Naofumi Nakagawa

Effects of habitat differences on feeding behaviors of Japanese monkeys: Comparison between Yakushima and Kinkazan

Feeding behaviors of Japanese monkeys (Macaca fuscata) were compared between a warm temperate habitat (Yakushima Island: 30°N, 131°E) and a cool temperate habitat (Kinkazan Island: 38°N, 141°E). The composition of diet and the activity budget in the two habitats were very different. Time spent feeding on Kinkazan Island was 1.7 times that on Yakushima Island. Two factors seem to be responsible for these: (1) the energy required for thermoregulation of monkeys on Kinkazan Island is greater than that on Yakushima Island; and (2) the food quality, which affects the intake speed of available energy, is lower on Kinkazan Island. However, monkeys in both habitats increased their moving time and decreased their feeding time when they fed on foods of relatively high quality. Such foraging strategies are predicted by optimal foraging models. Time spent social grooming on Yakushima Island was 1.9 times that on Kinkazan Island, although there were slight seasonal changes in both areas. The difference in time spent social grooming might be explained by the overall difference in feeding time and day length between the two habitats.

Determinants of the dramatic seasonal changes in the intake of energy and protein by Japanese monkeys in a cool temperate forest

Daily intake of gross energy (DGEI) and protein (DGPI) of Japanese monkeys in a cool temperature forest were investigated in different four seasons. As a result, dramatic seasonal differences in DGEI and DGPI were found: DGEI and DGPI in winter were significantly lower than those in spring and autumn, being only about 17–42% of those in the two seasons. DGEI and DGPI in summer were also lower than those in autumn and spring, being only about 29–52% of those in the two latter seasons. Seasonal comparisons of some variables on food qualities revealed that much lower values of DGEI and DGPI in winter and summer were influenced srongly not so much by the lower calorie and protein content of food as by the lower speed of dry weight intake. Multiple regression analyses for each food item revealed that the unit weight was a more important factor in determining the speed of dry weight intake than was the speed of unit intake. In addition, the speed of dry weight intake contributed much more to the speed of calorie and protein intake than did the content of calorie and protein. Multiple regression analyses, employing DGEI and DGPI (as dependent variables) and daily mean values of some variables related to food quality (as independent variables), revealed that the mean values of speed of calorie and protein intake on food items eaten in a day could explain 79.0% and 85.9% of the variance in DGEI and DGPI, respectively. In addition, the mean value of the speed of dry weight intake of food items eaten in a day can be used to explain 74.3% and 52.8% of the variance in DGEI and DGPI, respectively. These findings suggested that not only nutritional content of food but also the speed of dry weight intake strongly determined the nutritional condition of nonhuman primates. Am. J. Primatol. 41:267–288, 1997.

Feeding rate as valuable information in primate feeding ecology.

In this review I outline studies on wild non-human primates using information on feeding rate, which is defined as the food intake per minute on a dry-weight basis; further, I summarize the significance of feeding rate in primate feeding ecology. The optimal foraging theory has addressed three aspects of animal feeding: (1) optimal food patch choice, (2) optimal time allocation to different patches, and (3) optimal food choice. In order to gain a better understanding of these three aspects, the feeding rate itself or its relevance indices (e.g., rates of calorie and protein intake) could be appropriate measures to assess the quality of food and food patches. Moreover, the feeding rate plays an essential role in estimation of total food intake, because it varies greatly for different food items and the feeding time is not a precise measure. The feeding rate could also vary across individuals who simultaneously feed on the same food items in the same food patch. Body size-dependent and rank-dependent differences in the feeding rate sometimes cause individuals to take strategic behavioral options. In the closing remarks, I discuss the usefulness of even limited data on feeding rate obtained under adverse observational conditions in understanding primate feeding ecology.

Seasonal, Sex, and Interspecific Differences in Activity Time Budgets and Diets of Patas Monkeys (Erythrocebus patas) and Tantalus Monkeys (Cercopithecus aethiops tantalus), Living Sympatrically in Northern Cameroon

I examined seasonal, sex, and interspecific differences in activity time budgest and diets of patas (Erythrocebus patas) and sympatric tantalus monkeys (Cercopithecus aethiops tantalus) on the basis of 5-day data sets collected in three and two different seasons, respectively, by the method of focal animal sampling. The seasons included species-specific mating and birth seasons. As compared with not only the birth season but also conspecific females, both patas resident male and tantalus male spent less time feeding and more time resting, day and night, in their respective mating seasons. Given that day-resting time includes time for vigilance for non-resident males and receptive females, this may reflect that males should minimize time spent feeding to allow maximum participation in other fitness-increasing activities such as mating-relating activities asSchoener (1971) predicted. In both species, the males consumed fruits containing less protein but more calories and showed a high feeding rate to compensate for the shorter time spent feeding in the mating season. In contrast, females consumed protein-rich food types (i.e. animals, protein-rich seeds, leaves, and flowers) in the birth season to meet the high demand for protein due to pregnancy and lactation. Given that the season for males was considered to be not a calendar but a reproductive “season” (i.e. mating or birth season), both sexes of patas spent more time moving and less time day- and night-resting than did the tantalus counterparts irrespective of the “season”. Patas subsisted on fruits, gums, and supplementarily lipid-rich seeds as an energy source and animal matters and protein-rich seeds as a protein source. In contrast, tantalus subsisted on fruits and lipid-rich seeds as energy and flowers and leaves as protein.

Differential habitat utilization by patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus) living sympatrically in northern Cameroon

In order to obtain reliable evidence for differences in habitat preferences between two closely related savanna‐dwelling primate species, namely, patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus), I collected data on vegetation and patterns of range use concurrently at a single study site, Kala Maloue, Cameroon, in a similar manner for a group of each species. Kala Maloue consisted of 64% grassland mostly dominated by Gramineae spp. and the rest was woodland. Tantalus monkeys showed preference for woodland, especially gallery forest, much more than did the patas irrespective of the season. Moreover, patas preferentially established their home range in grassland in the wet season. Interspecific and seasonal differences in habitat preferences could be interpreted on the basis of interspecific and seasonal differences in preferences for main food. In dry season, tantalus utilized water‐containing areas at a frequency closely in proportion to the availability of such areas while the patas utilized water‐containing areas more frequently than expected. This is because tantalus established a smaller home range along the river where water was never completely depleted throughout the dry season. Both the patas and the tantalus preferred woodland to grassland as sleeping sites possibly owing to predation avoidance. Both the daily travel distance per group weight and the home range size per group weight were greater for patas than for tantalus partly because of higher preference for grassland with low habitat quality in the case of patas. It is suggested, however, that high locomotive ability enabled patas to effectively utilize small and widely dispersed items of food such as grasshoppers and to explore areas with high availability of food and water and with preferable sleeping sites. Am. J. Primatol. 49:243–264, 1999.

Ecological determinants of the behavior and social structure of Japanese monkeys: A synthesis

A review is presented of the results of the various studies in this volume and an attempt is made to establish connections among several features of the ecology, behavior, and social structure of Japanese monkeys. Several studies in this volume suggest that intergroup direct feeding competition has been much more severe in Yakushima, in the warm-temperate region, than in Kinkazan, in the cool-temperate region of Japan. This result is consistent with the predictions that moderate abundance and clumped distribution of food incur more severe intergroup direct competition. However, the number of adult females within a group in Yakushima was smaller than that in Kinkazan even though severe intergroup direct competition should favor large groups. This contradiction can be mainly explained by the less severe intergroup indirect competition in Kinkazan than in Yakushima. By contrast, some studies in this volume also indicate that adult male to female ratio within a group has been higher in Yakushima than in Kinkazan. This result can be explained in two ways: the females in Yakushima might have recruited more males to increase the competitive ability of the group under conditions of severe intergroup direct feeding competition; alternatively, it might be profitable that the males in Yakushima defend females cooperatively as group males against the males in other groups at a moderate density of females. Some studies in this volume suggest that grooming frequency was higher in Yakushima than in Kinkazan. The higher grooming frequency in Yakushima might have been partly due to a constant increase in engaging in social behavior from a decrease in feeding time. Another reason might be that there is a stronger effect of grooming on promotion of formation of coalitions among adults under conditions of severe intergroup direct and intragroup direct competition.

Difference in food selection between patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus) in Kala Maloue National Park, Cameroon, in relation to nutrient content.

Abstract. Phytochemical or nutrient analyses of primate diets have revealed clues to their food selection in a single species. On the other hand, few interspecific comparisons of phytochemical or nutrient composition of primate diets have been made, although diets are considered to differ in phytochemical or nutrient content from primate species to species, since different species have different body weights and different morphological and physiological characteristics. I compared the nutrient content of diet between patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus) living sympatrically in Cameroon. Patas subsisted on a smaller number of food items, most of which were also tantalus food items. Then, I compared the protein–fiber ratio and the available energy content of the food items eaten by patas (patas foods) with those items eaten only by tantalus (tantalus foods). Both variables were higher in patas than tantalus foods, although there was no significant difference in available energy of plant foods. Next, when I performed discriminant analysis for patas foods and tantalus foods, employing the above two variables, a discriminant function with positive coefficients for both variables was obtained. The mean discriminant-function score of patas foods was higher than that of tantalus foods. Despite being somewhat larger in weight, patas selectively fed on a smaller number of foods of higher quality than did tantalus. I discuss why the results are inconsistent with a well known body weight–diet relationship (Jarman–Bell principle). Energy-efficient locomotion enables patas to exploit not only small dispersed food items of high quality but also areas where high-quality foods are distributed in clumps.

Foraging energetics in patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus): Implications for reproductive seasonality

The patas monkeys (Erythrocebus patas) in Kala Maloue, Cameroon, have their birth season in the mid‐dry season, whereas closely related, sympatric tantalus monkeys (Cercopithecus aethiops tantalus) have their birth season in the wet season. To evaluate the optimality of a species‐specific birth season, I estimated the daily intake of available energy and gross protein, and energy expenditure for one individual of each sex of each species between respective birth and mating seasons. The monkeys obtained a larger amount of available energy and gross protein in the birth season than in the mating season. No significant seasonal differences in energy expenditure between the birth and mating season were found. Thus, the birth season appears to be timed to the season when the monkeys can obtain more surplus energy and protein. Interspecific differences in the optimality of birth season were attributed to widely exploitative foraging, supported by the patas’ high locomotive ability, which may enable them to obtain more energy from seeds of Acacia seyal and gums of A. sieberiana, and more protein from grasshoppers and seeds of A. seyal in the mid‐dry season than the tantalus monkeys. A review of preceding studies suggests that the availability of seeds of Acacia fruiting during the dry season may exert the dominant influence on timing of birth not only in patas but also in savanna monkeys (Cercopithecus aethiops), which include the tantalus monkeys. Am. J. Primatol. 52:169–185, 2000.

Intraspecific Differences in Social Structure of the Japanese Macaques: A Revival of Lost Legacy by Updated Knowledge and Perspective

The current socioecological models were developed to identify the type of food competition via ecological factors affecting female social relationships in primates (Wrangham 1980; van Schaik 1989; Isbell 1991; Sterck et al. 1997). There is a slight difference among the models (see Isbell and Young 2002 for details), but rough consensus in the following scenarios. The models predict that clumped or patchy food distributions bring about within-group contests over foods, which shape a linear and stable dominance hierarchy among females. If high-quality foods are clumped in intermediate-sized patches relative to the group size, a within-group contest would predominate. Only highly competitive females and her kin would be able to monopolize food resources, sometimes through coalition among kin (i.e., nepotism). Consequently, a linear and stable dominance hierarchy (i.e., despotic) and female philopatry would evolve among females [RN, or “Resident-Nepotistic,” in the terminology of Sterck et al. (1997)]. In contrast, if low-quality foods are highly dispersed or clumped in a patch large enough to accommodate all group members, a within-group scramble (not a within-group contest) would prevail, whereby all females could equally share the food resources without any coalition. As a result, a nonlinear and unstable dominance hierarchy (i.e., egalitarian) and female dispersal would evolve [DE, or “Dispersal-Egalitarian”; Sterck et al. (1997)]. Even under a weak within-group contest, however, female philopatric trait would evolve to defend such large food patches cooperatively against neighboring groups under severe between-group contest [RE or “Resident-Egalitarian,” Sterck et al. (1997)]. Moreover, van Schaik (1989) and Sterck et al. (1997) added a fourth category (RNT, or “Resident-Nepotistic-Tolerant”). When both types of contest were severe, dominant females would become tolerant to subordinates to derive cooperative forces from them at a group encounter although linear dominance hierarchy was found among females.

Embracing in a Wild Group of Yakushima Macaques (Macaca fuscata yakui) as an Example of Social Customs

Recently, some primatologists have begun studying social customs, which had been neglected in research despite their importance to human culture. We observed embracing behaviors 64 times during 543.8 hours of focal animal sampling, targeting adult females in a wild group of Japanese macaques in Yakushima, Japan, and compared the results with those in macaques in Kinkazan. Embracing occurred immediately after the spontaneous pause of allogrooming, aggressions, and approach between dyads frequently exchanging antagonistic interactions, all of which are considered to be stressful conditions. Embracing in Yakushima may, therefore, serve to reduce stress; this may also be the case in Kinkazan. Despite this functional similarity, the forms of embracing in Yakushima are slightly different from those in Kinkazan. First, not only ventro-ventral embraces, but also ventro-lateral and ventro-dorsal embraces were found in Yakushima. Second, kneading another’s fur by rhythmically opening and closing the palm occurred in Yakushima, instead of a rhythmic, body-rocking movement in Kinkazan. Because we cannot devise genetic or ecological explanations for the subtle local differences in embraces, this type of behavior may be identified as the first evidence for social customs in wild Japanese macaques.