The roles of acclimation and behaviour in buffering climate change impacts along elevational gradients

Abstract

The vulnerability of species to climate change is jointly influenced by geographic phenotypic variation, acclimation and behavioural thermoregulation. The importance of interactions between these factors, however, remains poorly understood.
We demonstrate how advances in mechanistic niche modelling can be used to integrate and assess the influence of these sources of uncertainty in forecasts of climate change impacts.
We explored geographic variation in thermal tolerance (i.e. maximum and minimum thermal limits) and its potential for acclimation in juvenile European common frogs Rana temporaria along elevational gradients. Furthermore, we employed a mechanistic niche model (NicheMapR) to assess the relative contributions of phenotypic variation, acclimation and thermoregulation in determining the impacts of climate change on thermal safety margins and activity windows.
Our analyses revealed that high-elevation populations had slightly wider tolerance ranges driven by increases in heat tolerance but lower potential for acclimation. Plausibly, wider thermal fluctuations at high elevations favour more tolerant but less plastic phenotypes, thus reducing the risk of encountering stressful temperatures during unpredictable extreme events. Biophysical models of thermal exposure indicated that observed phenotypic and plastic differences provide limited protection from changing climates. Indeed, the risk of reaching body temperatures beyond the species' thermal tolerance range was similar across elevations. In contrast, the ability to seek cooler retreat sites through behavioural adjustments played an essential role in buffering populations from thermal extremes predicted under climate change. Predicted climate change also altered current activity windows, but high‐elevation populations were predicted to remain more temporally constrained than lowland populations.
Our results demonstrate that elevational variation in thermal tolerances and acclimation capacity might be insufficient to buffer temperate amphibians from predicted climate change; instead, behavioural thermoregulation may be the only effective mechanism to avoid thermal stress under future climates.

Full text

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wileyonlinelibrary.com/journal/jane J Anim Ecol. 2020;89:1722–1734.© 2020 British Ecological Society
Received: 17 December 2019
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Accepted: 29 Februar y 2020
DOI : 10.1111/136 5-265 6.13222
RESEARCH ARTICLE
The roles of acclimation and behaviour in buffering climate
change impacts along elevational gradients
Urtzi Enriquez-Urzelai1,2 | Reid Tingley3,4 | Michael R. Kearney4 |
Martina Sacco1,2 | Antonio S. Palacio1,2 | Miguel Tejedo5 | Alfredo G. Nicieza1,2
1Departamento de Biología de Organismos
y Sistemas, Universidad de Oviedo, Oviedo,
Spain
2Research Unit of Biodiversity (UO-CSIC-
PA), Campus de Mieres, Mieres, Spain
3School of Biological Sciences, Monash
University, Clayton, Vic., Australia
4School of BioSciences, The University of
Melbourne, Parkville, Vic., Australia
5Department of Evolutionary Ecology,
Estación Biológica de Doñana, CSIC, Sevilla,
Spain
Correspondece
Urtzi Enriquez-Urzelai
Email: urtzi.enriquez@gmail.com
Funding information
Ministerio de Economía y Competitividad,
Grant/Award Number: BES-2013-063203,
CGL2012-40246-C02-01, CGL2012-
40246-C02-02 and CGL2017-86924-P;
ARC Discovery Early Career Researcher
Award
Handling Editor: Katharine Marske
Abstract
1. The vulnerability of species to climate change is jointly influenced by geographic
phenotypic variation, acclimation and behavioural thermoregulation. The impor-
tance of interactions between these factors, however, remains poorly understood.
2. We demonstrate how advances in mechanistic niche modelling can be used to
integrate and assess the influence of these sources of uncertainty in forecasts of
climate change impacts.
3. We explored geographic variation in thermal tolerance (i.e. maximum and
minimum thermal limits) and its potential for acclimation in juvenile European
common frogs Rana temporaria along elevational gradients. Furthermore, we
employed a mechanistic niche model (NicheMapR) to assess the relative con-
tributions of phenotypic variation, acclimation and thermoregulation in deter-
mining the impacts of climate change on thermal safety margins and activity
windows.
4. Our analyses revealed that high-elevation populations had slightly wider toler-
ance ranges driven by increases in heat tolerance but lower potential for ac-
climation. Plausibly, wider thermal fluctuations at high elevations favour more
tolerant but less plastic phenotypes, thus reducing the risk of encountering
stressful temperatures during unpredictable extreme events. Biophysical mod-
els of thermal exposure indicated that observed phenotypic and plastic dif-
ferences provide limited protection from changing climates. Indeed, the risk
of reaching body temperatures beyond the species' thermal tolerance range
was similar across elevations. In contrast, the ability to seek cooler retreat
sites through behavioural adjustments played an essential role in buffering
populations from thermal extremes predicted under climate change. Predicted
climate change also altered current activity windows, but high-elevation popu-
lations were predicted to remain more temporally constrained than lowland
populations.
5. Our results demonstrate that elevational variation in thermal tolerances and ac-
climation capacity might be insufficient to buffer temperate amphibians from
predicted climate change; instead, behavioural thermoregulation may be the only
effective mechanism to avoid thermal stress under future climates.

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ENRIQUE Z-URZELA I Et AL.
1 | INTRODUCTION
Anthropogenic climate change is a major threat to global biodiver-
sity, stimulating numerous attempts to predict the vulnerability of
populations, species and ecosystems (Buckley & Kingsolver, 2012;
McCain & Colwell, 2011; Orizaola & Laurila, 2016; Thomas et al.,
2004; Williams, Jackson, & Kutzbacht, 2007). Projected rates of
climate change may hinder species' abilities to adapt to novel con-
ditions or to track their climatic requirements through dispersal
(Araújo, Thuiller, & Pearson, 2006; Quintero & Wiens, 2013). Thus,
intraspecific phenotypic variation, acclimation and behavioural ther-
moregulation are critical for species' persistence in a warming cli-
mate (Kearney, Shine, & Porter, 2009; Richter-Boix et al., 2015).
Macrophysiological studies on the vulnerability of ectotherms
to climate change have flourished in recent years, largely due to
an increasing availability of physiological data and fine-resolution
climate layers. Many of these studies have suggested that species
occupying warmer and more stable environments will be dispro-
portionately vulnerable to warming (i.e. species occupying lower
elevations and latitudes; Deutsch et al., 2008; Duarte et al., 2012;
Tewksbury, Huey, & Deutsch, 2008; but see Overgaard, Kearney,
& Hoffmann, 2014; Overgaard, Kristensen, Mitchell, & Hoffmann,
2011). A number of recent investigations have challenged this view,
however, demonstrating that thermal safety margins (i.e. the dif-
ference between experienced maximum temperatures and heat
tolerance, sensu Sunday et al., 2014) and acclimation potential of
species from high elevations and latitudes may not be as high as
previously thought (Gerick, Munshaw, Palen, Combes, & O'Regan,
2014; Gunderson, Dillon, & Stillman, 2017; Gunderson & Stillman,
2015; Sunday et al., 2014). In addition, intraspecific variation in
environmental tolerances, acclimation capacity and the potential
for behavioural thermoregulation to buffer species from thermal
extremes have largely been overlooked in forecasts of species'
responses to climate change (Buckley, Ehrenberger, & Angilletta,
2015; Valladares et al., 2014).
Environmentally driven phenotypic and genetic variation among
populations is widespread (Conover & Schultz, 1995; Linhart & Grant,
1996). Yet, compromises between local adaptation, acclimation and
behavioural thermoregulation are emerging as key determinants of
vulnerability to climate change. Behavioural thermoregulation may
weaken selection on thermal tolerance and the potential for thermal
acclimation—a process known as the ‘Bogert effect’ (Bogert, 1949;
Huey, Hertz, & Sinervo, 2003; Huey & Kingsolver, 1993; Muñoz &
Losos, 2018). Furthermore, local adaptation to warmer environ-
ments may reduce acclimation potential (Stillman, 2003; but see
Calosi, Bilton, & Spicer, 2008). The trade-off between high tolerance
and reduced potential for acclimation of thermal performance may,
in turn, increase the vulnerability of populations to environmental
change (Buckley et al., 2015; Gunderson & Stillman, 2015). Thus, we
need to develop a deeper understanding of geographic variation in
thermal tolerances, acclimation potential and behavioural thermo-
regulation, as well as an increased appreciation of their potential
interconnections.
In ectotherms, daily and seasonal thermal fluctuations exert
strong selective pressures on thermal traits (Gutiérrez-Pesquera
et al., 2016; Richter-Boix et al., 2015). This could partly explain the
observed wider thermal tolerance breadths (i.e. the difference be-
tween maximum and minimum critical thermal limits) towards higher
elevations and latitudes (Addo-Bediako, Chown, & Gaston, 2000;
Gutiérrez-Pesquera et al., 2016; but see Brattstrom, 1968). Shorter
growing season lengths at high elevations and latitudes also restrict
the time available for growth and development (Dahl, Orizaola,
Nicieza, & Laurila, 2012). Consequently, individuals may need to ex-
pose themselves to large daily thermal fluctuations to exploit tran-
sient food re source s (Nic ieza & Metcal fe, 1997). In doing so, howeve r,
organismal body temperatures could approach critical thermal limits.
Accurate prediction of these risks for terrestrial species requires an
understanding of the processes of heat exchange (i.e. convection,
radiation, conduction, evaporation and metabolism; Heath, 1964;
Kearney & Porter, 2009; Tracy, 1976) and behavioural thermoregu-
lation; air temperatures alone may be uninformative of these events.
Moreover, the choice of appropriate spatial and temporal scales is
crucial to capture effective thermal environments and extreme tem-
peratures that, however short, may be more important than the daily
average in constraining a species' or a population's long-term per-
sistence (Gerick et al., 2014; Kearney, Matzelle, & Helmuth, 2012).
Here we experimentally study geographic variation in thermal
tolerance limits and the effects of thermal acclimation on those
limits in a temperate amphibian species. Amphibians are one of the
most vulnerable groups to global change, including climate change.
Our study models were juvenile European common frogs Rana
temporaria from populations distributed along elevation gradients.
We chose this life cycle stage because it has been understudied
despite being one of the weakest links in terms of climate change
impacts. Newly metamorphosed individuals must rapidly gain struc-
tural size and reserves prior to the onset of winter, but high summer
temperatures can impose severe temporal restrictions since they are
predominantly diurnal (Vences et al., 2000), and are thus more likely
to encounter highly stressful temperatures than are the nocturnal
adult or aquatic larval life stages. Moreover, the thermal tolerance
of newly metamorphosed amphibians is typically lower than that of
larval or adult stages, very likely due to the energetic costs of meta-
morphosis (Cupp, 1980; Enriquez-Urzelai et al., 2019; Lambrinos &
Kleier, 2003; Navas, Antoniazzi, Carvalho, Suzuki, & Jared, 2007).
Thus, a trade-off can arise between overwintering survival (en-
hanced by growth and reserve accumulation) and summer survival
KEY WORDS
acclimation, activity restrictions, behavioural thermoregulation, Bogert effect, global warming,
mechanistic niche modelling, NicheMapR, thermal-safety margins

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ENRIQUE Z-URZELA I Et AL.
(subjected to physiological constraints, i.e. thermal tolerance and
evaporative water loss). Therefore, global warming will likely in-
crease the risk of thermal stress for juvenile amphibians.
To realistically capture the potential thermal extremes expe-
rienced by juvenile amphibians, we apply a thermodynamically
grounded mechanistic niche model (NicheMapR v1.3; Kearney,
Munns, Moore, Malishev, & Bull, 2018; Kearney & Porter, 2017,
2020; Porter, Mitchell, Beckman, & DeWitt, 1973) in combina-
tion with daily gridded weather data for Europe (Brinckmann,
Krähenmann, & Bissolli, 2016; Haylock et al., 2008). NicheMapR
integrates a microclimate model of the conditions above- and
below-ground for a certain level of shade, with an animal biophys-
ical model that solves coupled heat- and mass-balance equations
to predict constraints on body temperatures given an individual's
behaviour, morphology and available microclimates. Specifically, we
address the following questions: (a) Do juvenile R. temporaria dif-
fer in thermal tolerance and acclimation potential along elevational
gradients? (b) How does geographic variation in phenotype, accli-
mation potential and behavioural thermoregulation influence the
species' vulnerability to climate change? (c) How will exposure to
thermal stress and resulting activity restrictions vary with climate
change at different elevations?
2 | MATERIALS AND METHODS
2.1 | Study system
Rana temporaria is widespread through most of Europe and con-
sequently encounters markedly different thermal environments
across its geographic range. The Iberian Peninsula, as one of the
main glacial refugia (Recuero & García-París, 2011; Veith et al., 2012;
Vences et al., 2013), harbours multiple lineages diverged during cli-
matic oscillations (Dufresnes et al., 2020; Veith et al., 2012). During
2015 (August–October) and 2016 (June–August) we sampled juve-
nile individuals (~2 weeks after metamorphosis) from two replicate
elevational gradients corresponding to two different lineages of
R. temporaria (from central and eastern Cantabrian Mountains,
hereafter ‘central’ and ‘eastern’; Choda, 2014). We sampled between
65 and 95 individuals from a total of seven populations (Table 1).
2.2 | Geographic variation in thermal tolerance
and plasticity
Upon arrival at the facilities of the Research Unit of Biodiversity
(University of Oviedo), the juveniles were randomly assigned to one
of two acclimation temperature treatments (14 or 24°C). These tem-
peratures approximate the average temperatures during the start/
end of the activity period (14°C) and the hottest period when ani-
mals are active (i.e. 24°C during July–August; see Figure S6). We
individualized juveniles in plastic containers with access to dechlo-
rinated tap water to prevent dehydration. We placed plastic con-
tainers in two different environmentally controlled rooms set at
14 ± 1°C and 24 ± 1°C, respectively, with a photoperiod of 12L:12D,
and let juveniles acclimate for 3–5 days. The acclimation period used
here represents enough time to stabilize critical thermal limits after
a large change in acclimation temperatures between field and labo-
ratory environments (Brattstrom, 1968; Navas, Úbeda, Logares, &
Jara, 2010). We supplied juveniles with small Acheta domestica crick-
ets ad libitum.
After the acclimation period, we estimated thermal tolerances
(critical thermal maxima and minima, CTmax and CT
min, respectively).
For each population and acclimation temperature, juveniles were
assigned to either CTmax or CT
min experiments. To estimate thermal
tolerances, we followed Hutchison's dynamic method (Lutterschmidt
& Hutchison, 1997). We placed individuals in 100-ml plastic contain-
ers with dechlorinated tap water at 20°C, and heated or cooled the
water at a constant rate of 0.25°C per minute using a refrigerated
heating bath (HUBER K15-cc-NR; Kältemaschinenbau AG), for CTmax
and CTmin, respectively. We considered that thermal limits had been
reached when individuals remained unresponsive to external stimuli
(10 gentle taps with a wooden stick). At that point, we recorded water
temperature with a quick-recording thermometer (Miller & Weber) to
the nearest 0.1°C. Because of the small size of the individuals, we as-
sumed that body temperatures equalled water temperature (Gutiérrez-
Pesquera et al., 2016; Lutterschmidt & Hutchison, 1997). After CTmax
and CTmin tests, we submerged individuals into cold (14°C) or warm
water (20°C), respectively, to allow recovery. After that, we placed
individuals in their respective controlled environment rooms and we
verified survival after 24 hr to ensure that thermal limits were not sur-
passed. Finally, we weighed each individual to the nearest 0.1 mg.
Population
(acronym) Lineage n
Mean
size
(in g) Longitude Latitude Elevation
Canopy
cover
(%)
Candioches (Can) Central 95 0.214 −5.92123 42.99991 1,707 (H) 0
Señales (Sen) Central 89 0.309 −5.24043 4 3 .0 74 40 1,716 (H) 0
Color (Col) Central 80 0.126 −5.27671 43.29492 377 (L) 85
Tornería (Tor) Central 78 0.156 −4.82462 4 3.38735 461 (L) 0
Hoyo Empedrado
(He)
Eastern 80 0.366 −4.75022 43.02275 2,076 (H) 0
Vidrieros (Vid) Eastern 77 0.536 −4.60121 42.95523 1,438 (H) 0
Huzmeana (Huz) Eastern 65 0.298 −4.23107 4 3.15771 448 (L) 80
TABLE 1 Lineage, sample size (n),
mean juvenile body size (in g), longitude,
latitude, elevation (H = high; L = low) and
percentage of canopy cover (i.e. tree and
shrub cover; extracted from the Spanish
Forest Map at a resolution of 1:50,000;
www.mapama.gob.es) for each population

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We used mixed effect ANCOVAs to test for effects of body
mass, elevation, lineage and acclimation temperature treatment.
Body mass (M) was used as a covariate, and population was treated
as a random effect. Elevation (H = high and L = low, Table 1), lin-
eage (‘central’ and ‘eastern’), acclimation treatment (14 and 24°C)
and their interactions were treated as fixed factors. Interactions in-
volving body mass that were non-significant (homogeneity of slopes)
were removed from models. We visually assessed the normality of
residuals using residual distribution and quantile–quantile plots.
2.3 | Biophysical modelling
We developed mechanistic niche models using NicheMapR—an
r implementation of the biophysical models developed by Porter
and colleagues (Kearney & Porter, 2017, 2020; Porter et al., 1973).
NicheMapR includes programmes that solve heat and mass budgets
for both microclimates and animals given the terrain and weather
conditions, and the animal's morphology, behaviour and physiology.
In this way it can estimate hourly operative temperatures (Te)—the
steady-state temperatures that the animal could achieve in a given
habitat. The microclimate model uses maximum and minimum air
temperatures, precipitation, cloud cover, relative humidity and
wind speed values to reconstruct available microclimates. We ob-
tained daily values for these parameters from the ECA&D (Haylock
et al., 2008) and DecReg/MiKlip (Brinckmann et al., 2016) projects
for each studied population during 2014 and 2015 (see Supporting
Information).
To estimate available microclimates under a climate warming
scenario, we examined projections for two time periods (2050
and 2070) using three global circulation models (GCMs: CCSM4,
HadGEM2-CC and GFDL-CM3) and two emission scenarios (low,
RCP 4.5, and high, RCP 8.5). We computed monthly differences
between current and projected climates (maximum and minimum
temperatures, and precipitation) using WorldClim layers—IPCC5—
at a spatial resolution of 30 arc-seconds (Hijmans, Cameron, Parra,
Jones, & Jarvis, 2005). We extracted projected monthly anomalies
fo r each po p u l at ion , in ter p o l a ted th o s e to da i l y da t a and added th e m
to the observed values from ECA&D (see Supporting Information).
We used weather data corresponding to the fir st modelled year (i.e.
2014) as the spin-up period (e.g. for snowpack); we only present
results for 2015.
We modelled a medium-sized early juvenile (0.3 g), with its mid-
point at 0.5 cm above the ground when active on the surface; a
shape equivalent to that of the leopard frog Lithobates pipiens; and
assumed that 90% of the skin acted as a free water surface when
individuals were active (see Kearney et al., 2008 and Fitzpatrick
et al., 2019 for more information). Since juveniles are predominantly
diurnal, we allowed only diurnal activity, bounded within the vol-
untary thermal maximum (VTmax, 18.5°C) and voluntary thermal
minimum (VTmin, 9.5°C), selected in a thermal gradient experiment
conducted on ~16 juveniles of each of the studied populations
(Enriquez-Urzelai, Palacio, Merino, Sacco, & Nicieza, 2018). When
Te fell outside these temperatures, we assumed that animals moved
underground to the depth with the closest temperature to their pre-
ferred temperature (Tpref, 13.1°C), obtained from the same thermal
gradient experiment (Enriquez-Urzelai et al., 2018). See Supporting
Information for detailed figures showing Te traces and behaviour for
example simulations.
To quantify exposure to stressful temperatures, we modelled
the Te of non-thermoregulating (remaining above-ground) or ther-
moregulating individuals (able to move underground) in full sun (0%
shade) or deep (90%) shade. Rana temporaria juveniles remain at the
edge of water bodies, where they forage on invertebrates (García-
París, Montori, & Herrero, 2004; Vences et al., 2000), and retreat to
small cracks and crevices in the soil during the hottest months of the
year (U. Enriquez-Urzelai & A.G. Nicieza, pers. obs.). However, like
other similar species (Lamoureux & Madison, 1999; Qi, Felix, Wang,
Gu, & Wang, 2011; Roznik & Johnson, 2009), radiotracked adult
R. temporaria also use small mammal burrows during summer
(U. Enriquez-Urzelai, A. Gandara, & A.G. Nicieza, unpubl. data).
Thus, we allowed thermoregulating juveniles to move up to 30 cm
underground to examine any potential change in the effectiveness
of behavioural thermoregulation (see Section 3). Subsequently,
we computed the thermal safety margins (TSM: CTmax − Te,max and
Te,min − CTmin; sensu Sunday et al., 2014) of individuals acclimated to
14 and 24°C at the studied populations, using population-specific
mean thermal limits at each acclimation treatment. Positive TSMs
indicate that critical thermal limits exceed experienced thermal ex-
tremes, while negative TSMs suggest exposure to temperatures out-
side the tolerance range.
To explore the impacts of climate change on activity windows for
populations at different elevations, we modelled thermoregulating
juveniles—using underground retreats up to 30 cm deep—both for
current and future climates, and with full sun or deep (90%) shade.
We defined activity windows as the number of hours juveniles that
was predicted to be active during the whole year (hr/year). We re-
peated all simulations with population-specific mean body sizes (see
weights in Table 1) but results were almost identical to those ob-
tained employing the overall sample mean size (0.3 g) for all pop-
ulations. Thus, we only present results for medium-sized juveniles
(see Supporting Information for results obtain including population-
specific sizes).
3 | RESULTS
3.1 | Geographic variation in thermal tolerance and
plasticity
We detected no evidence for heterogeneity of slopes for CTmax (no
significant interactions between body mass and fixed factors; see
Table S1). We found differences in CTmax due to mass, acclimation
treatment and elevation. Furthermore, we found differences in ac-
climation potential due to elevation (significant acclimation treat-
ment × elevation interaction; Table 2). Heavier juveniles showed

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ENRIQUE Z-URZELA I Et AL.
slightly higher CTmax values, and populations from high elevations
showed higher CTmax but lower acclimation potential than lowland
populations (Figure 1a). Lineage of origin did not affect CTmax.
CTmin varied with mass and acclimation treatment. We also
found differences in acclimation potential of CTmin due to mass
(mass × acclimation treatment), elevation (elevation × acclimation
treatment), and mass within lineage (mass × lineage × acclimation
treatment; Table 3). Smaller juveniles showed higher acclimation po-
tential, and this effect was more evident in the ‘central’ lineage. Similar
to CTmax, heavier juveniles showed higher CTmin value s, and ac climatio n
potential was lower in high-elevation populations compared to lowland
conspecifics (elevation × acclimation treatment; Figure 1b).
3.2 | Exposure to thermal extremes
3.2.1 | Physiological thermoconformity
Niche modelling simulations suggested that, under the current cli-
mate and full sun conditions, non-thermoregulating juveniles from
both high and low elevations had CTmax values that exceeded op-
erative temperatures (i.e. positive TSM), due to effects of evapora-
tive cooling (Figure 2a). The higher acclimation potential of CTmax
observed in lowland populations resulted in similar TSM among dif-
ferent elevations when individuals were acclimated to high tempera-
tures (Figure S10; compare panel a with b). However, acclimation to
warm temperatures had minor effects on individuals' TSMs and, for
the sake of simplicity, we only present the results of simulations run
with thermal limits of individuals acclimated to 14°C (see Figure S10
for all parameterizations). Conversely, all high-elevation popula-
tions and one low-elevation (Huz) population showed negative TSM
to cold extremes, for both warm and cold acclimation treatments
(Figure 2b; Figure S10).
TABLE 2 Analysis of covariance for heat tolerance as indexed
by the critical thermal maximum (CTmax), including mass (covariate;
M) and elevation (elev), lineage (lin), acclimation treatment (acc) and
their interactions. Population was included as random factor
F-value df p-value
Mass (M)18. 62 1, 272 <0.0001
Elevation (elev)13.78 1, 3 0.034
Lineage (lin)0.22 1, 3 0.672
Acclimation
treatment (acc)
37. 98 1, 272 <0.0001
elev × lin 0.12 1, 3 0.750
elev × acc 6.82 1, 272 0.010
lin × acc 0.66 1, 272 0.418
elev × lin × acc 0.00 1, 272 0.964
Bold represents significant p-values < 0.05.
FIGURE 1 (a) Heat tolerance—critical thermal maxima or
CTmax—and (b) cold tolerance—critical thermal minima or CTmin—of
Rana temporaria juveniles from high and low elevations, acclimated
to 14 (blue) or 24°C (red). Boxes represent 95% CIs, bold horizontal
lines the medians, vertical lines the higher and lower values within
third and first quantiles and dots outliers
30.0
32.5
35.0
CT (°C)
max
(a)
–3
–2
–1
0
1
High
Elevation
Low
CT (°C)
min
(b)
TABLE 3 Analysis of covariance for cold tolerance as indexed by
the critical thermal minimum (CTmin), including mass (covariate; M),
elevation (elev), lineage (lin), acclimation treatment (acc) and their
interactions. Population was included as random factor
F-value df p-value
Mass (M)9. 3 8 1, 261 0.002
Elevation (elev)0.00 1, 3 0.982
Lineage (lin)5.13 1, 3 0.109
Acclimation
treatment (acc)
95.68 1, 261 <0.0001
M × elev 0.83 1, 261 0.362
M × lin 0.34 1, 261 0.560
elev × lin 2.87 1, 3 0.189
M × acc 22.88 1, 261 <0.0001
elev × acc 26.76 1, 261 <0.0001
lin × acc 0.70 1, 261 0.404
M × elev × lin 0.11 1, 261 0. 742
M × elev × acc 3.05 1, 261 0.082
M × lin × acc 4.31 1, 261 0.039
elev × lin × acc 0.01 1, 261 0.920
M × elev × lin × acc 0.50 1, 261 0.480
Bold represents significant p-values < 0.05.

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Our simulations further suggest that, by 2050, evaporative cool-
ing may be insufficient to buffer low-elevation populations exposed
to full sun from extreme heat. By 2070, evaporative cooling may also
become insufficient for two high-elevation populations (Can and
Vid) under full sun conditions; the other two highland populations
(Sen and He) will experience Te close to their CTmax (Figure 2a). Deep
shade, by contrast, may protect individuals from overheating under
projected climates (Figure 2c). Regardless of shading level, by 2070,
only the lowland population that currently experiences negative
TSM to cold extremes (Huz) will be able to tolerate the lowest tem-
peratures during the year, according to the temperature scenarios
for 2070 (Figure 2b,d).
3.2.2 | Accounting for behavioural thermoregulation
Under current climatic conditions and both shading levels, retreating
to underground retreats as deep as 30 cm allowed juveniles to main-
tain positive TSM under both hot and cold extremes (Figure 3a,b);
however, by 2050, individuals from both high and low elevations
may need to seek deeper retreats to avoid exceeding their CTmax
when exposed to full sun (Figure 3a). Even individuals from the pop-
ulation at the highest elevation (He) may need to shelter deeper than
30 cm by 2070 to escape heat stress. Acclimation to warm tempera-
tures had limited impacts on these projections (Figure S10; compare
panel e with f, and m with n). Retreats in deep shade, however, are
predicted to remain thermally suitable under projected climates
(Figure 3c).
3.3 | Activity windows
Niche modelling simulations revealed that high-elevation popula-
tions have reduced opportunities for activity compared to lowland
conspecifics under current conditions (Figure 4). Interestingly,
while deep shade (90%) enabled individuals from lowland popula-
tions to be active for slightly longer periods, it strongly reduced
activity windows in high-elevation populations. Shade allowed ju-
veniles from all populations to be active during the hottest hours
during summer but prevented high-elevation populations from
achieving the temperatures required for activity during the cold-
est seasons.
Most of the studied populations were predicted to show a de-
cline in activity under climate change scenarios when individuals
were restricted to full sun. The only exception was the population
at the highest elevation (He), for which individuals were predicted
to have similar activity windows under current and future climates
(Figure 4a). Opportunities for activity of high-elevation populations
are predicted to decline most in summer and increase in spring, au-
tumn and winter. Lowland populations will experience reductions
FIGURE 2 Thermal safety margins
(TSM) of thermoconforming juveniles for
different populations ordered by elevation
(see acronyms and elevations in Table 1)
in (a and b) full sun (0% shade) and
(c and d) deep (90%) shade. Panels
(a) and (c) illustrate TSM to heat extremes,
and panels (b) and (d) TSM to cold
extremes. Note that, due to the negligible
impact of acclimation, we only present
results for individuals acclimated to 14°C.
See Figure S10 for all climatic scenarios
and acclimation treatments. Blue dots:
under the current climate; yellow bars:
under projected climates for 2050; red
bars: under projected climates for 2070;
orange: overlap between simulations for
2050 and 2070
−10
−5
0
5
10
He Sen Can Vid Tor Huz Col
(a)
Heat (0% shade)
–10
–5
0
5
10
(b)
Cold (0% shade)
−10
−5
0
5
10
15
High
Elevation
Low
Heat (90% shade)
Current climate
Overlap 2050–2070
2050
2070
–10
–5
0
5
10
15
(d) Cold (90% shade)
High
Elevation
Low
He Sen Can VidTor Huz Col
He Sen Can Vid Tor Huz Col He Sen Can VidTor Huz Col
(c)
Thermal safety margin (°C)
Thermal safety margin (°C)

1728
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Journal of Animal Ecology
ENRIQUE Z-URZELA I Et AL.
in activity during spring and autumn and increases during winter
(Figure 5a,c,e,g). Collectively, reductions in activity hours will ex-
ceed increases in full sun conditions under projected future climates
(Figure 4a).
When simulated to experience deep shade, activity windows
for high-elevation populations under climate change are pre-
dicted to decrease in summer but increase in spring and autumn
(Figure 5b,d,f,h). Overall, activity windows in deep shade are
predicted to increase under climate change for high-elevation
populations but were, nevertheless, predicted to be shorter than
when individuals were restricted to full sun. Lowland populations
were predicted to experience a marked reduction in activity times
during spring, summer and autumn, and an increase during win-
ter (Figure 5b,d,f,h). It should be noted, however, that although
high-elev ation populat ions show an incr ease in ac tivit y tim es un der
future climates in deep shade, they will remain more temporally
constrained than their lowland counterparts under the same con-
ditions (Figure 4b).
FIGURE 3 Thermal safety margins
(TSM) of thermoregulating juveniles
for different populations ordered by
elevation (see acronyms and elevations
in Table 1), using retreats of up to 30 cm
deep in (a and b) full sun (0% shade) and
(c and d) deep (90%) shade. Panels (a) and
(c) illustrate TSM to heat extremes, and
panels (b) and (d) TSM to cold extremes.
Note that, due to the negligible impact
of acclimation, we only present results
for individuals acclimated to 14°C. See
Figure S10 for all climatic scenarios
and acclimation treatments. Blue dots:
under the current climate; yellow bars:
under projected climates for 2050; red
bars: under projected climates for 2070;
orange: overlap between simulations for
2050 and 2070
Heat (0% shade)
–10
–5
0
5
10
He Sen Can Vid Tor Huz Col
(a)
Cold (0% shade)
–10
–5
0
5
10
He Sen Can Vid Tor Huz Col
(b)
High Elevation Low
(c)
Heat (90% shade)
–10
–5
0
5
10
15
He Sen Can Vid Tor Huz Col
Current climate
Overlap 2050–2070
2050
2070
(d) Cold (90% shade)
High
Elevation
Low
–10
–5
0
5
10
15
He Sen Can Vid Tor Huz Col
Thermal safety margin (°C)Thermal safety margin (°C)
FIGURE 4 Activity time in hours for
different populations ordered by elevation
(see acronyms and elevations in Table 1)
under (a) full sun (0% shade) and (b) deep
(90%) shade. Blue dots: under the current
climate; yellow bars: under projected
climates for 2050; red bars: under
projected climates for 2070; orange:
overlap between simulations for 2050 and
2070
500
1,000
1,500
He Sen Can Vid To r Huz Col
Activity time (hr)
(a)
500
1,000
1,500
He SenCan Vid TorHuz Col
(b)
0% shad
e9
0% shade
Current climate
2050
Overlap 2050–2070
2070
High
Elevation
Low High
Elevation
Low

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ENRIQUE Z-URZELA I Et AL.
4 | DISCUSSION
Most species constitute an array of locally adapted and unequally
plastic populations (Benito Garzón, Alía, Robson, & Zavala, 2011;
Hereford, 2009; Orizaola & Laurila, 2016). Accordingly, thermal
traits and their plasticity frequently vary among populations of
the same species, typically mirroring changes in the thermal envi-
ronment (Freidenburg & Skelly, 2004; Sinclair et al., 2016; Sinclair,
Williams, & Terblanche, 2012). Ultimately, geographic phenotypic
variation may result in an uneven sensitivity to thermal extremes
across the range of a species and consequently influence fore-
casts of climate change impacts (Matesanz, Gianoli, & Valladares,
2010; Pearson, Lago-Leston, & Mota, 2009; Valladares et al., 2014).
Behavioural thermoregulation, a mechanism by which animals can
buffer themselves against extreme temperatures, will also be de-
cisive for terrestrial ectotherms under changing climates (Kearney
et al., 2009; Sunday et al., 2014). Yet, we are just starting to un-
derstand the interplay between environmental tolerances, plasticity
and behavioural thermoregulation, and how this interplay will influ-
ence climate change impacts (Chevin, Lande, & Mace, 2010; Huey
et al., 2012; Jensen, Alemu, Alemneh, Pertoldi, & Bahrndorff, 2019;
Williams, Shoo, Isaac, Hoffmann, & Langham, 2008).
Previous interspecific studies have revealed higher variation in
cold tolerance (CTmin) compared to heat tolerance (CTmax) associ-
ated with latitudinal and elevational gradients (Sørensen, Dahlgaard,
& Loeschcke, 2001; Sunday, Bates, & Dulvy, 2011; von May et al.,
2017). Recently, von May et al. (2017) showed that both CTmax and
CTmin decreased with increasing elevation in tropical anurans
(see García-Robledo, Kuprewicz, Staines, Erwin, & Kress, 2016;
Pintanel, Tejedo, Ron, Llorente, & Merino-Viteri, 2019 for other ex-
amples in ectotherms). At the intraspecific level, patterns of ther-
mal limit variation along environmental gradients seem rather taxa
specific. In some ectotherms critical thermal limits decrease with
elevation (Miller & Packard, 1977) or latitude (Jensen et al., 2019);
in others thermal limits do not vary along environmental gradients
(Buckley et al., 2015; Gvoždík & Castilla, 2001; Slatyer & Schoville,
2016). Our results show that while CTmax of juvenile R. temporaria
increases slightly with elevation, CTmin does not, leading to wider
thermal breadths in mountain populations. At high elevations, strong
radiation along with diurnal behaviour can expose temperate mon-
tane amphibians to extremely high temperatures (Vences et al.,
20 0 0). This contra sts with the pat ter n observed in most tropica l high-
elevation anurans, which are mostly nocturnal and use shelters during
the day to avoid stressfully high temperatures (Pintanel et al., 2019;
von May et al., 2017). Thus, a larger thermal breadth (or a higher CTmax)
could widen activity windows. Furthermore, the cold tolerance of
R. temporaria is beyond the freezing point of water, regardless of el-
evation (Figure 1b), due to the risk of freezing both at high and low
elevations (Muir, Biek, & Mable, 2014). Previous studies have simi-
larly reported increased thermal tolerance ranges towards higher
latitudes and elevations (Araújo et al., 2013; Gaston & Chown, 1999;
Gutiérrez-Pesquera et al., 2016). Here we found that wider thermal
tolerance in high-elevation populations was driven by small shifts to-
wards higher heat tolerance.
Thermal fluctuations increase towards higher elevation and lati-
tudes and, thus, one might expect concurrent increases in acclimation
FIGURE 5 Monthly differences in activity time relative to current climates under the specified shading levels for (a–d) a low emission
scenario (i.e. RCP 4.5) and the most benign GCM (CCSM4), and for (e–h) a high emission scenario (i.e. RCP 8.5) and the GCM with the highest
projected temperature increases (GFDL-CM3). Blue polygons: high-elevation populations; red polygons: low-elevation populations
–200
–100
0
100
200
JanFeb Mar Apr MayJun JulAug SepOct NovDec
∆ Activity time (hr)
(a)
–200
–100
0
100
200
JanFeb MarApr MayJun Ju lAug Sep OctNov Dec
(b)
–200
–100
0
100
200
JanFeb MarApr MayJun Ju l Aug Sep OctNov Dec
(c)
–200
–100
0
100
200
JanFeb Mar Apr MayJun JulAug Sep OctNov Dec
(d)
–200
–100
0
100
200
JanFeb Mar Apr MayJun JulAug SepOct NovDec
(e)
–200
–100
0
100
200
JanFeb MarApr MayJun Ju lAug Sep OctNov Dec
(f)
–200
–100
0
100
200
JanFeb MarApr MayJun Ju l Aug Sep OctNov Dec
(g)
–200
–100
0
100
200
JanFeb Mar Apr MayJun JulAug Sep OctNov Dec
(h)
2050 (0% shade) 2050 (90% shade) 2070 (0% shade) 2070 (90% shade)
∆
Activity time (hr)

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Journal of Animal Ecology
ENRIQUE Z-URZELA I Et AL.
potential (i.e. plasticity). In a seminal paper, Brattstrom (1968) showed
that the potential for thermal acclimation was very limited and re-
markably similar between tropical and temperate anurans. Similarly,
Gunderson and Stillman's (2015) analysis revealed no change in upper
thermal tolerance and only a slight increase in CTmin plasticity of liz-
ards with latitude. However, the result s of other macroecological stud-
ies have shown that the acclimation potential in sublethal traits, such
as metabolic rates, decreases with increasing latitude (Gunderson &
Stillman, 2015; Seebacher, White, & Franklin, 2015). In line with those
studies, we found that juvenile R. temporaria originating from high-
elevation populations showed lower acclimation potential, not only in
he at, bu t als o in co ld to leran ce. Al thou gh pla stic therma l tol eranc es ma y
be adaptive (Sultan & Spencer, 2002), the wider thermal fluctuations
and shorter growing season lengths associated with high elevations
plausibly favour a variety of physiological adaptations (Brattstrom,
1968), including more tolerant and less plastic phenotypes, which avoid
paying the costs of plasticity (Dewitt, Sih, & Wilson, 1998).
Projected rates of climate change exceed the estimated pace of
historic niche evolution (Quintero & Wiens, 2013). The high similarity
in thermal tolerance observed here between phylogenetic lineages
of R. temporaria in northwestearn Iberia, coupled with only slight dif-
ferences in heat tolerance between populations from different ele-
vations, suggest that R. temporaria may not be capable of adapting
to novel conditions through niche evolution (but see von May et al.,
2017). Moreover, our mechanistic niche models revealed that acclima-
tion provides limited potential to buffer individuals from heat stress
under changing climates, in agreement with recent macrophysiolog-
ical studies (Gunderson et al., 2017; Gunderson & Stillman, 2015):
acclimation to either high or low temperatures had negligible effects
on estimates of current and future thermal safety margins, even in
the most plastic lowland populations. Indeed, the negligible degree of
local adaptation, together with the higher potential for acclimation of
lowland populations, led to similar thermal safety margins across el-
evations, as shown for other ectotherms across latitudes (Overgaard
et al., 2014). Thus, although we expect biodiversity to shift towards
higher elevations (McCain & Colwell, 2011), our results show that
the risk of overheating will be similar across environmental gradients
(Overgaard et al., 2014). This could lead to local extinctions of south-
ern populations regardless of elevation in most temperate amphib-
ians. But, the consequences might be particularly acute for species
endemic to small regions and mountainous areas (Parmesan, 2006;
Schwartz, Iverson, Prasad, Matthews, & O'Connor, 2006), where the
whole species or evolutionary significant units could go extinct (e.g.
Ahmadi, Hemami, Kaboli, Malekian, & Zimmermann, 2019).
Taken together, our results suggest that evolutionary potential
and acclimation capacity are largely insufficient to buffer juvenile
R. temporaria from thermal extremes under current and future climates.
Instead, our mechanistic niche model revealed that behavioural ther-
moregulation is a key mechanism to escape extreme cold tempera-
tures, especially for high-elevation populations (Figures 2 and 3), as
already shown by Ludwig, Sinsch, and Pelster (2013, 2015) for adult
R. Temporaria at high elevations in the Alps. The use of behavioural
thermoregulation to avoid extreme temperatures could partly
account for the observed low degree of local adaptation, through the
‘Bogert effect’ (Bogert, 1949; Buckley et al., 2015; Farallo, Wier, &
Miles, 2018; Muñoz & Losos, 2018). In addition, our model suggests
that behavioural thermoregulation will be key to compensating the
loss of effectiveness of evaporative cooling under future climates.
Evaporative cooling is a highly efficient mechanism that allows
wet skinned ectotherms, such as amphibians, to dissipate excessive
heat (Kearney & Porter, 20 09; Tracy, 1976). Our results show that,
due to evaporative cooling, juvenile frogs avoid overheating at all
elevations under current climates, even in full sun, as pointed out
by Sunday et al. (2014). Notwithstanding, by 2050, lowland popu-
lations are predicted to be incapable of buffering themselves from
extreme heat exclusively through evaporative cooling. Remarkably,
by 2070, evaporative cooling may not protect even some high-
elevation populations from overheating and others will experience
body temperatures close to their maximum heat tolerance (Figure 2).
Thus, although evaporative cooling represents an effective mecha-
nism for amphibians to avoid overheating under the current climate,
regardless of elevation, behavioural thermoregulation might become
crucial for juveniles to buffer heat stress in the future (Figures 2 and 3;
Kearney & Porter, 2009; Ruiz-Aravena et al., 2014; Sunday et al., 2014).
Our simulations suggest that juvenile amphibians could potentially
avoid high temperatures by seeking deep retreat sites or by restricting
their activity to shaded microhabitats. However, the thermal qualit y of
shelter s will decrease with climate change. We show, for ins tance, that
typical below-ground retreats for R. temporaria (30 cm) may become
insufficient to buffer rising temperatures at all elevations. Additionally,
canopy cover is minimal at the studied sites, especially those at high
elevations (Table 1). Thus, at high elevations, current shade levels
and currently occupied retreats are unlikely to protect juvenile frogs
from extreme temperatures. The availability of suitable microhabitats
has been proposed as an important driver of elevational range lim-
its (Jankowski, Londoño, Robinson, & Chappell, 2013; Wake & Lynch,
1976) and drives thermal tolerance evolution in tropical mountains
(Pintanel et al., 2019). Our results similarly suggest that the availabil-
ity of suitable microhabitats (and microclimates) could be essential
for the long-term persistence of R. temporaria populations and other
temperate amphibians at high elevations. A detailed understanding
of on-ground microhabitat structure, such as shade levels and retreat
depths, is thus critical to making realistic predictions of species vul-
nerability to climate change, as well as to informing climate change
mitigation strategies. For instance, ensuring thermally suited refugia
for juveniles, for example, around breeding ponds, could minimize the
impa c ts of tem per atur e rises as clima te chan ges , leading to bio log ica lly
sound, evidence-based mitigation strategies (Cuddington et al., 2013).
In theory, under a warmer climate, populations from colder envi-
ronments (e.g. the tops of mountains) could benefit from wider ac-
tivity windows (Levy, Buckley, Keitt, & Angilletta, 2016). However,
we demonstrate the opposite pattern: warming was predicted to de-
crease activity windows at all elevations. In general, decreases in ac-
tivity hours during warmer months exceeded increases during colder
months (Figure 5). Regardless of the available amount of shade, ac-
tivity windows will remain narrower with increasing elevation. In

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ENRIQUE Z-URZELA I Et AL.
mountainous areas, weather conditions can change suddenly and
unpredictably, and may vary substantially from valley to valley due
to the rain shadow effect: while in one valley the weather may be
sunny, in the adjacent valley a fog bank or a storm could increase
soil and air humidity (Baudier & O'Donnell, 2020). This effect could
widen the simulated activity periods of some populations but would
hardly change the general patterns reported here.
5 | CONCLUSIONS
Geographic phenotypic variation, the potential for plastic responses,
behavioural thermoregulation and their interactions may mediate
the impacts of climate change on the extinction risk of populations
throughout a species' distribution (Buckley et al., 2015; Gunderson
et al., 2017; Kolbe, Kearney, & Shine, 2010; Valladares et al., 2014).
We show that mechanistic niche models offer a flexible means to in-
tegrate and assess the influence of these sources of uncertainty in cli-
mate change forecasts (Kearney & Porter, 2009; Moran, Hartig, & Bell,
2016). Applying this modelling framework to juvenile R. temporaria
suggests that the primary source of forecast uncertainty is the role
of behavioural thermoregulation, in particular, the species' ability to
seek deeper retreats and shaded microhabitats, or wet microhabitats
to rehydrate. In this sense, our results stress the importance of fine-
scale patterns of thermal constraints on activity windows (see also
Gunderson & Leal, 2015). Despite observed phenotypic variation as-
sociated with elevational gradients, we found that the risk of reaching
detrimental body temperatures under changing climates was pre-
dicted to be similar across elevations. Furthermore, although we might
expect populations from colder environments to benefit from wider
activity windows under climate change (Levy et al., 2016), frogs from
high elevations were predicted to be more temporally constrained
th an low land counterpa r ts un der bo th cur rent and fut u re pr e dicte d cli -
mates. Hence, climate change vulnerability may be quite similar across
elevations, which could have highly detrimental consequences for en-
demic species and evolutionary significant units inhabiting mountain
areas, either as a result of physiological stress or derived from indirect
effects (e.g. competition with ecologically similar species).
ACKNOWLEDGEMENTS
We thank Florentino Braña, Miguel Ángel Carretero, Silvia
Matesanz, Rudolf von May and Ulrich Sinsch for useful com-
ments on previous versions of the manuscript. We thank the staff
from the Governing Council of Castile-León, the Principality of
Asturias and Cantabria for providing the permits to conduct this
inve stigation (Castile-León: EP/CyL/725/2015, EP/CyL/112/2017;
Asturias: 2015/008130, 2016/001092; Cantabria: EST-275/2016-
SEP). Experiments were carried out under the Ethics Board for
Animal Experimentation of the University of Oviedo Permit No.
8-INV-2012. The members of the research team have approved
licenses by the Service of Animal Welfare and Production of the
Principality of Asturias to design (A.G.N.) and execute (U.E.U.,
A.G.N.) experimental protocols with animals. This research was
supported by grants from MINECO (CGL2012-40246-C02-02 and
CGL2012-40246-C02-01), and MEC (CGL2017-86924-P). U.E.U.
was supported by a Ph.D. award (BES-2013-063203) from MEC.
R.T. was supported by an ARC Discovery Early Career Researcher
Award. The authors declare that they have no conflict of interests.
AUTHORS' CONTRIBUTIONS
U.E.U., M.T., A.G.N. and M.R.K. conceived the idea and designed
the study; U.E.U., M.S., A.S.P. and A.G.N. collected the data; U.E.U.,
M.R.K., R.T. and A.G.N. conducted statistical analyses and biophysi-
cal models; All authors contributed critically to the drafts and gave
final approval for publication.
DATA AVA ILAB ILITY STATE MEN T
Data are available from the Dryad Digital Repository: https://doi.
org/10.5061/dryad.dz08k prtv (Enriquez-Urzelai et al., 2020).
ORCID
Urtzi Enriquez-Urzelai https://orcid.org/0000-0001-5958-2250
Reid Tingley https://orcid.org/0000-0002-7630-7434
Michael R. Kearney https://orcid.org/0000-0002-3349-8744
Miguel Tejedo http://orcid.org/0000-0003-4183-184X
Alfredo G. Nicieza https://orcid.org/0000-0003-4062-569X
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How to cite this article: Enriquez-Urzelai U, Tingley R, Kearney
MR, et al. The roles of acclimation and behaviour in buffering
climate change impacts along elevational gradients. J Anim Ecol.
2020;89:1722–1734. https://doi.org/10.1111/1365-
2656.13222