Journal of Animal

Ecology 2007
76, 415 423

Role of larval host plants in the climate-driven range

expansion of the butterfly Polygonia c-album

Blackwell Publishing Ltd

BRIGITTE BRASCHLER and JANE K. HILL

Department of Biology, PO Box 373, University of York, Heslington, York YO10 5YW, UK

Summary
1. Some species have expanded their ranges during recent climate warming and the
availability of breeding habitat and species dispersal ability are two important factors
determining expansions. The exploitation of a wide range of larval host plants should
increase an herbivorous insect species ability to track climate by increasing habitat
availability. Therefore we investigated whether the performance of a species on different
host plants changed towards its range boundary, and under warmer temperatures.
2. We studied the polyphagous butterfly Polygonia c-album, which is currently expanding
its range in Britain and apparently has altered its host plant preference from Humulus
lupulus to include other hosts (particularly Ulmus glabra and Urtica dioica). We investigated insect performance (development time, larval growth rate, adult size, survival)
and adult flight morphology on these host plants under four rearing temperatures (18
285 C) in populations from core and range margin sites.
3. In general, differences between core and margin populations were small compared
with effects of rearing temperature and host plant. In terms of insect performance, host
plants were generally ranked U. glabra U. dioica > H. lupulus at all temperatures.
Adult P. c-album can either enter diapause or develop directly and higher temperatures
resulted in more directly developing adults, but lower survival rates (particularly on the
original host H. lupulus) and smaller adult size.
4. Adult flight morphology of wild-caught individuals from range margin populations
appeared to be related to increased dispersal potential relative to core populations.
However, there was no difference in laboratory reared individuals, and conflicting results
were obtained for different measures of flight morphology in relation to larval host
plant and temperature effects, making conclusions about dispersal potential difficult.
5. Current range expansion of P. c-album is associated with the exploitation of more
widespread host plants on which performance is improved. This study demonstrates how
polyphagy may enhance the ability of species to track climate change. Our findings suggest
that observed differences in climate-driven range shifts of generalist vs. specialist species may
increase in the future and are likely to lead to greatly altered community composition.
Key-words: climate change, dispersal, distribution, host shift, Lepidoptera.
Journal of Animal Ecology (2007) 76, 415423
doi: 10.1111/j.1365-2656.2007.01217.x

Introduction
During current climate warming, some insect species
are expanding their distributions northwards to track
climate changes (Parmesan & Yohe 2003; Root et al.
2003). However, not all species are responding and the

2007 The Authors.

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Correspondence and present address: Brigitte Braschler, Biodiversity and Macroecology Group, Department of Animal
and Plant Sciences, University of Sheffield, Sheffield S10 2TN,
UK. E-mail: b.braschler@sheffield.ac.uk

ability of species to colonize newly available climatically

suitable habitats beyond their range margin is affected by
factors such as species dispersal ability and the availability of breeding habitat (Hill et al. 2001; Warren
et al. 2001).
Understanding insecthost plant interactions and the
causes and consequences of changing hosts is a central
theme in ecology (Ehrlich & Raven 1964; Thompson &
Pellmyr 1991). Shifts on to novel host plants are important
in sympatric speciation (Berlocher & Feder 2002), in
allowing species to colonize new habitats (Singer &

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Thomas 1996), and in allowing species to escape predators

(Murphy 2004). Shifts in host plant preferences of insects
also affect colonization rates within metapopulations
(Hanski & Singer 2001), although changes in host
plant use have rarely been considered in the context of
species ability to track climate changes (Thomas et al.
2001). Many species have more restricted niches
towards the edges of their ranges (Hengeveld & Haeck
1982; Brown 1984), but warmer temperatures might
facilitate the exploitation of a wider range of larval host
plants, or increase larval survival on certain host plants
(Hellmann 2002). This would increase species
abundance and habitat availability at range margins
and thus would increase range expansion rates, but
data are lacking.
Dispersal is important for successful colonization of
new habitats and there is evidence that evolutionary
increases in dispersal ability may occur in insect populations during range expansion (Thomas et al. 2001;
Hughes, Hill & Dytham 2003; Simmons & Thomas
2004). This is because colonists are usually not a random
selection of the source population but share a suite of
traits associated with increased dispersal ability (Haag
et al. 2005). Such increases in dispersal ability in margin
populations would be expected to promote range shifts
by increasing the likelihood of colonization of new
habitat, and may result in unexpectedly rapid range
expansion rates (Thomas et al. 2001). Not only may there
be evolutionary changes in dispersal, but the expression
of dispersal traits may vary under different environments.
For example, insects developing on poor-quality hosts may
show increased dispersal ability (Coll & Yuval 2004).
Thus, the dispersal ability of individuals in margin
populations may reflect not only colonization effects
but also the host plants utilized by larvae, but this has
not been considered previously.
Global climates are predicted to continue warming
by up to 58 C by the end of the twenty-first century
(IPCC 2001), and so understanding how insect development is affected by temperature and host plant use,
and how patterns of host plant use interact with
temperature, may be crucial for predicting species
ranges in the future. In this study, we investigate the
polyphagous butterfly Polygonia c-album (L.), which is
showing the greatest range expansion of any butterfly
in Britain during current climate warming (Asher et al.
2001). In Britain, this species apparently has altered its
host plant preference from hop Humulus lupulus L. to
include other hosts, particularly Wych elm Ulmus glabra
Hudson and common nettle Urtica dioica L. (Pratt 1986,
1987). In this study, we investigate how the flight
morphology and performance of the butterfly is affected
by temperature and host plant use. We test the hypothesis
that butterfly performance on U. glabra and U. dioica is
improved under warmer temperatures, and we investigate
whether or not the effects of temperature and performance
on different host plants differ between populations from a
site within the core of the distribution and a site at the
expanding range margin.

Materials and methods

In the early nineteenth century, Polygonia c-album was
widespread in Britain but subsequently underwent
dramatic range retraction (Pratt 1986, 1987). This contraction may have been associated with a reduction in
the cultivation of hops H. lupulus (the main larval host
plant), but climate cooling at the end of the nineteenth
century may also have been important, especially as
retraction occurred even in areas where hops were still
widely grown (Pratt 1987). From the 1940s onwards, the
climate has been warming and P. c-album has successfully
re-colonized most of England and Wales (Fig. 1). This
expansion has been associated with a shift in the preferred
host plant from H. lupulus to include the closely related
and widespread species Urtica dioica and Ulmus glabra
(Pratt 1986, 1987), host plants that are widely used by
P. c-album in other parts of Europe (e.g. Nylin & Janz
1993). Polygonia c-album overwinters as an adult and
develops through either one or two generations per year
in Britain depending on location. Voltinism is primarily
determined by environmental factors (e.g. day length,
host plant, temperature; Wiklund, Wickman & Nylin
1992; Wedell, Nylin & Janz 1997), although genetic
effects may also play a role.

During April 2004, adult females were collected from
two sites in Britain; a core site in south Wales (Wye
Valley, Ordnance Survey 10-km grid reference ST 59;
Fig. 1) where P. c-album apparently persisted during
the nineteenth century range contraction (Pratt 1987),
and a margin site in northern England (York, SE 53;
Fig. 1) which according to recent sightings was recolonized in 1993 (Biological Records Centre data,
CEH Monks Wood). Four females from each site were
used to establish breeding lines for experiments. We also
collected males from each study site, as well as from two
additional sites in central England (Nottingham, SK 63,
re-colonized in 1985; Fig. 1), and in north-east England
(Newcastle, NZ 15, re-colonized in 1995; Fig. 1). Overall,
we collected 12 females (four from Wye Valley, and eight
from York) and 35 males (six from Wye Valley, six from
Nottingham, 12 from York, and 11 from Newcastle).
All wild-caught individuals were used to investigate
differences in adult flight morphology among sites
in relation to range expansion. Four females from the
York site did not lay fertile eggs and were also included
in this analysis.

Wild-collected females were allowed to lay eggs on potted
U. dioica plants in a greenhouse. In order to produce
sufficient insect material for the rearing experiments
and to maintain genetic diversity, F1 female offspring

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Fig. 1. Recent range expansion and present distribution of Polygonia c-album in Britain, and location of study sites. Distribution
records (10-km grid resolution) are plotted for two time periods corresponding with the publication of two butterfly atlases
(Heath, Pollard & Thomas 1984; Asher et al. 2001). Collection sites are from north to south: Newcastle (re-colonized in 1995),
York (1993), Nottingham (1985) and Wye Valley (core site). Females from York and Wye Valley were used in the laboratory
experiments, wild-caught individuals from all sites were used to determine differences in flight morphology between core and
range margin sites. Histogram bars show the number of 10-km Ordnance Survey grid cells with records of the species for each
decade of the twentieth century (P. c-album distribution data provided from the Butterflies for the New Millennium project,
courtesy of Butterfly Conservation and Biological Records Centre).

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from wild-caught females were mated with F1 male

offspring from a different mother, but the same site, to
create nine different F2 families per site.
We used a split-brood design to examine the effects of
host plant and temperature on performance and flight
morphology. Upon hatching, first instar larvae from each
of the 18 families were split equally among the three
different host plants (H. lupulus, U. dioica and U. glabra)
and four different temperatures (18 C, 215 C, 25 C
and 285 C (1 C); Sanyo MLR-350 growth cabinets).
Approximately eight to 11 larvae of the same age from the
same female were reared together in plastic containers
and provided daily with excess freshly cut young leaves
of host plants in vials of water (yielding 18 containers
with larvae (nine containers per site) in each of the 12
temperature by host plant treatments). Occasionally when
larvae fed very heavily, or when wilting was observed,
leaves were replaced up to twice daily. All leaves were
from young plants and were thus likely to be of high
nutritional quality. All larvae were reared under a long
photoperiod (20L : 4D) to maximize the incidence of
nondiapausing individuals. Upon pupation, individuals
were weighed and reared individually in plastic tubes under

the same light and temperature conditions as larvae.

Adults were killed by freezing within 12 h of emergence
after allowing time for wing expansion and release of pupal
waste products. After thawing, adult body parts were
dried at 60 C for 24 h and then weighed on a Sartorius
electrobalance (sensitivity 01 g). The sex and adult morph
(directly developing vs. diapausing) of all individuals
were determined. Directly developing morphs can be
identified easily by their lighter coloration.

Direct measures of dispersal are difficult to obtain in
insects (particularly in highly mobile species such as
P. c-album) and many studies have thus inferred dispersal
potential from indirect measures of adult flight morphology. In butterflies, individuals with greater flight
ability generally have relatively larger, broader thoraxes
(comprising predominantly flight muscle, e.g. Berwaerts,
Van Dyck & Aerts 2002). Therefore measures of adult
flight morphology were used in this study as an index
of dispersal ability. We measured thorax shape (width

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divided by length) in both wild-caught and laboratory

reared individuals. Thorax mass is likely to change with
age and so we only measured this variable in laboratory
reared individuals that were killed on emergence.
The following variables were used to assess insect
performance in different treatments: larval growth rate
(pupal fresh mass divided by time from hatching to
pupation), development time (time from hatching of the
larva until emergence of adult), adult dry mass, abdomen
dry mass and survival (proportion surviving from first
instar larva to adult). Adult mass is likely to be a good
indicator of host plant quality with larger butterflies
developing on higher quality plants being expected to
be more fecund, better competitors for mates, and able
to disperse over longer distances. Repeated measurements
for all mass variables proved to be reliable (less than 5%
difference). Physiological trade-offs between flight
and reproduction are expected such that individuals
with relatively large thoraxes are likely to be less fecund
(Hughes et al. 2003; but see Hanski, Saastamoinen &
Ovaskainen 2006). Growth rate in butterflies is related
to temperature (Wedell et al. 1997; Gotthard 2004) and
host plant quality (Janz, Nylin & Wedell 1994). It also
affects developmental pathway (diapause vs. direct development; Wedell et al. 1997) and thus will affect population
growth rate and size, and therefore range expansion.

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General Linear Mixed Models were used to examine

the effect of population (core vs. margin), temperature
(18 C, 215 C, 25 C, 285 C), host plant (H. lupulus,
U. glabra, U. dioica), sex, and developmental pathway
(direct development vs. diapause) on variables associated
with dispersal ability (thorax shape, relative thorax mass)
and performance (development time, adult mass, larval
growth rate, relative abdomen mass). Additional analyses
on pupal fresh weight and time to pupation were also
performed but generally gave the same results as those
for adult mass and time to adult development and are
thus not presented in depth. Interaction effects between
population and host plant, population and temperature,
host plant and temperature, and the threefold interaction
between population, host plant and temperature were
also included in analyses. Family effects were nested
within the population term and included as random
effects. TukeyKramer tests were used to test for differences between treatments. Some variables showed
allometric relationships and so we included total adult
body mass as a covariate in analyses of thorax mass
and abdomen mass.
To examine the effects of rearing treatments on the
propensity of individuals to enter diapause, a Generalized
Linear Mixed Model similar to those described above
was used but with a binomial error distribution and a logit
link function. A simplified version of this model was
used for analysing the effects of population, rearing
temperature, and host plant on survival as the sex was
known only for individuals that reached pupation, and

developmental pathway was known only for individuals

that reached adulthood. Family effects were nested
within the population term and included as random
effects in the analysis of developmental pathway but
could not be included in the analysis of survival as the
design of the experiment did not allow differentiation
between family and treatment effects in this respect.
Where appropriate, variables were ln-transformed
for analyses. SAS vs. 81 was used for all analyses. The
glimmix macro was used for Generalized Linear Mixed
Models with a binomial error distribution (Littell et al.
1996). We sampled only one core and one margin location,
and so analysing data for individual P. c-album may lead
to pseudo-replication. However, P. c-album is highly mobile
and so sampled individuals are probably representative
of a relatively large geographical area.

Results
In total, we analysed data from 1252 F2 laboratory
reared individuals and from 47 wild-caught adults. Overall, females had broader thoraxes than males (F1,1038 = 906,
P = 00027) but males had relatively heavier thoraxes
than females (F1,1035 = 117267, P < 00001), indicating no
clear pattern in our indices of dispersal ability between
the sexes. Larval growth rates did not differ between the
sexes, but adult males completed their development faster
than females (F1,1035 = 1592, P < 00001) because they
were smaller than females (F1,1036 = 6608, P < 00001).

Wild-caught individuals were collected in spring and so

were the diapausing morph, although directly developing
individuals have been reported from all study sites. In the
rearing experiments, there was no significant difference
between core and margin populations in the percentage
of individuals that entered diapause (458% vs. 319%;
F1,16 = 240, P = 01409). Individuals entering diapause
had broader and relatively heavier thoraxes (thorax
shape: F1,1038 = 1602, P < 0001; thorax mass: F1,1035 =
2576, P < 00001) indicating greater dispersal ability.
Males had a greater propensity to enter diapause compared with females (514% vs. 243%; F1,1039 = 10742,
P < 00001; Fig. 2), and adults entering diapause had
lower larval growth rates (F1,1038 = 3512, P 00001), and
longer development times (F1,1035 = 28764, P < 00001).
Overall, the host plant did not directly affect the
propensity of individuals to diapause, although this was
approaching significance (F2,1039 = 296, P = 00525),
but higher temperatures greatly increased the likelihood
that individuals developed directly (F3,1039 = 5206, P <
00001; Fig. 2). A significant host plant by temperature
interaction showed that at higher temperatures individuals
were more likely to develop directly on U. glabra and U.
dioica, but at lower temperatures individuals were more
likely to develop directly on H. lupulus (host plant
temperature interaction: F6,1039 = 689, P 00001; Fig. 2).

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Host plant and
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Fig. 2. Proportion of directly developing P. c-album adults from a range margin (hollow bars) and core (solid bars) population
reared under four different temperatures and on three different host plants. Upper row: females, lower row: males. Ug = U. glabra,
Hl = H. lupulus, Ud = U. dioica.

Fig. 3. Thorax shape of wild-caught individuals from a core

site and three newly colonized sites. Higher values correspond
to relatively broader thoraxes and indicate greater dispersal
ability. Mean values with standard errors for males (solid
symbols) and females (hollow symbols) are shown separately.
Data for females are displaced slightly for clarity. Numbers by
data points indicate sample sizes.

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In wild-caught individuals, there was an increase in

thorax breadth in individuals from populations from
the core to the range margin, suggesting increased dispersal ability at the range margin (regression for males
from four sites, weighted by sample size; F1,3 = 5290,
P = 0018, R2 = 096; Fig. 3). This effect was not evident
in wild-caught females (t-test comparing females from
two study sites; t10 = 150, P = 016; Fig. 3), although
this analysis lacked power due to the small sample sizes
and few sites sampled.
In laboratory reared butterflies, adult flight morphology (relative thorax mass, thorax shape) did not differ
significantly between core and margin populations. How-

ever, larval host plant and temperature had significant

but opposite effects on relative thorax mass and thorax
shape. Thus butterflies reared under higher temperatures
and on H. lupulus had relatively broader thoraxes (temperature effect, F3,1038 = 1139, P < 00001; host plant
effect, F2,1038 = 924, P = 00001) but relatively small thoraxes (temperature effect, F3,1035 = 2266, P < 00001;
host plant effect, F2,1035 = 2365, P < 00001). This makes
it difficult to deduce the impacts of host plant and temperature on flight morphology. There were also significant
interactions between host plant and temperature on
thorax shape (host plant temperature interaction:
F6,1038 = 413, P = 00004) and on relative thorax mass
(F6,1035 = 1016, P < 00001). Thus, individuals reared on
H. lupulus had increasingly broader but smaller thoraxes
at higher temperatures. There was also a significant
interaction between population and larval host plant on
relative thorax mass (population host plant interaction:
F2,1035 = 444, P = 00120). Thus individuals from the
core had relatively larger thoraxes on U. glabra but no
such difference was evident in the margin population.

Survival decreased with increasing temperature (F3,1150 =
622, P = 00003; Fig. 4) and was poorest on H. lupulus
compared with the other two host plants (F2,1150 = 3003,
P < 00001). Lower survival on H. lupulus was most
evident at high temperatures (285 C: 81% survival on
H. lupulus vs. 446% on U. glabra and 490% on U. dioica;
Fig. 4) while survival was similarly high on all three host
plants at low temperatures (e.g. 18 C: 606% survival on
H. lupulus vs. 636% on U. glabra and 676% on U. dioica;
temperature host plant interaction: F6,1150 = 283,
P = 00096; Fig. 4).
In general, effects of temperature and host plant were
similar between core and margin populations. Overall,
performance on the novel host plants was much better
than on H. lupulus regardless of temperature treatment
or population. However, there were some differences in
the ranking of the two novel larval host plants. While there

420
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& J. K. Hill

Fig. 4. Survival of P. c-album from a range margin (hollow bars) and core (solid bars) population reared under four different
temperatures and on three different host plants. Ug = U. glabra, Hl = H. lupulus, Ud = U. dioica.

Table 1. Performance of P. c-album on three different host plants (H. lupulus = original host, U. glabra and U. dioica are new
hosts). Results from Generalized Linear Models on ln-transformed variables. Back-transformed mean SEs are shown
Larval host plant

Larval growth rate (mg day1)

Time to pupation (days)
Pupal fresh mass (mg)
Development time (days)
Adult dry mass (mg)

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415423

H. lupulus

U. glabra

U. dioica

d.f.

110 10
206 10
2262 10
313 10
328 10

161 10
172 10
2765 10
262 10
448 10

146 10
185 10
2700 10
271 10
463 10

2
2
2
2
2

16355
4706
13118
2852
25220

< 00001
< 00001
< 00001
< 00001
< 00001

was no difference in performance on either U. glabra or

U. dioica in the core population, development time on
U. glabra was shorter than on U. dioica at the range
margin (TukeyKramer tests for difference between novel
host plants; core: t1035 = 025, P = 099, margin: t1035 =
625, P < 00001). This resulted in higher growth rates
on U. glabra than on U. dioica in the margin population
(TukeyKramer tests for difference between novel host
plants; core: t1038 = 226, P = 021, margin: t1038 = 739,
P < 00001). These findings support anecdotal reports
of the butterflies preference for U. glabra in northern
Britain. However, there were no differences in adult mass
in either population on the two novel host plants,
although adult mass was always much larger than on the
original host H. lupulus. Increased temperatures resulted
in higher larval growth rates (F3,1038 = 19577, P < 00001),
decreased development times (F3,1035 = 184109, P <
00001), and smaller adults (F3,1036 = 9426, P < 00001).
This indicated a trade-off between development time and
adult size. However, individuals reared on H. lupulus had
the slowest larval growth rates, the longest development
times, but also produced the smallest adults (Table 1).
In adult butterflies, thorax mass and abdomen mass
comprise c. 70% of total mass and therefore conditions
that resulted in increased investment in the thorax resulted
in decreased investment in the abdomen. Thus, relative
abdomen mass was smallest in individuals reared under
low temperatures (F3,1035 = 3190, P < 00001) and on
U. glabra (F2,1035 = 3388, P < 00001). However, a
significant interaction between host plant and rearing
temperature showed that the ranking of the host plants
changed with temperature. Individuals on H. lupulus
were generally small in terms of total mass (Table 1),
but had increasingly larger abdomens with increasing

temperatures compared with the other larval host plants

(temperature host plant interaction: F6,1035 = 1394,
P < 00001). Thus at the highest temperatures, individuals
on H. lupulus invested more in their abdomens compared
with those on U. glabra and U. dioica. A significant
population host plant interaction indicated that
ranking of larval host plants also differed between the
two populations; individuals in the core had relatively
large abdomens on both H. lupulus and U. dioica, whereas
at the margin they only had relatively large abdomens
on U. dioica (F2,1035 = 493, P = 00074).

Discussion
Polygonia c-album has shown the fastest rate of range
expansion of any resident butterfly species in Britain
during recent climate warming and is one of only a few
species that appears to be tracking climate changes
(Warren et al. 2001). In this study, we showed that both
adult flight morphology and insect performance depended
on the host plant used, as well as on temperature during
development (Janz et al. 1994; Wedell et al. 1997). In
addition, there were interaction effects between temperature and host plant, as well as between host plant and
population, showing that the consequences of developing
on different host plants may vary across the species
range, and with climate change. Overall, both novel
hosts were better than H. lupulus but U. glabra was the
superior host in the margin population while there were
few differences between U. glabra and U. dioica in the
core population. Interestingly, feeding on H. lupulus
led to greatest investment in the abdomen in the core
population, but was inferior to U. dioica in the margin
population. Thus the only instance where we found

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that the original host plant may be preferable in some

respect to the novel hosts was in the core population.

Individuals from recently founded populations at the
expanding range margin would be expected to have greater
dispersal ability compared with individuals from core
populations (Thomas et al. 2001; Travis & Dytham 2002;
Simmons & Thomas 2004). Indeed flight morphology
in wild-caught males indicated higher dispersal ability
at the range margin in this study. This was apparently due
to different environmental conditions at the study sites
(e.g. habitat quality) rather than due to any evolutionary
changes during range expansion because differences in
flight morphology were not evident between core and
margin populations when individuals were reared under
controlled conditions in the laboratory. Moreover, in
laboratory reared individuals, measures of thorax shape
and relative thorax mass gave conflicting results. Although
measures of flight morphology have been successfully
used in the past to deduce dispersal potential (Berwaerts
et al. 2002) our findings suggest that the relation between
thorax mass and shape is not straightforward in this
species. Wild-caught material was obtained from sites
spanning a greater range of distances from the range
margin, and thus may have had increased genetic
variation compared with laboratory reared individuals,
which may have affected our results. However, given that
few differences between core and margin populations were
detected in any of our measures of insect performance
it is possible that evolutionary changes during range
expansion play a minor role in such a mobile species
(Nylin et al. 2005). The absence of a clear adaptation to
the original host in the core population could also be
explained by high mobility and gene flow back into
the core.

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415423

In Britain, adults emerging in summer can either enter

diapause or develop through a second generation before
diapausing. The ability to develop through two generations per year will increase population growth
rates (Crozier 2004) and thus rates of range expansion
(Fric & Konvicka 2002). In our experiment, diapausing
individuals were more likely under cooler temperatures.
Previous studies on P. c-album have shown that host
plants affect the propensity to enter diapause through
effects on larval growth rates (Wedell et al. 1997). The
absence of a significant host plant effect on diapause in
our study may indicate that for British P. c-album there
is often sufficient time for a second generation even
when using a suboptimal host such as H. lupulus.

In relation to insect performance, host plants were
generally ranked U. glabra U. dioica > H. lupulus and

this ranking was not significantly affected by temperature. Differences between U. glabra and U. dioica were
relatively small compared with large differences between
these two host plants and H. lupulus, which was the
poorest host plant. Individuals on U. glabra completed
their development the fastest, and individuals reared
on U. glabra and U. dioica also had higher survival and
larger adult size than those on H. lupulus, confirming
that U. glabra and U. dioica are high ranking host plants
for P. c-album (Nylin & Janz 1993; Janz et al. 1994; Nylin
& Janz 1996; Nylin, Bergstrom & Janz 2000). Higher
temperatures also increased the proportion of directly
developing individuals on both of these host plants.
Thus overall we would expect the use of U. glabra and
U. dioica to increase the rate of range expansion of
P. c-album relative to using H. lupulus, especially under
increasing temperatures.
There is little information on the degree to which
P. c-album utilized U. dioica or U. glabra historically in
Britain except for anecdotal evidence that the first
generation may have used U. dioica early in the season
when H. lupulus had not yet developed sufficiently (Pratt
1987). However, the ability to exploit different host plants
may be facilitated if larvae retain the ability to develop on
former host plants even when the oviposition preferences
of the adults change (Janz, Nyblom & Nylin 2001). For
example, P. c-album is now exploiting U. dioica, which is
an ancestral host plant that is exploited by many other
closely related Nymphalini species and is also used by
many European populations of P. c-album (Janz et al.
2001). In addition, the three host plants examined in this
study are all closely related and comprise an ancestral
host plant clade for Polygonia species (Weingartner,
Wahlberg & Nylin 2006) and this may also explain the
shift on to new host plants by this species.
P. c-album uses different host plants throughout its
European range, and the degree of specialization on
different host plants varies geographically (Janz 1998).
H. lupulus is apparently the historically preferred host
plant in Britain (Pratt 1986, 1987), but our results showed
it is generally a poor host plant in both core and margin
sites. However, an historical advantage of H. lupulus may
have been its wide availability through cultivation for
the beer industry, particularly if such sites were situated
in warm locations (e.g. south-facing slopes). In addition,
our laboratory reared larvae were provided with highquality young leaves from a single location, but plant
quality may vary across the butterfly range, or with
temperature, and this deserves further study.
Further range expansion of P. c-album will be influenced
by the distribution of the host plant species within
Britain. H. lupulus is common in the south of Britain where
P. c-album is now ubiquitous, but is rare in the north
where the other host plants occur widely (Preston,
Pearman & Dines 2002). H. lupulus may increase its
distribution with climate warming, but exploitation of
U. dioica and U. glabra that occur widely in northern
Britain will allow the mobile insect to colonize new areas
without waiting for range expansion of its original

422
B. Braschler
& J. K. Hill

host. Thus future range expansion of P. c-album does not

appear to be limited by host plant availability and the
present range expansion is likely to continue.

Species are predicted to shift their distributions polewards
in order to track future climate warming (Hill, Thomas
& Huntley 1999; Hill et al. 2002; Thomas et al. 2004).
However, range shifts are likely to be limited to mobile
generalists, such as P. c-album, where range expansion
is not limited by the loss and fragmentation of natural
habitats (Warren et al. 2001). Results from this study
illustrate the flexibility of polyphagous generalist species
and demonstrate how the incorporation of novel host
plants into larval diets may result in species having
greatly enhanced abilities to track climatic changes. Our
results indicate that this flexibility may lead to unexpectedly rapid range expansion in generalist species, and
that current host plant preferences may underestimate
future range changes in some species. The degree to which
similar host-plant shifts will occur in other species
remains to be seen, but such shifts are likely to be the
exception rather than the rule. What is more clear is
that tracking of twenty-first century climate warming is
likely to be restricted to generalist and mobile species
of relatively low conservation value, and that this may
lead to greatly altered community composition in the
future (Menndez et al. 2006).

Acknowledgements
We would like to thank the Forestry Commission and
Tilhill Forestry Ltd for permission to work at their
sites. Sren Nylin and Nina Wedell gave helpful advice
on insect rearing, and Tim Yardley helped setting up
the experiment. We thank Butterfly Conservation and
the Biological Records Centre (CEH-Monks Wood) for
P. c-album distribution data. Comments by Thomas
Merckx and two anonymous referees improved an
earlier version of the manuscript. The project was
funded by NERC.

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Received 26 October 2006; accepted 10 January 2007