Hiroto Enari

Influences of Different Large Mammalian Fauna on Dung Beetle Diversity in Beech Forests

Abstract This paper focuses on biological relationships between mammalian species richness and the community structure of dung beetles in cool-temperate forests in the northernmost part of mainland Japan. The composition of beetle assemblages was evaluated at 3 sites in undisturbed beech forests with different mammalian fauna. In spring and summer 2009, beetles were collected at each site using pitfall traps baited with feces from Japanese macaques, Macaca fuscata Blyth (Primates: Cercopithecidae); Asiatic black bears, Ursus thibetanus Cuvier (Carnivora: Ursidae); Japanese serows, Capricornis crispus Temminck (Artiodactyla: Bovidae); and cattle. In the present study, 1,862 dung beetles representing 14 species were collected, and most dung beetles possessed the ecological characteristic of selecting specific mammalian feces. The present findings indicated that although species diversity in dung beetle assemblages was not necessarily positively correlated with mammalian species richness in cool-temperate forests, the absence of the macaque population directly resulted in the marked reduction of the beetle abundance, with the loss of the most frequent species, Aphodius eccoptus Bates (Coleoptera: Scarabaeidae) during spring.

Landscape-scale evaluation of habitat uses by sympatric mammals foraging for bark and buds in a heavy snowfall area of northern Japan

This study focused on influences of three different growing populations of mammals foraging for bark and buds—Japanese serows (Capricornis crispus), Tohoku hares (Lepus brachyurus angustidens), and Japanese macaques (Macaca fuscata)—on a cool-temperate forest in northern Japan. To acquire the initial knowledge to facilitate ecological monitoring of the influences, we evaluated habitat uses by each species on a landscape scale by using ecological niche factor analysis (ENFA), and identified commonalities and differences among the uses by using discriminant analysis (DA). Within a 50-km2 area, we selected five 5-km transects and recorded tracks of each mammal on the snow surface along transects during the month of March in 2008 and 2009. The track data were used as the proof of species presence for entry into ENFA and DA. Marginality and specialization of species habitat use, computed by ENFA, indicated that the macaque habitat represented the most heterogeneous distribution and the lowest environmental tolerance, which was strictly limited by altitude and terrain conditions to prevent exposure to severe cold climate conditions. This refuge selection by macaques resulted in habitat segregation from serows, although it appears that both mammals prefer the same young broadleaf forests. Meanwhile, the serow was observed to be distinctly inclined to use mountainous forests and to avoid artificial environments. As a result, its habitat could be differentiated from that of the hare, as confirmed by coefficients of a discriminant factor. These findings indicate that the impact of three different mammals foraging on the native vegetation could be quite restrictive.

Influence of Heavy Snow on the Feeding Behavior of Japanese Macaques (Macaca Fuscata) in Northern Japan

Natural disasters can degrade primate habitat and alter feeding behavior. Here, we examined the influence of unusually heavy snow on diet and feeding‐site use by Japanese macaques (Macaca fuscata) in northern Japan. To compare the winter‐feeding behavior under different snow conditions, we recorded the plant species foraged on by macaques in multiple transects of the Shirakami Mountains from 2008 to 2012 (excluding 2011). We used cluster analysis to describe foraged plant assemblages, and applied multiple dimensional scaling and decision tree modeling to evaluate annual variation in feeding‐site use by macaques. Our cluster analysis revealed five types of foraged plant assemblages. The proportion of each type present in transects varied considerably across the years, indicating that the diet of macaques in heavy snow conditions was influenced more by resource accessibility than by preference. Multiple dimensional scaling and decision tree modeling demonstrated that heavy snow conditions restricted feeding‐site use. Moreover, the distribution of refuges relative to severe external ambient environments was a stronger limiting factor for feeding‐site use than was the availability of food resources. While most primate species facing unexpected starvation employ risk‐prone foraging tactics (i.e., choosing the option with higher pay‐off by accepting risk), Japanese macaques have a tendency to adopt risk‐averse foraging behavior (i.e., minimizing energy loss when searching for preferred diet items under long‐lasting heavy snow conditions), because winters with temperatures below freezing have higher thermoregulatory costs. Am. J. Primatol. 75:534‐544, 2013.

Synergistic effects of primates and dung beetles on soil seed accumulation in snow regions

This study aimed to reveal the soil seed accumulation processes for endozoochorous plants in the heavy-snowfall forests of Japan, where seed dispersal agents are few when compared to tropical forests. We assessed (1) primary seed dispersal by Japanese macaques (Macaca fuscata) by identifying dispersed seeds found in their feces, and (2) secondary seed dispersal by dung beetles by using beads (as seeds mimics) of different sizes, to quantify the frequency of seed burial and burial depths. We studied this diplochorous system in different forest types (undisturbed beech forest, conifer plantation, and secondary beech-oak forest) and during the spring and summer seasons. The key findings were as follows: (1) macaques dispersed the seeds of 11 and 14 plant species during spring and summer, respectively; (2) seeds dispersed by macaques in the spring were smaller and twice as abundant than those dispersed in the summer; (3) although no differences were observed in the amount of beads buried by beetles between seasons, all bead sizes tended to be buried in deeper soil layers in the spring than in the summer; and (4) the seed supply to the soil in undisturbed beech forest and conifer plantation was greater than the one in secondary beech-oak forest. Similar to what has been observed in tropical forests, seeds defecated by frugivorous mammals can be successfully incorporated into the underground soil seed bank through a diplochorous macaque-beetle system in temperate forests of deep snow regions.

Ecological implications of mammal feces buried in snow through dung beetle activities

Abstract In early spring, snow-buried mammal feces simultaneously emerge on the ground with the melting of the snow across regions with heavy snowfall. Here, we evaluated the ecological implications of this phenomenon for the cool-temperate forest ecosystem in terms of the resource use of dung beetles (Coleoptera: Scarabaeidae), which play key roles in secondary seed dispersal and nutrient cycling. During May 2012 and 2013, we conducted cafeteria experiments in heavy snowfall regions with different types of forest cover in northern Japan by using pitfall traps baited with the snow-buried feces of Japanese macaques (Macaca fuscata), Japanese serows (Capricornis crispus), and Japanese hares (Lepus brachyurus angustidens). From the experiments, we identified 12 dung beetle species, indicating that the snow-buried feces could act as a valuable resource for vernal beetles. Most of the beetles had obvious fecal preferences. The snow-buried feces of serows were widely available resources for most vernal species, including dwellers and tunnelers, contributing to the biomass of those species. Although dung beetles using snow-buried feces in young broadleaf forests with rich feces supplies did not always exhibit the highest species richness, tunnelers frequently emerged in those forests, and Phelotrupes preferred macaque feces. This finding could have important implications for plant regeneration, as it relates to time-lagged mammal–beetle interactions. Endozoochorous seeds dispersed by macaques in the autumn have insufficient opportunities for secondary seed dispersal by beetles as the beetles are inactive in autumn, but those seeds are protected against predation by snow during winter and are safely preserved under soil by vernal tunnelers.

Predicting patterns of intentional introduction of non-native largemouth bass into farm ponds in northeastern Japan

Non-native species are difficult to eradicate or control once established. Thus, the prevention of invasions is a high priority for conserving native ecosystems. Our objective was to determine the factors that influence illegal introductions of non-native largemouth bass (Micropterus salmoides) and to develop a model that could be used to predict the pattern of future illegal introduction by anglers. We used generalized linear modeling (GLM) to evaluate the relationship between landscape and environmental factors and the presence of bass in farm ponds. Our results suggest that the occurrence of bass was primarily associated with pond size, distance of ponds from the urban center, and the proportion of the pond shoreline covered with a concrete revetment. We conclude that introductions occurred in ponds that were: easier to locate on a map, closer to anglers’ residential areas, and more easily accessible to the pond shore. Last, we suggest our predictive model could be used for preventive measures, such as identifying other ponds most at risk of future illegal introduction of non-native bass.

Impact assessment of dam construction and forest management for Japanese macaque habitats in snowy areas.

Japanese macaques (Macaca fuscata) in their northernmost habitats represent a keystone species and play a central role in heavy snowfall ecosystems. However, distributions have been restricted by pre‐war hunting, and populations are facing issues of natural forest losses caused by new dam constructions and massive conifer plantations. In the present study, we predicted the influences of these environmental conditions on macaque habitats during each season, and evaluated the effect of natural forest restoration as a mitigation measure. We constructed multiple habitat suitability models on the basis of different forest change scenarios, by using maximum entropy modeling (Maxent). We predicted the influence of each scenario by calculating the habitat unit (habitat quality × habitat quantity). We made the following predictions: (1) the influences of environmental conditions on habitat models vary seasonally, but dam construction destroys the optimum macaque habitats in every season; (2) restoration of conifer plantations to semi‐natural forests does not always contribute to the improvement of total habitat unit, except in snowy seasons; and (3) in comparison with encouraging natural forest restoration in plantation areas and maintaining the standard‐rotation plantation management, the implementation of long‐rotation plantation in existing plantation areas provides more suitable alternative habitats for macaques in non‐snowy seasons. Am. J. Primatol.

Snow Tolerance of Japanese Macaques Inhabiting High-Latitude Mountainous Forests of Japan

The Japanese macaque (Macaca fuscata) has flourished as a unique generalist species endemic to the Japanese archipelago, by acclimatizing to diverse environments along altitudinal and latitudinal clines. This chapter reviews recent studies on overwintering tactics of macaques inhabiting the Shirakami Mountains, northern Japan, by focusing on snow tolerance derived from dietary characteristics and habitat-use patterns. The Shirakami Mountains are one of the heaviest snowfall areas in the world, and constitute the northernmost habitats of any nonhuman primate. Macaques inhabiting snowy areas are exposed to the dangers of hypothermia and famine during winter, commonly resulting in pronounced energy deficit. To compensate for this deficit, they not only feed on the bark and buds of woody plants—fallback resources for most species of the genus macaque—but also use unique feeding tactics to access concealed dietary resources buried in snow, by seasonally changing their habitat-use patterns. Conifer plantations are often considered low-quality habitats, but macaques strategically use these artificial forests as their resting and feeding sites. In addition to describing biological interactions between macaques and their limited food plants in heavy-snowfall areas, this chapter characterizes the regional specialization of northernmost macaques.