Contributions to Zoology, 78 (2) - 2009Ya-Fu Lee; Tokushiro Takaso; Tzen-Yuh Chiang; Yen-Min Kuo; Nozomi Nakanishi; Hsy-Yu Tzeng; Keiko Yasuda: Variation in the nocturnal foraging distribution of and resource use by endangered Ryukyu flying foxes (Pteropus dasymallus) on Iriomotejima Island, Japan

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Discussion

Variation in nocturnal distributions and relative abundances

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Yaeyama fruit bats are solitary or form mostly very small groups while foraging, but at a larger scale, their nocturnal spatial distribution is slightly clumped. Among habitats, the mean abundance and density were lower in cultivated areas than in villages and inland forests. This explains the across-island variation in bat distribution, where higher abundances were found in western than in eastern village sites, and supported our predictions. Villagers appeared tolerant to flying foxes, including their excretion and sounds (Y.F. Lee, unpubl. data; M. Matsumoto, pers. comm.). On average, however, eastern villages devoted a four-fold larger area of land to agriculture/husbandry activities, areas presumably with a higher rate of disturbance and intensity of human activities. Eastern sites also had lower fruit-tree density and heterogeneity range in tree composition. On Daito Island, where a high intensity of cultivation has made mangrove forests one of the few remaining undisturbed habitats, fruit bats are consistently found roosting in the border of mangroves (Izawa et al., 2001).

The distribution of foraging bats was correlated with land use patterns, habitats, as well as with food supplies, which is consistent with that reported for grey-headed flying foxes P. poliocephalus in Australia (McDonald-Madden et al., 2005). Bat density was correlated moderately with heterogeneity of tree composition, strongly with the density of major fruiting trees, and supported our predictions. Shifts in foraging sites by flying foxes for better food availability have been frequently documented and may occur between types of forests in an area (Banack, 2002), across various distances within a short period of time (Tidemann and Nelson, 2004; McConkey and Drake, 2007), or during migration (Hall and Richards, 2000). Nakamoto et al. (2007a) reported Orii’s fruit bats using certain fruiting trees intensively in an urban area. On Iriomote, bats in larger groups were observed frequenting some village sites, such as Hoshidate and Sonai, where large fruiting trees and ample food supplies occurred.

We observed variation between habitats in the height and DFT of perching bats. Heights of bats were lower in cultivated areas, and were in correspondence with lower canopy and shrub heights, and less canopy coverage, in this habitat. The DFT of perching bats was probably, at least in part, due to environmental features that restrict accessibility, such as tidal patterns in mangroves, and paths tended to be narrower and tree boundaries closer to trails in inland and coastal forests. An alternative but not mutually exclusive explanation is that the height and DFT may reflect a perceived or actual risk of predation. Fruit bats may fall prey to snakes, raptors, and other mammals (Pierson and Rainey, 1992; Klose et al., 2009). On Iriomote these at least include Beauty Rat Snakes Elaphe taeniura (Cope, 1861), Japanese Lesser Sparrowhawk Accipiter gularis (Temminck and Schlegel, 1844), feral cats Felis catus Linnaeus, 1758, and Iriomote Cats Prio­nailurus iriomotensis (Imaizumi, 1967) (Watanabe et al., 2003). Lower perching heights may reduce the risk from aerial raptors, particularly at trees of less canopy coverage, and in more open cultivated areas; lower shrub heights may make terrestrial predators more difficult to conceal and less possible to approach a perching tree from surroundings. The latter is also supported by the negative correlation between shrub height and bat density. At greater distances from paths and often depending on tides, bats in mangroves may be free of predation pressure from most terrestrial predators. This is supported by the fact that with a generally higher mean upper-canopy layer, perching heights of bats in mangroves were among the lowest, where terrestrial predators are most restricted.

Diets and resource use

Food plants used by Yaeyama fruit bats, as previously reported based mostly on anecdotal and sporadic notes, include 16 species of fruits, ten species of flowers, and fibrous stalks of sugarcane, for a total of 25 species (Nakamoto et al., 2007b). This study added another 14 species of plants to this list. Overall, the diet was less diverse than that reported for Orii’s fruit bats on Okinawa (fruit: 53 species, flower: 20 species, leaf: 18 species; Nakamoto et al., 2007a), but broader than that of Erabu (fruit: 19 species, flower: eight species, leaf: 11 species, bark: two species) and Daito fruit bats (fruit: 22 species, flower: nine species, leaf: six species; Funakoshi et al., 1993; Nakamoto et al., 2007b). Compared to other tropical pteropodids (e.g., Marshall, 1985), Funakoshi et al. (1993) attributed the broader diet of Erabu fruit bats to the warm-temperate seasonality in the food supply. This was not fully supported by our study conducted at a lower latitude near the Tropical of Cancer, and equally or more-diverse diets reported more recently in other paleo-tropical fruit bats (e.g., on American Samoa, Banack, 1998; Malaysia, Tan et al., 1998).

Instead, the latitudinal variation in the diet breadth of Ryukyu flying foxes, and the fact that our assessments were conducted only in the prime summer season, suggest a connection between diversity and variation in diets of fruit bats with food availability that is influenced by local phenology and the size of the distribution area where bats occur. This is confirmed by results for other species in the Pacific (e.g., McConkey and Drake, 2007). We observed asynchronous fruiting among individual trees of the same fig species, which also explains the high variation in abundances of bats recorded among transect-nights, and is an indication of local movements (Funakoshi et al., 1993). Food availability to frugivorous bats is often difficult and complicated to accurately estimate (Stashko and Dinerstein, 1988; but see Kalko, 1998), and it has not been quantitatively assessed for most subspecies of Ryukyu flying foxes. Our data provide evidence of a positive correlation between bat abundances and heterogeneity of tree compositions and the density of fruiting trees.

The Moraceae is the single most important family of food plants for Yaeyama fruit bats, and figs are the predominant food type, which was reported in almost all previous studies on diets of flying foxes (Marshall, 1985; reviews in Shanahan et al., 2001) and even other non-pteropodid fruit bats (Kalko et al., 1996; Korine et al., 2000). On Iriomote where the human population is low and mature primary forests remain intact on a large proportion of the land, bats feed mainly on native fruit plants (32 of 39 species of plants, 82.1%). This is a proportion closer to but higher than the one observed in Erabu fruit bats on Kuchinoerabu (22 of 29 species of plants, 75.9%; Funakoshi et al., 1993), and much higher than the one found in Daito fruit bats (15 of 26 species of food plants, 57.7%; Nakamoto et al., 2007b). Nakamoto et al. (2007a) concluded that the diverse diet of Orii’s fruit bats results from adaptation to cultivated plants (30 of 78 species of food plants, 38.5%) in urbanized environments, as also has been noted in grey-headed flying foxes (McDonald-Madden et al., 2005; Williams et al., 2006). Yet, nutrient deficiencies may be the real drive why flying foxes feed on a more diverse group of plants, as high proportions of cultivated plants have replaced native species, especially figs (Nelson et al., 2000). Most of the major fruits identified in samples, i.e., figs and mulberries, contain small but many seeds, which is consistent with feeding behavior described for flying foxes (Richards, 1990). Common garcinia, which contains a few large seeds, is an exception and also a fruit found favored by Daito fruit bats (Kinjo et al. unpubl. data). The dropped fruit remains, retaining seeds, were often located beneath or very close to the trees where bats fed, and the distances the seeds were dispersed by bats appeared greatly reduced.

We found seven species of leaves in the diet, and various animals at a notable frequency (11.9%), but with a minute proportion in mass. These have not been reported previously in the Yaeyama subspecies (Nakamoto et al., 2007b). Leaves appear in an increasing number of species of fruit bats of both the Paleo- and Neotropics (e.g., Kunz and Diaz, 1995; Courts, 1998; Nelson et al., 2000), and support the idea that folivory provides essential nutrients (e.g., carbohydrates, proteins, and calcium) for daily requirements (Rajamani et al., 1999; Nelson et al., 2005). While animal items are not uncommon in diets of pteropodids (e.g., Barclay et al., 2006), they are often attributed to incidental ingestion. It requires further observations or experiments for us to fully verify this possibility or alternatives, such as a rare case of carnivory in megachiropterans (Courts, 1998).

Implications for flying fox conservation

Our study provides an opportunity to draw parallels for a comparison with another closer and less studied subspecies, and it offers insights important for the conservation of island flying foxes. Formosa fruit bats suffered a dramatic decline, starting over 30 years ago, from exploitation and habitat alteration and destruction, and remains extremely rare (Lin and Pei, 1999; Heaney et al. 2008; D.J. Lin, unpubl. data). The historical hunting episode on Lutao, lasting for 10-15 years, presumably arose from economic incentives, for most bats were snared and later exported (Lin and Pei, 1999), and coincided with significant trading during the same period in other Pacific islands (e.g., Guam and the Mariana Islands, Wiles and Payne 1986). Hunting has been officially banned and fruit bats are legally protected on Lutao, yet their future fate is far from certain due to other factors such as habitat alteration, lack of stable food availability, and possible human disturbance (Lin and Pei, 1999).

Unlike bats that inhibit Lutao (c. 17.3 km2 at low tide), Yaeyama fruit bats occur among islands of a total land area exceeding 550 km2. Typhoons frequent both areas, but have no apparent effects on flying foxes on larger islands, e.g., Iriomote (this study). Yet, remnant populations on small islands may still be vulnerable to disturbances, even by chance (Pierson et al., 1996). The resident density (c. 173.4/km2) and annual tourist numbers (> 300,000) on Lutao are 25-fold and one- or two-fold those on Iriomote (Statistics Bureau data, Japan; National Statistics data, Taiwan), and cause inevitably more intensive habitat alteration or destruction. Ota (1992) noted a rapid decline in bat colonies on Hateruma after plantings replaced native forests. Plantations may provide substitution, but over time bats may still suffer from nutrient deficiencies (Nelson et al., 2000), or need to travel farther for more foraging options, which will be increasingly more difficult for bats on isolated or small islands (Meyer and Kalko, 2008; Meyer et al., 2008), and poses additional threats.

Concerning the status of Ryukyu flying foxes, and Pacific Island flying foxes in general, Yaeyama fruit bats on Iriomote are a good learning case. Human attitudes toward bats are extremely important conservation aspects (Y.F. Lee, unpubl. data; McCallum and Hocking, 2005; Thiriet, 2005). Habitat preservation and restoration, preferably through efforts by the local communities (Entwistle, 2001), to recover native forests and suitable food plants (e.g., figs) need to be implemented. Tourism and development should be carefully evaluated and tightly regulated, particularly for critical and small islands, such as Lutao. It remains unclear whether the currently few bats on Lutao are returnees of dwindling colonies that left Lutao for refuges, remnants of a formerly larger population, or immigrants from elsewhere. Further studies should focus on dispersal patterns and population dynamics on multiple islands over the entire or most of the distribution area of this species to achieve a deeper understanding of the ecology of the species in support of improved and more effective conservation strategies.