Feeding Ecology

Japanese macaques (Macaca fuscata)

For Japanese macaques inhabiting Kinkazan Island which is covered with cool-temperate deciduous forest, their food condition deteriorates from autumn to winter because foods hardly become available during winter. I quantitatively showed the deterioration of food condition by feeding rate on two main food items with high-quality, i.e., beech nuts or torreya seeds, and thus revealed the feeding strategies against it as follows: 1) exploitation of new food patches; 2) extension of feeding time; and 3) change food items (Nakagawa, 1989a). Moreover, I estimated intake of calorie and macro-nutrients both in late autumn (November) and mid-winter (February), and found that both of calorie and protein intake exceeded their requirement in November but were far below in February.
I also found the macaques employed the strategies against deterioration of nutritional condition as follows: 1) increase in food diversity, 2) reduction in the daily travel distance; and 3) avoidance of repeated use of their range (Nakagawa, 1989c). On the other hand, even in Kojima Islet which is covered with warm-temperate evergreen forest, the macaques suffered from slight nutritional deficiency (Iwamoto, 1982). Then, we compared nutritional quality of food items both in autumn and winter among four populations, i.e., two belonging to cool-temperate zone (Kinkazan and Shimokita Peninsula) and two belonging to warm-temperate zone (Kojima and Takasakiyama).
In the analyses, we focused two constraints, i.e., gut volume and time, as well as comparisons of contents and intake rate of calorie and nutrients. In autumn, the macaques not only in warm-temperate zone but also in cool-temperate one fully satisfied the requirement due to high-quality food in terms both of contents and intake rate, enough not to be affected by two constraints. In winter, contrastingly, severe nutritional deficiency in cool-temperate zone were caused by not only low nutritional contents but also low intake rate relative to time spent feeding while slight nutritional deficiency in warm-temperate zone were caused by low nutritional content relative to gut volume (Nakagawa et al., 1996). I also estimated intake of calorie and macro-nutrients both in spring (May) and summer (August) at Kinkazan. As results, calorie intake in summer was low equivalent to winter, while that in spring was high equivalent to autumn. On the other hand, protein intake in summer were still low equivalent to winter, while that in spring were higher than that in autumn. I examined the factors underlying seasonal differences in calorie and protein intake by stepwise multiple regression analysis and found that intake rate on a dry weight basis of foods more strongly contributed to the seasonal differences in calorie intake rather than calorie content of foods (Nakagawa, 1997).

Patas monkeys (Erythrocebus patas) and Tantalus monkeys (Chlorocebus aethiops tantalus)

In Kala Maloue National Park, Cemeroon, which was located in sahel-savanna zone, I conducted comparative ecological studies on two phylogenetically close-related guenons, patas monkeys (Erythrocebus patas) and Tantalus monkeys (Chlorocebus aethiops tantalus). Because no quantified food list was available for patas monkeys at the onset of our long-term study, to begin with, I reported that they were strongly terrestrial and subsisted on flowers and buds of herbaceous plants and larva of insects in a wet season by a preliminary study (Nakagawa, 1989b). By the main study which was subsequently conducted, I found large differences in ranging pattern and range use between these two species. A group of tantalus set a small home range less overlapped with those of the other groups along the riverine forest, and preferred to use there. On the other hand, a group of patas set a large home range much overlapped with those of other groups in area including grassland and preferred to use there only in wet season (Nakagawa, 1999). As for difference in food types, patas fed on fruits and gums as energy source and insects and legume pods as protein source while tantalus fed on fruits and lipid-rich seeds as energy and flowers and leaves as protein. As for difference in activity budget, patas spent more time for moving and less time for resting than did tantalus (Nakagawa, 2000a). Calorie and protein intake was higher in birth season than in mating season in both species. On the other hand, there was no seasonal difference in energy consumption. As a matter of fact, reproductive seasons were completely reversed in these two species: the birth season corresponded to mid-dry season in patas while it corresponded to wet season in tantalus; the mating season corresponded to wet season in patas while it corresponded to mid-dry season in tantalus. Therefore, birth season in each species have been evolutionarily determined so that they maximized nutritional intake without increasing energy cost. Energy-rich gum of acacia and protein-rich pods of acacia and insects enable them to give birth in mid-dry season (Nakagawa, 2000b). Isbell (1988) insisted that high locomotive ability underlined by long limbs and digitigrady enable them to subsist on small and dispersed foods, such as insects irrespective of their relatively large body size. I agreed with her but I insisted that high locomotive ability also enables them to feed on foods which were highly dispersed but formed large patch, such as acacia (Nakagawa, 1999). Therefore, I concluded that utilization of gums and pods of acacia trees forming large patch located far away from the riverine forest where tantalus set their home range enable patas to give birth in mid-dry season (Nakagawa, 2000b). In addition, I suggested that high locomotive ability in patas made it possible to select higher-quality foods than did the tantalus (Nakagawa, 2003). Comparison of male and female in both species also provided new findings. While there were no seasonal differences of activity budget in females in both species, there was in males: male monkey drastically decreased time spent feeding and increased resting in species-specific mating season. Given that resting time include vigilance and/or monitoring bachelor males and estrus females, it can be explained that males set priority to resting time over feeding time irrespective of seasons, females preferred protein-rich foods, i.e., insects and pods of acacia for patas and leaves and flowers for tantalus while males preferred protein-poor foods (fruits for both species). It has been well known that female prefer protein-rich foods, such as insects and leaves, for milk production in birth season. Since there is no plausible reason females preferred protein-rich foods even in mating season, I think it is by-product of male’s preference for fruits with high feeding rate to compensate for reduced feeding time (Nakagawa, 2000a). Abovementioned studies and the results of vegetation survey are introduced by the book written in Japanese (Nakagawa, 2007).

General

I revealed that not only maximum rate of feeding but also average rate of feeding can be successfully scaled with body weight of primate species (Nakagawa, 2008b). Also, I insisted that feeding rate is important tool for primate feeding ecology in the book written in Japanese (Nakagawa, 2007) and a review paper in English (Nakagawa, 2009).

Behavioral Ecology

Japanese macaques (Macaca fuscata)

I tried to verify the theory of optimal patch choice and use, one of the intriguing theme in behavioral ecology, using a group of wild Japanese macaques in Kinkazan as a material, and obtained the following findings: 1) The macaques usually chose the higher-quality food patch (i.e., where the feeding rate was higher) and fed there (Nakagawa, 1990a); but 2) showed no significant tendency to feed for a longer time in the higher-quality patch. and 3) hardly leave the patch due to depletion of the patch since there were few cases that feeding rate in a bout dramatically dropped (Nakagawa, 1990b). I put not only such issues of food patch choice and patch use but also issue of food choice into optimal foraging theory in behavioral ecology and feeding ecology in primatology so far and reconsidered (Nakagawa, 1989 in Japanese). I also reviewed past studies on food selection in non-human primates from the viewpoint of optimal food selection. Key factors in the classical model of optimal food selection were “maximization” of the “intake rate” of “energy”. Later, the key factors were change to “maximization” of the “contents” of “energy-essential nutrients” and “minimization” of the “contents” of “digestion inhibitor-toxins” in a modified model for herbivores. Most studies on food selection in herbivorous non-human primates have been based on the modified model, and revealed that primates choose food so as to maximize protein, and to minimize digestion inhibitors (fiber, condensed tannin). However, the present review points out that the above key factors of the classical model are also important because food availability relating these factors correlates positively with feeding frequency (Nakagawa, 1996 in Japanese).

Patas monkeys (Erythrocebus patas)

I become interested in evolutional factors of frequent allo-mothering behavior among matrilineally non-related adult patas females. Its clue was rare observation on of infant kidnapping by members of a neighboring group. All the members of the neighboring group other than a harem male engaged in allo-mothering to a kidnapped infant and two adult females even nurse it (Nakagawa, 1995). Then, the playback experiments were designed to examine 1) whether infant distress call attract allo-mothers and 2), if so, whether any differences in responses exist between relatives and nonrelatives. Irrespective of relatives (not mother but grandmother) or matrilineally non-relatives, adult female patas more frequently and strongly responded to infant call, such as approach the speaker, than to allo-mother ‘s call. Given that allo-mothering were exchanged with grooming given (not grooming received) in patas (Muroyama, 1994), evolution of allo-mothering among matrilineally non-related adult patas females cannot be explained by reciprocal altruism. Then I hypothesized that it can be explained by kin selection through the patrilineal line on the ground that all the infants are patrilineal siblings since a harem holding male predominantly copulate with all the reproductive females in a harem. Then, selective pressure on the ability for matrilineal kin recognition might be low in patas monkeys (Nakagawa, 1998).

Animal Sociology

Patas monkeys (Erythrocebus patas)

I examined the distribution of affiliative behaviors among group members. So far, in captive or free-ranging patas monkeys released in an island, neither dominance nor kinship reportedly influences affiliative behaviors among females (Kaplan & Zucker, 1980). However, in a wild group at Kala Maloue, Cameroon, both of dominance rank and kinship influenced on four types of affiliative behaviors, i.e., proximity within a 3 meters, allo-grooming, contact call and co-night resting (Nakagawa, 1992; Nakagawa, 2007 in Japanese).

Japanese macaques (Macaca fuscata)

I examined the functions of embracing behaviors in Kinkazan, which has been known only in a few populations other than there. Embracing often occurred mainly among adult females just after intermissions of grooming, agonistic interactions, and just approach-being approached between non-relatives and shifted smoothly to allo-grooming. This suggested that embracing occur under stressful condition and may function to reduce tensions (Shimooka & Nakagawa, 2014).

Chimpanzees (Pan troglodytes)

We examined effects of familiarity and length of separation on the frequency of greeting behaviors in captive chimpanzees at Oji Zoo, Kobe. As results, firstly, separation per se, and secondly familiarity measured by proximity increased the frequency of greeting behaviors although no impact of length of separation (Hige, Kudo, & Nakagawa, 2003 in Japanese).

Socio-ecology

Japanese macaques (Macaca fuscata)

Dr. Agetsuma and I conducted inter-seasonal and inter-regional comparisons of activity budget and feeding time on each category (plant part and animal) of foods, targeting at Japanese macaques living in remarkably different environments: Kinkazan Island which is covered with cool-temperate deciduous forest in the north and Yakushima Island which is covered with warm-temperate evergreen forest in the south. In inter-seasonal comparisons, employing multi-regression analysis with each of moving time, resting time, and grooming time as dependent variables, and both of day length and feeding time as independent variables, the longer the day length were and/or the shorter the feeding time are in a month, both of moving time and resting time were longer in a month in both region. In contrast, any significant correlations in grooming time were not found except for a weak negative correlation between grooming time and feeding time in Yakusihma. We also examined correlations between feeding time on each food category in a month and each of total feeding time and moving time. In both of Kinkazan and Yakusima, we could discriminate two types of foods: 1) those showing negative correlations with total feeding time but positive ones with moving time (fruits in both regions and insects and fungi in Yakushima); 2) those showing positive correlations with total feeding time but negative ones with moving time (fallen seeds, mature leaves and young leaves in Yakushima, dormant buds, bark, and herbs in Kinkazan). The former category seems to be characterized as high nutritional intake and low density. On the other hand, the latter characterized as low nutritional intake and high density. In sum, the selection of main foods out of two distinct food types which differ in nutritional quality and density determines total feeding time and moving time but hardly affect grooming time. In inter-regional comparisons, the macaques in Kinkazan spent more time feeding due to lower rate of nutritional intake and higher thermoregulation cost than those in Yakusima, and hence less time grooming, which might cause lower cohesiveness of a group (Agetsuma & Nakagawa, 1998). I synthesized all the papers, including aforementioned one, appeared in special issue of “Primates” (volume 39, no. 3) entitled “Japanese macaques in natural habitats: Comparative Studies in Kinkazan and Yakushima” from the socio-ecological point of view (Nakagawa, 1998). The applicability of “Double Concentric Circle Structure Model” (Itani, 1954) to wild Japanese macaque troop was reconsidered from the socio-ecological point of view (Nakagawa, 2000 in Japanese). I also reviewed recent outcomes in primate socio-ecology (Nakagawa, 1999 in Japanese; Nakagawa & Okamoto, 2003 in Japanese).

4.2 Patas monkeys (Erythrocebus patas) and Tantalus monkeys (Chlorocebus aethiops tantalus)

Patas monkeys have been categorized as egalitarian (Sterk et al., 1997). Isbell & Prutez (1998) and Prutez & Isbell (2000) investigated antagonistic interactions among adult females in a wild group of Eastern patas monkeys (E. patas pyrrhonotus) living in Laikipia, Kenya in comparison with sympatric vervet monkeys (Chlorocebus aethiops pygerythrus) and concluded that patas categorized as egalitarian while vervet as despotic. Although I had reported that dominance rank influence the affiliative behaviors, such as grooming in a wild group of western patas (E. patas patas) (Nakagawa, 1992), Isbell & Prutez (1998) dismissed it as a result of provisioning. Then, I reanalyzed my data to provide the evidence that despotic social structure in western patas monkeys are not due to provisioning but to quality and distribution of natural foods. I compared agonistic interactions involving food between patas monkeys and sympatric tantalus monkeys (Chlorocebus aethiops tantalus) in Kala Maloue, Cameroon. I found linear dominance hierarchies not only in tantalus monkeys, but also in patas monkeys in Kala Maloue. The rates of agonistic interactions during feeding between patas monkeys were equivalent to those between tantalus monkeys in Kala Maloue; further, these rates were significantly higher than those of both Laikipia patas and vervet monkeys. The results imply that patas monkeys in Kala Maloue are not egalitarian, but are despotic, similar to tantalus monkeys. Disparity in the dominance hierarchies of patas monkeys between Kala Maloue and Laikipia were attributable to the differences in the characteristics of food resources. Whereas patas monkeys in Laikipia subsist on small and dispersed food resources within a high-density area, those in Kala Maloue subsisted on food resources that were clumped in intermediate-sized patches within a low-density area. This study shows that the socio-ecological model (Sterck et al., 1997) is applicable not only for inter-specific comparisons but also for intra-specific comparisons (Nakagawa, 2008a).

General

I reviewed the male-female friendship in non-human primates with special reference to its benefits. While I concluded most of such a relationship can be explained by socio-ecological viewpoint, its explanatory power is not enough to explain the following observations: tow non-troop males visit a group of Japanese macaques in Yakushima on separate days during mating season. They received grooming one-sidedly by a female and soon left the group without copulating. These two cases seemed to be interactions between old friends, but the reciprocity cannot be formed. As the reunion with an old female friend of a male after immigration rarely occurs, mal-adaptive behavior would not be a problem. Socio-ecology does not explain such rarely occurring events (Nakagawa, 2008 in Japanese).

Population Ecology

Patas monkeys (Erythrocebus patas)

Based on long-term, although intermittent, observations (2 years 4 months out of 14 years), we present data on birth seasonality, age at first birth, inter-birth intervals, mortality rates, age at first emigration, and population change of a wild population of West African patas monkeys (Etythrocebus patas patas) in northern Cameroon. Birth season was from the end of December until the middle of February, corresponding to the mid-dry season. In spite of large body size, the patas females had the earliest age at first birth (36.5-months-old) and the shortest inter-birth intervals (12 months) compared to the closely related wild forest guenons. Age at first emigration of the males was considered to occur between 2.5-4.5 years. The group size of the focal group drastically decreased between 1984 and 1987, and continued to steadily increase until 1994, then decreased again in 1997. The neighboring group also showed a similar trend in group size. The population decreases were likely to be caused by drought over three years. Annual crude adult mortality rate was 4% during population increase periods (PIP) between 1987 and 1994. It rose to 22% during all the periods (AP), including drought over three years. Despite their smaller body size, that of wild forest guenons (Cercopithecus mitis) (4%) was the same and much lower than those of the patas during PIP and AP, respectively. The annual average juvenile mortality rate was 13% during PIP and it also rose to 37% during AP. That of wild forest guenons (C. ascanius) (10-12%) was a little and much lower than those of the patas during PIP and AP, respectively. These findings were consistent with Charnov’s (1991) theoretical model of mammalian life-history evolution in that patas with high adult and juvenile mortality showed early and frequent reproduction in spite of large body size. Charnov (1991) also considered high adult mortality as a selective force and high juvenile mortality as a density-dependent consequence of high fecundity. Our results support the former but not the latter.

Human Evolution Studies

Study on social convention

We humans have a variety of cultures that cannot be categorized strictly as material culture. In primatology, however, these cultures of social behavior or “social conventions” that represent particular styles of sociality permeating an array of social behaviors, have been largely ignored because researchers have sought to shed more light on material cultures instead. However, recently inter-population differences in behavioral patterns of an embracing behavior that functions to reduce tension have been found in wild Japanese macaques (Macaca fuscata). In one population (Kinkazan Island), the macaques rock their bodies back and forth in a ventro-ventral position, whereas in another population (Yakushima Island), the embracing occurs in one of three positions—ventro-ventral, ventro-lateral, or ventro-dorsal—and is accompanied by kneading the fur by opening and closing their palms. On the other hand, such embracing behaviors have never been observed in some populations or groups, irrespective of long-term intensive observations. All these inter-population differences were considered to be cultural differences (Nakagawa et al., 2015).

Study on evolutionary history of social structure in early humans

With the recent development of molecular genetic techniques, the knowledge about sex-biased locational dispersal (i.e., which sex disperse further from place of birth) have been accumulated in non-human primates. When I put these knowledges on phylogenetic tree, I obtained the following preliminary results: ancestral type of primates exhibited male-biased dispersal, and appeared to evolve into female-biased dispersal till the stage of ancestral anthropoids. At a fifty-fifty possibility, female-biased dispersal has been kept until ancestral apes, and then early humans. Given that one male-one female group, monogamous mating, paternal care, and territoriality matches very well the female-biased dispersal and always appears to evolve in concert, I arrived at a conclusion that early humans exhibited monogamous one male-one females society (Nakagawa, 2013).