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Japanese macaque (Macaca fuscata) mothers huddle with their young offspring instead of adult females for thermoregulation
Behavioural Processes 129 (2016) 41–43
Contents lists available at ScienceDirect
Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Japanese macaque (Macaca fuscata) mothers huddle with their young offspring instead of adult females for thermoregulation Masataka Ueno ∗ , Masayuki Nakamichi Osaka University, Department of Ethology, Graduate School of Human Sciences, Osaka University, Suita, Osaka 565-0871, Japan
a r t i c l e
i n f o
Article history: Received 25 February 2016 Received in revised form 6 May 2016 Accepted 27 May 2016 Available online 1 June 2016 Keywords: Huddling Japanese macaque Maternal behavior Thermoregulation behavior
a b s t r a c t It is unclear whom animals select to huddle with for thermoregulation. In this study, we investigated whom Japanese macaque (Macaca fuscata) mothers huddled with—their young offspring or other adult group members—when there is need for thermoregulation. We used a focal-animal sampling method, targeting 17 females at Katsuyama, Okayama Prefecture, Japan. A majority of huddling among adult females was recorded during winter season (December, January, and February). Females who had young (0- or 1-year-old) offspring huddled less frequently with other adult females compared to females who did not have young offspring in winter. However, including young offspring, the frequency of huddling with any other individuals did not differ by whether females had young offspring. Moreover, the females who did not have young offspring huddled with other adult females more often in cloudy than in sunny weather during winter season. In contrast, females who had young offspring increased huddling with their young offspring in cloudy than in sunny weather, but did not do so with other adult females. This study indicates that Japanese macaque mothers huddle with their young offspring instead of other adult females when there is need for thermoregulation. © 2016 Elsevier B.V. All rights reserved.
1. Introduction Endothermal animals pay energy costs in order to maintain body temperature. Such energy cost is decreased by using thermoregulation behaviors. For example, Japanese macaques (Macaca fuscata) huddled with other group members more frequently as the air temperature decreased (Ogawa and Wada, 2011). During sunbathing and huddling, the skin temperature of Japanese macaques was higher than without thermoregulation behaviors (Hanya et al., 2007). Although huddling is regarded as a maternal behavior, not only infants but also their mothers may benefit from thermoregulation by huddling between the mother and the infant. In fact, baboon mothers huddled with their infants more frequently when the air temperature decreased (Brent et al., 2003). However, Schino and Troisi (1998) did not find that air temperature affected the amount of huddling (ventral contact) between Japanese macaque mothers and infants, as the mothers rejected attempts at physical contact from their infants. Since heat radiation is considered to reduce by huddling due to a decreased body surface area, mothers may not benefit from huddling small-sized individuals (i.e., their infants) when attempting to maintain their own body heat (Schino and
∗ Corresponding author. E-mail address: [email protected] (M. Ueno). http://dx.doi.org/10.1016/j.beproc.2016.05.008 0376-6357/© 2016 Elsevier B.V. All rights reserved.
Troisi, 1998). Empirical studies evaluating the influence of temperature and weather conditions on maternal huddling are rare in the primate literature, and it is unclear if primate mothers increase huddling with their young offspring to maintain their own body temperature. Thus, an unsolved question remains from previous studies: will primate mothers prefer to huddle with other adult group members for their own thermoregulation instead of with their young offspring? This study attempts to answer this question by investigating which group members Japanese macaque mothers huddled with—their young offspring or other adult group members—when there is need for thermoregulation, by comparing huddling frequency between females with young offspring and females without them, and between winter season and other seasons. 2. Material and methods We observed a group of free-ranging Japanese macaques at Katsuyama. This group has been artificially provisioned since 1958. During the study period (April 2012–March 2013), the group included 129 individuals. There were 55 adult females (≥5 years old) in September 2012. All group members were identified by facial and body features. More detailed information about the study group is described elsewhere (Nakamichi and Yamada, 2007). We used the same data set as Ueno et al. (2015), which were collected by focal observation from 17 females, for an average of
42
M. Ueno, M. Nakamichi / Behavioural Processes 129 (2016) 41–43
Fig. 1. (a) Frequency of huddling in which females with and without young offspring huddled with other adult females during winter. The vertical axis shows the ratios of huddling with other adult females per total resting points during winter. The bars indicate the median. Mann-Whitney test: **p < 0.01. (b) Frequency of huddling in which females with and without young offspring huddled with other group members during winter. The vertical axis shows the ratios of huddling with any other individuals (young offspring, juveniles, and adults) per total resting points during winter. The bars indicate the median.
14.05 ± 0.23 h (mean ± S.E.) per female over 98 days. Observations were conducted using 30-min focal-animal sampling with a digital video camera (HDR-CX370, Sony). If a female was in estrous, we did not conduct focal observation targeting the female. At the start of each focal observation, we recorded the weather condition (sunny or cloudy). Huddling is defined as trunk–trunk contact with other individuals (Hanya et al., 2007). We recorded “resting with huddling,” “resting without huddling,” and “other activities (allogrooming, feeding, and moving)” by using instantaneous sampling method with 60-s intervals. Then, the ratio of huddling was calculated as follows: dividing the total number of resting with huddling points by the total number of resting points for each focal female. The total number of focal observations included 1817 resting points in winter (106.9 points per one female) and 1908 resting points in other seasons (112.2 points per one female) by instantaneous sampling. We did not find the occurrence of huddles between focal females with adult males during the focal observation. With regard to huddling among adult females, 49 (11%) instantaneous huddling points consisted of three or more females (average huddle size: 2.2). We did not consider whether the huddles consisted of two or more females. Unless clear statement (Result 2), when females huddle with both their young offspring and other adult females, we counted huddles between adult females but did not count huddles between mothers and their young offspring. We divided the study period into winter (December, January, and February) and non-winter (April-November and March). We did not record air temperature in our study site. According to the Automated Meteorological Data Acquisition System (AMEDAS) at Kuse (E133◦ 45.2 N35◦ 4.1 ), which is the nearest observatory to our study site (the distance: 8.5 km), the mean air temperature during each study period was 2.2 ± 0.7 ◦ C (mean ± S.E.) during winter and 17.3 ± 2.4 ◦ C during non-winter. The observatory at Kuse has an elevation of 144 m, and our study site had an elevation of 405 m. Thus, the air temperature at our study site was predicted to be lower than values at Kuse. Of 17 focal females, five had 0-year-old offspring, three had 1year-old offspring, and four had 2-year-old offspring. In Japanese macaques, not only 0-year-old offspring but also 1-year-old offspring are often dependent on their mothers for nursing and maternal carrying, if they did not have young siblings. Thus, 0and 1- year-old offspring may huddle with their mothers more often than 2-year-old offspring. In fact, in the winter, 0-year-old offspring and 1-year-old offspring huddled with their mothers at similar frequencies (Mann-Whitney test, U = 7, p = 1), but 2-yearold offspring huddled less frequently with their mothers compared to 0-year-old offspring (U = 20, p < 0.05) and 1-year-old offspring
(U = 12, p < 0.05). Therefore, we analyzed the data based on whether females had 0- or 1-year-old offspring. All data were analyzed using the statistical software R, version 3.0.0 (Palo Alto, California). All analyses were two-tailed and a significance level of p < 0.05 was set.
3. Results 3.1. Seasonal changes In the winter, we collected 630 instantaneous sampling points of huddling for focal females who had young (0- or 1-year-old) offspring, and 555 points for females who did not have young offspring. The results showed that females who had young offspring huddled with other adult females in 109 of 630 huddling points (17%), and females without young offspring did so in 460 of 555 huddling points (83%). On the other hand, in non-winter season, huddling between adult females was recorded only 12 and 21 points in total for each female group. Huddling frequency between mothers and young offspring would also be influenced by developmental stages, outside of thermoregulation. To determine any seasonal changes, we compared the frequencies of huddling between mothers and 1-year-old offspring in the winter with huddling frequency in the four months before winter (i.e., from August to November). The results showed that, in all three mother-and-1-year-old offspring pairs, huddling frequencies increased from the period before winter (0.32, 0.19, 0.63) to winter (0.43, 0.69, 0.81). Overall, huddling behavior increased in winter, compared with non-winter.
3.2. Huddling partner We analyzed the number of huddles during winter season. Females who had young offspring huddled less frequently with other adult females compared to females who did not have young offspring (U = 9, p < 0.01, Fig. 1a). However, the frequency of huddling with other individuals, including young offspring, did not differ between the two female groups (U = 55, p = 0.07, Fig. 1b). In addition, we compared huddling frequencies of females with young offspring for three categories: huddling with adult females, young offspring, and both of them. We found that females with young offspring tended to huddle with their young offspring, compared with the other two categories (Fig. 2). These results indicated that female Japanese macaques that had young offspring did not huddle with other adult females, but huddled with their young offspring.
M. Ueno, M. Nakamichi / Behavioural Processes 129 (2016) 41–43
Fig. 2. Frequency of huddling of females with young offspring during winter (huddling with only adult females, young offspring, and both adult females and young offspring). The vertical axis shows the ratios of huddling with any other individuals per total resting points during winter. Wilcoxon’s signed rank tests with Bonferroni correction: *p < 0.05; huddles consisted only of females and their young offspring occurred more often than huddles consisted of adult females (V = 0, p < 0.05) and of both female and their young offspring (V = 1, p < 0.05), but huddling frequency only with adult females and huddling frequency with both adult females and their young offspring did not significantly differ (V = 5, p = 0.88).
3.3. Huddling in sunny and cloudy weather Females who did not have young offspring huddled with other adult females more often in cloudy than in sunny weather (sunny (median): 0.12; cloudy: 0.37, Wilcoxon’s signed rank test, V = 4, p < 0.05). In contrast, with regard to females with young offspring, the difference in huddling frequency with adult females did not differ by weather conditions (sunny: 0.007; cloudy: 0.07, V = 7, p = 0.24). Instead, they huddled with their young offspring at a higher rate in cloudy than in sunny weather (sunny: 0.27; cloudy: 0.70, V = 4, p < 0.05). That is, when there is more need for thermoregulation, females who had young offspring huddled with their offspring instead of other adult females. 4. Discussion In this study, there was a general tendency for female Japanese macaques to increase huddling behavior with other group members during winter season, compared with during other seasons. However, females who had 0- or 1-year-old offspring huddled with their offspring, and huddled infrequently with other adult individuals during winter. In addition, females who had young offspring huddled with their offspring more frequently in cloudy than in sunny weather. These mean that females who had young offspring huddled with their offspring instead of other group members when there was substantial need for thermoregulation. In line with our study, Brent et al. (2003) reported an increase in mother-infant huddling in colder conditions, but Schino and Troisi (1998) did not. This may be due to the difference in the range of air temperature. The temperature recorded in Brent et al. (2003) ranged from −2.2 to 41.1 ◦ C and the mean air temperature in our study was thought to be lower than 2.2 ◦ C during winter (see Section 2). In contrast, the infants in Schino and Troisi (1998) experienced air temperatures between 13.4 and 25.7 ◦ C during their first 12 weeks of life. The temperature in Schino and Troisi’s (1998) study might have made it costly for infants to maintain their body temperatures, but not for their mothers (Chaffee and Allen, 1973). On the other hand, the air temperatures of our study site were cold enough such that huddling between a mother and her young offspring would be beneficial for both. Schino and Troisi (1998) suggested that infants are less suitable huddling partners because of their small size. Nevertheless, in our
43
study, female Japanese macaques who had young offspring huddled with them, instead of with other adult individuals during winter. The reason may be that huddling with other adult group members causes anxiety. Previous studies showed that approaching and contact with other adult individuals cause anxiety in females macaques (e.g., Aureli et al., 1999). In addition, the average huddle size among adult individuals is smaller compared to in other study sites (e.g., average huddle size of Shodoshima island: 17.1 and 15.9, Zhang and Watanabe, 2007). This may reflect an intolerant society, which might lead to more anxiety for individuals to huddle. Thus, young offspring may be more profitable psychologically for contact compared to adult individuals. Moreover, huddling with young offspring may also be physically effective for thermoregulation. In Japanese macaques, the density of body hair in the ventral area is more sparse compared to in outer body parts (Zamma, 2002), suggesting that heat radiation easily occur through the ventral area. Japanese macaque mothers and their offspring tend to huddle at ventral–ventral positions; thus, huddling with young offspring can reduce body surface in the ventral area. This may offer enough thermoregulation benefits to their mothers. In conclusion, this study found that Japanese macaque mothers huddle with their young offspring, instead of with other adult group members, when there is need for thermoregulation. The weakness of our study was that we did not record the exact air temperature at the study site. However, given that Japanese macaques respond to seasonal changes in air temperature but not to absolute temperature (Hanya et al., 2007), this limitation may not be salient. In the future, whether the effectiveness of huddling differs by the size of huddling partners, and how individuals mitigate social tension caused by huddling with adult group members, would be valuable to investigate. Acknowledgments This study was supported by the Research Fellowships of the Japan Society for the Promotion of Science (JSPS) for Young Scientists (No. 232887). We are sincerely grateful to Kazunori Yamada and the members of the Department of Ethology, Graduate School of Human Sciences, Osaka University, for their encouragement. References Aureli, F., Preston, S.D., de Waal, F.B.M., 1999. Heart rate responses to social interactions in free-moving rhesus macaques (Macaca mulatta): a pilot study. J. Comp. Psychol. 113, 59–65. Brent, L., Koban, T., Evans, S., 2003. The influence of temperature on the behavior of captive mother-infant baboons. Behaviour 140, 209–224. Chaffee, R.R.J., Allen, J.R., 1973. Effects of ambient temperature on the resting metabolic rate of cold and heat-acclimated Macaca mulatta. Comp. Biochem. Physiol. 44, 1215–1225. Hanya, G., Kiyono, M., Hayaishi, S., 2007. Behavioral thermoregulation of wild Japanese macaques: comparisons between two subpopulations. Am. J. Primatol. 69, 802–815. Nakamichi, M., Yamada, K., 2007. Long-term grooming partnerships between unrelated adult females in a free ranging group of Japanese monkeys (Macaca fuscata). Am. J. Primatol. 69, 652–663. Ogawa, H., Wada, K., 2011. Shape of, and body direction in huddles of Japanese macaques (Macaca fuscata) in Arashiyama, Japan. Primates 52, 229–235. Schino, G., Troisi, A., 1998. Mother-infant conflict over behavioral thermoregulation in Japanese macaques. Behav. Ecol. Sociobiol. 43, 81–86. Ueno, M., Yamada, K., Nakamichi, M., 2015. Emotional states after grooming interactions in Japanese macaques (Macaca fuscata). J. Comp. Psychol. 129, 394–401. Zamma, K., 2002. Grooming site preferences determined by lice infection among Japanese macaques in Arashiyama. Primates 43, 41–49. Zhang, P., Watanabe, K., 2007. Extra-large cluster formation by Japanese macaques (Macaca fuscata) on Shodoshima Island central Japan, and related factors. Am. J. Primatol. 69, 1119–1130.
Contents lists available at ScienceDirect
Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Japanese macaque (Macaca fuscata) mothers huddle with their young offspring instead of adult females for thermoregulation Masataka Ueno ∗ , Masayuki Nakamichi Osaka University, Department of Ethology, Graduate School of Human Sciences, Osaka University, Suita, Osaka 565-0871, Japan
a r t i c l e
i n f o
Article history: Received 25 February 2016 Received in revised form 6 May 2016 Accepted 27 May 2016 Available online 1 June 2016 Keywords: Huddling Japanese macaque Maternal behavior Thermoregulation behavior
a b s t r a c t It is unclear whom animals select to huddle with for thermoregulation. In this study, we investigated whom Japanese macaque (Macaca fuscata) mothers huddled with—their young offspring or other adult group members—when there is need for thermoregulation. We used a focal-animal sampling method, targeting 17 females at Katsuyama, Okayama Prefecture, Japan. A majority of huddling among adult females was recorded during winter season (December, January, and February). Females who had young (0- or 1-year-old) offspring huddled less frequently with other adult females compared to females who did not have young offspring in winter. However, including young offspring, the frequency of huddling with any other individuals did not differ by whether females had young offspring. Moreover, the females who did not have young offspring huddled with other adult females more often in cloudy than in sunny weather during winter season. In contrast, females who had young offspring increased huddling with their young offspring in cloudy than in sunny weather, but did not do so with other adult females. This study indicates that Japanese macaque mothers huddle with their young offspring instead of other adult females when there is need for thermoregulation. © 2016 Elsevier B.V. All rights reserved.
1. Introduction Endothermal animals pay energy costs in order to maintain body temperature. Such energy cost is decreased by using thermoregulation behaviors. For example, Japanese macaques (Macaca fuscata) huddled with other group members more frequently as the air temperature decreased (Ogawa and Wada, 2011). During sunbathing and huddling, the skin temperature of Japanese macaques was higher than without thermoregulation behaviors (Hanya et al., 2007). Although huddling is regarded as a maternal behavior, not only infants but also their mothers may benefit from thermoregulation by huddling between the mother and the infant. In fact, baboon mothers huddled with their infants more frequently when the air temperature decreased (Brent et al., 2003). However, Schino and Troisi (1998) did not find that air temperature affected the amount of huddling (ventral contact) between Japanese macaque mothers and infants, as the mothers rejected attempts at physical contact from their infants. Since heat radiation is considered to reduce by huddling due to a decreased body surface area, mothers may not benefit from huddling small-sized individuals (i.e., their infants) when attempting to maintain their own body heat (Schino and
∗ Corresponding author. E-mail address: [email protected] (M. Ueno). http://dx.doi.org/10.1016/j.beproc.2016.05.008 0376-6357/© 2016 Elsevier B.V. All rights reserved.
Troisi, 1998). Empirical studies evaluating the influence of temperature and weather conditions on maternal huddling are rare in the primate literature, and it is unclear if primate mothers increase huddling with their young offspring to maintain their own body temperature. Thus, an unsolved question remains from previous studies: will primate mothers prefer to huddle with other adult group members for their own thermoregulation instead of with their young offspring? This study attempts to answer this question by investigating which group members Japanese macaque mothers huddled with—their young offspring or other adult group members—when there is need for thermoregulation, by comparing huddling frequency between females with young offspring and females without them, and between winter season and other seasons. 2. Material and methods We observed a group of free-ranging Japanese macaques at Katsuyama. This group has been artificially provisioned since 1958. During the study period (April 2012–March 2013), the group included 129 individuals. There were 55 adult females (≥5 years old) in September 2012. All group members were identified by facial and body features. More detailed information about the study group is described elsewhere (Nakamichi and Yamada, 2007). We used the same data set as Ueno et al. (2015), which were collected by focal observation from 17 females, for an average of
42
M. Ueno, M. Nakamichi / Behavioural Processes 129 (2016) 41–43
Fig. 1. (a) Frequency of huddling in which females with and without young offspring huddled with other adult females during winter. The vertical axis shows the ratios of huddling with other adult females per total resting points during winter. The bars indicate the median. Mann-Whitney test: **p < 0.01. (b) Frequency of huddling in which females with and without young offspring huddled with other group members during winter. The vertical axis shows the ratios of huddling with any other individuals (young offspring, juveniles, and adults) per total resting points during winter. The bars indicate the median.
14.05 ± 0.23 h (mean ± S.E.) per female over 98 days. Observations were conducted using 30-min focal-animal sampling with a digital video camera (HDR-CX370, Sony). If a female was in estrous, we did not conduct focal observation targeting the female. At the start of each focal observation, we recorded the weather condition (sunny or cloudy). Huddling is defined as trunk–trunk contact with other individuals (Hanya et al., 2007). We recorded “resting with huddling,” “resting without huddling,” and “other activities (allogrooming, feeding, and moving)” by using instantaneous sampling method with 60-s intervals. Then, the ratio of huddling was calculated as follows: dividing the total number of resting with huddling points by the total number of resting points for each focal female. The total number of focal observations included 1817 resting points in winter (106.9 points per one female) and 1908 resting points in other seasons (112.2 points per one female) by instantaneous sampling. We did not find the occurrence of huddles between focal females with adult males during the focal observation. With regard to huddling among adult females, 49 (11%) instantaneous huddling points consisted of three or more females (average huddle size: 2.2). We did not consider whether the huddles consisted of two or more females. Unless clear statement (Result 2), when females huddle with both their young offspring and other adult females, we counted huddles between adult females but did not count huddles between mothers and their young offspring. We divided the study period into winter (December, January, and February) and non-winter (April-November and March). We did not record air temperature in our study site. According to the Automated Meteorological Data Acquisition System (AMEDAS) at Kuse (E133◦ 45.2 N35◦ 4.1 ), which is the nearest observatory to our study site (the distance: 8.5 km), the mean air temperature during each study period was 2.2 ± 0.7 ◦ C (mean ± S.E.) during winter and 17.3 ± 2.4 ◦ C during non-winter. The observatory at Kuse has an elevation of 144 m, and our study site had an elevation of 405 m. Thus, the air temperature at our study site was predicted to be lower than values at Kuse. Of 17 focal females, five had 0-year-old offspring, three had 1year-old offspring, and four had 2-year-old offspring. In Japanese macaques, not only 0-year-old offspring but also 1-year-old offspring are often dependent on their mothers for nursing and maternal carrying, if they did not have young siblings. Thus, 0and 1- year-old offspring may huddle with their mothers more often than 2-year-old offspring. In fact, in the winter, 0-year-old offspring and 1-year-old offspring huddled with their mothers at similar frequencies (Mann-Whitney test, U = 7, p = 1), but 2-yearold offspring huddled less frequently with their mothers compared to 0-year-old offspring (U = 20, p < 0.05) and 1-year-old offspring
(U = 12, p < 0.05). Therefore, we analyzed the data based on whether females had 0- or 1-year-old offspring. All data were analyzed using the statistical software R, version 3.0.0 (Palo Alto, California). All analyses were two-tailed and a significance level of p < 0.05 was set.
3. Results 3.1. Seasonal changes In the winter, we collected 630 instantaneous sampling points of huddling for focal females who had young (0- or 1-year-old) offspring, and 555 points for females who did not have young offspring. The results showed that females who had young offspring huddled with other adult females in 109 of 630 huddling points (17%), and females without young offspring did so in 460 of 555 huddling points (83%). On the other hand, in non-winter season, huddling between adult females was recorded only 12 and 21 points in total for each female group. Huddling frequency between mothers and young offspring would also be influenced by developmental stages, outside of thermoregulation. To determine any seasonal changes, we compared the frequencies of huddling between mothers and 1-year-old offspring in the winter with huddling frequency in the four months before winter (i.e., from August to November). The results showed that, in all three mother-and-1-year-old offspring pairs, huddling frequencies increased from the period before winter (0.32, 0.19, 0.63) to winter (0.43, 0.69, 0.81). Overall, huddling behavior increased in winter, compared with non-winter.
3.2. Huddling partner We analyzed the number of huddles during winter season. Females who had young offspring huddled less frequently with other adult females compared to females who did not have young offspring (U = 9, p < 0.01, Fig. 1a). However, the frequency of huddling with other individuals, including young offspring, did not differ between the two female groups (U = 55, p = 0.07, Fig. 1b). In addition, we compared huddling frequencies of females with young offspring for three categories: huddling with adult females, young offspring, and both of them. We found that females with young offspring tended to huddle with their young offspring, compared with the other two categories (Fig. 2). These results indicated that female Japanese macaques that had young offspring did not huddle with other adult females, but huddled with their young offspring.
M. Ueno, M. Nakamichi / Behavioural Processes 129 (2016) 41–43
Fig. 2. Frequency of huddling of females with young offspring during winter (huddling with only adult females, young offspring, and both adult females and young offspring). The vertical axis shows the ratios of huddling with any other individuals per total resting points during winter. Wilcoxon’s signed rank tests with Bonferroni correction: *p < 0.05; huddles consisted only of females and their young offspring occurred more often than huddles consisted of adult females (V = 0, p < 0.05) and of both female and their young offspring (V = 1, p < 0.05), but huddling frequency only with adult females and huddling frequency with both adult females and their young offspring did not significantly differ (V = 5, p = 0.88).
3.3. Huddling in sunny and cloudy weather Females who did not have young offspring huddled with other adult females more often in cloudy than in sunny weather (sunny (median): 0.12; cloudy: 0.37, Wilcoxon’s signed rank test, V = 4, p < 0.05). In contrast, with regard to females with young offspring, the difference in huddling frequency with adult females did not differ by weather conditions (sunny: 0.007; cloudy: 0.07, V = 7, p = 0.24). Instead, they huddled with their young offspring at a higher rate in cloudy than in sunny weather (sunny: 0.27; cloudy: 0.70, V = 4, p < 0.05). That is, when there is more need for thermoregulation, females who had young offspring huddled with their offspring instead of other adult females. 4. Discussion In this study, there was a general tendency for female Japanese macaques to increase huddling behavior with other group members during winter season, compared with during other seasons. However, females who had 0- or 1-year-old offspring huddled with their offspring, and huddled infrequently with other adult individuals during winter. In addition, females who had young offspring huddled with their offspring more frequently in cloudy than in sunny weather. These mean that females who had young offspring huddled with their offspring instead of other group members when there was substantial need for thermoregulation. In line with our study, Brent et al. (2003) reported an increase in mother-infant huddling in colder conditions, but Schino and Troisi (1998) did not. This may be due to the difference in the range of air temperature. The temperature recorded in Brent et al. (2003) ranged from −2.2 to 41.1 ◦ C and the mean air temperature in our study was thought to be lower than 2.2 ◦ C during winter (see Section 2). In contrast, the infants in Schino and Troisi (1998) experienced air temperatures between 13.4 and 25.7 ◦ C during their first 12 weeks of life. The temperature in Schino and Troisi’s (1998) study might have made it costly for infants to maintain their body temperatures, but not for their mothers (Chaffee and Allen, 1973). On the other hand, the air temperatures of our study site were cold enough such that huddling between a mother and her young offspring would be beneficial for both. Schino and Troisi (1998) suggested that infants are less suitable huddling partners because of their small size. Nevertheless, in our
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study, female Japanese macaques who had young offspring huddled with them, instead of with other adult individuals during winter. The reason may be that huddling with other adult group members causes anxiety. Previous studies showed that approaching and contact with other adult individuals cause anxiety in females macaques (e.g., Aureli et al., 1999). In addition, the average huddle size among adult individuals is smaller compared to in other study sites (e.g., average huddle size of Shodoshima island: 17.1 and 15.9, Zhang and Watanabe, 2007). This may reflect an intolerant society, which might lead to more anxiety for individuals to huddle. Thus, young offspring may be more profitable psychologically for contact compared to adult individuals. Moreover, huddling with young offspring may also be physically effective for thermoregulation. In Japanese macaques, the density of body hair in the ventral area is more sparse compared to in outer body parts (Zamma, 2002), suggesting that heat radiation easily occur through the ventral area. Japanese macaque mothers and their offspring tend to huddle at ventral–ventral positions; thus, huddling with young offspring can reduce body surface in the ventral area. This may offer enough thermoregulation benefits to their mothers. In conclusion, this study found that Japanese macaque mothers huddle with their young offspring, instead of with other adult group members, when there is need for thermoregulation. The weakness of our study was that we did not record the exact air temperature at the study site. However, given that Japanese macaques respond to seasonal changes in air temperature but not to absolute temperature (Hanya et al., 2007), this limitation may not be salient. In the future, whether the effectiveness of huddling differs by the size of huddling partners, and how individuals mitigate social tension caused by huddling with adult group members, would be valuable to investigate. Acknowledgments This study was supported by the Research Fellowships of the Japan Society for the Promotion of Science (JSPS) for Young Scientists (No. 232887). We are sincerely grateful to Kazunori Yamada and the members of the Department of Ethology, Graduate School of Human Sciences, Osaka University, for their encouragement. References Aureli, F., Preston, S.D., de Waal, F.B.M., 1999. Heart rate responses to social interactions in free-moving rhesus macaques (Macaca mulatta): a pilot study. J. Comp. Psychol. 113, 59–65. Brent, L., Koban, T., Evans, S., 2003. The influence of temperature on the behavior of captive mother-infant baboons. Behaviour 140, 209–224. Chaffee, R.R.J., Allen, J.R., 1973. Effects of ambient temperature on the resting metabolic rate of cold and heat-acclimated Macaca mulatta. Comp. Biochem. Physiol. 44, 1215–1225. Hanya, G., Kiyono, M., Hayaishi, S., 2007. Behavioral thermoregulation of wild Japanese macaques: comparisons between two subpopulations. Am. J. Primatol. 69, 802–815. Nakamichi, M., Yamada, K., 2007. Long-term grooming partnerships between unrelated adult females in a free ranging group of Japanese monkeys (Macaca fuscata). Am. J. Primatol. 69, 652–663. Ogawa, H., Wada, K., 2011. Shape of, and body direction in huddles of Japanese macaques (Macaca fuscata) in Arashiyama, Japan. Primates 52, 229–235. Schino, G., Troisi, A., 1998. Mother-infant conflict over behavioral thermoregulation in Japanese macaques. Behav. Ecol. Sociobiol. 43, 81–86. Ueno, M., Yamada, K., Nakamichi, M., 2015. Emotional states after grooming interactions in Japanese macaques (Macaca fuscata). J. Comp. Psychol. 129, 394–401. Zamma, K., 2002. Grooming site preferences determined by lice infection among Japanese macaques in Arashiyama. Primates 43, 41–49. Zhang, P., Watanabe, K., 2007. Extra-large cluster formation by Japanese macaques (Macaca fuscata) on Shodoshima Island central Japan, and related factors. Am. J. Primatol. 69, 1119–1130.