Seasonal effects on thermoregulatory abilities of the Wahlberg’s epauletted
fruit bat (Epomophorus wahlbergi) in KwaZulu-Natal, South Africa
, M.M. Zungu, M. Brown
School of Biological and Conservation Sciences, University of KwaZulu-Natal, Private Bag X 01, Scottsville 3209, Pietermaritzburg, South Africa
Received 6 September 2011
Accepted 13 December 2011
Available online 28 December 2011
Seasonal variations in ambient temperature (T
) require changes in thermoregulatory responses of
endotherms. These responses vary according to several factors including taxon and energy constraints.
Despite a plethora of studies on chiropteran variations in thermoregulation, few have examined African
species. In this study, we used the Wahlberg’s epauletted fruit bat (Epomophorus wahlbergi, body
massE115 g) to determine how the thermoregulatory abilities of an Afrotropical chiropteran respond
to seasonal changes in T
. Mass speciﬁc Resting Metabolic Rates (RMR
) and basal metabolic rate
(BMR) were signiﬁcantly higher in winter than in summer. Furthermore, winter body mass was
signiﬁcantly higher than summer body mass. A broad thermoneutral zone (TNZ) was observed in
winter (15–35 1C) compared with summer (25–30 1C). This species exhibited heterothermy (rectal and
core body temperature) during the photophase (bats’ rest-phase) particularly at lower T
s and had a
low tolerance of high T
s. Overall, there was a signiﬁcant seasonal variation in the thermoregulatory
abilities of E. wahlbergi. The relative paucity of data relating to the seasonal thermoregulatory abilities
of Afrotropical bats suggest further work is needed for comparison and possible effects of climate
change, particularly extreme hot days.
&2011 Elsevier Ltd. All rights reserved.
Seasonal variation in climatic conditions occurs in most
habitats with the most pronounced variations occurring in tem-
perate and/or arctic regions (Stawski and Geiser, 2010). In the
latter the variations are more predictable whereas in more
tropical areas the variations are often unpredictable (Holmgren
et al., 2001;Landman and Goddard, 2010). A consequence of this
is seasonal ﬂuctuations in primary productivity of the environ-
ment, subsequently resulting in different physiological demands
on animals (Stawski and Geiser, 2010). Similarly unpredictable
adverse weather conditions may affect food availability and
impact negatively on an endotherm’s energy balance. Endotherms
have the ability to adapt morphologically, physiologically and
behaviorally to their thermal environment in order to obtain
thermal homeostasis in a changing thermal environment (Simeone
et al., 2004;Brown and Downs, 2003;Brown and Downs, 2005,
2007;Lindsay et al., 2009a,b). One of these adaptations is energy
conservation with the ability to enter a physiological state of
reduced metabolic requirements and allow body temperature (T
to decrease and so exhibit heterothermy, particularly torpor (Downs
and Brown, 2002;Matheson et al., 2010). During this period, the T
is maintained at a reduced set-point, usually several degrees below
, which helps in reducing heat loss and subsequently
energy requirements (Geiser, 2004). Seasonal changes in torpor
patterns are a characteristic of many mammals found in areas with
cold climates or energetic stress (Geiser, 2004;Stawski, 2010).
Usually torpor is more pronounced in winter with some species
not exhibiting it during summer with others using it regularly
irrespective of season (Turbill et al., 2003;Geiser, 2004;Stawski,
2010;Stawski and Geiser, 2010).
Another endothermic adaptation in response to different
seasonal ambient temperatures (T
) is change in basal metabolic
rate (BMR) (Coburn and Geiser, 1998;Saarela et al., 1995;Bush
et al., 2008;Nzama et al., 2010;Wilson et al., 2011). Although
BMR and metabolic rate (MR) were considered speciﬁc for a
, seasonal variations in both of these physiological
parameters have been documented in a number of avian species
(Hart, 1962;Dawson, 2003;McKechnie, 2008;Wilson et al., 2011)
as well as several mammals (Geiser and Baudinette, 1987;Feist
and White, 1989;Arnold et al., 2006). Bats are an ecologically and
taxonomically diverse group of ﬂying mammals with a broad range
in body mass (Bishop, 2008) belonging to the order Chiroptera
which was previously subdivided into two sub-orders, the Micro-
chiroptera (insectivorous bats) and Megachiroptera (fruit/nectar
eating bats) (Taylor, 2005). However, recent molecular evidence
Contents lists available at SciVerse ScienceDirect
journal homepage: www.elsevier.com/locate/jtherbio
Journal of Thermal Biology
0306-4565/$ - see front matter &2011 Elsevier Ltd. All rights reserved.
Corresponding author. Tel.: þ27 33 2605127; fax: þ27 33 2605105.
E-mail address: email@example.com (C.T. Downs).
Journal of Thermal Biology 37 (2012) 144–150
(Hutcheon and Kirsch, 2006) has shown that there is a close
alliance between Old World fruit bats (Pteropodidae) and certain
families belonging to the Microchiroptera. Therefore this suborder
has been named Pterododiformes with Vespertilioniformes sub-
order applying to accommodate the remaining Microchiropteran
families (Monadjem et al., 2010).
One of the earliest reviews on bat thermal physiology (Hock,
1951) concluded that bats differ from other endotherms as T
rest, irrespective of season, approximates that of the environment
thereby minimizing energy expenditure. Since then there have
been a plethora of laboratory and ﬁeld studies on thermoregula-
tory ability of a range of bat families from temperate, subtropical
and tropical regions (Herreid and Schmidt-Nielsen, 1966;Licht
and Leitner, 1967;McNab, 1969;Lyman, 1970;Studier and
Wilson, 1970,1979;Holyoak and Stones, 1971;Studier and
O’Farrell, 1972;Kurta and Kunz, 1988,Audet and Fenton, 1988;
Genoud et al., 1990;Genoud, 1993;Rodrı
Webb et al., 1995;Hosken and Withers, 1997,1999;Choi et al.,
˜a and Kunz, 1999;Cryan and Wolf, 2003;
Turbill et al., 2003;Geiser, 2004;Willis et al., 2005;Marom
et al., 2006;Solick and Barclay, 2007;Wojciechowski et al., 2007;
Stawski, 2010;Stawski and Geiser, 2010;Storm and Boyles,
2011). Most of these studies documented changes in bats’ T
response to cold or unfavorable conditions, most insectivorous
bats decrease T
with the use of heterothermy, particularly torpor,
to conserve energy (Herreid and Schmidt-Nielsen, 1966;Lyman,
1982;Marom et al., 2006). There is usually a concomitant
reduction in MR reducing energy expenditure (Geiser and Ruf,
1995). Bats lose heat rapidly at low T
sbecause of their large
surface area to volume ratios (Bartels et al., 1998). This, coupled
with periods of food scarcity, highly energy-expensive ﬂight and
low internal energy stores (Bartels et al., 1998), suggests they
avoid costly energy requirements to maintain constant T
contrast to Microchiroptera, the former sub-order Megachiroptera
in the past was thought to be homeothermic (Ransome, 1990).
Due to their relatively large sizes, and that they are restricted to
tropical and subtropical regions where the ﬂuctuations in food
availability are less severe than in temperate regions, it was
believed they had no need for heterothermy (Bartels et al., 1998).
However, studies on Australasian fruit- and blossom-eating bats
of various body sizes have shown that they are indeed hetero-
thermic irrespective of season and particularly if weather is
unpredictable (Bartholomew et al., 1964;1970;Geiser et al.,
1996;Bonaccorso and McNab, 1997;Ochoa-Acun
˜a and Kunz,
1999;Coburn and Geiser, 1998;Bartels et al., 1998;McNab and
Armstrong, 2001;McNab and Bonaccorso, 2001;Geiser et al.,
2005;Riek et al., 2010). Relatively little is known about the
thermoregulatory abilities, particularly plasticity in energetics, of
Chiroptera from Africa, with most published work on insectivores
(Stegeman, 1989;Bronner et al., 1999;Maloney et al., 1999;
Jacobs et al., 2007;Vivier and van der Merwe, 2007;Cory
Toussaint et al., 2010).
To establish how physiological variables are affected by seasonal
changes in temperature in an Afrotropical chiropteran, we investi-
gated seasonal thermoregulatory abilities of the Wahlberg’s epau-
letted fruit bat (Epomophorus wahlbergi, Sundevall, 1846). It is a
nocturnal Old World species restricted to the continent of Africa
(Taylor, 2005). In the southern African region, this species is
conﬁned to eastern parts, penetrating westwards into the drier
areas up river valleys such as Zambezi and Limpopo (Taylor, 2005).
Since this region is largely affected by El Nin
˜o Southern Oscillations
(ENSO) (Jury and Nkosi, 2000), the rainfall patterns of this regions;
and subsequently primary production of the environment, remain
The aim of this study was to investigate the effect of season on
the MR of E. wahlbergi. The objectives were to determine oxygen
) at various T
sin both seasons (summer and
winter) and to examine changes in the Resting Metabolic Rate
(RMR), BMR and the thermoneutral zone (TNZ) between seasons.
There has been debate in the literature regarding the deﬁnition of
RMR. The most widely accepted deﬁnition of this term is that
RMR is the metabolic rate of a resting and post-absorptive
endotherm measured within its thermoneutral zone, and when
this is in the thermoneutral zone is called BMR (Withers, 1992;
Hill et al., 2004). Another deﬁnition which has been suggested is
that RMR is the metabolic rate of an endotherm in its thermo-
neutral zone but not in a post-absorptive state (IUPS Thermal
Physiology Terms, 2001). For this study, we refer to RMR as
the metabolic rate of an endotherm in a post-absorptive state
and measured at a speciﬁc T
). We further investigated
whether E. wahlbergi regulates its T
or is heterothermic. We
predicted that BMR and RMR would be higher in winter compared
with summer. Furthermore, since an increase in the range of TNZ
is coupled with a decrease in conductance (Cooper and Gessaman,
2004), we predicted the TNZ to be broader in winter compared
2. Materials and methods
2.1. Study animals, capture and maintenance
Ten adult E. wahlbergi (5 males, 5 ﬁve females) captured in
Pietermaritzburg, KwaZulu-Natal (KZN) (291370
ing September 2009 under the permit from Ezemvelo KZN Wildlife
were used for this study. Directly after capture, bats were trans-
ferred to the Animal House of the University of KwaZulu-Natal,
Pietermaritzburg, at an altitude of 660 m, where they were housed
in outdoor aviaries (2.44.1 2.0 m
) separated according to
gender. Bats were fed a maintenance diet each day consisting of
chopped up mixed fruits including bananas, apples, pears, pawpaw
and guavas with a supplement (AviPlus Lorikeet Special; Avipro-
ducts, Waterfall, KZN), with water or sugar solution provided
2.2. Metabolic rate measurement
During summer (February 2010) and winter (late July–early
August 2010) E. wahlbergi metabolic measurements during the
photophase (bats’ rest phase) were indirectly made by measuring
using the open-ﬂow respirometry system described in
Lindsay et al. (2009a). Measurements in each season were at
seven respective T
s(5, 10, 15, 20, 25, 30 and 35 1C) in random
order and only one T
per day. Bats were only measured on
alternate days. Bats were caught with sweep nets in the morning
and placed in separate respirometers (35 20 25 cm
(Winnipeg, Manitoba, Canada) at 07h15. They were
removed from their respirometers at 15h00, except at 35 1C when
they were removed at 12h00. Body mass and rectal T
measured before and after each trial. Rectal T
using a digital thermometer (Yu Fing Electronics; range 50 to
1300 1C), with a thermocouple inserted 70.4 mm into the rectum
of each bat.
An oxygen analyzer (model S-3A/1, Ametek, Pittsburgh, PA,
USA) was used to determine the fractional concentration of O
dry air samples (Lindsay et al., 2009a). Air ﬂow was controlled
using a computerized open-ﬂow-through system. Atmospheric air
was pumped in and dried using a silica gel column before reaching
the temperature control cabinet Conviron
. Flow rate was main-
tained at a level ensuring o1% change in oxygen consumption
(Lindsay et al., 2009a) and varied between 0.5 and 0.9 L min
Flow rate of each chamber was measured using Brooks thermal
C.T. Downs et al. / Journal of Thermal Biology 37 (2012) 144–150 145
mass ﬂow meter (Model 580E: Hatﬁeld, PA, USA) factory cali-
brated to standard temperature and pressure (STP). Solenoid
valves and a separate pump for each chamber were used to take
simultaneous measurements of six chambers (ﬁve experimental
and one control chamber) (Lindsay et al., 2009a). Excurrent air
passed through a water condenser to remove most of the water
vapor, then a silica gel column to remove any residual water, and
soda lime to remove CO
before the oxygen analyzer. Water vapor
extracted by the condenser was used as an indirect measure of
evaporative water loss (EWL) for each bat at each temperature
during summer and winter respectively. Measurements of various
parameters for each chamber (T
, ﬂow rate and fractional O
concentrations) were recorded as described in Lindsay et al.
(2009a). Air from each chamber was allowed to stabilize for 45 s
before measurement. The ﬁrst 2 h (before 09h00) of data recorded
were excluded from analyses so bats were post-absorptive and
resting. The lowest hourly mean VO
during the day for each
individual was taken as its RMR
2.3. Core body temperature
Early in June 2010, each E. wahlbergi had a calibrated data
(Model DS 1922 L70.06 1C, Dallas semicon-
ductor, USA), covered with parafﬁn wax, surgically implanted into
the peritoneal cavity under anesthetic by a veterinarian. These
recorded core T
severy 20 min while bats were in their outdoor
aviary. The ﬁrst 2 day of data were ignored and regarded as
2.4. Data analysis
Statistical analyses were performed using STATISTICA (Statsoft
Inc., version 7, Tulsa, USA). As seven metabolic measurements
were performed on each individual bat in a particular season,
Generalized Linear Models (GLM) Repeated Measures of ANOVA
(RMANOVA) was used to analyze RMR
s to determine change
. Post hoc Tukey’s HSD tests were used to determine
signiﬁcant differences in RMR
at various T
s. These results were
used to determine the width of the TNZ in both summer and
winter (Lindsay et al., 2009a,b). Body mass and EWL were also
analyzed in a similar way. Data obtained are presented as
3.1. Body mass
Body mass of E. wahlbergi ranged from 86.42 to 144.51 g
(mean 115.61717.79 g) in both seasons. As individuals varied
in body mass metabolic measurements were expressed as speciﬁc
values. Generally males were heavier than females. Body mass
was signiﬁcantly higher in winter than in summer at different T
¼3.487, P¼0.006, Fig. 1). However, within
seasons, no differences in body mass were observed (Post hoc
Tukey’s HSD test, P40.05). Furthermore, body mass before each
trial was signiﬁcantly higher than body mass after each trial for
both summer and winter respectively (RMANOVA, F
3.2. Metabolic measurements
There was a signiﬁcant difference in RMR
at various T
E. wahlbergi between summer and winter (RMANOVA, F
5.113, P¼0.002, Fig. 2a). In winter, there was a signiﬁcant difference
in metabolic rate between 5 1Cand101C (Post hoc Tukeys’ HSD test,
Po0.05), and between 10 1Cand151C (Post hoc Tukey’s HSD test,
P¼0.0004), but not between 15 1Cand201C (Post hoc Tukeys’ HSD
test, P40.05). In summer, a signiﬁcant difference in metabolic rate
was observed between 20 1Cand251C (Post hoc HSD test, Po0.05).
The TNZ was broad in winter, ranging from 15 to 35 1C while in
summer it was narrower from 25 to 30 1C(Fig. 2a). Mini-
mum metabolic rate in the TNZ which was taken as
BMR was recorded at 30 1C for both seasons. The winter BMR
(1.26070.070 ml O
) was signiﬁcantly higher than the
summer BMR (1.03470.182 ml O
82.1% of winter BMR) (T-test, df¼9, t¼5.312, P¼0.013). At the
Vertical bars denote +/- standard errors
Ambient temperature (°C)
Initial body mass (g)
Fig. 1. Seasonal variation in initial body mass of Wahlberg’s epauletted fruit bats
at various ambient temperatures in winter and summer.
Ambient temperature (°C)
VO (ml O g h )
Vertical bars denote +/- standard errors
Vertical bars denote +/- standard errors
Ambient temperature (°C)
10 15 20 25 30 35
10 15 20 25 30 35
Fig. 2. (a) Oxygen consumption (RMR
) of Wahlberg’s epau-
letted fruit bats and (b) time when this was reached at various ambient
temperatures in winter and summer.
C.T. Downs et al. / Journal of Thermal Biology 37 (2012) 144–150146
sin both seasons, the time when RMR
was reached for E.
wahlbergi did not differ signiﬁcantly (RMANOVA, F
P¼0.134, Fig. 2b). However, there was individual variation and the
time for 35 1C was signiﬁcantly earlier in both seasons compared
with other ambient temperatures (Post hoc HSD test, Po0.05;
Fig. 2b). The time to reach RMR
at 10 1C may have affected the
value in winter (Fig. 2a and b) as it appears that the bats increased
MR possibly to defend T
3.3. Body temperature
There was no signiﬁcant difference in ﬁnal rectal T
E. wahlbergi between both summer and winter at various T
¼1.948, P¼0.090, Fig. 3). Rectal T
strongly correlated with T
particularly in summer (summer
¼0.98, P¼0.00; winter r
¼0.93, P¼0.004; with ﬁtted linear
lines summer Y¼32.24þ0.89x; winter Y¼31.48þ0.93x;Fig. 3).
of E. wahlbergi during winter showed that the bats
exhibited heterothermy but not torpor (Figs. 4 and 5). Individual
variation was evident but all had the lowest core T
rest-phase photophase (Fig. 5b) with lowest recorded 31.99 1C
and maximum 41.78 1C during the June–July winter period
(Fig. 5). In contrast T
sshowed far greater variation during this
period (June 2010 lowest daily meanþSD 8.66þ5.93 1C, highest
daily mean 22.05þ5.10 1C, lowest minimum 0.20 1C, highest
maximum 31.60 1C; July 2010 lowest daily mean 11.00 þ2.55 1C,
highest daily mean 18.00þ5.44 1C, lowest minimum 2.60 1C,
highest maximum 28.00 1C; (Wilson et al., 2011, South African
Weather Service). For one individual core body temperature was
recorded from June to September (MeanþSD, 36.57þ1.17 1C; Min
29.65 1C, Max 41.12 1C).
3.4. Evaporative water loss
There was a signiﬁcant difference in EWL between T
two seasons (RMANOVA F
¼4.638, P¼0.0014). In winter
there were signiﬁcant differences in EWL of E. wahlbergi between
¼24.340, P¼0.0005; Fig. 6). EWL at
51C and 10 1C were signiﬁcantly lower than at any other T
hoc Tukey’s HSD test, Po0.05). Similarly in summer there were
signiﬁcant differences in EWL of E. wahlbergi between various T
¼22.060, P¼0.0005; Fig. 6). EWL in summer at
25 1C, 30 1C and 35 1C were signiﬁcantly higher than the other T
(Post hoc Tukey’s HSD test, Po0.05). At 35 1C in both summer and
winter, the bats were removed earlier from the respirometer as a
result of salivation and dehydration.
Afrotropical regions, including South Africa, are rendered unpre-
dictable by ENSO (Landman and Goddard, 2010). Animals inhabit-
ing regions rendered unpredictable by ENSO should have a lower
BMR in comparison to regions with predictable environments in
Ambient temperature (°C)
Rectal body temperature (°C)
10 15 20 25 30 35
Fig. 3. Rectal body temperature of Wahlberg’s epauletted fruit bats at different
ambient temperatures in summer and winter. Dotted lines indicate regression
July 2010 - Bat 4
Core body temperature (°C)
Fig. 4. Core body temperature of a Wahlberg’s epauletted fruit bat during winter
(July) when in an outdoor aviary.
Vertical bars denote +/- standard errors
Body temperature (°C)
Vertical bars denote +/- standard errors
Core body temperature (°C)
5911 13 15 17 19 21 2373
11 13 15 17 19 21 23
Fig. 5. Individual variation in hourly mean core body temperature of Wahlberg’s
epauletted fruit bats during winter (June–July) where (a) is with time (n¼31 day)
and (b) is with day (n¼31 day).
C.T. Downs et al. / Journal of Thermal Biology 37 (2012) 144–150 147
order to offset the effects of low resource availability (Lovegrove,
2000). In this study, the mass-speciﬁc BMR of E. wahlbergi was
found to be 137% in winter and 106% in summer of that predicted
by allometric scaling for a mammal of its size using the Chiropteran
equation (Hayssen and Lacy, 1985). This unexpectedly suggests
winter upregulation rather than summer down-regulation of BMR.
This differs to Smit and McKechnie’s (2010) assertion that Afro-
tropical endotherms (in particular birds) should show down-
regulation of BMR in winter as a consequence of the unpredictable
environment, but is similar to data from red-winged starlings
Onychognathus morio (Chamane and Downs, 2009). The greater
vasa parrot Caracopsis vasa showed summer upregulation of BMR,
which also differed with this assertion (Lovegrove et al., 2011). It
also questions the use of allometric scaling to predict mammalian
BMR, as it has been argued in many previous studies that a single
allometric relationship cannot sufﬁciently predict the BMR for all
mammals (McNab, 1988;Lovegrove, 2000), particularly if the value
used for a species was for a particular season.
A recent study (Almeida and Cruz-Neto, 2011) examined the
phenotypic capacity of three species of fruit-eating phyllostomid
bats from Brazil and found no variation in BMR between seasons.
Environmental conditions, rather than season, determine torpor use
and temperature selection in large mouse-eared bats (Myotis myotis)
(Wojciechowski et al., 2007), and in a relatively small subtropical
blossom-bat (Syconycteris australis) in Australia (Geiser et al., 2005).
In contrast, our E. wahlbergi data show that thermal energetics of
Afrotropical fruit-eating bats may be more affected by season.
Winter BMR of E. wahlbergi was higher than summer BMR,
consistent with our prediction that BMR would be elevated in
winter compared with summer. These results differ to a number
of studies which have found no seasonal differences in BMR
for mammal species (Geiser and Baudinette, 1987;Feist and
White, 1989;Coburn and Geiser, 1998). Interestingly, the latter
study found S. australis enter torpor with a higher frequency in
summer suggesting this is the season when they experience the
greatest pressure in maintaining a constant T
due to energy and
ecological constraints including unpredictable climate and food
supply (Coburn and Geiser, 1998).
According to Hill et al. (2004), species experiencing a high
seasonal variability in ambient conditions are predicted to show a
great seasonal variation in physiological parameters such as MR
and BMR. Furthermore, the South East Africa regions, the area
where E. wahlbergi occur, show the highest degree of seasonal
variation in T
across the whole of the Afrotropical region (Jury
and Nkosi, 2000). The increase in BMR during winter in
E. wahlbergi appears to be a metabolic process that helps this
species overcome heat loss during winter.
Winter body mass of E. wahlbergi was signiﬁcantly higher than
the summer body mass. An animal’s body mass is governed by
several factors such as ambient temperatures, physiological status
and food availability (Zheng et al., 2008). Seasonal thermoregu-
latory responses in small mammals (o500 g) are centered more
on increasing the thermogenic capacity through an increase in
non-shivering thermogenesis (NST) capacity and large reductions
in conductance (Lovegrove, 2005). However, bats are known to
have a labile body mass, with the greatest variation in body mass
over a 24 h period recorded for any mammal species (Studier
et al., 1970). Furthermore, the body mass of bats is largely
dependent upon the nutritive status of an individual (i.e. a hungry
bat weighs far less than a well-fed bat) (McNab, 1982). Therefore
the seasonal increase in body mass of E. wahlbergi may not be as a
result of increased fat deposits for insulation or metabolizing
tissues as observed in other endotherms (Zheng et al., 2008), but
since it coincides with an increase in BMR, it may occur as a result
of excessive eating as a result of increased metabolic costs
associated with an increase in BMR. Of interest, is the elevated
at 10 1C in winter, which we speculate could be an attempt
to defend T
at low T
sin winter when resources are not limiting.
The TNZ of E. wahlbergi showed a signiﬁcant seasonal shift
from a narrow TNZ in summer to a very broad TNZ in winter,
which was consistent with our predictions. A broad TNZ can serve
as an energy saving mechanism, allowing an organism to tolerate
a wide range of temperatures without having to increase its
metabolism (Hill et al., 2004). Furthermore, since an increase in
TNZ is coupled with a decrease in conductance and an increase
in insulation (Hill et al., 2004), this further reduces the energy
expenditure by an organism (Cooper and Gessaman, 2004). There-
fore an increase in TNZ during winter is advantageous, as it allows
maintenance of a minimal normothermic MR over a wide range of
ambient temperatures (Hill et al., 2004).
Although no evidence of torpor (see Geiser, 2004 for deﬁni-
tion) was observed in this study, E. wahlbergi was heterothermic.
Individuals generally lowered core T
by only a few degrees
during their daytime rest-phase despite much lower T
In both winter and summer, rectal T
of the bats decreased
linearly with T
s. These results correspond with a number of
studies conducted on fruit- and blossom-eating chiropterans
(Bartholomew et al., 1964;1970;McNab, 1989;Genoud et al.,
1990;Geiser et al., 1996;Bonaccorso and McNab, 1997;Ochoa-
˜a and Kunz, 1999;Coburn and Geiser, 1998;Bartels et al.,
1998;McNab and Armstrong, 2001;McNab and Bonaccorso,
2001;Geiser et al., 2005;Riek et al., 2010). This shows that these
chiropterans adopt the energy saving strategy of heterothermy
particularly during their rest-phase, and with decreased T
scarcity irrespective of body size. Furthermore, E. wahlbergi is
signiﬁcantly bigger than many fruit- and blossom-eating bats,
making it less likely to rely on torpor, but rather some degree of
heterothermy as a means of conserving energy.
There was a signiﬁcant increase in EWL in E. wahlbergi with an
increase in T
in summer and winter. Although there was such a
high rate of EWL at high T
s, no signiﬁcant increase in metabolic
rate was observed. At low T
s, EWL occurs as a by-product of
ventilation since the mammalian skin is not perfectly imperme-
able to water (Maloney et al., 1999). EWL during the hottest part
of the day poses a considerable dehydration stress on this species
since at 35 1C, excessive salivation was observed in this species.
Furthermore, in another similar study, when this species was
placed in a respirometer at 40 1C, one of the bats died, and some
deaths of bats were observed in outside aviaries on extreme hot
days (440 1C) (M.M. Zungu, Downs, C.T. pers. obs.). Furthermore,
bats do not have sweat glands, and thus depend on less-efﬁcient
means of dissipating excess heat such as salivation, panting, body
licking and wing fanning (McNab, 1982). This provides further
support that this species is intolerant of high T
sas a result of
ineffective means of ofﬂoading excess heat.
Vertical bars denote +/- standard errors
Ambient temperature (°C)
Evaporative water loss (ml g-1 h-1)
Fig. 6. Evaporative water loss of Wahlberg’s epauletted fruit bats at various
ambient temperatures in summer and winter.
C.T. Downs et al. / Journal of Thermal Biology 37 (2012) 144–150148
In conclusion, the E. wahlbergi increased their RMR
during winter. This increase is important for winter survival as it
leads to an increase in metabolically-produced heat. The increase
in E. wahlbergi’s TNZ range during winter is also important for
their winter survival, as they use less energy to keep warm when
drops. The observation of heterothermy in E. wahlbergi con-
ﬁrmed the results of previous studies which have shown that the
former sub-order Megachiropterans are indeed heterothermic,
particularly during the rest-phase. The ability of E. wahlbergi to
use heterothermy is important as it spends less energy maintain-
ing elevated T
s. This study also showed that E. wahlbergi is
intolerant of high T
s, as at high T
s, excessive salivation was
observed, and may lead to death if T
sgo higher. The intolerance
of high T
sby E. wahlbergi have signiﬁcant implications about the
inﬂuence global warming would have on this species, as it
suggests that it is likely to be impacted. Furthermore, this study
shows the importance of microclimate on roost selection during
daytime rest phase period by the species (Boyles, 2007), improv-
ing our understanding of the ecology of this species. Lack of data
on the energetics and seasonal variation of physiological para-
meters for Afrotropical bats in general suggest that more work
is required for comparison with results of those in other regions
and improve our understanding of the ecophysiology, particularly
energetics, of fruit and nectar feeding bats, particularly given the
climate change scenarios.
Joy Coleman, Musi Mkhohlwa, Robyn Khoury and Alex Baxter
are thanked for assisting with data collection. Thami Mjwara is
thanked for feeding the bats during weekdays.
Almeida, M.C., Cruz-Neto, A.P., 2011. Thermogenic capacity of three species of
fruit-eating phyllostomid bats. J. Therm. Biol. 36, 225–231.
Arnold, W., Ruf, T., Kunz, R., 2006. Seasonal adjustment of energy budget in a large
wild mammal, the Przewalski horse (Equus ferus przewalskii) II. Energy
expenditure. J. Exp. Biol. 209, 4566–4573.
Audet, D., Fenton, M.B., 1988. Heterothermy and the use of torpor by the bat
Eptesicus fuscus (Chiroptera: Vespertilionidae): a ﬁeld study. Physiol. Zool. 61,
Bartels, W., Law, B.S., Geiser, F., 1998. Daily torpor and energetics in a tropical
mammal, the northern blossom-bat, Macroglossus minimus (Megachiroptera).
J. Comp. Physiol. B 168, 233–239.
Bartholomew, G.A., Dawson, W.R., Lasiewski, R.C., 1970. Thermoregulation and
heterothermy in some of the smaller ﬂying foxes (Megachiroptera) of New
Guinea. Z. Vergl. Physiol. 70, 196–209.
Bartholomew, G.A., Leitner, P., Nelson, J.E., 1964. Body temperature, oxygen
consumption, and heart rate in three species of Australian ﬂying foxes. Physiol.
Zool. 37, 179–198.
Bishop, K.L., 2008. The evolution of ﬂight in bats: narrowing the ﬁeld of plausible
hypotheses. Quart. Rev. Biol. 83, 153–168.
Bonaccorso, F.J., McNab, B.K., 1997. Plasticity of energetics in blossom bats
(Pteropodidae): impact of distribution. J. Mammal. 78, 1073–1088.
Boyles, J.G., 2007. Describing roosts used by forest bats: the importance of
microclimate. Acta Chirop. 9, 297–303.
Bronner, G.N., Maloney, S.K., Buffenstein, R., 1999. Survival tactics within ther-
mally-challenging roosts: heat tolerance and cold sensitivity in the Angolan
free-tailed bat, Mops condylurus. S. Afr. J. Zool. 34, 1–10.
Brown, M., Downs, C.T., 2003. The role of shading behaviour in the thermoregula-
tion of breeding crowned plovers (Vanellus coronatus). J. Therm. Biol. 28,
Brown, K., Downs, C.T., 2005. Seasonal behavioural patterns of free-living rock
hyrax (Procavia capensis). J. Zool. London 265, 311–326.
Brown, K., Downs, C.T., 2007. Basking behaviour in rock hyrax (Procavia capensis)
during winter. Afr. Zool. 42, 70–79.
Bush, N.G., Downs, C.T., Brown, M., 2008. Seasonal effects of thermoregulatory
responses of rock kestrels, Falco rupicolis. J. Therm. Biol. 33, 404–412.
Chamane, S.C., Downs, C.T., 2009. Seasonal effects on metabolism and thermo-
regulation abilities of the red-winged starling (Onychognathus morio). J. Therm.
Biol. 34, 337–341.
Choi, I.-H., Oh, Y.K., Jung, N.-P., Gwag, B.J., Shin, H.-C., 1998. Metabolic rate and
thermolabile properties of Ognev’s great tube-nosed bat Murina leucogaster in
response to variable ambient temperature. Korean J. Biol. Sci. 2, 49–53.
Coburn, D.K., Geiser, F., 1998. Seasonal changes in the energetics and torpor
patterns in the sub-tropical blossom-bat, Synconyctesis australis. Oecologia
Cooper, S.J., Gessaman, J.A., 2004. Thermoregulation and habitat preference in
mountain chickadees and juniper titmice. Condor 106, 852–861.
Cory Toussaint, D., McKechnie, A.E., van der Merwe, M., 2010. Heterothermy in
free-ranging male Egyptian free-tailed bats (Tadarida aegyptica) in a subtro-
pical climate. Mamm. Biol. 75, 466–470.
Cryan, P.M., Wolf, B.O., 2003. Sex differences in the thermoregulation and
evaporative water loss of a heterothermic bat, Lasiurus cinereus, during its
spring migration. J. Exp. Biol. 206, 3381–3390.
Dawson, W.R., 2003. Plasticity in avian responses to thermal changes- an essay in
honour of Jacob Marder. Isr. J. Zool. 49, 95–109.
Downs, C.T., Brown, M., 2002. Nocturnal heterothermy and torpor in the malachite
sunbird (Nectarinia famosa). Auk 119, 251–260.
Feist, D.D., White, R.G., 1989. Terrestrial mammals in cold. In: Wang, L.C.H. (Ed.),
Advances in Comparative and Environmental Physiology, Springer, Berlin,
Geiser, F., 2004. Metabolic rate and body temperature reduction during hiberna-
tion and torpor. Ann. Rev. Physiol. 66, 239–374.
Geiser, F., Baudinette, R.V., 1987. Seasonality of torpor and thermoregulation in
three dasyurid marsupials. J. Comp. Biochem. Physiol. B 157, 335–344.
Geiser, F., Coburn, D.K., K¨
ortner, G., Law, B.S., 1996. Thermoregulation, energy
metabolism, and torpor in blossom-bats,Syconycteris australis (Megachiroptera).
J. Zool. Londo n 239, 583–590 .
Geiser, F., Law, B.S., K ¨
ortner, G., 2005. Daily torpor in relation to photoperiod in a
subtropical blossom-bat, Syconycteris australis (Megachiroptera). J. Therm.
Biol. 30, 574–579.
Geiser, F., Ruf, T., 1995. Hibernation versus daily torpor in mammals and birds:
physiological variables and classiﬁcation of torpor patterns. Physiol. Zool. 68,
Genoud, M., 1993. Temperature regulation in subtropical tree bats. Comp.
Biochem. Physiol. A 104, 321–331.
Genoud, M., Bonaccorso, F.J., Arends, A., 1990. Rate of metabolism and tempera-
ture regulation in two small tropical insectivorous bats (Peropteryx macrotis
and Natalus tumidirostris). Comp. Biochem. Physiol. A 97, 229–234.
Hart, J.S., 1962. Seasonal acclimatization in four species of small wild birds.
Physiol. Zool. 35, 224–236.
Hayssen, V., Lacy, R.C., 1985. Basal metabolic rates in mammals: taxonomic
differences in the allometry of BMR and body mass. Comp. Biochem. Physiol.
A 81, 741–754.
Herreid, C.F., Schmidt-Nielsen, K., 1966. Oxygen consumption, temperature and
water loss in bats from different environments. Am. J. Physiol. 211, 108–1112.
Hill, R.W., Wyse, G.A., Anderson, M., 2004. Animal Physiology. Sinauer, Sunderland.
Hock, R.J., 1951. The metabolic rates and body temperatures of bats. Biol. Bull. 101,
Holmgren, M., Scheffer, M., Ezcurra, E., Gutie
´rrez, J.R., Mohren, G.M.J., 2001. El Nin
effects on the dynamics of terrestrial ecosystems. TREE 16, 89–94.
Holyoak, G.W., Stones, R.C., 1971. Temperature regulation of the little brown bat,
Myotis lucifugus after acclimation at various ambient temperatures. Comp.
Biochem. Physiol. A 39, 413–420.
Hosken, D.J., Withers, P.C., 1997. Temperature regulation and metabolism of an
Australian bat, Chalinolobus gouldii (Chiroptera: Vespertilionidae) when
euthermic and torpid. J. Comp. Physiol. B 167, 71–80.
Hosken, D.J., Withers, P.C., 1999. Metabolic physiology of euthermic and torpid
lesser long-eared bats, Nyctophilus geoffroyi (Chiroptera: Vespertilionidae).
J. Mammal. 80, 42–52.
Hutcheon, J.M., Kirsch, J.A.W., 2006. A moveable face: deconstructing the Micro-
chiroptera and a new classiﬁcation of extant bats. Acta Chirop. 8, 1–10.
International Union of Physiological Sciences (IUPS), 2001. Glossary of terms for
thermal physiology. Japn. J. Physiol. 51, 1–36.
Jacobs, D.S., Kelly, E.J., Mason, M., Stoffberg, S., 2007. Thermoregulation in two free-
ranging subtropical insectivorous bats: Scotophilus species (Vespertilionidae).
Can. J. Zool. 85, 883–890.
Jury, M.R., Nkosi, S.E., 2000. Easterly ﬂow in the tropical Indian Ocean and climate
variability over south-east. Afr. Water S.A. 26, 147–152.
Kurta, A., Kunz, T.H., 1988. Roosting metabolic rate and body temperature of male
little brown bats (Myotis lucifugus) in summer. J. Mammal. 69, 645–651.
Landman, W.A., Goddard, L., 2010. Statistical recalibration of GCM Forecasts over
Southern Africa using model output statistics. J. Climate 15, 2038–2055.
Licht, P., Leitner, P., 1967. Physiological responses to high environmental tem-
peratures in three species of microchiropteran bats. Comp. Biochem. Physiol.
Lindsay, C.V., Downs, C.T., Brown, M., 2009a. Physiological variation in amethyst
sunbirds (Chalcomitra amethystina) over an altitudinal gradient in winter.
J. Exp. Biol. 212, 483–493.
Lindsay, C.V., Downs, C.T., Brown, M., 2009b. Physiological variation in amethyst
sunbirds (Chalcomitra amethystina) over an altitudinal gradient in summer.
J. Therm. Biol. 34, 190–191.
Lovegrove, B.G., 2000. The zoogeography of mammalian basal metabolic rate.
Am. Nat. 156, 201–219.
Lovegrove, B.G., 2005. Seasonal thermoregulatory responses in mammals. J. Comp.
Biol. B 175, 231–247.
C.T. Downs et al. / Journal of Thermal Biology 37 (2012) 144–150 149
Lovegrove, B.G., Perrin, M.R., Brown, M., 2011. The allometry of parrot BMR:
seasonal data for the greater vasa parrot, Caracopsis vasa, from Madagascar.
J. Comp. Biol. B 181, 1075–1087.
Lyman, C.P., 1970. Thermoregulation and metabolism in bats. In: Wimsatt, W.A.
(Ed.), Biology of Bats, vol. 1. , Academic Press, London, pp. 301–330.
Lyman, C.P., 1982. Who is who among hibernators?. In: Lyman, C.P., Willis, J.S.,
Malan, A., Wang, L.C.H. (Eds.), Hibernation and Torpor in Mammals and Birds,
Academic Press, New York, pp. 12–36.
Maloney, S.K., Bronner, G.N., Buffenstein, R., 1999. Thermoregulation in the
Angolan free-tailed bat Mops condylurus: a small mammal that uses hot
roosts. Physiol. Zool. 72, 385–396.
Marom, S., Korine, C., Wojciechowski, M.S., Tracy, C.R., Pinshow, B., 2006. Energy
metabolism and evaporative water loss in the European free-tailed bat and
Hemprich’s long-eared bat (Microchiroptera): species sympatric in the Negev
Desert. Physiol. Biochem. Zool. 79, 944–956.
Matheson, A.L., Campbell, K.L., Willis, C.K.R., 2010. Feasting, fasting and freezing:
energetic effects of meal size temperature on torpor expression by little brown
bats, Myotis lucifugus. J. Exp. Biol. 213, 2165–2173.
McKechnie, A.E., 2008. Phenotypic plasticity in basal metabolic rate and the
changing view of avian physiological diversity: a review. J. Comp. Physiol. B
McNab, B.K., 1969. The economics of temperature regulation in neotropical bats.
Comp. Biochem. Physiol. 31, 227–268.
McNab, B.K., 1982. Evolutionary alternatives in the physiological ecology of bats.
In: Kunz, T.H. (Ed.), Ecology of Bats, Plenum, New York, pp. 151–163.
McNab, B.K., 1988. Complications inherent in scaling the basal metabolic rate of
metabolism in mammals. Quart. Rev. Biol. 63, 25–54.
McNab, B.K., 1989. Temperature regulation and rate of metabolism in three
Bornean bats. J. Mammal. 70, 153–161.
McNab, B.K., Armstrong, M.I., 2001. Sexual dimorphism and scaling of energetics
in ﬂying foxes of the genus Pteropus. J. Mammal. 82, 709–720.
McNab, B.K., Bonaccorso, F.J., 2001. The metabolism of New Guinean pteropodid
bats. J. Comp. Physiol. B 171, 201–214.
Monadjem, A., Taylor, P.J., Cotterill, F.P.D., Schoeman, S.C., 2010. Bats of Southern
Africa and Central Africa. Wits University Press, Johannesburg.
Nzama, S.N., Downs, C.T., Brown, M., 2010. Seasonal variation in metabolism-
temperature regulation of house sparrows (Passer domesticus)inKwaZulu-Natal,
South Africa. J. Therm. Biol. 35, 100–104.
˜a, H., Kunz, T.H., 1999. Thermoregulatory behavior in the small island
ﬂying fox, Pteropus hypomelanus (Chiroptera: Pteropodidae). J. Therm. Biol. 24,
Ransome, R.D., 1990. The Natural History of Hibernating Bats. Helm, Bromley.
Riek, A., K¨
ortner, G., Geiser, F., 2010. Thermobiology, energetic and activity
patterns of the Eastern tube-nose bat (Nyctimene robinsoni) in the Australasian
tropics: effect of temperature and lunar cycle. J. Exp. Biol. 213, 2557–2564.
´n, A., 1995. Metabolic rates and thermal conductance in four
species of neotropical bats roosting in hot caves. Comp. Biochem. Physiol. A
Saarela, S., Klapper, B., Heldmaier, G., 1995. Daily rhythm of oxygen consumption and
thermoregulatory responses in some European winter- or summer-acclimatized
ﬁnches at different ambient temperatures. J. Comp. Physiol. Biochem. B 165,
Simeone, A., Luna-Jorquera, G., Wilson, R.P., 2004. Seasonal variations in the
behavioural thermoregulation of roosting Humboldt penguins (Spheniscus
humboldti) in northern Chile. J. Ornithol. 145, 35–40.
Smit, B., McKechnie, A.E., 2010. Avian seasonal metabolic variation in a subtropical
desert: basal metabolic rates are lower in winter than in summer. Funct. Ecol.
Solick, D.I., Barclay, R.M.R., 2007. Geographic variation in the use of torpor and
roosting behaviour of female western long-eared bats. J. Zool. London 272,
Stawski, C., 2010. Torpor during the reproductive season in a free-ranging
subtropical bat, Nyctophilus bifax. J. Therm. Biol. 35, 245–249.
Stawski, C., Geiser, F., 2010. Seasonality of torpor patterns and physiological
variables of a free-ranging sub-tropical bat. J. Exp. Biol. 213, 393–399.
Stegeman, J., 1989. Selected metabolic studies of the fruit bat, Epomophorus
wahlbergi, in captivity. M.Sc. Thesis, University of Natal, Durban.
Storm, J., Boyles, J., 2011. Body temperature and body mass of hibernating little
brown bats Myotis lucifugus; in hibernacula affected by white-nose syndrome.
Acta Theriol. 56, 123–127.
Studier, E.H., O’Farrell, M.J., 1972. Biology of Myotis thysanodes and M. lucifugus
(Chiroptera: Vespertilionidae)—I. Thermoregulation. Comp. Biochem. Physiol.
A 41, 567–595.
Studier, E.H., Procter, J.W., Howell, D.J., 1970. Diurnal body weight loss and
tolerance of weight loss in ﬁve species of Myotis. J. Mammal. 5, 302–309.
Studier, E.H., Wilson, D.E., 1970. Thermoregulation in some neotropical bats.
Comp. Biochem. Physiol. 34, 251–262.
Studier, E.H., Wilson, D.E., 1979. Effects of captivity on thermoregulation and
metabolism in Artibeus jamaicensis (Chiroptera: Phyllostomatidae). Comp.
Biochem. Physiol. A 62, 347–350.
Taylor, P.J., 2005. Order Chiroptera (Bats). In: Skinner, J.D., Chimimba, C.T. (Eds.),
The Mammals of Southern Africa Subregion, third edition , Cambridge Uni-
versity Press, Cambridge.
Turbill, C., Law, B.S., Geiser, F., 2003. Summer torpor in a free ranging bat from
subtropical Australia. J. Therm. Biol. 28, 223–226.
Vivier, L., van der Merwe, M., 2007. The incidence of torpor in winter and summer
in the Angolan free-tailed bat, Mops condylurus (Microchiroptera: Molossidae),
in a subtropical environment, Mpumalanga, South Africa. Afr. Zool. 42, 50–58.
Webb, P.I., Speakman, J.R., Racy, P.A., 1995. Evaporative water loss in two
sympatric species of vespertilionid bat, Plecotus auritus and Myotis daubentoni:
relation to foraging mode and implications for roost site selection. J. Zool.
London 235, 269–278.
Willis, C.K.R., Lane, J.E., Likenes, E.T., Swanson, D.L., Brigham, R.M., 2005. Thermal
energetics of female big brown bats (Eptesicus fuscus). Can. J. Zool. 83,
Wilson, A.-L., Downs, C.T., Brown, M., 2011. Seasonal variation in metabolic rate of
a medium-sized frugivore, the Knysna turaco (Tauraco corythaix). J. Therm.
Biol. 36, 167–172.
Wojciechowski, M., Jeﬁmow, M., T˛egowska, E., 2007. Environmental conditions,
rather than season, determine torpor use and temperature selection in large
mouse-eared bats (Myotis myotis). Comp. Biochem. Physiol. A 147, 828–840.
Withers, P.C., 1992. Comparative Animal Physiology. Saunders, College, Orlando.
Zheng, W., Liu, J., Jiang, X., Fang, Y., Zhang, G., 2008. Seasonal variation on
metabolism and thermoregulation in Chinese bulbul. J. Therm. Biol. 33,
C.T. Downs et al. / Journal of Thermal Biology 37 (2012) 144–150150