Eat the fruit earlier: Sakis (Pithecia chrysocephala) show enhanced temporal fruit resource access compared with squirrel monkeys (Saimiri sciureus) in an urban forest fragment in Brazil.

Fruit availability experienced by different primate species is likely to vary due to species-specific fruit use, even within the same habitat and timeframe. Pitheciines, primates of the subfamily Pitheciinae, particularly favor the seeds of unripe fruits. Researchers consider this dietary characteristic an adaptation to increase access to fruit resources. However, the relative advantages of pitheciines over sympatric non-pitheciine non-seed-eating primates regarding species-specific fruit availability is not well studied. In a 26-ha forest within the city of Manaus, Amazonian Brazil, we assessed the wild-food feeding behavior of free-ranging groups of golden-faced sakis (Pithecia chrysocephala) and sympatric common squirrel monkeys (Saimiri sciureus). We hypothesized that sakis would have greater and more consistent access to wild fruit due to (1) a wider variety of fruit species in their diet, and (2) longer consumption periods per fruit species. We recorded the plant species, part (pulp or seed), and developmental stage (ripe or unripe) of wild fruit consumed by both species. We also conducted monthly fruit censuses of 1000 trees and vines to estimate overall wild fruit abundance. As an indicator of fruit availability, we calculated the proportion of available fruiting trees and vines for each primate species separately based on their observed diet. Throughout the year, the proportion of available trees and vines was significantly higher and more temporally stable for sakis than for squirrel monkeys. This was because sakis used shared fruit species longer than squirrel monkeys by consuming both ripe and unripe fruit. Although sakis had a broader fruit repertoire than squirrel monkeys, it did not contribute to the higher fruit availability. Thus, the fruit feeding system of sakis identifies aspects of a niche that is less restricted in the timing of fruit consumption, which led to a relative advantage in fruit availability.

The diet and feeding behavior of the black-and-white colobus (Colobus guereza) in the Kalinzu Forest, Uganda.

One of the goals for primate feeding ecology is to understand the factors that affect inter- and intra-specific variations. Therefore, a detailed description of basic feeding ecology in as many populations as possible is necessary and warrants further understanding. The black-and-white colobus (Colobus guereza) or guereza is widely distributed in Africa and is one of the well-studied colobines in terms of their feeding; they demonstrate considerable variation in their diets in response to local conditions. We studied the diet of a group of guerezas in the Kalinzu Forest, Uganda, for over 30 consecutive months using behavioral observation (4308 h in total), phenology, and vegetation surveys. A total of 31 plant species were consumed by the study group. This study group was predominantly folivorous; the majority of their feeding time was involved in feeding on young leaves (87%). However, during certain times of the year, fruits and seeds accounted for 45% of monthly feeding time. Young leaves of Celtis durandii were by far the most important food, which constituted 58% of the total feeding records. There was a significant increase in the consumption of fruits and flowers once young leaf availability was low, but their consumption of fruits did not significantly increase even when fruit availability was high. Their monthly dietary diversity increased as the number of available plants with young leaves declined, suggesting that much of the dietary diversity in the study group may be attributable to the young leaf portion of their diet. Our findings may help contribute to a better understanding of the dietary adaptations and feeding ecology of guerezas in response to local environmental conditions.

Correction: Factors affecting forest area change in Southeast Asia during 1980-2010.

[This corrects the article DOI: 10.1371/journal.pone.0197391.].

Factors affecting forest area change in Southeast Asia during 1980-2010.

While many tropical countries are experiencing rapid deforestation, some have experienced forest transition (FT) from net deforestation to net reforestation. Numerous studies have identified causative factors of FT, among which forest scarcity has been considered as a prerequisite for FT. In fact, in SE Asia, the Philippines, Thailand and Viet Nam, which experienced FT since 1990, exhibited a lower remaining forest area (30±8%) than the other five countries (68±6%, Cambodia, Indonesia, Laos, Malaysia, and Myanmar) where forest loss continues. In this study, we examined 1) the factors associated with forest scarcity, 2) the proximate and/or underlying factors that have driven forest area change, and 3) whether causative factors changed across FT phases (from deforestation to net forest gain) during 1980-2010 in the eight SE Asian countries. We used production of wood, food, and export-oriented food commodities as proximate causes and demographic, social, economic and environmental factors, as well as land-use efficiency, and wood and food trade as underlying causes that affect forest area change. Remaining forest area in 1990 was negatively correlated with population density and potential land area of lowland forests, while positively correlated with per capita wood production. This implies that countries rich in accessible and productive forests, and higher population pressures are the ones that have experienced forest scarcity, and eventually FT. Food production and agricultural input were negatively and positively correlated, respectively, with forest area change during 1980-2009. This indicates that more food production drives deforestation, but higher efficiency of agriculture is correlated with forest gain. We also found a U-shaped response of forest area change to social openness, suggesting that forest gain can be achieved in both open and closed countries, but deforestation might be accelerated in countries undergoing societal transition. These results indicate the importance of environmental, agricultural and social variables on forest area dynamics, and have important implications for predicting future tropical forest change.

Factors Affecting Leaf Selection by Foregut-fermenting Proboscis Monkeys: New Insight from in vitro Digestibility and Toughness of Leaves.

Free-living animals must make dietary choices in terms of chemical and physical properties, depending on their digestive physiology and availability of food resources. Here we comprehensively evaluated the dietary choices of proboscis monkeys (Nasalis larvatus) consuming young leaves. We analysed the data for leaf toughness and digestibility measured by an in vitro gas production method, in addition to previously reported data on nutrient composition. Leaf toughness, in general, negatively correlated with the crude protein content, one of the most important nutritional factors affecting food selection by leaf-eating primates. This result suggests that leaf toughness assessed by oral sensation might be a proximate cue for its protein content. We confirmed the importance of the leaf chemical properties in terms of preference shown by N. larvatus; leaves with high protein content and low neutral detergent fibre levels were preferred to those of the common plant species. We also found that these preferred leaves were less tough and more digestible than the alternatives. Our in vitro results also suggested that N. larvatus were little affected by secondary plant compounds. However, the spatial distribution pattern of plant species was the strongest factor explaining the selection of the preferred leaf species.

Homogeneous diet of contemporary Japanese inferred from stable isotope ratios of hair.

The globalization of food production and distribution has homogenized human dietary patterns irrespective of geography, but it is uncertain how far this homogenization has progressed. This study investigated the carbon and nitrogen isotope ratios in the scalp hair of 1305 contemporary Japanese and found values of -19.4 ± 0.6‰ and 9.4 ± 0.6‰ (mean ± SD), respectively. Within Japan, the inter-regional differences for both isotope ratios was less than 1‰, which indicates low dietary heterogeneity among prefectural divisions. The carbon and nitrogen isotope ratios of the hair showed a significant correlation with the results of questionnaires on self-reported dietary habits. The carbon isotope ratios from Japan were lower than those in samples from the USA but higher than those in samples from Europe. These differences stem from the varying dietary proportions of food products originally derived from C3 and C4 plants. The dietary variation of Japan is as small as those of Europe and USA and smaller than those of some Asian countries. These results indicate that dietary homogeneity has progressed in Japan, which may indicate the influence from the spread of the Western-style diet and food globalization, although dietary heterogeneity among countries is still preserved.

Habitat use of bonobos (Pan paniscus) at Wamba: Selection of vegetation types for ranging, feeding, and night-sleeping.

Understanding the habitat requirements of great apes is essential for effective conservation strategies. We examined annual habitat use of a bonobo group in the Wamba field site within the Luo Scientific Reserve, Democratic Republic of the Congo. Using satellite imagery, we categorized the group's ranging area into three forest types: (1) primary and old secondary forest (P/OS), (2) young secondary forest and agriculture (YS/Ag), and (3) swamp forest (Sw). We tracked the group for 1 year (2007-2008) and compared usage of the three forest types for ranging, feeding, and night-sleeping. We also recorded what the bonobos ate and monitored monthly fruit availability in each forest type. The group ranged and fed more often in P/OS and less often in YS/Ag and Sw than expected based on habitat availability. Also, the group slept mostly in P/OS (94% of nights monitored), but also in YS/Ag (1%), and Sw (5%). Fruit availability in P/OS had no significant effect on habitat selection, but the group fed in YS/Ag most often during the two months when fruits in P/OS were least abundant. In June, when fruit of Uapaca spp. (selectively eaten by bonobos) was generally abundant in Sw, the group mostly ranged and slept there. The bonobos fed most often on herbaceous plants in all three forest types. In Sw, the bonobos frequently ate mushrooms. Our results show that semi-open forest with abundant herbaceous plants such as YS/Ag could be an important feeding habitat and may provide fallback food for bonobos when fruits are scarce. Furthermore, Sw can serve seasonally as a main habitat to complement P/OS if adequate food resources and tree nesting opportunities are available. We conclude that bonobos use diverse habitats depending on their needs and we highlight the importance of minor-use habitats for sustaining populations of target species in conservation planning.

Problems associated with the seed-trap method when measuring seed dispersal in forests inhabited by Japanese macaques.

Despite the widespread use of seed/litter traps in seed dispersal ecology, several problems have arisen when using this method in forests inhabited by semi-terrestrial monkeys. The first issue is the height of the trap relative to the location where macaques spit seeds and/or defecate. For Japanese macaques in the lowland forests of Yakushima Island, southern Japan, 30-50% of the seeds emitted from cheek pouches and faeces will not be caught by seed traps, leading to underestimation of seed fall. The second issue is the attractiveness of seed traps. Macaques sometimes play with the traps, potentially affecting the results of the seed-trap method in complex ways, including both negative and positive effects. To obtain reasonable estimates of total seed dispersal, we recommend that researchers conduct the seed-trap method concurrently with monkey observations, and that they should affix traps more securely to prevent macaques from destroying the traps.

Degradation of Abies veitchii wave-regeneration on Mt. Misen in Ohmine Mountains: effects of sika deer population.

How has the degradation of Abies veitchii wave-regeneration occurred under the sika deer (Cervus nippon) pressure? We conducted tree census and ground vegetation survey in a 1 ha plot in Mt. Misen (Nara prefecture, Japan). We found 15 tree species (over 50 cm in height). Abies accounted for 60.0 % of all living trees, and 46.9 % of Abies were damaged (herbivory, bark stripping and/or fraying) by deer. Spatial distribution of Abies trees showed Abies-wave, although there were few saplings in the dieback zone. Estimated deer population density in 2009 was 57.3 head/km(2). Number of living Abies and standing dead conifer trees, and ground vegetation cover for each quadrat (5 × 5 m) were used to assign the quadrats into 6 clusters. The hierarchical clustering-approach revealed that living Abies distributed mainly on the moss and/or Carex fernaldiana dominated quadrats, but did not on the Dennstaedtia scabra, or Brachypodium sylvaticum dominated quadrats. While standing dead conifer trees distributed mainly on the Carex dominated quadrats, they hardly occur on the moss, the Dennstaedtia or the Brachypodium dominated quadrats. Regeneration of Abies tree and thus the wave-regeneration is hindered for now owing to deer herbivory and bark-stripping. The ground vegetation under the dieback zone has changed from the moss and/or the Carex dominated one to the Carex, the Dennstaedtia or the Brachypodium covered vegetation with the canopy remained open and without Abies regeneration.

Vascular plant species richness along environmental gradients in a cool temperate to sub-alpine mountainous zone in central Japan.

In order to clarify how vegetation types change along the environmental gradients in a cool temperate to sub-alpine mountainous zone and the determinant factors that define plant species richness, we established 360 plots (each 4 × 10 m) within which the vegetation type, species richness, elevation, topographic position index (TPI), slope inclination, and ground light index (GLI) of the natural vegetation were surveyed. Mean elevation, TPI, slope inclination, and GLI differed across vegetation types. Tree species richness was negatively correlated with elevation, whereas fern and herb species richness were positively correlated. Tree species richness was greater in the upper slope area than the lower slope area, whereas fern and herb species richness were greater in the lower slope area. Ferns and trees species richness were smaller in the open canopy, whereas herb species richness was greater in the open canopy. Vegetation types were determined firstly by elevation and secondary by topographic configurations, such as topographic position, and slope inclination. Elevation and topography were the most important factors affecting plant richness, but the most influential variables differed among plant life-form groups. Moreover, the species richness responses to these environmental gradients greatly differed among ferns, herbs, and trees.

Genetic structure of an endemic Japanese conifer, Sciadopitys verticillata (Sciadopityaceae), by using microsatellite markers.

We investigated the genetic structure of Sciadopitys verticillata, an endemic conifer in Japan, using 11 microsatellite markers. Average expected heterozygosity varied from 0.282 to 0.450, with between 2 and 17 alleles per locus, and allelic richness varied from 2.14 to 2.94 within a population. Wilcoxon signed-rank tests suggested that there was a recent bottleneck in the southwestern populations in the Kinki district and in isolated northeastern populations in the Tohoku district. Bayesian clustering analysis showed that the populations of the Chubu, Kinki, and Shikoku districts were admixed from several clusters. Archaeological data suggest past anthropogenic exploitation for building and coffin material.

Topography-specific seed dispersal by Japanese macaques in a lowland forest on Yakushima Island, Japan.

1. We investigated patterns of seed dispersal (i.e. dispersal distances and topography of seed-deposition sites) via the cheek pouches of Japanese macaques (Macaca fuscata yakui) during three seasons in a lowland forest on Yakushima Island, Japan. 2. The mean seed-dispersal distances were 16.7, 26.1, 41.8, and 32.4 m from the trunks of mother trees of Myrica rubra, Persea thunbergii, Neolitsea sericea, and Litsea acuminata, respectively. 3. We assessed the possible effect of macaque foraging patterns and the spatial distribution of fruiting trees on topography-specific seed dispersal. The topography of the locations of macaques differed across seasons, likely because the spatial distribution of fruiting trees determined the seasonal foraging patterns of macaques. 4. In early summer, macaques foraged on a ridge and fed on fruits of M. rubra and P. thunbergii, which were primarily distributed and dispersed within this area. In contrast, during the winter, macaques foraged within a valley and fed on fruits of L. acuminata, which were chiefly distributed and dispersed within the valley. 5. Seeds of M. rubra, P. thunbergii, and L. acuminata were directly dispersed to the specific topographic areas in which adult trees were distributed and in which juveniles have a predictably high probability of survival relative to random sites.

Seedling establishment of five evergreen tree species in relation to topography, sika deer (Cervus nippon yakushimae) and soil surface environments.

We investigated the seedling survival of five evergreen tree species over 3 years inside and outside deer-exclusion fences in a warm temperate evergreen broad-leaved forest on Yakushima Island, Japan. Seedling survival was examined in relation to topography, herbivory by sika deer, and the soil surface environment (i.e., soil surface wetness, light conditions, slope inclination, and soil disturbance). The study species included Myrsine seguinii Lév., Syzygium buxifolium Hook. et Arn. (Group A: species distributed on the upper slope of the study site), Litsea accuminata (Bl.) Kurata, Schefflera octophylla (Lour.) Harms (Group B: species distributed on the lower slope), and Cleyera japonica Thunb. p.p. emend. Sieb. et Zucc. (Group C: species distributed on both slopes). The soil surface environment on the upper slope was drier, lighter, and more easily disturbed than the lower slope. Generalized linear model analyses indicated that seedling survival in fenced and unfenced quadrats was greater on the upper slope than on the lower slope for Group A and B species but not for Group C species. A micro-spatial scale analysis revealed that seedling survival was correlated with soil wetness, ground light conditions, and soil disturbance but not slope inclination. These results indicate that seedling survival was correlated with topography, sika deer herbivory, and the micro-spatial scale environment. Topography-related differences in seedling survival appear to adequately reflect the observed adult plant distributions for Group A and C species but not for Group B species.

Spatial distribution patterns of trees at different life stages in a warm temperate forest.

We have investigated tree distributions in relation to topography between different tree life history stages, from the seed-dispersal stage to the adult stage in a warm temperate evergreen broadleaved forest on Yakushima Island, Japan, to clarify the critical stages in determining adult tree distributions. We conducted a census of all living trees > or =30 cm tall and collected seed falls over three years using 25 seed traps in a 50 m x 50 m quadrat. Four life stages were defined: stage 1, dispersed seed; stage 2, individuals taller than 30 cm and diameter at breast height (DBH) < 1 cm; stage 3, trunks 1 cm < or = DBH < 10 cm; stage 4, trunks with DBH > or = 10 cm. We classified 17 common tree species into three groups; group A was distributed mainly on the upper slope, group B on the lower slope, and group C on both. Most of group A and B trees at stages 2-4 showed an aggregated distribution along the topographical gradient. The densities at stage 1 showed weaker aggregations according to slope. Topography-specific tree distribution was probably determined at the regeneration stage, and later survival was less effective as a mechanism of vegetation differentiation.

Cryptic species and host specificity in the ectomycorrhizal genus Strobilomyces (Strobilomycetaceae).

Taxonomical classification of higher fungi remains an important challenge and can benefit from the application of molecular analysis. We propose that the ectomycorrhizal (EM) fungal taxa might include a number of cryptic species because there are few morphological characteristics useful for distinguishing among these fungi. Previously, host specificity in most EM fungi was thought to be low, but we suspect that confusion of cryptic species has led to an underestimate of fungal host specificity. We analyzed both nuclear and mitochondrial DNA sequences from Strobilomyces fungi and obtained evidence that what were previously described as four species can be grouped into 14 distinct lineages, suggesting that these lineages might be distinct biological species. Moreover, we identified host plants for Strobilomyces via nucleotide sequencing of both fungal and plant DNA from EM samples. Most lineages of Strobilomyces tested in this study were associated only with Fagaceae trees, even though Strobilomyces species were previously thought to be generalists with regard to hosts. Thus, we present an approach useful for identifying cryptic species and detecting the true host range of a set of EM fungi in natural conditions.

Interactions between fleshy fruits and frugivores in a tropical seasonal forest in Thailand.

Large frugivores are considered to be important seed dispersers for many tropical plant species. Their roles as seed dispersers are not well known in Southeast Asia, where degraded landscapes typically lack these animals. Interactions between 259 (65 families) vertebrate-dispersed fruits and frugivorous animals (including 7 species of bulbul, 1 species of pigeon, 4 species of hornbill, 2 species of squirrel, 3 species of civet, 2 species of gibbon, 1 species of macaque, 2 species of bear, 2 species of deer, and 1 species of elephant) were studied for 3 years in a tropical seasonal forest in Khao Yai National Park, Thailand. The purpose was to examine the dietary overlaps among the large frugivores and the characteristics of fruits they consumed. Most fruit species are eaten by various kinds of frugivores; no close relationship between a particular fruit and a frugivore was found. The number of frugivore groups that served a given plant species was negatively correlated with seed size. Additionally, the fruit/seed diameters consumed by bulbuls were significantly smaller than consumed by the other nine groups. These trends of fruit characteristics were consistent with those observed elsewhere in Southeast Asia: small fruits and large, soft fruits with many small seeds are consumed by a wide spectrum of frugivores while larger fruits with a single large seed are consumed by relatively few potential dispersers. Importantly, these large, single-seed fruits are not consumed by the small frugivores that thrive in small forest fragments and degraded areas in Southeast Asia. To insure the natural seed dispersal process in the forest, an evaluation of all frugivore groups in the forest is urgently needed in Southeast Asia.