Foraging dispersion of Ryukyu flying-foxes and relationships with fig abundance in East-Asian subtropical island forests
- Ya-Fu Lee†1Email authorView ORCID ID profile,
- Yen-Min Kuo†1,
- Hsin-Yi Chang1,
- Chi-Feng Tsai1 and
- Shigeyuki Baba2, 3
© The Author(s) 2017
Received: 14 May 2017
Accepted: 2 November 2017
Published: 14 November 2017
Figs are widely distributed key resources to many tropical-subtropical animals, and flying-foxes are major consumers and seed dispersers of figs. Bat-fig interrelationships, however, may vary among species differing in fruiting traits, i.e., bat- versus bird-dispersed figs. We examined Ryukyu flying-fox foraging dispersion and the relationships with tree species composition and fig abundance in forests of Iriomote Island.
Bat foraging dispersion showed no spatial patterns with respect to different areas of the island, and was not explained by heterogeneity, density, or basal area (BA) of total trees, nor by relative density or BA of fruiting trees or total fruiting figs among sites. Instead, bat densities were positively dependent on the relative density of total figs, and particularly the relative BA of bat-dispersed figs Ficus septica and F. variegata. Both species were dominant figs in forests, fruiting asynchronously with long crop seasons, and were used as predominant foods. Bats foraged mostly solitarily and the mean density was in a hump-shaped relationship with crop sizes of the dominant bat-figs. These two species and Ficus benguetensis are larger-sized bat-figs, all contained more seeds, higher dry-pulp mass and water mass, but not necessarily water content. By approximate estimation, higher proportions of seeds of these bat-figs would have been removed from fruits through the bat consumption, than that of small-sized bird-figs like F. virgata, F. superba, and F. microcarpa.
The foraging dispersion of Ryukyu flying-foxes in forests depends on the availability of the most abundant bat-figs that serve as predominant foods. Intermediate levels of crop sizes of theses figs appear most fit with their solitary foraging. Our results suggest that as density and BA coverage of these dominant bat-figs are below a certain level, their effectiveness to attract bats may dwindle and so would their chance of dispersal by bats.
The genus Ficus (Moraceae) is widely distributed in tropical areas with its distribution and diversification centering around the equatorial Indomalay-Australasian region and extending poleward to around 35°N and 35°S [1, 2]. The 800 or so extant Ficus species constitute one of the most speciose genera of flowering plants. They occur in diverse habitats in various growth forms and engage with their pollinators (i.e., agaonid wasps) in complex and intriguing coevolutionary relationships [3–8].
Ficus plants play a key ecosystem role in contributing to the diversity of global tropical forests [9, 10]. The majority of known Ficus species produce edible inflorescences (syconia), so-called figs, that are largely apparent, accessible, easy to handle by various volant, arboreal, or even terrestrial animals, and nutritionally attractive [11, 12]. Many Ficus species have multiple crops year round, with asynchronous ripening phases among plants or even within a plant, which enhances their availability to foragers [9, 13]. This can be particularly crucial in lean times when other plants cease to produce fruits (but see [14, 15]). Globally, a variety of frugivorous or omnivorous vertebrates, predominantly birds and mammals that comprise nearly 1300 species, have been identified as fig-eating to various extents , although probably few depend solely on figs .
Among mammalian families, the Old World fruit bats (pteropodids) account for the highest proportion (ca. 16.5%) of the 284 species of fig-eating mammals, with at least 47 species confirmed . They appear all rely on figs as predominant food resources [12, 16–19]. In return, pteropodid fruit bats are significant seed dispersers of Ficus and various other plants, including many large-seeded fruits, in the Indomalayan and Australasian regions [20–23]. Yet, dominant palaeotropical plants in early successions are rarely bat-dispersed except the Moraceae, which is comprised mostly of Ficus . This further pinpoints potential effects of fruit bat-fig interactions on forest structure, successional patterns, and fate of large-seeded fruits, particularly in areas where suitable seed-dispersers may be scarce, such as remote oceanic islands .
Ficus plants may be categorized based on certain noticeable traits of fig morphology and phenology and their associated major dispersers . Unlike bird-dispersed figs, those that are preferentially fed on by phyllostomid fruit bats in the Neotropics (i.e., bat syndrome figs, hereafter as bat-figs) are generally green or dull in color, aromatic, span a wider range in fig size among species, and ripen more synchronously [25, 26]. Greater variation occurs with species that are typified as bird syndrome figs (i.e., small-sized and orange-red in color, hereafter as bird-figs) and may be fed on by mixed forager groups, particularly in the Old World tropics [27, 28]. On the other hand, pteropodids appear attracted to functionally dioecious (gyno-dioecious) Ficus species  that are more diverse and abundant than monoecious species in the Indomalay-Australasian region. Dioecious figs that fail to attract birds are predicted to produce smaller crops of larger-sized and dull-colored figs .
We examined foraging dispersion patterns of pteropodid bats and their relationships with fig assemblages in the subtropical forests of an Indomalayan oceanic island. The dispersion of foraging pteropodids may be affected by factors associated with land use patterns, habitats, and food availability (e.g., grey-headed flying fox Pteropus poliocephalus in Australia ). We tested the hypothesis that the availability of bat-figs affects nocturnal foraging dispersion of pteropodids and predicted that bat presence and abundance will depend on the availability of bat-figs that serve as predominant food resources. Frugivorous bats and birds are often attracted to fleshy fruits that are characterized by high water content [3, 30]. When consuming figs, however, pteropodid bats typically compress fruits against the ridged palate with the tongue, so the pulp-juice is squeezed out and swallowed along with numerous tiny seeds [12, 31]. Bats then eject deformed pulps as pellets, instead of swallowing the whole fig as do most birds [12, 17, 31]. Thus different water content in figs may contribute to different proportions of seeds being ingested, which indirectly affect the chance of seeds being further dispersed [32, 33]. We additionally tested that proportions of seeds remaining in ejected pellets are affected by water content, and predicted that figs containing higher water content aid to higher proportions of seeds being removed from fruits through the feeding process of fruit bats.
Study area and species
Iriomote (24°15′ ~ 25′N, 123°40′ ~ 55′E) is located at the southernmost tip of the Ryukyu Islands. It is the largest among the nine islets of the Yaeyama Islands, with an area of 289 km2 and its highest peak at 470 m above sea level. This subtropical island is typified by hot and humid summers and warm but windy winters. Temperatures generally rise above 25 °C from May to October, peaking at ca. 29 °C in July, and descend to 17 ~ 18 °C in January, with a mean annual rainfall of over 2300 mm (Japan Meteorological Agency data).
Intact primary or secondary broadleaf forests cover about 80% of this mountainous inland and are characterized by Castanopsis spp., Quercus spp., Schima spp. and various figs (Ficus spp.). Hernanadia nymphaeifolia (Presl) Kubitzki and horsetail pine Casuarina equisetifolia L. are common in coastal forests, whereas Bruguiera gymnorrhiza (L.) Lam, Rhizophora mucronata, and R. stylosa mangroves prevail along estuaries and rivers. Ficus, such as cedar fig F. superba Miq. and white fig F. virgata Blume, are mixed with Cerbera manghas L., Heritiera littoralis, hanging-flower checkerboard foot Barringtonia racemosa (L.) Blume ex DC, and screwpine Pandanus odoratissimus L. f. in swampy wetland forests . Human residences and cultivated areas are located in lowlands below 100 m along the shoreline and are more prominent on the eastern and northern coasts.
The near-threatened Ryukyu flying-fox (Pteropus dasymallus Temminck, 1825) is among the most northerly distributed pteropodids [35, 36]. Its five subspecies are each narrowly distributed but collectively cover a broad latitudinal range along the West Pacific island chain from Tokara Islands, Okinawa Island, Yaeyama Islands, and small islets of the Nansei Islands in southern Japan to Batan and other northern Philippine islets [35, 37]. Among the subspecies, P. d. yayeyamae occurs on most of the Yaeyama Islands . In Iriomote, F. septica Burm. f. and F. variegata Blume are their predominant foods, followed by F. benguetensis Merr., banyan (F. microcarpa L. f.), and at least 35 other fig and non-fig species .
Forest structure and tree composition
We conducted field surveys adopting the point-centered quarter method [38, 39] to assess forest structure in July, 2012, along 12 forest transects 1-km in length each. Four transects were established on each of the west, north, and east sides of the island. These transect sites had been previously surveyed for flying-fox abundance and activity , making comparisons between the two assessments possible. We did not survey the southern-most side of the island where forest transects were limited by rough terrain, and the southwestern-most corner, Funauki, due to its inaccessibility by land.
In each transect site, we randomly picked six 100-m long sections and six random points within each section to collect measurements using 2-digit random numbers from 01 to 99 in increasing order. We specifically kept the difference of any two successive numbers greater than five, so each pair of random points selected were at least 5 m apart and individual trees would not be measured repeatedly [40, 41]. Our sampling proceeded from the coast toward the forest interior, and the smallest random number selected was set as the initial point along a transect line. At each sampling point, we determined four quarters divided by the transect line and its perpendicular line. In each quarter, the nearest tree to the sampling point with at least 4 cm in diameter was located. The quarter, distance from the nearest tree to the sampling point, species, and CCH (circumference at chest height of 130 cm ) were recorded, and fruiting or blooming trees were noted. We calculated density and basal area (BA) using distance and CCH data  for total trees, total fig trees, fruiting trees, and fruiting fig trees at each site, and obtained the relative density and relative BA of total fig trees, fruiting trees, and fruiting fig trees in relation to that of total trees . We calculated the relative frequency of occurrence (FO) and relative abundance (RA) for each tree species at each forest site and for the entire sampling across sites. We further adopted and modified Curtis and McIntosh’s  use of the arithmetic mean of these standardized measures to obtain an estimate of the relative importance (RI) of each species in samples . The converted Simpson index, 1 − D = 1 − Σ (p i 2 ), was used to assess the heterogeneity (SH) in species composition , where p i is the relative abundance of particular species i (i = 1 to s, s being the total number of species in a sample).
Foraging bat dispersion and abundance
From 28 June to 22 September, 2012, we conducted 50 bat surveys along the 12 transect sites (mean 4.2 ± 0.11 nights per site) where forest tree composition was assessed. Transect lines followed previously adopted outskirt routes leading toward inland forests , except that Aira-gawa and Nanama-gawa forest sites replaced two routes where no traces of bats were recorded. Any two proximate transects were roughly 2 ~ 4 km apart, and collectively they covered areas ranging up to 5 km from the coast. In each survey run, we alternated among the western, northern, and eastern sites of the island and randomly picked transects until all transects were assessed over a period of 2 ~ 3 weeks. We also alternated the nightly proceeding direction within any transect so that no point was ever visited at the same time.
We arrived at a site at least 30 min before sunset to observe bat arrivals or passing until sunset. Assessments began within 30 min after sunset and ended usually within 2 h, and transects were walked at roughly 1 km/h. A group of 2 ~ 3 workers searched for bats with binoculars (Leica 10 × 42 BN, Solms, Germany), aided with head- or spotlights and by bat sounds while feeding or interacting with each other. Upon each encounter, we tallied the number of bats present and recorded the species of trees where bat perched or searched for fruits, perch heights, and bats’ behaviors (e.g., moving, searching, feeding, individual interactions). We restricted our searches to a strip of 30 m on either side and assumed a complete census. Our prior tests indicated that this is a suitable distance in most habitats, but in inner forests we acknowledge that observations were more limited. After each transect survey, we remained following and monitoring bats present until past the midnight or an hour since the last bat observed left a site, whichever came first.
Fig phenology, fruit sampling, and feeding traces
Along with each bat survey at each transect, we assessed tree phenology in the early afternoon, sampled bat feeding traces after each bat survey, and sampled fresh mature fruits at dawn. We estimated crop size in the mature edible stages (i.e. the post-floral phase defined in ) of each fruiting monoecious fig tree and for dioecious female figs that produced seed-carrying syconia. We visually estimated crop sizes for trees with few or small amounts of fruits , but applied a stratified sampling method  when fruits were too many to count reliably. For each tree, we divided branches into three classes and defined the largest fig-bearing branches as the 3rd class, which merged into the 2nd class and then further merged into the 1st class, often bifurcating directly from the main trunk. We randomly selected 30 tertiary branches, tallied the number of figs on each branch, and then obtained the mean value (n). The number of the 1st class branches was counted (b 1 ), then six 1st class branches were randomly selected to estimate the mean number of 2nd class branches per 1st class branch (b 2 ) and the mean number of the 3rd class branches per 2nd class branch (b 3 ). Total crop size was estimated as crop size = n × b 1 × b 2 × b 3 .
We randomly collected accessible mature figs (the stage E ) directly from each fig tree where bat feeding was observed. Ryukyu flying-foxes usually drop ejecta pellets beneath the feeding tree, only occasionally mouth-carrying a large fruit to a feeding perch [46 YFL unpubl. data], thus we searched feeding traces underneath each feeding fig tree after our nightly observations, mostly discarded pellets but also culled fruits and fecal samples. Fresh mass (fm) and volume size of intact fruits and pellets were measured, and the numbers of seed they contained were tallied. We obtained dry mass (dm) of intact fruits and pellets after oven drying overnight at 50 °C. Water mass (wm, g) was determined as the difference between fresh fruit mass and dry fruit mass and water content (%) was calculated as WC = wm/fm × 100 . It was not possible to count the actual number of seeds of each fig fed on by bats, particularly in field conditions. Thus we used the difference in mean seed numbers between sampled fresh intact fruits and ejecta pellets to obtain an approximate estimate of the proportions of seeds being removed away from different species of fig fruits after bat feeding.
Data are presented as the mean ± standard error (SE) unless otherwise noted. Statistical tests were conducted using Statistica 12.0 (StatSoft, Tulsa, USA) with the significance level set at α = 0.05. Proportional data were arcsine-transformed to meet the normality requirement . We assessed the correlation (Pearson’s r) between relative frequency of occurrence (FO) and relative abundance (RA) for dominant tree species, among tree density, basal area (BA) coverage, and heterogeneity for forest transect sites, and between bat densities estimated over sites between the 2005 and 2012 assessments. A χ2 test was used to determine if the frequency distribution was random among abundance levels. We used analysis of variance (ANOVA) to examine the effects of site location on variances in bat density. Multivariate analysis of variance (MANOVA) was also used to examine the effects of site location on variances in tree density, BA coverage, and heterogeneity, and that in mean volume size, seed number, dry-pulp mass, water mass, and water content of fresh fruits and pellets among different fig species. We used additional multiple-range comparisons (HSD for unequal sample sizes) to locate the differences when significant differences were observed. We performed multiple regression analysis to examine the relationship of bat abundance with density, BA coverage, and heterogeneity of total trees among forest sites. The same analysis was conducted with relative density and relative BA for fruiting trees, total fig trees, fruiting fig trees, and selected predominant food fig species (i.e., F. septica and F. variegata combined), respectively. Linear regression was also conducted to examine the respective relationships of bat density and pellet number with canopy volume .
Tree composition and forest structure
The dominant tree species and their respective relative frequency of occurrence (FO), abundance (RA), and importance values (RI)
Bischofia javanica (Euphorbiaceae)*
Clerodendrum trichotomum (Verbenaceae)
Diospyros maritima (Ebenaceae)*
Elaeocarpus sylvestris (Elaeocarpaceae)*
Ficus benguetensis (Moraceae)*
F. septica (Moraceae)*
F. variegata (Moraceae)*
F. virgate (Moraceae)*
Fraxinus formosana (Oleaceae)
Leucaena leucocephala (Mimosaceae)
Macaranga tanarius (Euphorbiaceae)*
Mallotus japonicus (Euphorbiaceae)
Melanolepis multiglandulosa (Euphorbiaceae)*
Melia azedarach (Meliaceae)*
Pinus luchuensis (Pinaceae)
Rhus succedanea (Anacardiaceae)*
Schefflera octophylla (Araliaceae)*
Schima superba (Theaceae)*
Styrax japonica (Styracaceae)
Trema oreintalis (Ulmaceae)*
Trochodendron aralioides (Trochodendraceae)
Turpinia ternata (Staphyleaceae)*
Moraceae and Euphorbiaceae each contributed four dominant tree species, accounting for a combined 33.2% importance, and were represented by 11 and 9 species, respectively. Wax tree (Rhus succedanea Linn.), large-leaved tree (Macaranga tanarius (L.) Műll.Arg.), F. variegata, Melanolepis multiglandulosa [(Reinw. ex Blume) Rchb.f. & Zoll.], and F. septica topped others in both measures, collectively contributing a total importance value of 21.5%, and all are fed on by Ryukyu flying foxes (Table 1). Ficus benguentensis and white fig ranked relatively low among these top 22 species, whereas the rest of the figs, including dioecious F. ampelas, F. erecta, and F. irisana, and monoecious F. caulocarpa, F. microcarpa, and F. superba, altogether accounted for only 2.88% of the total importance value.
Mean (± SE) linear density of fruit bats (bats/km-h) of the 12 forest transect sites and their respective tree heterogeneity, density (trees/ha), and basal area coverage (BA; m2/ha)
5.53 ± 1.143
10.28 ± 2.492
2.94 ± 0.69
1.42 ± 0.44
3.0 ± 0.116
1.52 ± 0.20
2.42 ± 0.98
5.22 ± 1.294
1.54 ± 0.40
3.49 ± 1.295
2.64 ± 1.50
12.33 ± 2.161
Bat abundance and relationships with forest structure and tree composition
Fruiting figs, fig consumption, and seed removal
Mean (± SE) fruit volume (mm3), dry mass (dm, g), water mass (wm, g), water content (wc, %), ripe color, and seed numbers in mature fresh fruits and ejecta pellets analyzed for monoecious1 vs. dioecious2 figs from three subgenera
Sycidium (Sect. Palaeomorphe)
F. virgata 2
694.08 ± 43.50
0.25 ± 0.09
0.65 ± 0.11
0.75 ± 0.03
136.50 ± 9.32
0.18 ± 0.02
0.31 ± 0.12
0.59 ± 0.12
54.25 ± 9.04
Sycomorus (Sect. Sycocarpus)
F. bengue 2
3445.35 ± 291.04**
1.02 ± 0.09**
3.08 ± 0.18**
0.75 ± 0.02
1182.50 ± 65.97**
0.56 ± 0.07
1.1 ± 0.16
0.63 ± 0.05
183.40 ± 29.37
F. septica 2
5368.62 ± 213.26**
1.46 ± 0.06**
4.92 ± 0.17**
0.78 ± 0.01
1129.39 ± 98.72**
0.48 ± 0.02
1.08 ± 0.05
0.60 ± 0.02
92.91 ± 6.05
Sycomorus (Sect. Neomorphe)
F. variegata 2
8004.55 ± 281.16**
1.47 ± 0.05**
7.13 ± 0.23**
0.83 ± 0.003*
1681.76 ± 49.58**
0.52 ± 0.02
1.69 ± 0.08
0.71 ± 0.01
93.42 ± 8.59
Urostigma (Sect. Urostigma/Sect. Conosycea)
F. superba 1
786.58 ± 43.89
0.16 ± 0.02
1.06 ± 0.16
0.86 ± 0.02*
99.06 ± 8.37
0.11 ± 0.02
0.39 ± 0.05
0.74 ± 0.05
69.13 ± 10.39
F. microcarpa 1
849.86 ± 128.34
0.22 ± 0.01
0.54 ± 0.10
0.75 ± 0.03
34.92 ± 4.95
0.09 ± 0.01
0.15 ± 0.02
0.58 ± 0.04
Sycomorus figs (F. variegata, F. septica, and F. benguetensis) were significantly greater in fruit size, contained more seeds, and higher dry-pulp mass and water mass (Pillai’s trace V = 0.985, F (20, 1052) = 17.19, p < 0.001) than urostigma figs (F. superba and F. microcarpa) and F. virgata (all p values < 0.01 in paired comparisons). Water content was higher in F. superba and F. variegata than in other species (p values < 0.05; Table 3). In approximate estimation, lower proportions of seeds remained in pellets of F. variegata, F. septica, and F. benguetensis. Seed proportion in each of these species being removed from fruits via bat feeding was about 1.7 ~ 1.4 times and 3.1 ~ 2.8 times that in F. virgata and F. superba, respectively.
A previous assessment over multiple habitats in Iriomote indicates higher bat abundances in areas with lower land proportions under cultivation and human residences, and higher tree heterogeneity and fruit-tree densities in villages . Our present study instead focused solely on inland forests that serve as roosting and also main foraging habitats of fruit bats. We found no correlation of bat abundance with tree heterogeneity, nor to density and basal area of total trees. Tree heterogeneity, density, and basal area varied among forest sites across the island with no apparent spatial patterns, as did bat abundance. Yet, bat abundances were comparable and significantly positively correlated to those previous data assessed with the same methods in the same forests . This seeming difference in dispersion patterns pinpoints the necessity for a finer examination of habitat and resource use by fruit bats in forested areas.
Our data indicate that the abundance of fruit bats foraging in forests positively depended on the relative density of fig trees, and the relative basal area of fruiting F. variegata and F. septica, but not that of total fruiting figs. Both species are characterized by the typical traits of bat-dispersed figs, including size, color (but note regional variation in ripe colors of F. variegata [49, 50]) and presumably scent (e.g., monoterpenes, ). Ficus variegata and F. septica were also the most common figs at our sites. This conforms to our prediction that fruit bat abundance depends on the availability of the most abundant bat syndrome figs, but not necessarily on bird-figs, and provides support for the dispersal syndrome hypothesis based on the color, size, and scent of figs [25, 50].
Phenologically, bat-dispersed figs are assumed to ripen more synchronously , yet dioecious bat-figs display complex patterns, being inter-tree asynchronous, or inter-tree synchronous but intra-tree asynchronous and with a relatively long crop season [49, 52, 53]. Being largely solitary, fruit bats in Iriomote find ample food supplies by spreading out while foraging where there are abundant bat-figs in forested areas. In contrast, monoecious figs are intra-tree synchronous with an apparent fruit availability peak and a shorter crop period. Bats feeding on these figs are likely forced to aggregate and potentially cause resource competition. This is consistent with our finding of higher mean bat abundances at intermediate crop sizes, as that noted in frugivorous birds . We also observed aggressive behaviors like fighting screams, wing-beating display, and chasing each other, on occasions when multiple bats perched and fed on the same trees (YFL unpubl. data).
Both F. septica and F. variegata are the predominant foods of fruit bats in Iriomote . This concurs with the relationship of bat abundance with fig tree abundance. In addition to external traits, F. septica and F. variegata contained higher dry pulp mass and may be nutritionally advantageous as well. For instance, F. variegata contains a high calcium content  that is essential for animals and fruit bats often obtain it by folivory . Ficus septica and F. variegata, along with other palaeotropical dioecious figs (mostly of the sycomorus group), also tend to contain higher proportions of carbohydrates and sugars favored by frugivores than many monoecious figs assessed . In contrast, monoecious figs like F. caulocarpa and F. superba, although higher in lipids and fiber, are lower in calcium and protein than dioecious sycidium figs (e.g., F. irisana and F. ampela ).
As food resources, F. variegata and F. septica were among the dominant trees in our forest sites. Ficus benguetensis (a bat-fig) and F. virgata (a bird-fig) ranked in the last quarter of the top 22 species, and all the rest of the bird-figs were ranked much lower in importance. On the other hand, F. microcarpa and F. superba have been widely planted as common ornamental trees in urban or human residential areas throughout their distributional range in tropical-subtropical East Asia [49, 53]. This may explain the observations that Ryukyu flying foxes elsewhere may feed on more diverse items in forests but use F. microcarpa as a core food plant in urbanized areas . Urbanization is less intensive in Iriomote and fruit bats are still capable of finding a sufficient food supply in more natural habitats. Yet in places within or near villages with abundant F. microcarpa, bats were observed frequently visiting and feeding substantially at crop peaks (YFL, unpubl. data).
This is consistent with an opportunistic foraging mode adopted by flying-foxes with spatiotemporal variation that reflects local phenology, availability, and the diversity of fruits [17, 29, 31, 58, 59]. In addition, a mix of fig species often provides a more complete set of nutrients . In contrast, major avian frugivores in Iriomote such as brown-eared bulbuls (Hypsipetes amaurotis), emerald doves (Chalcophaps indica), whistling green pigeons (Treron formosae), and white-eyes (Zosterops japonica) are all gape-limited and feed only on small-sized bird-figs like F. microcarpa and F. superba [46, 53, YFL unpubl. data]. Other pigeons or doves (e.g., Columba, Streptopelia) may even be seed predators [12, 21, 22]. Fruit bats in Iriomote thus likely play an extremely important role, and also represent a very low redundancy, in seed dispersal of those larger-sized figs .
Compared to bird-figs, mean remaining seeds in pellets of those large-sized bat-figs were much lower than that in fresh fruits. This suggests that higher proportions of seeds in large bat-figs may be more easily removed from fruits through bat feeding, and concurs with the tight inter-dependent relationship between fruit bats and bat-figs. Our estimates were less precise due to lack of direct fig-pellet match in seed counts, yet obtaining seed counts of fresh fruits prior to bat feeding is impossible or impractical in the field or feeding experiments. We collected fresh figs from parent trees where bat feeding and pellet ejection were observed, and pellets were collected timely and directly beneath parent trees. The chance and extent of secondary seed removal by other animals would be very slight or trivial. Given the observed variation, the dramatic difference in seed remains between bat- and bird-figs suggests further considering distinctive traits that separate them. Yet, our results don’t fully support the prediction regarding water content that is complicated by dry pulp mass and fruit size. Instead, water mass contained by bat-figs was significantly higher than that in bird-figs. Water mass in fruits generally rises with fruit size , whereas fig pulp mass tends to increase at a lowered rate depending on the investment on seeds . Further studies may examine water mass of figs over a broader size range and the effect of water on seed removal from fruits through the feeding of bats by more detailed behavioral experiments.
Yet, the function and effectiveness of fruit bats in seed dispersal may cease as bat abundance drops below certain thresholds [64, 65], due to various factors. In Fiji, landscape mosaics and declining forest habitats have resulted in the preferential foraging in farmland by Pacific flying-foxes, Pteropus tonganus . This seemingly suggests flexible and adaptive behavior by fruit bats; however, nutrient deficiencies may drive bats to feed on a diversity of plants, as cultivated plants have largely replaced native species, especially figs . Habitat fragmentation and alteration unavoidably force fruit bats to travel over an even larger area for foods  or enter places where food can be found with relative ease (e.g., Pteropus in Australia ), yet threats to fruit bats facing a changing world will also increase, such as conflicts with human economic demands [69, 70]. This is evidenced by the recently revealed incidents of illegally killing fruit bats on Yaeyama Islands , that along with other factors has drawn alarming calls for reassessments and reconsideration of its status .
Foraging dispersion of Ryukyu flying-foxes in East-Asian subtropical island forests depended on the availability of the most abundant bat-figs that serve as predominant foods to bats. Intermediate levels of crop sizes of theses figs appear most fit with their solitary foraging. At sites where density and basal area coverage of these bat-figs were below a certain level, their ability to attract and support foraging fruit bats appeared dwindled, which in a long run may lead to risks to both parties. This calls for considering fruit bat conservation with sufficient effort focusing on natural habitat protection [65, 72], particularly ways to aid for forests, figs, and fig-bat interactions.
YFL and YMK planned the study and experimental design with inputs from SB; YFL, YMK, SYC, and CFT conducted field assessments of bat abundance, forest composition, and fig phenology; SYC and CFT contributed to plant taxonomy with major inputs from YMK and others; SB took charge of logistic supports. YFL and YMK conducted statistical analyses and YFL completed the manuscript. All authors read and approved the final manuscript.
We thank the Iriomote Station of the Tropical Biosphere Research Center (TBRC), University of the Ryukyus, Chief Director S. Watanabe, H. Tsutsumi, and all staff for logistic support and assistance. JH Chen, CK Huang, and CC Chou assisted with field and lab works. YFL and YMK owe special gratitude to S Baba, M Izawa, S Matsumura, N Kidera, N Nakanishi, M Matsumoto, Nakama Fumio, and Yokoda San for their friendship, kind assistances, and hospitality, and to M Yoshihiro for an extraordinary rescue. Three anonymous reviewers critically improved the early versions of this manuscript.
The authors declare that they have no competing interests.
Availability of data and materials
Please contact the corresponding author.
Consent for publication
Ethics approval and consent to participate
Our work was ethically approved by NSC permit (99-2621-B-006-003) and complied with the current laws of Taiwan and Japan. No animals were handled inappropriately and special care was taken to prevent or minimize stress or disturbance to animals in all stages of the study.
This study and YFL were supported through a visiting research grant from TBRC, University of the Ryukyus. Additional support came from a grant (99-2621-B-006-003-MY3) funded by National Science Council (NSC, now as Ministry of Science and Technology), Taiwan.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Berg CC. Classification and distribution of Ficus. Experientia. 1989;45:605–11.View ArticleGoogle Scholar
- Berg CC, Corner EJH. Moraceae (Ficus). In: Noteboom HP, editor. Flora Malesiana. National Herbarium of Nederland. the Netherlands: Leiden; 2005. p. 1–730.Google Scholar
- Janzen DH. How to be a fig. Ann Review Ecol Syst. 1979;10:13–51.View ArticleGoogle Scholar
- Anstett MC, Hossaert-McKey M, Kjellberg F. Figs and fig pollinators: evolutionary conflicts in a coevolved mutualism. Trends Ecol Evol. 1997;12:94–9.View ArticlePubMedGoogle Scholar
- Weiblen GD. How to be a fig wasp. Ann Review Entomol. 2002;47:299–330.View ArticleGoogle Scholar
- Cook JM, Rasplus JY. Mutualists with attitude: coevolving fig wasps and figs. Trends Ecol Evol. 2003;18:241–8.View ArticleGoogle Scholar
- Rønsted N, Weiblen GD, Clement WL, Zerega NJC, Savolainen V. Reconstructing the phylogeny of figs (Ficus, Moraceae) to reveal the history of the fig pollination mutualism. Symbiosis. 2008;45:45–56.Google Scholar
- McLeish MJ, van Noort S. Codivergence and multiple host species use by fig wasp populations of the Ficus pollination mutualism. BMC Evol Biol. 2012;12:1.View ArticlePubMedPubMed CentralGoogle Scholar
- Terborgh J. Keystone plant resources in the tropical forest. In: Soule ME, editor. Conservation biology. New York: Academic Press; 1986. p. 330–44.Google Scholar
- Harrison RD. Figs and the diversity of tropical rainforests. Bioscience. 2005;55:1053–64.View ArticleGoogle Scholar
- O’Brien TG, Kinnaird MF, Dierenfeld ES, Conklin-Brittain NL, Wrangham RW, Silver SC. What’s so special about figs? Nature. 1998;392:668.View ArticleGoogle Scholar
- Shanahan M, So S, Compton SG, Corlett R. Fig-eating by vertebrate frugivores: a global review. Biol Rev. 2001;76:529–72.View ArticlePubMedGoogle Scholar
- Lambert FR, Marshall AG. Keystone characteristics of bird-dispersed Ficus in a Malaysian lowland rain forest. J Ecol. 1991;79:793–809.View ArticleGoogle Scholar
- Gautier-Hion A, Michaloud G. Are figs always keystone resources for tropical frugivorous vertebrates? A test in Gabon. Ecology. 1989;70:1826–33.View ArticleGoogle Scholar
- Patel A. Variation in a mutualism: phenology and the maintenance gynodioecy in tow Indian fig species. J Ecol. 1996;84:667–80.View ArticleGoogle Scholar
- Utzurrum RCB. Feeding ecology of Philippine fruit bats: patterns of resource use and seed dispersal. Symp Zool Soc Lond. 1995;67:63–77.Google Scholar
- Lee YF, Takaso T, Chiang TY, Kuo YM, Nakanishi N, et al. Variation in the nocturnal foraging distribution of and resource use by endangered Ryukyu flying-foxes (Pteropus dasymallus) on Iriomotejima, Japan. Contrib Zool. 2009;78:51–64.Google Scholar
- Nakamoto A, Kinjo K, Izawa M. Dietary plasticity in the Ryukyu flying fox on a subtropical island at the northern range limit of Pteropus. Acta Chiropt. 2015;17:105–16.View ArticleGoogle Scholar
- Marshall AG. Old World phytophagous bats (Megachiroptera) and their food plants: a survey. Zool J Linnean Soc. 1985;83:351–69.View ArticleGoogle Scholar
- Rainey WE, Pierson ED, Elmquist T, Cox PA. The role of flying foxes (Pteropodidae) in oceanic island ecosystems of the Pacific. Symp Zool Soc Lond. 1995;67:47–62.Google Scholar
- Corlett RT. Frugivory and seed dispersal by vertebrates in the Oriental (Indomalayan) region. Biol Rev. 1998;73:413–48.View ArticlePubMedGoogle Scholar
- Corlett RT. Frugivory and seed dispersal by vertebrates in tropical and subtropical Asia: an update. Global Ecol Conserv. 2017;11:1–22.View ArticleGoogle Scholar
- Hall L, Richards R. Flying foxes and fruit and blossom bats of Australia. Australia: UNSW Press; 2000.Google Scholar
- Muscarella R, Fleming TH. The role of frugivorous bats in tropical forest succession. Biol Rev. 2007;82:573–90.View ArticlePubMedGoogle Scholar
- Kalko EKV, Herre EA, Handley CO Jr. Relation of fig fruit characteristics to fruit-eating bats in the new and old world tropics. J Biogeogra. 1996;23:565–76.View ArticleGoogle Scholar
- Korine C, Kalko EKV, Herre EA. Fruit characteristics and factors affecting fruit removal in a Panamanian community of strangler figs. Oecologia. 2000;123:560–8.View ArticlePubMedGoogle Scholar
- Shanahan M, Compton SG. Vertical stratification of figs and fig-eaters in a Bornean lowland rain forest: how is the canopy different. Plant Ecol. 2001;153:121–32.View ArticleGoogle Scholar
- Lomáscolo SB, Levey DJ, Kimball RT, Bolker BM, Alborn HT. Dispersers shape fruit diversity in Ficus (Moraceae). PNAS. 2010;107:14668–72.View ArticlePubMedPubMed CentralGoogle Scholar
- McDonald-Madden E, Schreiber ESG, Forsyth DM, Choquenot D, Clancy TF. Factors affecting Grey-headed flying-fox (Pteropus poliocephalus: Pteropodidae) foraging in the Melbourne metropolitan area Australia. Aust Ecol. 2005;30:600–8.View ArticleGoogle Scholar
- Herrera CM. Seasonal variation in the quality of fruits and diffuse coevolution between plants and avian dispersers. Ecology. 1982;63:773–85.View ArticleGoogle Scholar
- Banack SA. Diet selection and resource use by flying foxes (genus Pteropus). Ecology. 1998;79:1949–67.View ArticleGoogle Scholar
- Corlett RT. How to be a frugivore (in a changing world). Acta Oecologica. 2011;37:674–81.View ArticleGoogle Scholar
- Chang SY, Lee YF, Kuo YM, Chen JH. Frugivory by barbets and the effects of de-inhibition and scarification on seed germination. Can J Zool. 2012;90:640–50.View ArticleGoogle Scholar
- Walker EH. Flora of Okinawa and the Southern Ryukyu Islands. Washington, D.C.: Smithsonian Institution Press; 1976.Google Scholar
- Mickleburgh SP, Hutson AM, Racey PA. Old World fruit bats: an action plan for their conservation. Gland: IUCN; 1992.View ArticleGoogle Scholar
- Vincenot CE, Collazo AM, Russo D. The Ryukyu flying fox (Pteropus dasymallus)—a review of conservation threats and call for reassessment. Mamm Biol. 2017;83:71–7.View ArticleGoogle Scholar
- Heaney L, Rosell-Ambal G, Tabaranza B, Izawa M. Pteropus dasymallus. IUCN 2008 Red List of Threatened Species. 2008. IUCN. www.iucnredlist.org.
- Cottam G, Curtis JT, Hale BW. Some sampling characteristics of a population of randomly dispersed individuals. Ecology. 1953;34:741–57.View ArticleGoogle Scholar
- Krebs CJ. Ecological methodology. New York: Addison-Welsey Longman; 1999.Google Scholar
- Dahdouh-Guebas F, Koedam N. Empirical estimate of the reliability of the use of point-centered quarter method (PCQM): solutions to ambiguous field situations and description of the PCQM protocol. Forest Ecol Manag. 2006;228:1–18.View ArticleGoogle Scholar
- Mitchell K. Quantitative analysis by the point-centered quarter method. 2010. arXiv: 1010.3303 [q-bio.QM].Google Scholar
- Brokaw N, Thompson J. The H for DBH. Forest Ecol Manag. 2000;129:89–91.View ArticleGoogle Scholar
- Curtis JT, McIntosh RP. An upland forest continuum in the prairie-forest border region of Wisconsin. Ecology. 1951;32:476–96.View ArticleGoogle Scholar
- Galil J, Eisikowitch D. On the pollination ecology of Ficus sycomorus in East Africa. Ecology. 1968;49:259–69.View ArticleGoogle Scholar
- Chapman CA, Chapman LJ, Wangham RW, Hunt K, Gebo D, Gardner L. Estimators of fruit abundance of tropical trees. Biotropica. 1992;24:527–31.View ArticleGoogle Scholar
- Nakamoto A, Kinjo K, Izawa M. The role of Orii’s flying fox (Pteropus dasymallus inopinatus) as a pollinator and a seed disperser on Okinawa-jima Island, Japan. Ecol Res. 2009;24:405–14.View ArticleGoogle Scholar
- Izhaki I, Tsahar E, Paluy I, Friedman J. Within population variation and interrelationships between morphology, nutritional content, and secondary compounds of Rhamnus alaternus fruits. New Phytol. 2002;156:217–23.View ArticleGoogle Scholar
- Zar JH. Biostatistical analysis. NJ: Prentice Hall; 2010.Google Scholar
- Tzeng HY. Taxonomy study of the genus Ficus in Taiwan. 2004. National Chunghsin Univ Ph.D. Dissertation. Taichung, Taiwan.Google Scholar
- Lomáscolo SB, Speranza P, Kimball RT. Correlated evolution of fig size and color supports the dispersal syndrome hypothesis. Oecologia. 2008;156:783–96.View ArticlePubMedGoogle Scholar
- Hodgkison R, Ayasse M, Haberlein C, Schulz S, Zubaid A, Mustapha WAW, et al. Fruit bats and bat fruits: the evolution of fruit scent in relation to the foraging behaviour of bats in the new nad old world tropic. Funct Ecol. 2013;27:1075–84.View ArticleGoogle Scholar
- Corlett RT. The phenology of Ficus fistulosa in Singapore. Biotropica. 1987;19:122–4.View ArticleGoogle Scholar
- Corlett RT. Figs (Ficus, Moraceae) in urban Hong Kong, South China. Biotropica. 2006;38:116–21.Google Scholar
- Manasse RS, Howe HF. Competition for dispersal agents among tropical trees: influences of neighbors. Oecologia. 1983;59:185–90.View ArticlePubMedGoogle Scholar
- Weiblen GD, Lomascolo SB, Oono R, Dumont ER. Nutritional dimorphism in New Guinea Dioecious figs. Biotropica. 2010;42:656–63.View ArticleGoogle Scholar
- Nelson SL, Kunz TH, Humphrey SR. Folivory in fruit bats: leaves provide a natural source of calcium. J Chem Ecol. 2005;31:1683–91.View ArticlePubMedGoogle Scholar
- Huang YT. Interspecific and intraspecific differences in fig functional traits and their ecological correlates. 2015. Natioanl Cheng Kung Univ Master thesis, Taiwan.Google Scholar
- Nakamoto A, Kinjo K, Izawa M. Food habits of Orii’s flying-fox, Pteropus dasymallus inopinatus, in relation to food availability in an urban area of Okinawa-jima Island, the Ryukyu Archipelago, Japan. Acta Chiroptero. 2007;9:237–49.View ArticleGoogle Scholar
- Mahmood-Ul-Hassan M, Gulraiz TL, Rana SA, Javid A. The diet of Indian flying-foxes (Pteropus giganteus) in urban habitats of Pakistan. Acta Chiroptero. 2010;12:341–7.View ArticleGoogle Scholar
- Wendeln MC, Runkle JR, Kalko EKV. Nutritional values of 14 fig species and bat feeding preferences in Panama. Biotropica. 2000;32:489–501.View ArticleGoogle Scholar
- McConkey KR, Drake DR. Flying foxes cease to function as seed dispersers long before they become rare. Ecology. 2006;87:271–6.View ArticlePubMedGoogle Scholar
- Lotan A, Izhaki I. Could abiotic environment shape fleshy fruit traits? A field study of the desert shrub Ochradenus baccatus. J Arid Environ. 2013;92:34–41.View ArticleGoogle Scholar
- Herrera CM. Vertebrate-dispersed plants of the Iberian Peninsula: a study of fruit characteristics. Ecol Monogr. 1987;57:305–31.View ArticleGoogle Scholar
- McConkey KR, O’Farrill G. Cryptic function loss in animal populations. Trends Ecol Evol. 2015;30:182–9.View ArticlePubMedGoogle Scholar
- Vincenot CE, Florens FBV, Kingston T. Can we protect island flying foxes? Science. 2017;355:1368–70.View ArticlePubMedGoogle Scholar
- Luskin MS. Flying foxes prefer to forage in farmland in a tropical dry forest landscape mosaic in Fiji. Biotropica. 2010;42:246–50.View ArticleGoogle Scholar
- Nelson SL, Miller MA, Heske EJ, Fahey GC Jr. Nutritional consequences of a change in diet from native to agricultural fruits for the Samoan fruit bat. Ecography. 2000;23:393–401.View ArticleGoogle Scholar
- McConkey KR, Drake DR. Indirect evidence that flying foxes track food resources among islands in a Pacific Archipelago. Biotropica. 2007;39:436–40.View ArticleGoogle Scholar
- Mildenstein T, Tanshi I, Racey PA. Exploitation of bats for bushmeat and medicine. In: Voigt CC, Kingston T, editors. Bats in the anthropocene: conservation of bats in a changing world. New York: Springer; 2016. p. 32–376.Google Scholar
- Aziz SA, Olival KJ, Bumrungrsi S, Richards GC, Racey PA. The conflict between pteropodid bats and fruit growers: species, legislation and mitigation. In: Voigt CC, Kingston T, editors. Bats in the anthropocene: conservation of bats in a changing world. New York: Springer; 2016. p. 326–77.Google Scholar
- Vincenot CE, Koyama L, Russo D. Near threatened? First report of unsuspected human driven decline factors in the Ryukyu flying fox (Pteropus dasymallus) in Japan. Mamm Biol. 2015;80:273–7.View ArticleGoogle Scholar
- Wiles GJ, Brooke AP. Conservation threats to bats in the tropical pacific islands and insular southeast Asia. In: Fleming TH, Racey PA, editors. Island bats: evolution, ecology, and conservation. Chicago: Univ Chicago Press; 2010. p. 405–59.Google Scholar