Yamato Tsuji

Feeding strategies of primates in temperate and alpine forests: comparison of Asian macaques and colobines

We analyzed regional variation in the diets of two primate clades, Asian macaques and colobines, whose distributions include temperate–alpine forests. We addressed feeding strategies that enabled them to adapt to harsh environments characterized by relatively low mean temperatures and strong seasonality in both temperature and food availability. Macaques in tropical–lowland forests feed mainly on fruit and animal matter whereas populations in temperate–alpine forests feed more on foliage and on such items as bark and fungi. In comparison, colobines in tropical–lowland forests feed more on fruit and foliage whereas populations in temperate–alpine forests feed less on flowers and more on lichens. Annual precipitation and mean temperature, both of which reflect primary production, had the most significant effects on the feeding behavior of the macaques, whereas only mean temperature had a significant effect on that of colobines. We found two behavioral strategies used by both clades to cope with severe environmental conditions in temperate–alpine forests—shifting to other food items and adjusting feeding plasticity for fruit and foliage. Macaques responded to latitudinal changes by use of both strategies whereas the colobines adapted by using the latter only. By contrast, changes in altitude resulted in the macaques’ using the latter strategy and colobines’ using both. The different current distributions of Asian macaques and colobines could be attributed to differences in their feeding strategies originating in their digestive systems.

Food habits and home range use of Japanese macaques on an island inhabited by deer

Food habits and home range use of a troop of Japanese macaque Macaca fuscata Blyth on Kinkazan Island (9.6 km2), northern Japan, were studied from the spring of 2000 to the winter of 2002. The home range of this troop covers the area where vegetation is modified by foraging of sika deer Cervus nippon Temminck. The core areas of the home ranges of the macaque troop corresponded closely to the distributions of the staple food plants in every season. For example, leaves of Berberis thunbergii DC. and leaves of Zelkova serrata Makino in spring, berries of Berchemia racemosa Sieb. & Zucc. in summer, nuts of Zelkova serrata and Carpinus spp. in the fall of 2000 and winter of 2001, seeds of Torreya nucifera Sieb. & Zucc. in the fall of 2001, and bark of Zanthoxylum piperitum DC. in winter of 2002. Among the staple food plants, Berberis thunbergii and Zanthoxylum piperitum are more abundant on Kinkazan Island than other macaque habitats in northern Japan because they are spiny and unpalatable to sika deer, hence survive under the heavy foraging by the deer. Further, another staple food plant, Berchemia racemosa, a liana, grows abundantly at the edges of Illicium forests. Illicium anisatur is toxic and is not consumed by sika deer. Monkeys of this troop using the unique vegetation induced by sika deer grazing, fed on several plants which are not consumed by monkeys in other areas, and the home range was heavily affected by the distributions of these plants.

Regional, Temporal, and Interindividual Variation in the Feeding Ecology of Japanese Macaques

The feeding ecology of primate species often reflects their foraging behavior, as primates are faced with decisions about what, when, and where to feed (Oates 1987). The feeding behaviors in turn affect their feeding success, which ultimately influences population parameters such as mortality and birth rate. Thus, primate research must consider factors affecting variation in feeding ecology to better understand population dynamics (e.g., Dunber 1987; Cheney et al. 1988; Clutton-Brock and Pemberton 2004), to appropriately test socioecological theory (e.g., Nakagawa 1998, see also Chap. 12), and to apply the knowledge to primate pest management (Naughton-Treves et al. 1998; Yamada and Muroyama 2010, see also Chap. 7).

Effects of a Typhoon on Foraging Behavior and Foraging Success of Macaca fuscata on Kinkazan Island, Northern Japan

We studied the effects of typhoon damage on the food habits, time budgets, and moving distances of Japanese macaques (Macaca fuscata) on Kinkazan Island, northern Japan. Before the typhoon (pre-typhoon phase), the macaques fed on various food items, including fruit in trees (Swida macrophylla) and nuts (Torreya nucifera) on the ground. After the typhoon passed (post-typhoon phase), the macaques fed intensively on the seeds of Perilla frutescens (a forb) and the nuts of Quercus serrata on the ground. One may attribute the changes to decreased food availability or foraging efficiency of fruits and nuts on the ground, due to their concealment by leaf litter and mud and their consumption by other animals, such as sika deer (Cervus nippon) and field mice (Apodemus argenteus). In the post-typhoon phase, the macaques fed more quickly on seeds of Perilla frutescens, spent less time traveling, and moved over shorter distances. The differences may be due to changes in the distribution of staple foods between the 2 phases. We also evaluated the energy intake and energy balance of the macaques in both phases, based on observations of foraging and nutritional analyses of the food items. There is no significant difference in either parameter between the 2 phases. The changes in food habits and movement behavior may have compensated for the reduced food availability or foraging efficiency caused by the typhoon. Both behavioral changes and nutritional issues are important when investigating the effects of storms on animal ecology.

Endozoochorous seed dispersal by Japanese macaques (Macaca fuscata): Effects of temporal variation in ranging and seed characteristics on seed shadows.

Variation in seed shadows generated by frugivores is caused by daily, seasonal, and inter‐annual variation in ranging, as well as inter‐specific variability in gut passage times according to seed characteristics. We studied the extent to which seed weight, specific gravity, and daily (morning, afternoon, and evening) and inter‐annual (2004 vs. 2005) variation in ranging affected seed shadows generated by wild Japanese macaques (Macaca fuscata) in northern Japan. The macaques ingested fleshy fruits of 11 species during the two year study period; Viburnum dilatatum (Caprifoliaceae: heavier seeds with higher specific gravity) and Rosa multiflora (Rosaceae: lighter seeds with lower specific gravity) were eaten frequently in both years. The travel distances of macaques after feeding on V. dilatatum and R. multiflora fruits were estimated by combining feeding locations and ranging patterns measured in the field with gut passage times of model seeds in captive animals. Median travel distances after fruit feeding were 431 (quantile range: 277–654) and 478 m (265–646), respectively, with a maximum of 1,261 m. Neither year nor time of day affected travel distances. The gut passage time of model V. dilatatum seeds was longer than that of model R. multiflora seed, but this did not affect dispersal distances. Seed shadows for both species over 2 years showed unimodal distribution (peak: 101–500 m) and more than 90%, 20%, and 3% of ingested seeds were estimated to be dispersed >100, >500, and >1000 m, respectively, the longest known distances among macaque species. R. multiflora seeds tended to be dispersed further in 2004 than 2005, but V. dilatatum seeds were not, implying that inter‐annual variations in ranging pattern due to the distribution and abundance of nut fruiting could affect dispersal distance. Am. J. Primatol. 78:185–191, 2016.

Multi-annual variation in the diet composition and frugivory of the Japanese marten (Martes melampus) in western Tokyo, central Japan

To examine multi-annual variations in the food habits of the Japanese marten (Martes melampus), we analyzed the composition of marten feces in the Bonbori Forest Path in western Tokyo, central Japan, in two time periods a decade apart (1997–1998 and 2007–2008). The staple foods of martens in both periods were fruits/seeds and animal materials (mainly insects and mammals). The martens fed frequently on fruits/seeds and insects throughout the year in both periods, but the consumption of mammals, birds, and arthropods/other animals showed seasonal variations. The composition of fruits/seeds and the frequency of occurrence for each fruit-bearing species differed between the two periods. These results suggest that both the foraging strategy and role of martens as a seed dispersal agent changes yearly, presumably according to multi-annual variation in the availability of prey animals and/or fruits. We emphasize the importance of multi-annual studies both on food habits and to monitor food availability in the temperate region where the food environment changes among seasons, as well as years.

Identification of individual adult female Javan lutungs (Trachypithecus auratus sondaicus) by using patterns of dark pigmentation in the pubic area.

In a series of field surveys of wild Javan lutungs (Trachypithecus auratus sondaicus) conducted at Pangandaran Nature Reserve in West Java, Indonesia, from 2011 to 2012, we tried to use a method of individual identification by using individual-specific patterns of dark pigmentation in the pubic area. During the 2011 dry season, we used a digital SLR camera with a 400-mm telephoto lens to photograph the pubic area of each individual of a habituated group. These photographs were the basis for identifying 14 different adult females. During the rainy season of 2011 and the dry season of 2012, we checked the presence/absence of each of the identified individuals and found that these patterns were stable, at least during our study period. We found that two adult females and one adult female disappeared from the subject group between the first and second and between the second and third surveys, respectively, and that one adult female gave birth between the first and second surveys, but the infant had disappeared from the group between the second and third surveys. We could not confirm the validity of the method for juvenile females because of the dense white hair in their pubic areas and the fact that few individuals had clear patterns. Furthermore, we could not use this method for males because of the lack of pigmentation in the pubic area. As patterns of pigmentation in the pubic area are known to be present in other Trachypithecus species, our method can be useful for identification of individual adult females of these species, on which few individual-based behavioral studies have been conducted. Collecting individual-based behavioral data would enable us to track the presence of individuals in groups or movements between groups; determine the effects of social rank and age on within-group competition and copulation; and examine population data.

Sleeping-site preferences of wild Japanese macaques (Macaca fuscata): the importance of nonpredatory factors

Abstract I investigated sleeping-site preference in habituated wild Japanese macaques (Macaca fuscata) for each season (254 days total) on predator-free Kinkazan Island, northern Japan, during 2000–2007. I focused on the effectsof nonpredatory, environmental factors (vegetation type, altitude, and topography), to which little attention has been paid. Macaques used 24–79 sleeping sites in each season (227 sites in total, all on the ground). The frequencies of sleeping sites in each season followed a Poisson distribution, except for spring when several sites were used repeatedly. In spring macaques preferred sleeping in Zoysia japonica grassland, where several staple food species (Berberis thunbergii and Zelkova serrata) are abundant in this season. In summer and fall macaques avoided sleeping in high-altitude forest dominated by Fagus spp., and in the latter season they also preferred Zoysia grassland; these preferences likely reflect an avoidance of strong winds rather than the lower food availability at higher altitudes. In winter macaques avoided sleeping in Zoysia grassland, mainly due to the poor food supply. Macaques preferred valleys to ridges in spring and winter, possibly due to greater densities of shelters such as rocks and fallen trees that facilitate energy conservation in the face of strong/cold winds at night. Additional quantitative data for other mammalian species are needed for generalizations to be made about the importance of nonpredatory factors on sleeping-site preferences.

Diurnal Resting Site Selection and Daytime Feeding Behaviour of Wild Malayan Flying Lemur Galeopterus variegatus in Western Java, Indonesia

The Malayan flying lemur (Galeopterus variegatus) belongs to the Order Dermoptera, and is mainly distributed in the southern parts of Thailand, Indochina, Malay Peninsula, Sumatra, Java, Borneo, and the islands nearby (Lim 2007). It inhabits both lowland and mountainous areas, and is found in a large variety of habitats, including primary and secondary forests, coconut groves, and rubber plantations (Lim 2007; Baba 2008). Recent data on mitochondrial DNA of the flying lemurs have shown that this species is closely related to primates, likely related to our distant relatives (Schmitz et al. 2002; Lim 2007). Feeding, ranging, social, and reproductive behaviour data are fundamental information on animal ecology. However, to the best of our knowledge, information on habitat utilisation by flying lemurs and its determinants remains limited, and basically, we only know that flying lemurs are arboreal and nocturnal animals (Byrnes et al. 2011), that during the daytime they can be found in tree holes or hollows (Yasuma 1994), hanging from branches, or holding onto tree trunks, and that they are active at dusk (Lim 2007). Recent studies have reported about their home range size, nocturnal activity, and habitat preference (Baba 2008; Lim et al. 2013). With regard to feeding behaviour, information about Malayan flying lemur is fragmental (Agoramoorthy et al. 2006; Lim 2007; Baba 2008; Dzulhelmi and Abdullah 2009), compared to its sister Philippine species (Wischusen and Richmond 1998). In this study, we investigated diurnal resting site selection by the wild Malayan flying lemurs inhabiting West Java, Indonesia, at the plant-species and landscape level. We focused on forest structure, such as the extent of concealed areas and canopy cover, as these often influence resting site selection in other mammal species (Heymann 1995; Di Bitetti et al. 2000; Tsuji 2011). Lim et al. (2013) reported that flying lemurs in Singapore preferred forested areas with higher coverage; therefore, we aimed to confirm this finding in our study site. Besides we record several food items eaten in daytime. The relative importance of the daytime feeding seems lower than nocturnal one, but providing fundamental information on diet of the rarely studied-mammalian species would be meaningful.

Inter-annual variation in characteristics of endozoochory by wild Japanese macaques.

Endozoochory is important to the dynamics and regeneration of forest ecosystems. Despite the universality of inter-annual variation in fruit production, few studies have addressed the sign (seed predation versus seed dispersal) and strength (frequency and quantity) of fruit-frugivore interaction and the effectiveness of endozoochory in response to the long-term temporal context. In this study I evaluated the characteristics of endozoochorous dispersal by wild Japanese macaques Macaca fuscata inhabiting deciduous forest in northern Japan for five different years. I collected 378 fecal samples from the macaques in fall (September to November) and quantified the proportion of feces containing seeds, number of seeds per fecal sample, ratio of intact seeds, and seed diversity. The proportion of feces containing seeds of any species (five-year mean: 85.9%, range: 78–97%) did not show significant inter-annual variation, while species-level proportions did. The intact ratio of seeds (mean: 83%, range: 61–98%) varied significantly both between years and between months, and this varied among dominant plant species. The number of seeds per fecal sample (mean: 78, range: 32–102) varied monthly but did not between years, and the seed diversity (mean: 0.66, range: 0.57–0.81) did not show significant inter-annual variation, both of which were attributed to longer duration of macaques’ gastro-intestinal passage time of seeds exceed their feeding bouts. This study demonstrated that frequency and success of seed dispersal over seed predation of macaque endozoochory showed inter-annual variation, indicating low specificity across the seed–macaque network. The temporal variability in the quality of seed dispersal may provide evidence of high resilience in response to fluctuating environmental conditions in the temperate forests.