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Behavioral thermoregulation of wild Japanese macaques comparisons between two subpopulations.

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American Journal of Primatology 69:802–815 (2007)
RESEARCH ARTICLE
Behavioral Thermoregulation of Wild Japanese Macaques:
Comparisons Between Two Subpopulations
GORO HANYA1, MIEKO KIYONO2, AND SHUHEI HAYAISHI3
1
Primate Research Institute, Kyoto University, Inuyama, Aichi
2
Department of Zoology, Graduate School of Science, Kyoto University Inuyama, Aichi
3
University of Ryukyus, Nishihara, Okinawa
We studied the behavioral thermoregulation of Japanese macaques in two
troops that live in the coniferous (1,000–1,200 m in elevation) and coastal
forests (0–200 m in elevation) of Yakushima. Frequency of sunbathing,
huddling, and microhabitat selection during inactivity was compared.
The difference in mean annual air temperature between the forests was
more than 71C. In both forests, when the weather was clear, macaques
spent more time being inactive in the sunshine in winter than in autumn.
In winter, they huddled more often when it was clear than when cloudy.
Microhabitat selection to stay in the sunshine during winter differed
between the two forests. In winter, macaques spent more time inactive in
open habitats in the coniferous forest and in the trees in the coastal forest
than in autumn, respectively. This difference is related to the lower
crown height in the coastal forest and the large open habitats (logged
area) available only in the coniferous forest. In winter, skin temperature
measured by temperature-sensitive transmitters was 1.32–1.711C higher
when sunbathing, and 0.83–4.751C higher when huddling than staying in
the shade without huddling. In winter, the proportion with which they
stayed in the sunshine or huddled in winter did not differ between the
two forests, in spite of the difference in air temperature. This suggests
that Japanese macaques respond to seasonal changes in air temperature,
not the absolute temperature, and that they acclimatize themselves to
thermal conditions that require behavioral thermoregulation only during
the season when thermoregulation is most costly. Am. J. Primatol.
69:802–815, 2007. c 2007 Wiley-Liss, Inc.
Key words: acclimatization; huddling; Macaca fuscata; sunbathing;
Yakushima
Contract grant sponsor: Cooperation Research Program of KUPRI; Contract grant sponsor: MEXT
Grant-in Aid for JSPS Fellows; Contract grant sponsor: MEXT Grant-in Aid for the 21st Century
COE Program (A2).
Correspondence to: Goro Hanya, Primate Research Institute, Kyoto University, Inuyama, Aichi,
484-8506, Japan. E-mail: hanya@pri.kyoto-u.ac.jp
Received 16 May 2006; revision accepted 2 November 2006
DOI 10.1002/ajp.20397
Published online 9 February 2007 in Wiley InterScience (www.interscience.wiley.com).
r 2007 Wiley-Liss, Inc.
Behavioral Thermoregulation of Japanese Macaques / 803
INTRODUCTION
Endothermal animals pay considerable energy costs to maintain constant
body temperature. For example, captive Japanese macaques double their heat
production when air temperature (Ta) decreases from 29 to 51C [Nakayama et al.,
1971]. Animals have the ability to adjust their physiology or morphology in
response to the changes in their thermal environment without genetic changes
(acclimatization), thus the result does not necessarily indicate that Japanese
macaques always increase their metabolism under cold conditions. Therefore, the
energy costs of physiological thermoregulation are not usually clear among wild
populations. However, it has been reported that cold directly confines the feeding
and traveling of overwintering wild endothermal animals [Agetsuma, 1995;
Hanya, 2004a]. Therefore, the energy costs of thermoregulation might also be
considerable in wild populations.
Endotherms can reduce the physiological cost of thermoregulation in
behavioral ways, including adjustment of posture [Morland, 1993; Stelzner &
Hausfater, 1986], huddling [Schino & Troisi, 1990], and sunbathing by selecting
climatically different microhabitats [Bicca-Marques & Calegaro-Marques, 1998;
Sargeant et al., 1994; Takemoto, 2004]. These behaviors are referred to as
‘behavioral thermoregulation.’ The principle of heat radiation reduction by
decreasing body surface/volume ratio explains the first two behaviors. When it is
cold, their postures are expected to be more curled, and they huddle often to
reduce surface/volume ratio. The third behavior is explained as animals reducing
their physiological thermoregulatory cost by selecting the microhabitats whose
thermal condition is closest to their thermoneutral zones. The thermal
environment can vary within microhabitats such as sunshine, shade, on the
ground, or in trees.
Although behavioral thermoregulation has been described for many animals,
its ecological or energetic effectiveness has not been clarified for most
endotherms. One way to estimate the energetic effectiveness of behavioral
thermoregulation is to reveal the changes in body (core or skin) temperature in
correspondence to behavioral thermoregulation. A few examples of such study
include that by Brain and Mitchell [1999], who revealed that sandbathing
significantly decreased the body temperature of baboons in the Namib Desert,
and by McKechnie et al. [2004], who revealed that clustering effectively
maintained the body temperature of white-backed mousebirds.
Animals in cooler environments are often assumed to require more
energy for thermoregulation than those in warmer environments [Agetsuma &
Nakagawa, 1998; Iwamoto & Dunbar, 1983]. However, this may not always
be true considering acclimatization [Hori et al., 1977]. It is difficult to assess
the acclimatization ability of wild animals by measuring physiological
parameters. However, comparison of the frequency of behavioral thermoregulation between animals under different thermal conditions might be one
way to assess their acclimatization ability. If behavioral thermoregulation is
frequent, the cost of physiological thermoregulation can be regarded as high, at
least potentially.
The purpose of this study is to document and interpret the effectiveness
of behavioral thermoregulation and the acclimatization ability of Japanese
macaques (Macaca fuscata) against cold in two subpopulations on Yakushima.
First, we clarified whether macaques spent inactive time in winter in
such predicted ways as huddling or sunbathing. Second, we assessed the
effectiveness of behavioral thermoregulation through skin temperature (Ts)
Am. J. Primatol. DOI 10.1002/ajp
804 / Hanya et al.
measured by temperature-sensitive transmitters. Finally, we compared the
results between two subpopulations whose thermal environment is different
to determine the acclimatization ability of this species in thermoregulation.
It is important to reveal the thermoregulatory ability of this species because
among non-human primates, they are distributed in the northernmost areas.
Although Yakushima is the southern limit of the species’ distribution, altitudinal
variation in thermal environments here is as large as the latitudinal variation
between central and southern Japan. Thus, they are ideal subjects to study
acclimatization.
METHODS
Study Site
The study sites were in the coniferous and coastal forests of Yakushima
(301N, 1311E), an island in southern Japan. Yakushima occupied an area of
503 km2, with the highest peak being 1,936 m in elevation. The altitudes were
1,000–1,200 and 0–200 m in elevation, respectively and these two study sites
were located 7 km from each other. In the coniferous forest, annual precipitation
was 4,986 mm, and the mean annual temperature was 12.41C [Hanya,
2004b]. Warm temperate evergreen broad-leaved trees such as Quercus acuta,
Q. salicina, and Distylium racemosum, as well as conifers such as Cryptomeria
japonica, Abies firma, and Tsuga sieboldii were interspersed. The canopy height
reached 30 m. These primary coniferous forests occupied 83% of the annual home
range of the study troop (2.7 km2; Hanya [2004b]), and the remaining part was
logged 6–17 years ago. The logged forests were regenerated naturally, and they
are often used by macaques [Hanya et al., 2005]. In the coastal forest study
site, the mean annual precipitation was 2,500 mm [Eguchi, 1984], and the
mean annual temperature was 201C [Tagawa, 1980]. Warm temperate evergreen
broad-leaved trees, such as Castanopsis cuspidata, Q. salicina, and D. racemosum
were mixed with subtropical plants such as Ficus superba. Canopy height ranged
from 5 to 20 m.
Study Period
The study was conducted from October 2003 to January 2004 in the
coniferous forest and from October 2003 to March 2004 in the coastal forest.
We divided the study period into autumn (October and November) and winter
(December–March), since the changes in Ta were the largest between November
and December, and the monthly mean, maximum, and minimum temperature
of the December–March period was consistently lower than those in October–
November (Fig. 1, method below). The mean Ta during each period in each forest
was 13.11C (coniferous, autumn), 4.01C (coniferous, winter), 19.31C (coastal,
autumn), and 11.81C (coastal, winter).
Air Temperature
Air temperature was recorded by automatic data loggers (Tidbitr Computer
Onset Co. Ltd; Bourne, MA) within the home range of the study troops. The
precision of the data loggers is less than 0.011C. The data loggers were shaded in a
small white can and set 1.5 m above the ground inside the forest. The data logger
recorded temperature at intervals of 15 min (0:00, 0:15, etc.) 24 h a day during the
study period.
Am. J. Primatol. DOI 10.1002/ajp
Behavioral Thermoregulation of Japanese Macaques / 805
(a) Coniferous forest
(b)
25
25
20
20
15
15
10
10
5
5
0
Oct-03
Nov-03
Dec-03
Jan-04
Maximum temperature
Coastal forest
0
Oct-03
Nov-03
Minimum temperature
Dec-03
Jan-04
Feb-04
Mar-04
Mean temperature
Fig. 1. Seasonal variation in air temperature during study period. (a) Coniferous forest and
(b) coastal forest.
Behavioral Observations
We observed the behavior of the HR troop in the coniferous forest and the NA
troop in the coastal forest. The HR troop consisted of 24 individuals, including
seven adult females, seven adult males, and ten juveniles. The NA troop consisted
of 18 individuals, including five adult females, three adult males and ten
juveniles. All of the animals in both troops were individually identified. Before
starting behavioral observations (in July in the coniferous and in September
in the coastal forest), we captured two adult females from each troop.
We immobilized them using a blowpipe and darts containing ketamine at
an estimated dose of 10 mg/kg. We followed the target and waited until she
was resting on the ground, facing away from the immobilizer in a relatively flat
area. We darted the macaques from around 5 m, and after fully immobilized, we
removed them from the other troop members. A collar was fitted with a
temperature-sensitive transmitter (MI-2 Tr Holohil Systems Ltd; Carp, Ontario,
Canada) on the ventral side. The transmitters (thermometers) were packed in a
black plastic case of approximately 6 cm3 that directly touched with skin of their
necks. They were released after being fit for the collar, and observed until they
could move freely (approximately 3 h). The pulse interval of the transmitters
changed with temperature, and the relationship between temperature and pulse
interval was supplied by Holohil Systems Ltd for each transmitter. The precision
of the thermometers are less than 0.51C.
We conducted focal animal sampling of five adult females, including the
collared ones, in each troop. Two females in the HR troop were excluded because
they were less habituated. No female carried infants during the study period.
We continuously followed the focal animals for 1 h and then changed subjects.
We tried to select animals whose cumulative observation time was shortest as the
next focal subject. Every 15 min, we conducted instantaneous scan sampling of
the focal animal and recorded pulse intervals of the transmitters (if collared),
activity/inactivity (activity includes feeding, foraging, and traveling and inactivity
includes resting and grooming), place (terrestrial/arboreal, forest/open habitats,
sunshine/shade, snow cover/no snow cover), weather (clear, when the sun is not
covered with clouds/cloudy, when the sun is covered with clouds), and huddling
(defined as trunk–trunk contact with other individuals). Averaging all seasons,
Ta when it was clear was 1.871C higher than when cloudy in the coniferous forest
and 3.581C higher in the coastal forest. When collared animals were visible during
Am. J. Primatol. DOI 10.1002/ajp
806 / Hanya et al.
the instantaneous sampling of another focal individual, the data of the collared
animals were also taken ad libitum to increase the data on the relationship
between behavioral thermoregulation and Ts. These ad libitum data were not
used to calculate the proportion of thermoregulatory behaviors. Total observation
time was 193 h (109 h in autumn and 84 h in winter) in the coniferous and 489 h
(172 h in autumn and 317 h in winter) in the coastal forests. We only analyzed
behaviors during inactivity (resting and grooming) since other factors, mostly
foods, rather than thermoregulatory requirements, more strongly affected
microhabitat selection during active behaviors (feeding and traveling).
In autumn, this inactivity constituted 23% (99/438 scans) and 51% (351/690)
of the scans from HR and NA troops, respectively. In winter, inactivity
constituted 40% (135/337) and 41% (499/1229) of the scans from HR and NA
troops, respectively. We excluded mating-related huddling (huddling with a male
with whom mating was observed on that day) from analysis.
We calculated the average value of the frequency of sunbathing or huddling
for each individual and examined the effects of troop, season, and weather by twoway (sunbathing) or three-way (huddling) repeated measures of ANOVA.
In the analysis of microhabitat selection, data were too few for each individual
in some cases, so data from all the individuals were pooled and we compared
the proportion of scans using the G test or Fisher’s exact probability test (when
zero values were included). We compared (1) autumn vs. winter for the same
weather and troop, (2) clear vs. cloudy for the same season and troop, or (3)
coniferous vs. coastal troops for the same weather and season. In addition, we
conducted a post-hoc test on the proportion of sunbathing or huddling between
coniferous autumn vs. coastal winter, both of which are within similar Ta values.
Frequency of sunbathing and huddling did not differ between radio-collared
and non-radio-collared individuals (coniferous forest, sunbathing: G 5 0.084,
P40.1; huddling: G 5 0.47, P40.1; coastal forest, sunbathing: G 5 1.2, P40.1;
huddling: G 5 0.034, P40.1). Therefore, individual difference in thermoregulatory
behavior is small in the same troop, and it is justifiable to relate data on behavioral
thermoregulation and Ts, which were taken from different sets of individuals.
RESULTS
Sunbathing and Microhabitat Selection
In both troops, when it was clear, the tendency of macaques to be inactive
in the sunshine was greater during winter than during autumn, and the
proportion of inactive time spent in sunshine did not differ between troops in
winter. Under similar Ta, the frequency of sunbathing in the coniferous forest in
autumn was lower than in the coastal forest in winter. Two-way ANOVA revealed
that both troop and season were significant factors of the frequency of sunbathing
(troop: F 5 13.5, P 5 0.0021; season: F 5 87.6, Po0.0001; Fig. 2). Difference
between troops were mostly derived from the autumn results, since a post-hoc
test on the frequency of sunbathing revealed that the difference between troops
was significant in autumn (t 5 3.09, P 5 0.013) but not in winter (t 5 1.58,
P 5 0.15). The proportion of inactive time they spend in the sunshine in the
coniferous forest in autumn (55%) was significantly lower than in the coastal
forest in winter (76%; t 5 3.79, P 5 0.0053).
The tendency of microhabitat selection differed between the troops. In winter
(when thermoregulation is more strongly required) and when it is clear (sunshine
is available), macaques in the coniferous troop selected ground in open habitat as
a place to spend inactive time in clear autumn or cloudy winter conditions.
Am. J. Primatol. DOI 10.1002/ajp
Behavioral Thermoregulation of Japanese Macaques / 807
autumn
winter
1
0.8
0.6
0.4
0.2
0
Coniferous
Coastal
Fig. 2. Frequency of sunbathing during inactivity when it was clear. Mean7SD values are shown.
In contrast, in the coastal forest, macaques selected trees in the forest, as a place
to spend inactive time in clear winter rather than in clear autumn or cloudy
winter conditions. In the coniferous troop, the proportion of inactive time that
macaques spent in open habitats was higher in winter when it was clear than
in clear autumn or in cloudy winter conditions (Fig. 3a). Among the inactive scans
recorded in forests, the proportion of scans in which they stayed in trees was
higher in winter when it was cloudy than when it was clear (Fig. 3b). In the
coastal troop, on the other hand, the proportion of scans that macaques were
inactive in open habitats was lower in winter when it was clear than in clear
autumn or in cloudy winter conditions (Fig. 4a). The time they stayed in trees was
greater in winter than in autumn, in particular when it was clear (Fig. 4b).
In the coniferous forest, when the ground was covered with snow, macaques
spent inactive time in trees more often than when there was no snow coverage.
To examine the effect of snow, we used data only in winter in the coniferous
forest, because no snow fell in autumn or in the coastal forest. The proportion
of inactive time spent in the forest was greater when the ground was covered with
snow (100% 5 27/27) than when there was no snow (40% 5 43/108, Fisher’s exact
probability test, Po0.001). When they spent inactive time in forests,
the proportion of inactivity in trees was higher when there was snow
(100% 5 27/27) than when there was no snow (14% 5 6/43, Fisher’s exact
probability test, Po0.001).
Huddling
In both troops, macaques huddled more frequently in winter than in autumn,
and when clear than when cloudy. However, there was no significant difference
between troops. Three-way ANOVA revealed that season (F 5 7.10, P 5 0.012)
and weather (F 5 13.8, P 5 0.0008) were significant factors but troop was not
(F 5 0.179, P 5 0.68; Fig. 5). Interaction factor was significant only for
season weather (F 5 4.28, P 5 0.047). In the coniferous forest, macaques
huddled only in winter, and they huddled more often when it was cloudy.
In the coastal troop, the proportion of time that they huddled was higher in
winter than in autumn. In winter, the proportion of time was higher when it was
Am. J. Primatol. DOI 10.1002/ajp
808 / Hanya et al.
(a)
0.6
0.5
G=9.23
p=0.0024
G=10.6
p=0.0011
0.4
0.3
0.4
0.2
0.1
0
Clear, autumn
(N=78)
Clear, winter
(N=86)
Cloudy, autumn
(N=21)
Cloudy, winter
(N=55)
(b)
0.8
G =10.3
p=0.0014
0.6
0.4
0.2
0
Clear, autumn
(N=52)
Clear, winter
(N=35)
Cloudy, autumn
(N=14)
Cloudy, winter
(N=39)
Fig. 3. Microhabitat selection in the coniferous troop. (a) Proportion of scans of inactivity when
focal animals were in open habitats, (b) proportion of scans in which focal animals were inactive
in trees in the forest. Numbers in parentheses are sample sizes of inactivity scans. There were no
significant differences between pairs except for those shown by bars.
cloudy than when it was clear. Post-hoc test revealed that when it was cloudy,
the frequency of huddling was significantly higher in winter in the coastal forest
than in autumn in the coniferous forest (t 5 4.30, P 5 0.0036). This difference was
not significant when it was clear (t 5 1.68, P 5 0.14).
Effectiveness of Behavioral Thermoregulation
Ts and Ta had a significant positive correlation among individuals in the
coniferous forest, but not among individuals in the coastal forest (Fig. 6;
Am. J. Primatol. DOI 10.1002/ajp
Behavioral Thermoregulation of Japanese Macaques / 809
(a)
0.16
G=9.23
p=0.0024
G=4.24
p=0.039
0.12
0.08
0.04
0
Clear, autumn
(N=233)
Clear,winter
(N=218)
Cloudy, autumn
(N=145)
Cloudy, winter
(N=252)
(b)
0.2
G=10.0
p=0.0015
0.15
0.1
0.05
0
Clear, autumn
(N=199)
Clear, winter
(N=206)
Cloudy, autumn
(N=128)
Cloudy, winter
(N=225)
Fig. 4. Microhabitat selection in the coastal troop. (a) Proportion of scans of inactivity when focal
animals were in open habitats. (b) Proportion of scans in which focal animals were inactive in trees
in the forest. Numbers in parentheses are sample sizes of inactive scans. There were no significant
differences between pairs except for those shown by bars.
coniferous individual. 1: r 5 0.45, Po0.01; individual 2: r 5 0.63, Po0.001; coastal
individual 1: r 5 0.13, P40.1; individual 2: r 5 0.006, P40.1). Combining the
results of these two habitats, Ts seemed to begin to drop when Ta became less
than 81C. Therefore, for coastal forest individuals, we directly used Ts data as
an indicator of the effectiveness of behavioral thermoregulation. In the case
of coniferous forest individuals, we calculated the ‘expected’ Ts by the use
of regression of Ts to Ta (individual 1: Ts 5 27.610.97 Ta; individual 2: Ts 5 34.31
0.29 Ta). We used the residuals between the expected and actual Ts as an
indicator. We divided the inactivity data into sunbathing (excluding huddling
in the sunshine), huddling (including huddling in the sunshine), and no
behavioral thermoregulation. Then, we compared the residuals (in the case of
coniferous individuals) or Ts between thermoregulatory behaviors (in the case of
coastal individuals).
Am. J. Primatol. DOI 10.1002/ajp
810 / Hanya et al.
No huddling occurred
cloudy
clear
1
0.8
0.6
0.4
0.2
0
Autumn Winter
Coniferous
Autumn Winter
Coastal
Fig. 5. Frequency of huddling. Mean7SD values are shown.
Fig. 6. Relationship between air and skin temperatures. Only winter data were used. Black circles,
sunbathing; crosses, huddling; white circle, no behavioral thermoregulation. (a) Coniferous forest,
individual 1 (indi. 1), (b) coniferous forest, individual 2 (indi. 2), (c) costal forest, individual 1 (indi.
1), and (d) costal forest individual 2 (indi. 2).
Am. J. Primatol. DOI 10.1002/ajp
Behavioral Thermoregulation of Japanese Macaques / 811
Although Ts increased during both sunbathing and huddling activities,
the effect was generally larger for sunbathing than for huddling. For sunbathing,
Ts was significantly higher than for no behavioral thermoregulation (Fig. 7B,
Figs. 8A and B), except for individual 1 (Fig. 7A) in the coniferous forest. Even in
case of individual 1 in the coniferous forest, the difference was almost significant
(t 5 2.22, P 5 0.071). For huddling, Ts was significantly higher than for no
behavioral thermoregulation only for individual 1 in the coniferous forest (Fig. 7A).
For other individuals, Ts was not significantly different between huddling and
no behavioral thermoregulation (Fig. 7B, Figs. 8A and B). Averaging the
values for each individual, Ts or the residual was 1.32–1.711C higher when
sunbathing and 0.83–4.751C higher when huddling than without behavioral
thermoregulation.
Fig. 7. Comparisons of residuals between the measured skin temperature (Ts) and the regression
line of Ts to air temperature (Ta) (individual 1: Ts 5 27.610.97 Ta; individual 2: Ts 5 34.310.29 Ta)
between different thermoregulatory behaviors for coniferous forest individuals. Only winter data
were used. There was no significant difference between pairs except those shown by bars.
Mean7SD values are shown. (a) Individual 1 and (b) individual 2.
Am. J. Primatol. DOI 10.1002/ajp
812 / Hanya et al.
Fig. 8. Comparisons of skin temperature between different thermoregulatory behaviors for coastal
forest individuals. Only winter data were used. There was no significant difference between pairs
except those shown by bars. Mean7SD values are shown. (a) Individual 1 and (b) individual 2.
DISCUSSION
Selection of Microhabitats
As predicted, Japanese macaques selected thermally favorable microhabitats
during inactivity in both subpopulations. In winter (thus when thermoregulation
against cold is necessary), they stayed in the sunshine when it was clear, and
when it was cloudy (thus when sunshine was not available), they frequently
huddled. However, the macaques in the two different subpopulations selected
different microhabitats to stay in the sunshine.
In the coniferous forest, in winter and when it was clear, they remained
in open habitats to stay in the sunshine (Fig. 3A). In the coastal forest, in winter
and when it was clear, they stayed in the trees, presumably out in the open on
the canopy (Fig. 4). This difference probably results from differences in the
availability of open habitats and canopy height. The open habitat of logged areas
Am. J. Primatol. DOI 10.1002/ajp
Behavioral Thermoregulation of Japanese Macaques / 813
is abundant within the home range of the coniferous forest troop. In the coastal
forest troop, only small open patches, such as gaps or rocky coasts are available.
Chimpanzees and lemurs are also known to stay in the higher parts of the canopy
when it is cold to receive more sunlight [Takemoto, 2004; Vasey, 2004] as well as
macaques in the coastal forest. The canopy height in the coniferous forest reaches
30 m, but in the coastal forest it is often less than 5 m. Since the canopy is low
in the coastal forest, they can access it to receive sunlight more easily than in the
coniferous forest.
The tendency of macaques to spend inactive time in open habitats
disappeared when the ground was covered with snow. With snow coverage,
macaques stayed in trees, which can also be explained in terms of thermoregulation;
they avoided touching the snow on the ground.
When it was clear in autumn, macaques in the coastal forest stayed
in sunshine less often than their coniferous forest counterparts. Although
thermoregulation against heat is out of the scope of this study, this tendency
might be explained as avoiding heat. In October, the maximum Ta reaches
251C. Temperature in sunshine might be higher than macaques’ thermoneutral
zones on hot autumn days in the coastal forest. In the coniferous troop, when
macaques spent inactive time in the forest, they stayed in trees more often when
it was cloudy than when it was clear (Fig. 3B). This tendency remains to be
explained.
Effectiveness of Behavioral Thermoregulation
Ts data suggested that behavioral thermoregulation was effective, although
caution should be taken to interpret the data. Nakayama et al. [1971] found that
although Ts decreased linearly with ambient temperature, the decrease was large
for peripheral sites and small in central sites of the body. How precisely
the present Ts data around the neck reflect actual energy consumption cannot
be answered without further studies, probably on captive animals. Without those
physiological data, the present results remain preliminary. However, these kinds
of data are extremely deficient in wild primates (see, ‘Introduction’ section) and
worth being discussed to understand the energetic importance of behavioral
thermoregulation.
During sunbathing and huddling, Ts was on average 1.32–1.711C
or 0.83–4.751C higher than without behavioral thermoregulation, respectively.
Ts data cannot be directly used to estimate energy expenditure since the
difference between skin and core temperature is great in large (4300 g)
endotherms [Audet & Thomas, 1996; Dausmann, 2005]. Ts along the trunk
(stomach) of lightly dressed Finnish men was 21C higher when exposed to room
temperatures of 221C than to 101C, and metabolism was 12% less at 221C than at
101C [Mäkinen et al., 2004]. Such results cannot be directly linked to macaques
owing to the existence of clothing, hair, and a difference in body weight of more
than ten times. However, they suggest that the observed difference in Ts, thus the
energetic effect of sunbathing and huddling, is not negligible in macaques.
The increment of Ts tended to be larger when sunbathing than when
huddling, although it was difficult to assess because of inter-individual
differences. Macaques huddled less often when it was clear, when sunbathing
was possible, than when cloudy. This might be related to the fact that huddling
is less effective than sunbathing to raise Ts or that it results in increased
social tension because of physical contact with non-affiliative individuals
[Takahashi, 1997].
Am. J. Primatol. DOI 10.1002/ajp
814 / Hanya et al.
Implications for Acclimatization Ability in Thermoregulation
The differences in mean annual Ta between the two forests were more than
71C, and the mean temperature during winter in the coastal forest was almost the
same as autumn in the coniferous forest. According to the preliminary average
wind speed data taken only during behavioral observations, wind speed was
significantly stronger in the coniferous forest (0.69 m/s) than in the coastal forest
(0.41 m/s; F 5 79.5, Po0.0001). Wind speed data suggest that thermal condition
in the coniferous forest was even harsher when wind speed was taken into
account. The correlation between Ts and Ta suggested that the threshold
Ta, below which macaques cannot maintain Ts, was 81C. In winter, Ta in the
coniferous forest was often lower than 81C, but not in the coastal forest. This
indicates that the cold perceived by macaques on their skin actually differed
between the coniferous and coastal forests. However, the proportion of behavioral
thermoregulation in winter was the same between the two forests. Macaques
in the coastal forest in winter spent considerable time sunbathing or huddling,
but macaques in the coniferous forest in autumn, with similar Ta, did not spent
time in behavioral thermoregulation. They never huddled, and they sunbathed
less frequently than macaques in the coastal forest in winter in spite of the
similar Ta.
The present results suggest that macaques do not respond to absolute Ta,
but seasonal changes in the Ta in the area. Since these two forests are only 7 km
apart, there should be no genetic differentiation among macaques. South African
shrikes (Lanius collaris) acclimatize along an elevation gradient of 1,800 m
by changing various physiological parameters [Soobramoney et al., 2003].
Perhaps Japanese macaques in Yakushima acclimatize to each thermal condition
physiologically as the South-African shrikes or morphologically, such as hair
density [Inagaki & Hamada, 1985]. Behavioral thermoregulation enables
endotherms to reduce physiological costs, but it confines non-thermoregulatory
activities, such as feeding, traveling or predator avoidance. For example, Japanese
macaques in Yakushima decrease fruit-feeding time in winter, although fruits are
available. In response to the increased thermoregulatory cost, macaques save the
time and energy needed for traveling in search of the high-quality but low-density
fruit resources, and thus they increase their level of inactivity for the sake
of behavioral thermoregulation [Agetsuma, 1995; Hanya, 2004a]. Sunbathing
black rat snakes suffer from high risk of predation [Blouin-Demers & Weatherhead, 2002]. To avoid such costs, it is reasonable to acclimatize to each
thermal condition to require behavioral thermoregulation only during the
thermally worst season.
ACKNOWLEDGMENTS
We thank our friends and colleagues in Yakushima for their hospitality and
help. S. Yoshihiro initially guided GH to this field site. K. Fuse and M. Nishikawa
assisted us in the field. H. Takemoto, the staff at the Laboratory of Human
Evolution Studies and Primate Research Institute, Kyoto University (KUPRI),
and the editors and reviewers of this journal gave us helpful comments.
The Sarugoya Committee and Field Research Center of KUPRI offered us
excellent facilities. The Yakushima Forest Environment Conservation Center
and Kirishima-Yaku National Park gave us permission to study in the area.
Kagoshima Prefecture and Ministry of Environment, Japan approved the capture
of macaques. We are grateful to these people and organizations.
Am. J. Primatol. DOI 10.1002/ajp
Behavioral Thermoregulation of Japanese Macaques / 815
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Am. J. Primatol. DOI 10.1002/ajp
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