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Animal behaviour
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Research
Cite this article: Briscoe NJ, Handasyde KA,
Griffiths SR, Porter WP, Krockenberger A,
Kearney MR. 2014 Tree-hugging koalas
demonstrate a novel thermoregulatory
mechanism for arboreal mammals. Biol. Lett.
10: 20140235.
http://dx.doi.org/10.1098/rsbl.2014.0235
Received: 18 March 2014
Accepted: 9 May 2014
Subject Areas:
behaviour, ecology
Keywords:
behavioural thermoregulation, biophysical
models, koala, climate change, microclimate
selection
Author for correspondence:
Natalie J. Briscoe
e-mail: [email protected]
†
Present address: National Environmental
Research Program (NERP), School of Botany,
University of Melbourne, Melbourne, Victoria,
Australia.
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rsbl.2014.0235 or
via http://rsbl.royalsocietypublishing.org.
Tree-hugging koalas demonstrate a novel
thermoregulatory mechanism for arboreal
mammals
Natalie J. Briscoe1,†, Kathrine A. Handasyde1, Stephen R. Griffiths2,
Warren P. Porter3, Andrew Krockenberger4 and Michael R. Kearney1
1
Department of Zoology, University of Melbourne, Melbourne, Victoria, Australia
Department of Zoology, La Trobe University, Bundoora, Victoria, Australia
3
Department of Zoology, University of Wisconsin, Madison, WI, USA
4
School of Marine and Tropical Biology, James Cook University, Cairns, Australia
2
How climate impacts organisms depends not only on their physiology, but
also whether they can buffer themselves against climate variability via their
behaviour. One of the way species can withstand hot temperatures is by seeking
out cool microclimates, but only if their habitat provides such refugia. Here, we
describe a novel thermoregulatory strategy in an arboreal mammal, the koala
Phascolarctos cinereus. During hot weather, koalas enhanced conductive heat
loss by seeking out and resting against tree trunks that were substantially
cooler than ambient air temperature. Using a biophysical model of heat
exchange, we show that this behaviour greatly reduces the amount of heat
that must be lost via evaporative cooling, potentially increasing koala survival
during extreme heat events. While it has long been known that internal temperatures of trees differ from ambient air temperatures, the relevance of this for
arboreal and semi-arboreal mammals has not previously been explored. Our
results highlight the important role of tree trunks as aboveground ‘heat
sinks’, providing cool local microenvironments not only for koalas, but also
for all tree-dwelling species.
1. Introduction
During extreme heat events, terrestrial endotherms must avoid gaining excessive
heat from their environment, while simultaneously losing the heat produced by
their own metabolism [1]. Low water availability or high humidity can further
compound this problem by constraining the use of evaporative cooling, which
is the primary method of heat loss in many endothermic species [2,3]. Behavioural
thermoregulation—selecting microclimates or adopting postures or orientations
that aid with the regulation of body temperature—has been cited as a key strategy
that can buffer animals against future climate change [4–6]. However, use of behavioural thermoregulation may be constrained by the availability of suitable
microclimates or associated costs such as lost foraging time or increased predation
risk [7,8]. With extreme heat events predicted to become more severe and frequent
under anthropogenic climate change [9], a thorough understanding of how organisms regulate their exposure to extreme conditions at the microclimate scale is
crucial if we are to predict their performance under future climate change and
protect habitats that provide suitable refugia [10,11].
We investigated behavioural thermoregulation in a broadly distributed
arboreal mammal, the koala (Phascolarctos cinereus). Koalas do not seek shelter
in dens and can suffer high mortality during extreme heat events, which often
coincide with periods of low rainfall [12]. When exposed to air temperatures
above 25 –308C in the laboratory, koalas maintain a relatively constant body
temperature by greatly increasing evaporative water loss [13]. In the wild,
& 2014 The Author(s) Published by the Royal Society. All rights reserved.
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0.4
2
hot
mild
0.3
0.2
Biol. Lett. 10: 20140235
proportion of observations
0.5
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however, koalas rarely drink and during dry periods may not
have access to free water (e.g. dew on leaves)—potentially
restricting this species’ capacity to sustain high levels of evaporative cooling; [14]. We therefore predicted that in the wild
koalas would use behavioural adjustments to minimize their
reliance on evaporative cooling. To investigate this, we tested
whether koalas altered their behaviour and microhabitat use
during hot weather. We then used a biophysical model of
heat exchange to predict heat loss requirements of koalas
adopting different behavioural strategies.
0.1
2. Methods
(a) Behaviour and microclimate data
Koalas (n ¼ 37) in southeastern Australia (388200 S, 1458220 E)
fitted with radio collars (Sirtrack, New Zealand) were radiotracked during the day in both winter (June – August 2009) and
summer (December – March 2010 and 2011). Behavioural observations ( posture, activity, height and location in the tree) and
tree species were recorded before microclimatic data were
measured for 10 min as close as possible to the koala (less than
0.5 m) using a portable weather station (WeatherHawk, USA)
mounted on an extendable pole. To measure available microclimates and tree species composition within the study site, a set
of random GPS coordinates were generated (n ¼ 319) and, at
each point, microclimate and habitat data were collected from
the closest tree (more than 1 m tall) at a randomly generated
compass direction, height and distance from the trunk. Records
were divided into ‘hot’ (air temperature . 308C) and ‘mild’ (air
temperature 258C) weather, coinciding with temperatures at
which koalas greatly increase the use of evaporative cooling in
the laboratory [13]. Additional behavioural data were collected
by walking a 600 m long 50 m wide transect within the
study site and recording posture and location in the tree of all
observed individuals (n ¼ 130) during hot and mild weather.
0
koala posture
Figure 1. Koala posture under mild (grey; n ¼ 121) and hot (black; n ¼ 102)
conditions in southeastern Australia. Postures were divided into five categories,
ranging from lowest surface area (left) to highest surface area (right), with
examples provided below the axis.
properties and environmental conditions. The model was modified to include conductive heat exchange based on the equation
for conductive heat exchange of a flat plate:
qcond ¼
kA(T1 T2 )
,
d
where k is the thermal conductivity of compressed ventral fur, A is
the surface area in contact with the trunk, T1 and T2 are skin and
trunk surface temperatures, respectively and d is the depth of compressed ventral fur (see the electronic supplementary material,
tables S1 and S2).
(b) Tree trunk temperatures
Data on tree trunk temperatures during hot weather were collected (January 2011) to assess whether trunk temperature
profiles could explain observed patterns of koala behaviour.
Thermal images of trees within the study site were taken with
a thermal imaging camera (FLIR ThermaCAM SC660) and analysed using ThermaCAM Researcher Professional v. 2.9 (FLIR
Systems Inc., Wilsonville, OR). Five individual trees from each
of the four dominant tree species (Eucalyptus ovata, E. obliqua,
E. viminalis and Acacia mearnsii) were randomly selected along
a 600 50 m transect within the study site and photographed
during hot weather (average air temperature while photos were
taken was 36.48C, and this did not differ between species).
Photos were taken of the south or east side of the trunk, which
had the lowest exposure to incident solar radiation, from a distance of 2 – 7 m, giving a clear view of the trunk, branches and
canopy. We determined mean temperatures in a standardized
area for the base of the trunk, mid-trunk (1.5– 3.5 m), lateral
branches and canopy for each tree, assuming a trunk emissivity
of 0.95 and accounting for distance and air temperature.
(c) Koala heat loss requirements
To further assess whether differences in tree trunk temperatures
were likely to be driving koala behaviour patterns, we used an
analytical model of heat exchange for an ellipsoid furred
endotherm [15] to predict potential heat loss via conduction to
tree trunks. This model predicts metabolic rate and required
heat loss of an endotherm based on a specified set of organism
3. Results
Koala posture during the day varied between hot and mild
weather (figure 1). During hot weather, animals adopted
postures with higher surface area exposed (Fisher’s exact test:
p , 0.001, n ¼ 223), were more frequently observed with all
limbs outstretched and oriented themselves so that they
appeared to be hugging the trunks or large lower branches
of trees (figure 2a). Consistent with this, koalas were observed sitting on the main trunks of trees much more
frequently during hot weather (65%) than in mild weather
(30%; x 2 ¼ 25.85, p , 0.001, n ¼ 223) and were also lower in
the tree, with koala height negatively related to air temperature
(F1,110 ¼ 22.81, p , 0.001). Tree use also differed between hot
and mild weather: koalas significantly increased their use of
A. mearnsii from 5% in mild (air temperature 258C) conditions to 29% during hot weather (Fisher’s exact test: p ¼ 0.009,
odds ratio ¼ 7.95).
Air temperature, humidity and wind speed at sites occupied by koalas did not differ from available microclimates in
either hot or mild weather (all p-values . 0.41). Microclimates selected by koalas did, however, have lower solar
radiation in hot weather (t1,35 ¼ 2.174, p ¼ 0.046, mean difference: 111 W m22), but solar radiation in microclimates used
by koalas showed no relationship with height or location in
the tree, and was not lower in A. mearnsii trees (although it
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(a)
(b)
–2
–4
–6
py
ca
no
br
an
ch
es
k
tru
n
ba
se
–8
A. mearnsii
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0
–2
4
py
ca
no
br
an
ch
es
nk
tru
ba
se
–6
E. ovata
ca
no
py
–8
es
16
–4
ch
8
–2
an
heat loss (W)
24
E. obliqua
0
br
32
12
air temperature (°C)
40
nk
16
–8
tru
(c)
–6
se
41.0° C
ba
temperature difference (°C)
–4
29.0° C
8
0
0
0
10
12
14
16
18
20
hour of the day
–2
–4
–6
py
E. viminalis
ca
no
es
ch
br
an
nk
tru
ba
se
–8
Figure 2. (a) Thermal image of a koala hugging the cool lower limb of a tree, illustrating a posture typically observed during hot weather, (b) Thermal profiles
(mean surface temperature – air temperature + s.e.m.) of four dominant tree species (Eucalyptus obliqua, E. viminalis, Acacia mearnsii and E. ovata), (c) Predicted
heat loss requirements (W) of koalas with (grey) and without (black) tree-hugging behaviour during a typical hot day in southeastern Australia. Dashed line
indicates air temperature (right axis).
was lower in E. obliqua and non-Eucalyptus species other than
A. mearnsii; electronic supplementary material, table S3).
By contrast, tree temperature profiles showed strong congruence with observed koala behaviour patterns. During hot
weather, average tree surface temperatures of the four dominant tree species at the site were significantly lower than
local air temperatures (t1,18 ¼ 28.1544, p , 0.001). Relative to
air temperature, surface temperatures of the base and lower
trunk were significantly cooler than the branches and
canopy, and the magnitude of these differences varied between
tree species (species F3,15 ¼ 1.863, p ¼ 0.179; region F3,45 ¼
95.494, p , 0.001; species region F9,45 ¼ 8.996, p , 0.001).
The coolest surfaces recorded belonged to the non-food tree
species, A. mearnsii (figure 2b), which was more frequently
used during hot weather. This species had base and mid-trunk
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air temp. = 37.3° C
3
0
temperatures that were up to 8.98C (average 6.78C) and 6.78C
(average 5.18C) cooler than air temperature, respectively. By contrast, average base and mid-trunk surface temperatures of
E. obliqua were just 1.878 and 1.468C cooler than air temperature.
Average branch and canopy temperatures of all species were
within 1.48C of air temperature (figure 2b).
(a) Koala heat loss requirements
Predicted conductive heat lost to tree trunks during hot
weather was substantial, with simulations indicating that
this behaviour could reduce or even prevent the need for evaporative cooling (figure 2c and electronic supplementary
material, table S1). For example, an 11.3 kg male koala sitting
in full shade and experiencing an air temperature of 358C and
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The ability of an organism to behaviourally thermoregulate is
dependent on the availability and spatial arrangement of
microclimates within their environment [4,5]. Many terrestrial species can exploit cooler, more stable, subterranean
environments during hot environmental conditions [16] or
lose heat conductively to cool ground surfaces [17]. Animals
restricted to the arboreal environment cannot exploit these
thermoregulatory options—however, our study reveals, for
the first time, that analogous cool microclimates can be available to these species in the form of cool tree trunks. For
koalas, tree-hugging behaviour greatly reduced predicted
heat loss requirements, and water savings from this behaviour could be critical for the survival of this species during
heat waves when water availability is limited [14], or under
high humidity when evaporative cooling is inefficient [2].
Our results are consistent with, and may help explain, previous studies of koalas in more northern populations that
found seasonal [18] and weather-dependent differences in
tree use, with koalas using non-food trees more frequently
during hot days [6,19]. Combined, these results emphasize
the importance of behavioural thermoregulation for koalas
Acknowledgements. We thank J. Larson for conducting measurements of
fur conductivity and the Arthur Rylah Institute for Environmental
Research (DEPI) for providing access to the thermal camera.
Data accessibility. Spreadsheet model of heat exchange for an ellipsoid
furred endotherm (modified for koalas) uploaded as the electronic
supplementary material. Koala behaviour, microclimate and tree
temperature data uploaded to Dryad Digital Repository: doi:10.
5061/dryad.49j7t.
Funding statement. This research was supported by a Holsworth Wildlife
Research Endowment to N.J.B. and an Australian Research Council
linkage grant to M.R.K. (LP0989537) and was conducted with
AEC approval (University of Melbourne) and permits from the
Department of Environment and Primary Industries, Victoria.
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4. Discussion
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