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

Shoji Naoe,Ichiro Tayasu,Akiko Nakajima,Yoichiro Sakai,Takashi Masaki,Kazuki Kobayashi,Hiroki Kiyokawa,Koji Yamazaki,Yoshikazu Sato,Shinsuke Koike

doi:10.1038/s41598-019-51376-6

Abstract

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.

Highlights

Vertical seed dispersal, i.e. seed dispersal towards a higher or lower altitude, is considered a critical process for plant escape from climate change
We hypothesized that the seeds of autumn- and winter-fruiting plants are dispersed towards lower altitudes because of the downhill movement of frugivorous animals following the autumn-to-winter phenology of their food plants
We evaluated the vertical seed dispersal of the autumn-fruiting wild kiwi Actinidia arguta, which is dispersed by temperate mammals[27,28] (Fig. 2)

Summary

Introduction

I.e. seed dispersal towards a higher or lower altitude, is considered a critical process for plant escape from climate change. Naoe et al developed a method to detect vertical seed dispersal itself, using the altitudinal gradient of the oxygen isotope ratios of seeds to locate the altitudes of mother plants[8,13] They targeted summer-fruiting wild cherries in temperate forests in Japan and showed that their seeds are dispersed towards the mountain tops by frugivorous mammals, thereby successfully escaping global warming. They concluded that this biased seed dispersal was due to the ascent of mammals following the spring-to-summer phenology of their food plants, proceeding from the foot to the tops of mountains in the temperate zone[16,17] (Fig. 1a) These data suggest that spring- and summer-fruiting plants dispersed by animals have a possibility to escape global warming. Considering that seed dispersal towards lower altitudes under global warming can lead to plant population reductions because reduced plant performance is expected at lower altitudes due to competition with more warm-adapted plants[23,24,25] and that many of temperate woody species depend on animals for seed dispersal and produce fruits in autumn and winter[26], testing this hypothesis is essential from both a biodiversity conservation and ecosystem functioning of temperate forests perspective

Methods

Results

Conclusion