Research Article: Limited directed seed dispersal in the canopy as one of the determinants of the low hemi-epiphytic figs’ recruitments in Bornean rainforests

Date Published: June 13, 2019

Publisher: Public Library of Science

Author(s): Miyabi Nakabayashi, Yoichi Inoue, Abdul Hamid Ahmad, Masako Izawa, Kim R. McConkey.


Ficus species are keystone plants in tropical rainforests, and hemi-epiphytic figs play a notably important role in forest ecosystems. Because hemi-epiphytic figs have strict germination requirements, germination and establishment stages regulate their populations. Despite the ecological importance of hemi-epiphytic figs in the rainforests, seed dispersal systems by fig-eating animals under natural conditions remain unknown because of the difficulty in tracing the destiny of dispersed seeds in the canopy. Therefore, seed dispersal effectiveness (SDE) has never been evaluated for hemi-epiphytic figs. We evaluated the SDE of hemi-epiphytic figs using qualitative and quantitative components by three relatively large-sized (> 3 kg) arboreal and volant animals in Bornean rainforests that largely depend on fig fruits in their diets: binturongs Arctictis binturong, Mueller’s gibbons Hylobates muelleri, and helmeted hornbills Rhinoplax vigil. The SDE values of binturongs was by far the highest among the three study animals. Meanwhile, successful seed dispersal of hemi-epiphytic figs by gibbons and helmeted hornbills is aleatory and rare. Given that seed deposition determines the fate of hemi-epiphytic figs, the defecatory habits of binturongs, depositing feces on specific microsites in the canopy, is the most reliable dispersal method, compared to scattering feces from the air or upper canopy. We showed that reliable directed dispersal of hemi-epiphytic figs occurs in high and uneven canopy of Bornean rainforests. This type of dispersal is limited to specific animal species, and therefore it may become one of the main factors regulating low-success hemi-epiphytic fig recruitment in Bornean rainforests.

Partial Text

Ficus (Moraceae) is one of the world’s largest woody plant genera with approximately 750 species of various growth forms: trees, shrubs, climbers, epiphytes, and hemi-epiphytes [1]. Ficus species are distributed pantropically, but the majority are found in Malesia and Australia [2]. Each individual produces ripe fig fruits asynchronously and aseasonally; therefore, each fig population exhibits continual fruiting throughout the year [3]. This fruiting pattern enables obligate pollination mutualism with wasps (Agaonidae) by maintaining the pollinating wasp population [4]. Moreover, because of their year-round fruiting patterns, Ficus species are considered keystone food resources for animals in tropical rainforests, especially when the availability of preferred fruits is low [3,5–7]. Although this usually applies to whole Ficus communities, Ficus species vary considerably in reproductive system, growth form, frugivore guild (e.g. generalist and specialist), and habitat [6]. Among the Ficus species, hemi-epiphytes include approximately 300 species [1] and occupy one-third to over one-half of the fig species in the rainforest community [8]. They are a major component of canopy ecosystems across tropical regions [9], and they increase population turnover and forest regeneration by causing host tree-fall [10]. Therefore, hemi-epiphytic figs play a notably important role in forest ecosystems.

Permission to conduct the research was granted by the Sabah Biodiversity Centre of Sabah State Government. We were granted permission to capture and attach radio-collars to binturongs by the Sabah Biodiversity Council and the Sabah Wildlife Department (permission number: JKM/MBS.1000-2/2 JLD.4 (170), JKM/MBS.1000-2/2 JLD.5 (137), JKM/MBS.1000-2/2 JLD.7 (64)). Trapping and handling of the animals conformed to guidelines of the American Society of Mammalogists [25]. Research on gibbons and helmeted hornbills was non-invasive and involved direct observations. We kept certain distance from the animals so as not to disturb their behaviors.