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

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.

Timing of fruiting rather than topography determines the direction of vertical seed dispersal by mammals and birds

“…Vertical seed dispersal, that is, seed dispersal toward higher or lower altitudes, has now been recognized as one of the critical processes for plant migration, especially under climate change (1,2). Uphill or downhill seed dispersal is advantageous or disadvantageous, respectively, for plant escape and expansion under global warming, and vice versa under global cooling (3). Under current global warming, which shifts suitable plant habitats to colder areas (i.e., higher altitudes and latitudes) (4), uphill seed dispersal is essential for plants to maintain their populations.…”

“…At present, it is important to accumulate observations of vertical seed dispersal in the field and set up hypotheses based on them. However, there are only three studies that have investigated vertical seed dispersal itself, due to the technical difficulty or high cost (1)(2)(3).…”

“…Recently, Naoe et al hypothesized that the timing of fruiting determines the direction of vertical seed dispersal: uphill seed dispersal occurs in spring-and summer-fruiting plants and downhill seed dispersal occurs in autumn-and winter-fruiting plants because frugivores ascend or descend mountains following food plant phenology in the temperate zone (1), which proceeds from the foot to the top of mountains in spring-summer and from the top to the foot in autumnwinter (11,12). Considering that most animal-dispersed trees fruit in autumn-winter in the temperate zone (10), this hypothesis suggests that populations of autumn-to-winter fruiting trees dispersed by animals may not sufficiently escape from current global warming in the temperate zone (3). However, this hypothesis is based on observations of vertical seed dispersal by mammals on one mountain range, and thus its generality should be tested in several aspects, including topography, the extinction of megafauna, and seed dispersal by birds.…”

“…Previous studies did not explicitly evaluate the effect of topography. On steep mountains, farther vertical seed dispersal is expected to occur compared to gently sloping mountains because frugivores can ascend and descend more efficiently (2,3). Surface areas at lower altitudes are generally larger than those at higher altitudes (13), and thus downhill seed dispersal is likely to occur if frugivores move randomly in the mountains (3).…”

“…On steep mountains, farther vertical seed dispersal is expected to occur compared to gently sloping mountains because frugivores can ascend and descend more efficiently (2,3). Surface areas at lower altitudes are generally larger than those at higher altitudes (13), and thus downhill seed dispersal is likely to occur if frugivores move randomly in the mountains (3). Human activities represented by habitat fragmentation and hunting can dramatically change frugivore composition, often resulting in the local extinction of megafauna, which plays an important role in seed dispersal (14)(15)(16).…”