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Foraging Dispersion of Ryukyu Flying-Foxes and Relationships with Fig Abundance in East-Asian Subtropical Island Forests

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Foraging Dispersion of Ryukyu Flying-Foxes and Relationships with Fig Abundance in East-Asian Subtropical Island Forests Lee et al. BMC Ecol (2017) 17:35 DOI 10.1186/s12898-017-0146-8 BMC Ecology RESEARCH ARTICLE Open Access Foraging dispersion of Ryukyu fying‑foxes and relationships with fg abundance in East‑Asian subtropical island forests Ya‑Fu Lee1*† , Yen‑Min Kuo1†, Hsin‑Yi Chang1, Chi‑Feng Tsai1 and Shigeyuki Baba2,3 Abstract Background: Figs are widely distributed key resources to many tropical-subtropical animals, and fying-foxes are major consumers and seed dispersers of fgs. Bat-fg interrelationships, however, may vary among species difering in fruiting traits, i.e., bat- versus bird-dispersed fgs. We examined Ryukyu fying-fox foraging dispersion and the relation‑ ships with tree species composition and fg abundance in forests of Iriomote Island. Results: Bat foraging dispersion showed no spatial patterns with respect to diferent 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 fgs among sites. Instead, bat densities were positively dependent on the relative density of total fgs, and particularly the relative BA of bat-dispersed fgs Ficus septica and F. variegata. Both species were dominant fgs 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-fgs. These two species and Ficus benguetensis are larger-sized bat-fgs, 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-fgs would have been removed from fruits through the bat consumption, than that of small-sized bird-fgs like F. virgata, F. superba, and F. microcarpa. Conclusions: The foraging dispersion of Ryukyu fying-foxes in forests depends on the availability of the most abun‑ dant bat-fgs that serve as predominant foods. Intermediate levels of crop sizes of theses fgs appear most ft with their solitary foraging. Our results suggest that as density and BA coverage of these dominant bat-fgs are below a certain level, their efectiveness to attract bats may dwindle and so would their chance of dispersal by bats. Keywords: Abundance, Bats, Chiroptera, Figs, Flying-foxes, Frugivores, Iriomote island Background most speciose genera of fowering plants. Tey occur in Te genus Ficus (Moraceae) is widely distributed in tropi- diverse habitats in various growth forms and engage with cal areas with its distribution and diversifcation center- their pollinators (i.e., agaonid wasps) in complex and ing around the equatorial Indomalay-Australasian region intriguing coevolutionary relationships [3–8]. and extending poleward to around 35°N and 35°S [1, 2]. Ficus plants play a key ecosystem role in contribut- Te 800 or so extant Ficus species constitute one of the ing to the diversity of global tropical forests [9, 10]. Te majority of known Ficus species produce edible infores- cences (syconia), so-called fgs, that are largely apparent, *Correspondence: [email protected] †Ya-Fu Lee and Yen-Min Kuo contributed equally to this work. accessible, easy to handle by various volant, arboreal, or 1 Department of Life Sciences, National Cheng Kung University, even terrestrial animals, and nutritionally attractive [11, Tainan 701, Taiwan 12]. Many Ficus species have multiple crops year round, Full list of author information is available at the end of the article © The Author(s) 2017. This 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. Lee et al. BMC Ecol (2017) 17:35 Page 2 of 12 with asynchronous ripening phases among plants or of bat-fgs that serve as predominant food resources. even within a plant, which enhances their availability to Frugivorous bats and birds are often attracted to feshy foragers [9, 13]. Tis can be particularly crucial in lean fruits that are characterized by high water content [3, times when other plants cease to produce fruits (but see 30]. When consuming fgs, however, pteropodid bats [14, 15]). Globally, a variety of frugivorous or omnivo- typically compress fruits against the ridged palate with rous vertebrates, predominantly birds and mammals that the tongue, so the pulp-juice is squeezed out and swal- comprise nearly 1300 species, have been identifed as lowed along with numerous tiny seeds [12, 31]. Bats then fg-eating to various extents [12], although probably few eject deformed pulps as pellets, instead of swallowing depend solely on fgs [13]. the whole fg as do most birds [12, 17, 31]. Tus difer- Among mammalian families, the Old World fruit bats ent water content in fgs may contribute to diferent pro- (pteropodids) account for the highest proportion (ca. portions of seeds being ingested, which indirectly afect 16.5%) of the 284 species of fg-eating mammals, with the chance of seeds being further dispersed [32, 33]. We at least 47 species confrmed [12]. Tey appear all rely additionally tested that proportions of seeds remain- on fgs as predominant food resources [12, 16–19]. In ing in ejected pellets are afected by water content, and return, pteropodid fruit bats are signifcant seed dispers- predicted that fgs containing higher water content aid to ers of Ficus and various other plants, including many higher proportions of seeds being removed from fruits large-seeded fruits, in the Indomalayan and Australa- through the feeding process of fruit bats. sian regions [20–23]. Yet, dominant palaeotropical plants in early successions are rarely bat-dispersed except the Methods Moraceae, which is comprised mostly of Ficus [24]. Tis Study area and species further pinpoints potential efects of fruit bat-fg interac- Iriomote (24°15′ ~ 25′N, 123°40′ ~ 55′E) is located at the tions on forest structure, successional patterns, and fate southernmost tip of the Ryukyu Islands. It is the largest of large-seeded fruits, particularly in areas where suitable among the nine islets of the Yaeyama Islands, with an seed-dispersers may be scarce, such as remote oceanic area of 289 km2 and its highest peak at 470 m above sea islands [20]. level. Tis subtropical island is typifed by hot and humid Ficus plants may be categorized based on certain summers and warm but windy winters. Temperatures noticeable traits of fg morphology and phenology and generally rise above 25 °C from May to October, peaking their associated major dispersers [25]. Unlike bird-dis- at ca. 29 °C in July, and descend to 17 ~ 18 °C in Janu- persed fgs, those that are preferentially fed on by phyl- ary, with a mean annual rainfall of over 2300 mm (Japan lostomid fruit bats in the Neotropics (i.e., bat syndrome Meteorological Agency data). fgs, hereafter as bat-fgs) are generally green or dull Intact primary or secondary broadleaf forests cover in color, aromatic, span a wider range in fg size among about 80% of this mountainous inland and are charac- species, and ripen more synchronously [25, 26]. Greater terized by Castanopsis spp., Quercus spp., Schima spp. variation occurs with species that are typifed as bird syn- and various fgs (Ficus spp.). Hernanadia nymphaeifolia drome fgs (i.e., small-sized and orange-red in color, here- (Presl) Kubitzki and horsetail pine Casuarina equiseti- after as bird-fgs) and may be fed on by mixed forager folia L. are common in coastal forests, whereas Brugui- groups, particularly in the Old World tropics [27, 28]. On era gymnorrhiza (L.) Lam, Rhizophora mucronata, and the other hand, pteropodids appear attracted to function- R. stylosa mangroves prevail along estuaries and rivers. ally dioecious (gyno-dioecious) Ficus species [27] that Ficus, such as cedar fg F. superba Miq. and white fg F. are more diverse and abundant than monoecious spe- virgata Blume, are mixed with Cerbera manghas L., Heri- cies in the Indomalay-Australasian region. Dioecious fgs tiera littoralis, hanging-fower checkerboard foot Bar- that fail to attract birds are predicted to produce smaller ringtonia racemosa (L.) Blume ex DC, and screwpine crops of larger-sized and dull-colored fgs [12]. Pandanus odoratissimus L. f. in swampy wetland forests We examined foraging dispersion patterns of pteropo- [34]. Human residences and cultivated areas are located did bats and their relationships with fg assemblages in in lowlands below 100 m along the shoreline and are the subtropical forests of an Indomalayan oceanic island. more prominent on the eastern and northern coasts. Te dispersion of foraging pteropodids may be afected Te near-threatened Ryukyu fying-fox (Pteropus dasy- by factors associated with land use patterns, habitats, and mallus Temminck, 1825) is among the most northerly food availability (e.g., grey-headed fying fox Pteropus distributed pteropodids [35, 36]. Its fve subspecies are poliocephalus in Australia [29]). We tested the hypoth- each narrowly distributed but collectively cover a broad esis that the availability of bat-fgs afects nocturnal for- latitudinal range along the West Pacifc island chain aging dispersion of pteropodids and predicted that bat from Tokara Islands, Okinawa Island, Yaeyama Islands, presence and abundance will depend on the availability and small islets of the Nansei Islands in southern Japan Lee et al. BMC Ecol (2017) 17:35 Page 3 of 12 to Batan and other northern Philippine islets [35, 37]. Foraging bat dispersion and abundance Among the subspecies, P.
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