díez, unpublished data).
Instead, we show that egg and young larval survival increases
with elevation, with > 75% estimated mortality below the current
lower elevation margin. Increased mortality at low elevations
because of increased temperatures in the region since 1967–
73 could represent a mechanism behind the range contraction
of A. crataegi, but further experimental work is needed to rule out
other competing explanations. For example, egg transplant
© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 145–155
154
R. M. Merrill et al.
experiments that exclude predators or parasitoids could be
particularly informative (e.g. Crozier 2004), as well as translocation experiments using the progeny of females from
lower elevation populations, to test for a potential role of
adaptation across the elevational range.
Predictions indicate further warming of up to 4 °C by
2100 (IPCC 2007), corresponding to a c. 650 m shift in the
elevational distribution of isotherms. Considering that A.
crataegi is currently restricted to a 900 m band in the Sierra de
Guadarrama and may have little capacity to move to higher
elevations, a considerable contraction of its current range
seems inevitable. If the distribution patterns revealed by this
study also apply to other areas in southern Europe and North
Africa where the species is restricted to mountains (García
Barros et al. 2004; J. Tennent, personal communication), then
the future of A. crataegi, and indeed other plant and animal
species with ranges limited in similar ways, may not be as
secure as its current widespread status implies.
Acknowledgements
We thank V. J. Monserrat for access to historical data, and J. Bridle and J.
Harcourt for assistance in the field. Funding to D.G., R.J.W. and J.G. was provided
by the Ministerio de Educación y Ciencia (grant reference CGL2005-06820/
BOS), Spain. R.M.M. was supported by an MSc studentship from the Biotechnology and Biological Sciences Research Council (BBSRC) and by a travel
grant from St Peter’s College, University of Oxford. O.T.L. is a Royal Society
University Research Fellow and was also supported by the Ernest Cook
Research Fellowship, Somerville College, University of Oxford. Access and
research permits were provided by Comunidad de Madrid, Parque Regional de
la Cuenca Alta de Manzanares, Parque Natural de Peñalara, and Parque
Regional del Curso Medio del Río Guadarrama.
References
Alonso, C. (1999) Variation in herbivory by Yponomeuta mahalabella on its only
host plant Prunus mahaleb along an elevational gradient. Ecological Entomology, 24, 371–379.
Andrew, N.R. & Hughes, L. (2004) Species diversity and structure of phytophagous beetle assemblages along a latitudinal gradient: predicting the
potential impacts of climate change. Ecological Entomology, 29, 527–542.
Andrew, N.R. & Hughes, L. (2005) Diversity and assemblage structure of phytophagous Hemiptera along a latitudinal gradient: predicting the potential
impacts of climate change. Global Ecology and Biogeography, 14, 249–262.
Araújo, M.B. & Guisan, A. (2006) Five (or so) challenges for species distribution modelling. Journal of Biogeography, 33, 1677–1688.
Asher, J., Warren, M., Fox, R., Harding, P., Jeffcoate, G. & Jeffcoate, S. (2001)
The Millennium Atlas of Butterflies in Britain and Ireland. Oxford University
Press, Oxford.
Bale, J.S., Masters, G.J., Hodkinson, I.D., Awmack, C., Bezemer, T.M.,
Brown, V.K., Butterfield, J., Buse, A., Coulson, J.C., Farrar, J., Good,
J.E.G., Harrington, R., Hartley, S., Jones, T.H., Lindroth, R.L., Press,
M.C., Symrnioudis, I., Watt, A.D. & Whittaker, J.B. (2002) Herbivory in
global climate change research: direct effects of rising temperatures on insect
herbivores. Global Change Biology, 8, 1–16.
Blumthaler, M., Ambach, W. & Ellinger, R. (1997) Increase in solar UV
radiation with altitude. Journal of Photochemistry and Photobiology, 39,
130 –134.
Brown, J.H., Stevens, G.C. & Kaufman, D.M. (1996) The geographic range:
size, shape, boundaries and internal structure. Annual Review of Ecology and
Systematics, 27, 597–623.
Bryant, S.R., Thomas, C.D. & Bale, J.S. (1997) Nettle-feeding nymphalid butterflies: temperature, development and distribution. Ecological Entomology,
22, 390–398.
Caldwell, M.M., Bjorn, L.O., Bornman, J.F., Flint, S.D., Kulandaivelu, G.,
Teramura, A.H. & Tevini, M. (1998) Effects of solar ultraviolet radiation on
terrestrial ecosystems. Journal of Photochemistry and Phytobiology, Series
B, Biology, 46, 40–52.
Crawley, M.J. (2002) Statistical Computing – an Introduction to Data Analysis
Using S-Plus. John Wiley & Sons, Chichester.
Crozier, L.G. (2004) Field transplants reveal summer constraints on a
butterfly range expansion. Oecologia, 141, 148–157.
Davies, Z.G., Wilson, R.J., Coles, S. & Thomas, C.D. (2006) Changing habitat
associations of a thermally constrained species, the silver-spotted skipper
butterfly, in response to climate warming. Journal of Animal Ecology, 75,
247–256.
Emmet, A.M. & Heath, J. (1989) The Moths and Butterflies of Great Britain
and Ireland, vol. 7, Part 1. Harley Books, Colchester.
Environmental Systems Research Institute (ESRI) (1996) Arc View Spatial
Analyst. Advanced Spatial Analysis Using Raster and Vector Data. Environmental Systems Research Institute, Redlands, CA.
Fielding, C.A., Whittaker, J.B., Butterfield, J.E.L. & Coulson, J.C. (1999)
Predicting responses to climate change: the effect of altitude on the phenology
of the spittlebug Neophilaenus lineatus. Functional Ecology, 12 (Suppl. 1),
65–73.
Franco, A.M.A., Hill, J.K., Kitschke, C., Collingham, Y.C., Roy, D.B., Fox, R.,
Huntley, B. & Thomas, C.D. (2006) Impacts of climate warming and habitat
loss on extinctions at species’ low-latitude range boundaries. Global Change
Biology, 12, 1545–1553.
García-Barros, E., Munguira, M.L., Martín Cano, J., Romo Benito, H.,
Garcia-Pereira, P. & Maravalhas, E.S. (2004) Atlas of the Butterflies of the
Iberian Peninsula and Balearic Islands (Lepidoptera: Papilionoidea & Hesperioidea). Sociedad Entomológica Aragonesa, Zaragoza, Spain.
Gaston, K.J. (2003) The Structure and Dynamics of Geographical Ranges. Oxford
University Press, Oxford.
Gilbert, L.E. & Singer, M.C. (1977) Butterfly ecology. Annual Review of Ecology
and Systematics, 6, 365–397.
Hampe, A. & Petit, R.J. (2005) Conserving biodiversity under climate change:
the rear edge matters. Ecology Letters, 8, 461–467.
Hill, J.K. & Hodkinson, I.D. (1995) Effects of temperature on phenological
synchrony and altitudinal distribution of jumping plant-lice (Hemiptera:
Psylloidea) on dwarf willow (Salix lapponum) in Norway. Ecological Entomology, 20, 237–244.
Hodkinson, I.D. (1999) Species response to global environmental change or
why ecophysiological models are important: a reply to Davis et al. Journal of
Animal Ecology, 68, 1259–1262.
Hodkinson, I.D. (2005) Terrestrial insects along elevation gradients: species
and community responses to altitude. Biological Reviews, 80, 489–513.
Ibáñez, I., Clark, J.S., Dietze, M.C., Feeley, K., Hersh, M., LaDeau, S.,
McBride, A., Welch, N.E. & Wolosin, N.S. (2006) Predicting biodiversity
change: outside the climate envelope, beyond the species–area curve. Ecology, 87, 1896–1906.
Intergovernmental Panel on Climate Change (IPCC) (2007) Climate Change
2007: the Physical Science Basis. Summary for Policymakers. UNEP Intergovernmental Panel on Climate Change, Geneva, Switzerland.
MacArthur, R.H. (1972) Geographyraphical Ecology: Patterns in the Distribution
of Species. Princeton University Press, Princeton, NJ.
Mazza, C.A., Izaguirre, M.M., Zavala, J., Scopel, A.L. & Ballaré, C.L.
(2002) Insect perception of ambient ultraviolet-B radiation. Ecology Letters,
5, 722–726.
McLaughlin, J.F., Hellmann, J.J., Boggs, C.L. & Ehrlich, P.R. (2002) Climate
change hastens population extinctions. Proceedings of the National Academy
of Sciences USA, 99, 6070–6974.
Monserrat, V.J. (1976) La distribución ecológica de las mariposas diurnas del
Guadarrama. Thesis, Universidad Complutense de Madrid, Madrid, Spain.
Nagelkerke, N.J.D. (1991) A note on a general definition of the coefficient of
determination. Biometrika, 78, 691–692.
NASA/JPL-Caltech (2004) Shuttle Radar Topography Mission. Available at:
http://www2.jpl.nasa.gov/srtm/ (acessed 9 June 2007).
Oksanen, J. & Minchin, P.R. (2002) Continuum theory revisited: what shape
are species responses along ecological gradients? Ecological Modelling, 157,
119–129.
Parmesan, C. (1996) Climate and species range. Nature, 382, 765–766.
Parmesan, C. (2005) Detection at multiple levels: Euphydryas editha and climate
change. Climate Change and Biodiversity (eds T.E. Lovejoy & L. Hannah),
pp. 56– 60. Yale University Press, New Haven CT/London.
Parmesan, C., Gaines, S., Gonzalez, L., Kaufman, D.M., Kingsolver, J., Peterson, A.T. & Sagarin, R. (2005) Empirical perspectives on species borders: from
traditional biogeography to global change. Oikos, 108, 58–75.
Pearson, R.G. & Dawson, T.P. (2003) Predicting the impacts of climate change
on the distribution of species: are bioclimatic envelope models useful? Global
Ecology and Biogeography, 12, 361–371.
Pollard, E. & Yates, T.J. (1993) Monitoring Butterflies for Ecology and Conservation. Chapman & Hall, London.
© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 145–155
Host and climate constraints at range margins 155
Randall, M.G.M. (1982) The dynamics of an insect population throughout its altitudinal distribution: Coleophora alticolella (Lepidoptera) in northern England.
Journal of Animal Ecology, 51, 993–1016.
Stefanescu, C., Peñuelas, J. & Filella, I. (2003) Effects of climate change on the
phenology of butterflies in the northwest Mediterranean Basin. Global
Change Biology, 9, 1494–1506.
Thomas, J.A. (1993) Holocene climate changes and warm man-made refugia
may explain why a sixth of British butterflies possess unnatural earlysuccessional habitats. Ecography, 16, 278–284.
Thomas, C.D., Bodsworth, E.J., Wilson, R.J., Simmons, A.D., Davies, Z.G.,
Musche, M. & Conradt, L. (2001) Ecological and evolutionary processes at
expanding range margins. Nature, 411, 577–581.
Thomas, C.D., Cameron, A., Green, R.E., Bakkenes, M., Beaumont, L.J.,
Collingham, Y.C., Erasmus, B.F.N., Ferreira de Siqueira, M., 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, 145–148.
Thomas, C.D., Franco, A.M.A. & Hill, J.K. (2006) Range retractions and
extinctions in the face of climate warming. Trends in Ecology and Evolution,
21, 415– 416.
Thomas, J.A., Rose, R.J., Clarke, R.T., Thomas, C.D. & Webb, N.R. (1999)
Intraspecific variation in habitat availability among ectothermic animals
near their climatic limits and their centres of range. Functional Ecology, 13,
55 – 64.
Tolman, T. & Lewington, R. (1997) Butterflies of Britain and Europe. HarperCollins, London.
Walther, G.-R., Berger, S. & Sykes, M.T. (2005) An ecological ‘footprint’ of
climate change. Proceedings of the Royal Society, Series B, 272, 1427–1432.
Walther, G.-R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C.,
Fromentin, J.-M., Hoegh-Guildberg, O. & Bairlein, F. (2002) Ecological
responses to recent climate change. Nature, 416, 389–395.
Weiss, S.B., Murphy, D.D. & White, R.R. (1988) Sun, slope and butterflies:
topographic determinants of habitat quality for Euphydryas editha bayensis.
Ecology, 69, 1486–1496.
Wilson, R.J., Davies, Z.G. & Thomas, C.D. (2007) Insects and climate change:
processes, patterns and implications for conservation. Insect Conservation
Biology (eds A.J.A. Stewart, T.R. New & O.T. Lewis). CABI Publishing,
Wallingford, UK.
Wilson, R.J., Gutiérrez, D., Gutiérrez, J., Martínez, D., Agudo, R. & Monserrat,
V.J. (2005) Changes to the elevational limits and extent of species ranges
associated with climate change. Ecology Letters, 8, 1138–1146.
Received 19 February 2007; accepted 19 July 2007
Handling Editor: Simon Leather
Supplementary material
The following supplementary material is available for this
article.
Appendix S1. Methods: Huisman–Olff–Fresco (HOF) models.
Table S1. HOF models for the elevational range of A. crataegi
and its host plants.
Fig. S1. The elevational range and abundance of Rosa spp.
(a) Proportion of occupied sites against elevation (km). (b) Rosa
abundance against site elevation.
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j.1365-2656.2007.01303.x
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© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 145–155