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Seasonal effects on thermoregulatory abilities of the Wahlberg's epauletted fruit bat (Epomophorus wahlbergi) in KwaZulu-Natal, South Africa

Seasonal effects on thermoregulatory abilities of the Wahlberg’s epauletted
fruit bat (Epomophorus wahlbergi) in KwaZulu-Natal, South Africa
C.T. Downs
, M.M. Zungu, M. Brown
School of Biological and Conservation Sciences, University of KwaZulu-Natal, Private Bag X 01, Scottsville 3209, Pietermaritzburg, South Africa
article info
Article history:
Received 6 September 2011
Accepted 13 December 2011
Available online 28 December 2011
Seasonal variation
Metabolic rate
Body temperature
Fruit bat
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.
1. Introduction
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
normal T
, 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
particular T
, 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
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Journal of Thermal Biology
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E-mail address: (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
´n, 1995;
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
highly unpredictable.
The aim of this study was to investigate the effect of season on
the MR of E. wahlbergi. The objectives were to determine oxygen
consumption (VO
) 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
with summer.
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
S; 30123
E) dur-
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
ad lib.
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
was measured
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
logger i-Buttons
(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
recovery time.
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
with T
. 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
means7standard error.
3. Results
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
(6, 54)
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
(6, 54)
3.2. Metabolic measurements
There was a significant difference in RMR
at various T
E. wahlbergi between summer and winter (RMANOVA, F
(6, 24)
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)
Time (Hours)
10 15 20 25 30 35
10 15 20 25 30 35
Fig. 2. (a) Oxygen consumption (RMR
ml g
) 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
various T
sin both seasons, the time when RMR
was reached for E.
wahlbergi did not differ significantly (RMANOVA, F
(6, 24)
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
(6, 54)
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).
Core T
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
sduring the
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
sin the
two seasons (RMANOVA F
(6, 36)
¼4.638, P¼0.0014). In winter
there were significant differences in EWL of E. wahlbergi between
various T
(6, 54)
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
(6, 52)
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.
4. Discussion
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
Time (Hours)
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
sin winter.
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
or food
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
and BMR
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
113, 467–473.
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,
pp. 327–360.
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.
22, 371–387.
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
178, 235–247.
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
110, 347–355.
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.
24, 330–339.
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
... The members of fruit bats are often vulnerable to high temperatures (Downs et al. 2012) as they are devoid of sweat glands (Burbank and Young 1934). So, they need to dissipate body heat by increasing the area of exposed wing surface or enhanced evaporative cooling by salivating and licking their wing membrane (Nelson 1965a). ...
... So, they need to dissipate body heat by increasing the area of exposed wing surface or enhanced evaporative cooling by salivating and licking their wing membrane (Nelson 1965a). Among Pteropus bats, evaporative cooling through salivating and licking their wing membranes, wing spreading, wing flapping and panting are considered to be a part of their thermoregulatory strategy (Nelson 1965a;Puddicombe 1981;McNab 1982;Ochoa-Acuña and Kunz 1999;Welbergen et al. 2008;Downs et al. 2012). Bartholomew et al. (1964) reported that grey-headed flying fox (Pteropus poliocephalus Temminck, 1825) adopt body licking as a thermoregulatory strategy when the ambient temperature reaches 40°C. ...
... Hence, with rise in temperature, thermoregulation was significantly higher in summer than winter subsequently reducing their duration of sleep. Studies on other pteropodid species also showed sleeplessness during summer than winter as they need to involve in more thermoregulation to efficiently dissipate their body heat (Hock 1951;McNab 1982;Downs et al. 2012). But, Biologia evaporative water loss is inversely related to ambient water vapour pressures (Procter and Studier 1970;Studier 1970). ...
Full-text available
Indian flying fox Pteropus giganteus (Brünnich, 1782) is one of the largest fruit bats (Pteropodidae) in the world. However, studies on seasonal variations and influence of weather parameters on diurnal roosting of this species in urban areas are almost non-existent. We carried out this study in a major urban landscape of India to determine which weather parameters influence diurnal roosting behaviours of Indian flying fox. Behavioural data was assessed through scan sampling method. Sleeping, thermoregulatory, locomotion and communicative behaviour, all of which varied significantly, showing highest incidences of sleeping followed by thermoregulatory, locomotion and communicative behaviours. Sleeping was negatively related with thermoregulatory, locomotion and communicative behaviours; thermoregulatory behaviour was positively related with locomotion and locomotion with communicative behaviour. Except sleeping, all other behaviours were positively related to temperature and were higher in summer than winter. Cloud cover negatively influenced sleeping and positively influenced thermoregulatory and locomotion behaviour; humidity negatively influenced thermoregulatory behaviour and rainfall negatively influenced locomotion behaviour of Indian flying foxes. Our findings might be useful for conservation of diurnal roosting sites of fruit bats in many urban landscapes in the recent scenario of changing climate and rapid urbanization throughout the globe.
... Bats are among the smallest endotherms and there is a wealth of data regarding their responses to low ambient temperatures (T a ) (reviewed by Ruf and Geiser, 2015). However, fewer studies have examined bats' response to high T a (Bonaccorso and McNab, 1997;Downs et al., 2012;Korine and Arad, 1993;McNab, 1989;McNab and Bonaccorso, 2001;Noll, 1979;Procter and Studier, 1970;Studier, 1970;Studier and Wilson, 1970) and fewer still have examined responses at T a � 40 � C Cory Toussaint and McKechnie, 2012;Cryan and Wolf, 2003;Leitner, 1967a, 1967b;Ochoa-Acuña and Kunz, 1999). ...
... The mean resting T b we recorded for R. aegyptiacus (36.1 � C) is similar to values previously reported for this species (35.2 -36.5 � C; Korine and Arad, 1993;Noll, 1979) and other pteropodids (33.8-38.3 � C; Bartholomew et al., 1964;Bonaccorso and McNab, 1997;Downs et al., 2012;Jones, 1972;McNab, 1989;McNab and Armstrong, 2001;McNab and Bonaccorso, 2001;Ochoa-Acuña and Kunz, 1999) However, the mass-specific BMR (8.2 mW g -1 ) we report here is higher than previously recorded values from the same species (4.6 -5.2 mW g -1 ; Korine and Arad, 1993;Noll, 1979). Our study involved free-ranging individuals held overnight, whereas Korine and Arad (1993) held individuals in captivity for 2-3 weeks, and Noll's (1979) measurements involved captive individuals acclimated to 15 � C or 30 � C for six weeks. ...
... Compared to the BMRs of bats in general, the BMR of R. aegyptiacus was equivalent to ~173% of their allometrically predicted values (Cory Toussaint and McKechnie, 2012), but falls within the range of other pteropodids (Bartholomew et al., 1964;Bonaccorso and McNab, 1997;Downs et al., 2012;McNab, 1989;McNab and Armstrong, 2001;McNab and Bonaccorso, 2001;Minnaar et al., 2014). The BMR of T. mauritianus was equivalent to 140% of predicted values, and that of E. hottentotus only 64% of predicted values (Cory Toussaint and McKechnie, 2012). ...
... Due to the absence of sweat glands and a high surface-volume ratio, bats are unable to dissipate heat efficiently making them extremely vulnerable to the ill effects of high temperatures (Downs et al., 2012;Korine et al., 2016). One such instance was observed in New South Wales when temperatures reached up to 42°C (Welbergen et al., 2008). ...
... Highly variable habitat temperature because of climate change has an adverse effect on many different bat behavioural patterns. Downs et al. (2012) studied the effects of different seasons on the sleep patterns of the bats, observing that bats slept less in summer than in winter. They reported that high temperatures reduce sleep duration considerably as the bats spent most of their time trying to cool themselves. ...
Climate change has a significant impact on domesticated and wildlife animals globally. Projections for a 2°C rise in atmospheric temperature will result in catastrophic impacts globally. Animal welfare is an integral component of human-animal interaction and it is of paramount importance for wildlife rehabilitation and domestic animals. Animal welfare can be assessed using the five domains model, which includes nutrition, environment, physical health, behaviour, and mental attributes of an animal's response to environmental change. Researchers use some of these domain attributes to evaluate the effects of stress on their animals and to improve the management and welfare of animals. Although there are variations in how animals respond biologically to stress, in general, the five domains model provides a robust tool for research use, and to evaluate the proximate effects of climatic variability on animals. In this review, our research group (The Stress Lab; presents a series of wildlife and domesticated animal examples to showcase how climate change impacts animal welfare. We provide examples of animals from various countries, across both aquatic and terrestrial systems, and provide an overview of the impacts of climate change on each of the five domains of animal welfare. We hope that future researchers will apply the animal welfare domains to evaluate how climate change impacts animals, and further research will pave the way to the protection of animals from the catastrophic impacts of climate change.
... Their limited potential for fat storage means that a substantial reduction of metabolic rate is the only possible option for non-migratory species when faced with longer periods of food shortage during winter at northern latitudes (Wermundsen and Siivonen 2010). Nevertheless, when and to which extent bats utilize torpor differs between species and environmental conditions (Stawski and Geiser 2010;Boyles et al. 2017), such as extreme heat (Reher and Dausmann 2021), unpredictable weather (Downs et al. 2012), or less suitable foraging conditions . ...
Full-text available
To cope with periods of low food availability and unsuitable environmental conditions (e.g., short photoperiod or challenging weather), many heterothermic mammals can readily go into torpor to save energy. However, torpor also entails several potential costs, and quantitative energetics can, therefore, be influenced by the individual state, such as available energy reserves. We studied the thermal energetics of brown long-eared bats (Plecotus auritus) in the northern part of its distributional range, including torpor entry, thermoregulatory ability during torpor and how they responded metabolically to an increasing ambient temperature (Ta) during arousal from torpor. Torpor entry occurred later in bats with higher body mass (Mb). During torpor, only 10 out of 21 bats increased oxygen consumption (V̇O2) to a greater extent above the mean torpor metabolic rates (TMR) when exposed to low Ta. The slope of the torpid thermoregulatory curve was shallower than that of resting metabolic rate (RMR) during normothermic conditions, indicating a higher thermal insulation during torpor. During exposure to an increasing Ta, all bats increased metabolic rate exponentially, but the bats with higher Mb aroused at a lower Ta than those with lower Mb. In bats with low Mb, arousal was postponed to an Ta above the lower critical temperature of the thermoneutral zone. Our results demonstrate that physiological traits, which are often considered fixed, can be more flexible than previously assumed and vary with individual state. Thus, future studies of thermal physiology should to a greater extent take individual state-dependent effects into account.
... Fruit bats do not have sweat glands, making it difficult for them to lose heat and therefore predisposing them to be vulnerable to high temperatures (Downs et al., 2012). If they are unable to dissipate enough body heat to prevent body temperature from increasing above a threshold, then this can result in mortality. ...
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Fruit bats are important pollinators and seed dispersers whose distribution may be affected by climate change and extreme-temperature events. We assessed the potential impacts of those changes and events on the future distribution of fruit bats in Australia. Correlative species distribution modelling was used to predict the distribution of seven (based on data availability) tropical and temperate fruit bat species. We used bioclimatic variables, the number of days where temperature ≥ 42 °C (known to induce extreme heat stress and mortality in fruit bats), and land cover (a proxy for habitat) as predictors. An ensemble of machine-learning algorithms was used to make predictions for the current-day distribution and future (2050 and 2070) scenarios, using multiple emission scenarios (RCP 4.5 and 8.5) and global circulation models (Australian Community Climate and Earth System Simulator, Hadley Centre Global Environment Model Carbon Cycle, and the Model for Interdisciplinary Research on Climate). Our results predict, under current conditions, on average, 9.1% and 90.8% of the area are suitable and unsuitable, respectively. Under future scenarios, on average, 6.7% and 89.7% continued to be suitable and unsuitable, respectively, while there was a 1.1% gain and 2.4% loss in suitable areas. Under current conditions, we predict, on average, 5.6% and 3.4% are suitable inside and outside species’ IUCN-defined range, respectively. While under future scenarios, 4.8% (4.4% stable and 0.4% gain) and 2.9% (2.2% stable and 0.6% gain) are suitable inside and outside the range respectively. On average, the gain in areas inside the range covers 2703.5 grid cells of size 5 km, while outside the range it is 4070.3 cells. Under future scenarios, the loss in areas is predicted to be 1.2% and 1.1% on average, inside and outside species range respectively. Fruit bats are likely to respond to climate change and extreme temperatures by migrating to more suitable areas, including regions not historically inhabited by those species. Our results can be used for identifying areas at risk of new fruit-bat colonisation, such as human settlements and orchards, as well as areas that might be important for habitat conservation.
... Cependant, des cas de thermorégulation ont été déjà notés chez certaines espèces se trouvant dans les tropiques, notamment les frugivores du Nouveau Monde (Audet & Thomas, 1997) et de l'Ancien Monde (Bartels et al., 1998 ;Downs et al., 2015). Certaines Pteropodidae de ces régions peuvent réguler leurs températures corporelles lorsque la température ambiante est trop élevée (Bartholomew et al., 1970) étant donné qu'une importante élévation de la température peut entrainer une mortalité élevée chez ce groupe de chauve-souris (Welbergen et al., 2008 ;Downs et al., 2012 ;Dey et al., 2015). Des réactions reliées aux aspects de regroupements des individus dans une colonie peuvent aussi être adoptées par les chauves-souris pour faire face aux difficultés d'origine climatique (Baudinette et al., 1994 ;Webber & Willis, 2018 (Fleming & Heithaus, 1981 ;Francis, 1994 ;Hall & Richards, 2000 ;Bonaccorso et al., 2002 ;Richter & Cumming, 2005), qui généralement varie selon la saison. ...
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L’écologie comportementale de Rousettus madagascariensis (Pteropodidae), une chauve-souris frugivore endémique de Madagascar qui forme une colonie dans une grotte au sein la Réserve Spéciale d’Ankarana (extrême nord de Madagascar), est rapportée dans ce travail Les activités diurnes de cette espèce ont été filmées dans la grotte à l’aide d’un caméscope à lumière infrarouge en saisons sèche et humide, de 2017 à 2018. Différentes sessions de captures ont été effectuées dans la même grotte entre 2014 et 2018. Les résultats ont indiqué une variation saisonnière significative de tous les comportements filmés sous l’influence de la température régionale moyenne, de la température et de l’humidité relative (rapport entre la pression partielle de la vapeur d’eau dans l’air et la pression de vapeur saturée à la même température) à l’intérieur de la grotte. La saison sèche était caractérisée par une faible valeur de l’indice d’état corporel ou BCI (rapport entre le poids de l’animal et la longueur de l’avant-bras), la fréquence élevée des comportements de repos, la consommation de mouches ectoparasites hématophages, l’accouplement et la configuration en groupe serrés des individus. Durant cette saison, il a été estimé 37 mouches ectoparasites consommées par jour par un individu adulte de Rousettus, menant à une moyenne de 57 905 ectoparasites ingérés par jour par la colonie. Il n’y avait pas de différence statistiquement significative entre le taux ingéré par les adultes mâles et femelles. Pendant la saison humide, la fréquence des comportements de toilettage et de déplacement (vol et rampement) était plus élevée ; les individus se regroupent d’une manière desserrée avec une fréquence élevée des individus solitaires et les valeurs de BCI étaient plus élevées. L'accouplement était principalement observé, par ordre d’importance, au mois de septembre et juillet (saison sèche) ainsi qu’en janvier (saison humide). Ce comportement était en correlation négative avec la précipitation. Les accouplements entre le mois de juillet et septembre sont associés à des naissances, juste avant ou pendant la saison des pluies, une période où les fruits sont les plus abondants à Ankarana. Les accouplements du mois de janvier sont associés à des parturitions en mi-avril ou vers le mois de juillet en cas de retardement de l’implantation de l’oeuf, quand les fruits sont moins abondants. Les périodes de naissance présentaient une synchronie inter-annuelle et semblaient principalement être régulées par la précipitation et la température régionale.
... Thomas et al. (1991), andSpeakman (1995) and Reher et al. (2018) have shown that the risk of hyperthermia in tropical bats, including Pteropodidae, is positively correlated with the ambient temperature. In addition, Pteropodidae have difficulty flying during heavy rains Roy et al. 2020), when they might have problems with hypothermia given their limited cold tolerance (Downs et al. 2012). Hence, taking these aspects into account, during the wet season, particularly on nights with heavy or continuous rain, R. madagascariensis might be forced to forage for shorter bouts, and probably in the vicinity of the cave. ...
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Bats emerge from their day roost after dusk and different factors can affect the timing of departure, return, and duration of nocturnal activities. This study provides information on the time of emergence and return of an endemic Malagasy fruit bat, Rousettus madagascariensis, in a cave located in the Réserve Spéciale d’Ankarana, northern Madagascar. Individuals were captured in a narrow passage between the roost and cave exit and capture time for each individual was noted. Variation according to sex, age, and body condition, as well as the influence of season, and the sunset and sunrise time were analyzed. During the dry season, individuals started to emerge at 1913 hours and returned to the cave generally by 0505 hours; the duration of time outside the cave during the dry season was higher in adult females (0952 hours) followed by subadult males (0937 hours), sub-adult females (0931 hours), and adult males (0910 hours). During the wet season, individuals exited at 1926 hours and returned at 0351 hours; as in the dry season, adult females spent more time outside the cave (0833 hours), than sub-adult females (0800 hours), and adult males (0752 hours). The period of emergence varied according to the age and sex classes, and time of predawn return associated with the previous nocturnal activity. The period of return was influenced by season, and age and sex classes. Such information is useful to quantify shifts in bat ecology, especially for endemic species with limited distribution or those playing an important role in ecosystem services.
... Areas of high rainfall and temperature have a greater diversity of plants, and thus a more varied and abundant food supply for fruit bats (Andrews and O'Brien, 2000;Kerr and Packer, 1997;Qian et al., 2009). Moreover, seasonal temperature variation significantly impacts the basal metabolic rate of E. wahlbergi (Downs et al., 2012). Future climate projections for southern Africa predict increased aridity in large parts of the region, as a result of increased temperature and reduced rainfall (Christensen et al., 2007;Hulme et al., 2001;Stringer et al., 2009). ...
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There is growing evidence that biotic factors such as predator-prey interactions play significant roles in driving species distribution across large spatial scales. The relative influence of abiotic and biotic factors on species distribution, however, may change under climate change. We investigated the relative influence of abiotic and biotic variables on the potential current and future distributions of three fruit bat species, Epomophorus angolensis (Gray, 1870), E. wahlbergi (Sundevall, 1846) and Rousettus aegyptiacus (E. Geoffroy St.-Hilaire, 1810), in southern Africa. We tested three hypotheses, namely that bat species’ distribution is primarily driven by (1) productivity; (2) physiological tolerance to climate; and (3) biotic interactions, specifically fig distribution. We adopted an ensemble niche modelling approach to project the suitable habitat of fruit bat species for current and future climate scenarios, and assessed variable importance in the models using a randomised variable shuffle procedure. We predicted that both biotic and abiotic factors influence suitable habitat of fruit bats, the relative influence of factors on habitat suitability of bat species are taxon specific, and the relative influence of abiotic and biotic factors will change from current to future climate scenarios. Abiotic variables associated with productivity were the primary determinants of habitat suitability for E. wahlbergi and E. angolensis under both current and future conditions. By contrast, suitable habitat of R. aegyptiacus was primarily mediated by temperature under current climatic conditions yet by freestanding fig distribution under both moderate and extreme future climate change scenarios. Freestanding fig distribution was also the most significant factor of habitat suitability for E. angolensis under the extreme future climate change scenario. Our results were congruent with our predictions and suggest that biotic variables play important roles in determining habitat suitability of species at relatively large spatial scales, contrary to the conventional assumptions of the Grinnellian niche.
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Fruit bats serve as crucial bioindicators, seed dispersers, pollinators, and contributors to food security within ecosystems. However, their population and distribution were threatened by climate change and anthropogenic pressures. Understanding the impacts of these pressures through mapping distribution and habitat suitability is crucial for identifying high-priority areas and implementing effective conservation and management plans. We predicted the distribution and extent of habitat suitability for Rousettus aegyptiacus and Epomophorus labiatus under climate change scenarios using average predictions from four different algorithms to produce an ensemble model. Seasonal precipitation, population index, land-use land cover, vegetation, and the mean temperature of the driest quarter majorly contributed to the predicted habitat suitability for both species. The current predicted sizes of suitable habitats for R. aegyptiacus and E. labiatus were varied, on average 60,271.4 and 85,176.1 km 2 , respectively. The change in species range size for R. aegyptiacus showed gains in suitable areas of 24.4% and 22.8% in 2050 and 2070, respectively. However, for E. labiatus, suitable areas decreased by 0.95% and 2% in 2050 and 2070, respectively. The range size change of suitable areas between 2050 and 2070 for R. aegyptiacus and E. labia-tus shows losses of 1.5% and 1.2%, respectively. The predicted maps indicate that the midlands and highlands of southern and eastern Ethiopia harbor highly suitable areas for both species. In contrast, the areas in the northern and central highlands are fragmented. The current model findings show that climate change and anthropogenic pressures have notable impacts on the geographic ranges of two species. Moreover, the predicted suitable habitats for both species are found both within and outside of their historical ranges, which has important implications for conservation efforts. Our ensemble predictions are vital for identifying high-priority areas for fruit bat species conservation efforts and management to mitigate climate change and anthropogenic pressures.
A variety of responses to climate seasonality have evolved by small mammals, including adjustments of the basal rate of metabolism (BMR) and the use of daily or seasonal torpor (here referred to as short-bout and long-bout torpor). The seasonal variation of their BMR is known to depend mainly on the concurrent variation of body mass, but it should also be affected by structural and functional changes occurring within the body that could depend on the expression of torpor. Thus it was hypothesized that BMR seasonality is related to the expression of torpor at an interspecific level. Seasonal BMR and body mass data were gathered from the literature and phylogenetic comparative analyses were done to test this hypothesis among mammals of less than 1 kg. BMR seasonality (dBMR) was quantified as the log-transformed ratio of the mean whole-animal BMR reported for the period P2 (autumn-winter) over that for the period P1 (spring-summer). Predictors were the seasonal body mass adjustment (dm), mean body mass (m) and torpor expression (TO, a three-level factor: no torpor, short-bout torpor, long-bout torpor). The seasonal variation of BMR was significantly related to dm but also to. Accounting for dm, species expressing long-bout torpor, but not those entering short-bout torpor, collectively exhibited a lower dBMR than species not entering torpor. Fat storage and use by species entering long-bout torpor, alone, could not explain their lower dBMR, as the TO:dm interaction was not significant. The low dBMR of species entering long-bout torpor may result from their collective tendency to down-regulate more strongly costly visceral organs during P2. The dBMR of the different TO categories overlapped appreciably, which highlights our still limited knowledge of the BMR seasonality among small mammals.
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Basking is a behaviour frequently observed in the rock hyrax (Procavia capensis) during winter that supposedly plays a significant role in rewarming from nocturnal hypothermia. This behaviour, together with changes in body temperature and changes in black bulb temperatures (Tbb) were investigated in the natural environment. In this study, rock hyraxes did not reduce their body temperature substantially overnight and thus basking was not used for rewarming but rather to maintain constant body temperatures under low ambient conditions. Frequency of basking changed throughout the day as Tbb increased and decreased. Different basking postures (hunched or flat), orientations to the sun and basking bout lengths were modified depending on Tbb experienced. There was no difference in body temperature between the two basking postures at any Tbb. It appears that rock hyraxes did not use basking behaviour as a way of warming up after night-time but used it during the day as a diurnal energy conserving mechanism.
The incidence of torpor during summer and winter in response to cold exposure in Mops condylurus was studied in a subtropical environment. Body temperature changes under natural roosting conditions during winter and summer were monitored using bats fitted with temperature-sensitive radio transmitters. Rectal temperatures of free-roosting bats were also measured during winter. During summer, the effect of clustering on the incidence of torpor under different climatic conditions was investigated. Mops condylurus were thermolabile and displayed daily bouts of torpor during winter and summer, with body temperatures closely conforming to ambient temperatures. Body temperatures as low as 12.0°C were recorded during winter. Regression analysis showed a positive correlation between body and ambient temperatures in winter and summer. There was no difference in the incidence of torpor between single and clustering bats, although single bats maintained slightly higher body temperatures. Results indicate that M. condylurus maintained an optimally small Tb–Ta differential by readily becoming torpid under roosting conditions, thereby minimizing energy expenditure.
Radiotelemetry studies of free-living Eptesicus fuscus demonstrated that the occurrence of daily torpor was influenced by ambient temperature and varied with the reproductive state of the bat. Lactating females were torpid significantly less often than pregnant and nonpregnant bats. Although the bats had the potential for behavioral thermoregulation, there was evidence that they actively controlled entry into and arousal from torpor. For pregnant females, prolonged periods of torpor coincided with prolonged gestation.