Green greenhouse: leaf enclosure for fruit development of an androdioecious vine, Schizopepon bryoniifolius.

Individual plants can produce leaves that differ substantially in size, morphology and many other traits. However, leaves that play a specific role in reproduction have rarely been reported. Here, we report leaves specialized to enclose fruit clusters and enhance seed production in an annual vine, Schizopepon bryoniifolius. Enclosure leaves were produced at the end of the growing season in late autumn. They were different in greenness and structure from other leaves. Under solar radiation, the ambient temperature inside an intact enclosure was up to 4.6°C higher than that near a fruit cluster whose enclosure leaves had been removed. We found that enclosures were thicker at colder sites. Removal of enclosing leaves negatively affected fruit survival and/or growth, but we could not identify the exact mechanism. The results suggested that enclosures allow the plant to produce seeds under the cold weather the plant encounters at the end of its life. Vegetative and reproductive traits of plants have usually been studied separately. This study indicates how they can dynamically interact, as shown by an examination of associations among leaf and reproductive trait changes according to life stages.

Survival rate and environmental response of current-year seedlings of the temperate liana Wisteria floribunda across a heterogeneous environment.

Lianas have a huge influence on forest structure and function. However, it is unclear how the surrounding environment affects the establishment of liana seedlings in temperate forests. We addressed the following questions: (1) Can current-year seedlings persist under a closed canopy? (2) Do current-year seedlings form aggregated distribution and how has their spatial distribution varied over the years? (3) How does the light condition, soil moisture content, forest floor litter, understory vegetation, and the distance from the conspecific adults affect the establishment and survival of seedlings? We examined the distribution pattern and survivorship of current-year seedlings of the temperate liana species, Wisteria floribunda, across a heterogeneous environment for 6 years using 1 m2 sub-quadrats (n = 651) in a 6 ha plot within the Ogawa Forest Reserve, an old-growth, temperate, deciduous forest in central Japan. In total, 908 current-year seedlings were observed during the study period, 87% of which emerged in 2014. Over half (56%) of these seedlings survived until 1 year after germination, which was relatively high compared with other tree species in this forest. The seedlings formed significantly aggregated distribution, but the degree of aggregation decreased over time. The number of emerged seedlings was negatively associated with the presence of dwarf bamboo (Sasa borealis) and the distance from the nearest conspecific adult. However, the survival rate of the seedlings was negatively associated with the presence of dwarf bamboo and soil moisture content and was positively associated with the openness of the canopy and the distance from the nearest conspecific adult. An enhanced survival rate under more intense light conditions and the ability to persist within the shaded understory may be important for the survival of this species in the earlier stage of the life history.

Effects of temporal variation in community-level fruit abundance on seed dispersal by birds across woody species.

PREMISE OF THE STUDY: In animal-dispersed plants, seed dispersal patterns of the same species in the same habitat can greatly differ among individuals and temporally. Many studies have revealed the pervasive effects of spatial variation in fruit abundance on seed dispersal of individual plants. By contrast, very few studies have investigated the temporal variation in seed dispersal. METHODS: We investigated the effects of conspecific and community-level fruit abundance on fruit removal rate and seed dispersal distance of six bird-dispersed woody species in a Japanese temperate forest for 3 yr. The six species share similar fruit characteristics but have different fruiting seasons. In addition, we also considered the effects of bird seasonality in diet and species composition on seed dispersal. KEY RESULTS: Inter-annual and inter-seasonal variation in community-level fruit abundance determined both fruit removal and the seed dispersal distance across species, but the effect differed with seasonal changes in bird behavior. Abundant fruit satiated fruit removal by birds only during fruit-feeding periods, not during insect-feeding periods. A scarcity of fruit increased the dispersal distance, but only during the migratory period. This difference was probably due to the different foraging behaviors of passing migrants and territorial birds. CONCLUSIONS: Our results illustrated that temporal variation in community-level fruit abundance could be a determining factor for seed dispersal in temperate forests. The effects of temporal variations in fruit abundance on seed dispersal patterns should be investigated in other ecosystems in order to understand their importance and associations with frugivore phenology.

Fleshy fruit characteristics in a temperate deciduous forest of Japan: how unique are they?

This study investigated the fleshy fruit characteristics of 28 woody species in a Japanese temperate forest where large sedentary seed-dispersing mammals are present. We tested whether the findings in previous studies in temperate forests of Europe and North America are universal or not. Results have suggested that fruits of all species were eaten both by birds and mammals except for four species with larger fruits, which were eaten only by mammals. A gradient was found from a syndrome characterized by small, oily, and large-seeded fruits to a syndrome characterized by large, succulent, non-oily, and small-seeded fruits. The sizes and colors of the fruits were not conspicuously different from previous findings in Europe and North America. On the other hand, nitrogen and lipids in the fleshy part did not show seasonally increasing trends, or even seasonally decreasing trends in terms of dry weight. This result, suggesting the absence of community-level adaptation of fruit traits to migratory bird dispersers, contrasted with findings in Europe and North America. Large sedentary arboreal or tree-climbing mammals may have a greater effect on the evolution of fruit-disperser relations than opportunistic migratory birds.

Multiscale spatial genetic structure within and between populations of wild cherry trees in nuclear genotypes and chloroplast haplotypes.

Spatial genetic structure (SGS) of plants mainly depends on the effective population size and gene dispersal. Maternally inherited loci are expected to have higher genetic differentiation between populations and more intensive SGS within populations than biparentally inherited loci because of smaller effective population sizes and fewer opportunities of gene dispersal in the maternally inherited loci. We investigated biparentally inherited nuclear genotypes and maternally inherited chloroplast haplotypes of microsatellites in 17 tree populations of three wild cherry species under different conditions of tree distribution and seed dispersal. As expected, interpopulation genetic differentiation was 6-9 times higher in chloroplast haplotypes than in nuclear genotypes. This difference indicated that pollen flow 4-7 times exceeded seed flow between populations. However, no difference between nuclear and chloroplast loci was detected in within-population SGS intensity due to their substantial variation among the populations. The SGS intensity tended to increase as trees became more aggregated, suggesting that tree aggregation biased pollen and seed dispersal distances toward shorter. The loss of effective seed dispersers, Asian black bears, did not affect the SGS intensity probably because of mitigation of the bear loss by other vertebrate dispersers and too few tree generations after the bear loss to alter SGS. The findings suggest that SGS is more variable in smaller spatial scales due to various ecological factors in local populations.

Downhill seed dispersal by temperate mammals: a potential threat to plant escape from global warming.

Vertical seed dispersal, i.e. seed dispersal towards a higher or lower altitude, is considered a critical process for plant escape from climate change. However, studies exploring vertical seed dispersal are scarce, and thus, its direction, frequency, and mechanisms are little known. In the temperate zone, evaluating vertical seed dispersal of animal-dispersed plants fruiting in autumn and/or winter is essential considering the dominance of such plants in temperate forests. We hypothesized that their seeds are dispersed towards lower altitudes because of the downhill movement of frugivorous animals following the autumn-to-winter phenology of their food plants which proceeds from the mountain tops to the foot in the temperate zone. We evaluated the vertical seed dispersal of the autumn-fruiting wild kiwi, Actinidia arguta, which is dispersed by temperate mammals. We collected dispersed seeds from mammal faeces in the Kanto Mountains of central Japan and estimated the distance of vertical seed dispersal using the oxygen isotope ratios of the dispersed seeds. We found the intensive downhill seed dispersal of wild kiwi by all seed dispersers, except the raccoon dog (bear: mean -393.1 m; marten: -245.3 m; macaque: -98.5 m; and raccoon dog: +4.5 m). Mammals with larger home ranges dispersed seeds longer towards the foot of the mountains. Furthermore, we found that seeds produced at higher altitudes were dispersed a greater distance towards the foot of the mountains. Altitudinal gradients in autumn-to-winter plant phenology and other mountain characteristics, i.e. larger surface areas and more attractive human crops at lower altitudes compared to higher altitudes, were considered drivers of downhill seed dispersal via animal movement. Strong downhill seed dispersal by mammals suggests that populations of autumn-to-winter fruiting plants dispersed by animals may not be able to sufficiently escape from current global warming in the temperate zone.

Negative correlation between altitudes and oxygen isotope ratios of seeds: exploring its applicability to assess vertical seed dispersal.

Vertical seed dispersal, which plays a key role in plant escape and/or expansion under climate change, was recently evaluated for the first time using negative correlation between altitudes and oxygen isotope ratio of seeds. Although this method is innovative, its applicability to other plants is unknown. To explore the applicability of the method, we regressed altitudes on δ18O of seeds of five woody species constituting three families in temperate forests in central Japan. Because climatic factors, including temperature and precipitation that influence δ18O of plant materials, demonstrate intensive seasonal fluctuation in the temperate zone, we also evaluated the effect of fruiting season of each species on δ18O of seeds using generalized linear mixed models (GLMM). Negative correlation between altitudes and δ18O of seeds was found in four of five species tested. The slope of regression lines tended to be lower in late-fruiting species. The GLMM analysis revealed that altitudes and date of fruiting peak negatively affected δ18O of seeds. These results indicate that the estimation of vertical seed dispersal using δ18O of seeds can be applicable for various species, not just confined to specific taxa, by identifying the altitudes of plants that produced seeds. The results also suggest that the regression line between altitudes and δ18O of seeds is rather species specific and that vertical seed dispersal in late-fruiting species is estimated at a low resolution due to their small regression slopes. A future study on the identification of environmental factors and plant traits that cause a difference in δ18O of seeds, combined with an improvement of analysis, will lead to effective evaluation of vertical seed dispersal in various species and thereby promote our understanding about the mechanism and ecological functions of vertical seed dispersal.

Mountain-climbing bears protect cherry species from global warming through vertical seed dispersal.

In a warming climate, temperature-sensitive plants must move toward colder areas, that is, higher latitude or altitude, by seed dispersal [1]. Considering that the temperature drop with increasing altitude (-0.65°C per 100 m altitude) is one hundred to a thousand times larger than that of the equivalent latitudinal distance [2], vertical seed dispersal is probably a key process for plant escape from warming temperatures. In fact, plant geographical distributions are tracking global warming altitudinally rather than latitudinally, and the extent of tracking is considered to be large in plants with better-dispersed traits (e.g., lighter seeds in wind-dispersed plants) [1]. However, no study has evaluated vertical seed dispersal itself due to technical difficulty or high cost. Here, we show using a stable oxygen isotope that black bears disperse seeds of wild cherry over several hundred meters vertically, and that the dispersal direction is heavily biased towards the mountain tops. Mountain climbing by bears following spring-to-summer plant phenology is likely the cause of this biased seed dispersal. These results suggest that spring- and summer-fruiting plants dispersed by animals may have high potential to escape global warming. Our results also indicate that the direction of vertical seed dispersal can be unexpectedly biased, and highlight the importance of considering seed dispersal direction to understand plant responses to past and future climate change.

Landscape heterogeneity-biodiversity relationship: effect of range size.

The importance of landscape heterogeneity to biodiversity may depend on the size of the geographic range of species, which in turn can reflect species traits (such as habitat generalization) and the effects of historical and contemporary land covers. We used nationwide bird survey data from Japan, where heterogeneous landscapes predominate, to test the hypothesis that wide-ranging species are positively associated with landscape heterogeneity in terms of species richness and abundance, whereas narrow-ranging species are positively associated with landscape homogeneity in the form of either open or forest habitats. We used simultaneous autoregressive models to explore the effects of climate, evapotranspiration, and landscape heterogeneity on the richness and abundance of breeding land-bird species. The richness of wide-ranging species and the total species richness were highest in heterogeneous landscapes, where many wide-ranging species showed the highest abundance. In contrast, the richness of narrow-ranging species was not highest in heterogeneous landscapes; most of those species were abundant in either open or forest landscapes. Moreover, in open landscapes, narrow-ranging species increased their species richness with decreasing temperature. These results indicate that heterogeneous landscapes are associated with rich bird diversity but that most narrow-ranging species prefer homogeneous landscapes--particularly open habitats in colder regions, where grasslands have historically predominated. There is a need to reassess the generality of the heterogeneity-biodiversity relationship, with attention to the characteristics of species assemblages determined by environments at large spatiotemporal scales.