Journal of Threatened Taxa | www.threatenedtaxa.org | 26 June 2019 | 11(8): 13977–13983

Dietary analysis of the Indian Flying Fox Pteropus giganteus (Brunnich, 1782) (Chiroptera: Pteropodidae) in Myanmar through the analysis of faecal and chewed remnants

Moe Moe Aung ¹ & Than Than Htay ²

¹ Department of Zoology, University of Mandalay, Mandalay 05032, Myanmar.

² Department of Zoology, Pyay University, Pyay 081051, Myanmar.

¹ moeaung189@gmail.com (corresponding author), ² thtay4367@gmail.com

doi: https://doi.org/10.11609/jott.4972.11.8.13977-13983

Editor: Paul Racey, University of Exeter, Penryn, UK. Date of publication: 26 June 2019 (online & print)

Manuscript details: #4972 | Received 28 March 2019 | Final received 02 June 2019 | Finally accepted 14 June 2019

Citation: Moe Moe Aung & Than Than Htay (2019). Dietary analysis of the Indian Flying Fox Pteropus giganteus (Brunnich, 1782) (Chiroptera: Pteropodidae) in Myanmar through the analysis of faecal and chewed remnants. Journal of Threatened Taxa 11(8): 13977–13983. https://doi.org/10.11609/jott.4972.11.8.13977-13983

Copyright: © Moe Moe Aung & Htay 2019. Creative Commons Attribution 4.0 International License. JoTT allows unrestricted use, reproduction, and distribution of this article in any medium by adequate credit to the author(s) and the source of publication.

Funding: None.

Competing interests: The authors declare no competing interests.

Author details: Moe Moe Aung is an Associate Professor from Zoology Department of Mandalay University. She is currently working on bat ecology and taxonomy. She teaches biodiversity conservation and environmental studies. Than Than Htay is a Lecturer from Zoology Department of Pyay University. She is also a PhD student working on bat ecology. She teaches biodiversity conservation.

Author contribution: MMA - developed research design and hypothesis. She made the collection of some data, most of the manuscript writing and reviewing. TTH - collected most of the sample, took sample photos, made data arrangement and wrote a few part of manuscript.

Acknowledgements: We would like to thank Dr Nyo Nyo, Head of the Department of Zoology, Pyay University, for her encouragement throughout the study. We are also thankful to the staff of the Zoology Department for their help during the study. We are greatly indebted to Prof Dr Thant Zin, Head of the Department, Prof Dr Naw Dolly Wilbur and Prof (Rtd.) Dr Khin Mya Mya, Head of the Department of Zoology, University of Mandalay, for their encouragement towards various aspects of our research. We wish to express our gratitude and sincere appreciation to Prof Paul Racey from the University of Exeter for reading the earlier drafts of the paper.

Abstract: The diet of Indian Flying Fox Pteropus giganteus in southern Myanmar was analyzed from June 2017 to April 2018. Food resources were identified by collecting faeces, food remnants, and rejecta pellets beneath day roosts. Pteropus giganteus consumed fruits, flowers, and leaves of 14 species of plants. Six species of fruits were found in the faeces below the day roosts, 13 species of fruits and two species of leaves in the rejecta, and seven species of fruits and one species of leaf at the day roost. These observations indicate that P. giganteus is a phytophagous bat with rapid intestinal passage.

Keywords: Flying fox, food resources, pollination, seed dispersal.

introduction

The Old World bat family Pteropodidae is distributed throughout the tropics and subtropics of Australasia, Africa, and Oceania (Marshall 1983; Mickleburgh et al. 1992). It comprises 196 species (Simmons 2005) that feed primarily on fruits, flowers (nectar, pollen, petals, and bracts), and leaves of at least 188 plant genera from 64 families (Lobova et al. 2009; Fleming & Kress 2011; Aziz et al. 2015). Some species were also recorded eating insects (Clulow & Blundell 2011; Scanlon et al. 2013).

Seed dispersal plays a significant role in forest regeneration and maintenance. Flying foxes are often posited as effective long-distance seed dispersers due to their large home ranges and ability to disperse seeds while flying (Oleksy et al. 2017). Long-distance seed dispersal can be important for the regeneration of forested habitats, especially in regions where deforestation has been severe. Old World fruit bats (Pteropodidae) have considerable potential for long-distance seed dispersal (Oleksy et al. 2015). Pteropodid bats, however, also damage a wide range of fruit crops in some countries, leading to persecution. In some of these countries, bats are not legally protected. In others, legal protection is either not implemented or over-ridden by legislation specifically allowing the killing of bats (Aziz et al. 2015).

Pteropodids primarily eat ripe fruits; the seeds are often swallowed and defecated unharmed or dropped during food processing (Banack 1998; Dumont & Irvine 1998). Moreover, bat-dispersed fruits in the Palaeotropics are morphologically variable and have a variety of colours, and some are strongly scented (Thomas 1984; Tan et al. 1998). Many fruit-eating bats depend heavily on plant resources throughout the year (Banack 1998; Fleming 1998; Tan et al. 1998). Figs, in particular, are thought to be staples in fruit bat diets because of their nutritional value and year-round asynchronous fruiting cycle (Shanahan et al. 2001; Stier & Mildenstein 2005). These ecosystem services are dependent on large populations of flying foxes and are necessary to maintain the Old World tropical forests (Fujita & Tuttle 1991; Nyhagen et al. 2005; McConkey & Drake 2006). The aim of this study was to provide information on food resources of P. giganteus and to confirm whether this species is a seed disperser in Myanmar, where the fruit bats remain the limited number of publication. Pteropus giganteus, therefore, plays an essential role in seed dispersal and pollination (Whitaker & Jones 1994) and thereby in structuring forest communities.

Materials and Methods

Study site and study colony

This study was conducted within the Municipal Office Compound in Pyay Township (18°49’19.662’’N & 95°12’47.368’’E) in the Bago region on the eastern bank of the Ayeyarwady River in Myanmar (Fig. 1; Images 1 & 2). Some bat roosting trees are on the eastern bank of the river. The northern and northeastern parts of the district are forest-covered and contain numerous valleys and ravines. The Bago and Yakhine range forests are found on the western bank of the Ayeyarwady River opposite Pyay. Pyay has a tropical savanna climate. Temperatures are high throughout the year, especially before the monsoon from March to May when the average maximum temperature exceeds 36⁰C.

The colony size was estimated by counting the bats emerging after sunset with the help of two observers following Moe Moe Aung (2013).

Dietary analysis

Two main methods were used to investigate the diet of P. giganteus in the study area. These are:

(i) regular faecal and rejecta collections at day roosts and nocturnal perches and

(ii) chance discovery of food items carried into day roosts by the bats.

Regular faecal and rejecta collections at day roosts

The diet of P. giganteus was investigated throughout the year using plastic sheets which were placed directly below the day roosts to catch faeces and discarded fruit parts.

Chance collections of seeds and fruits

Dietary information was occasionally collected by chance, either when a bat carried fruit and/or other feed remnants directly into day roosts. These were also collected from the plastic sheets.

Identification of food plants

Seeds, fruits, flowers, and leaves from dropped, defecated, and rejecta plant parts were identified following Kress et al. (2003) to determine the different food items consumed seasonally.

Results

Study colony

The study colony comprised 1799±128 individuals (n=4) in June 2017 on the first count. The number of bats did not markedly change until March 2018 although this month was the breeding season of the bats—juveniles were not able to fly and therefore could not be counted. The number of bats increased in April 2018 to 2171±271 individuals as young bats were volant and could be counted at that time.

Food resources

Pteropus giganteus was found to feed on 10 species of fruits, flowers and fruits of a single species, and both fruits and leaves of three species (Table 1). Of these, six species of fruits were observed in faeces below the day roosts and feeding perches and 13 species of fruits and three species of leaves as rejecta and large seeds under the day roosts. Five species of fruits, one species of fruit and flower, and two species of leaves were carried into the day roost by bats and eaten there.

Feeding habits

Fourteen species of plant resources were consumed by Pteropus giganteus (Table 1). Of these, the seeds of Ficus racemosa, F. virens, and Psidium guajava were observed from faecal pellets. The pulp of these fruits was consumed and the seeds appeared to be swallowed. The leaves of Albizzia lebbek and Ficus virens were chewed and the soluble contents were extracted. The fibrous contents were discarded as fibrous pellets. Petioles and veins were common in these pellets. The flowers of Bombax ceiba were also observed beneath the day roost.

Characteristics of food resources

Colour

Pteropus giganteus within the Municipal Office Compound consumed fruits of a variety of different colours, including yellow, green, red, and purple (Table 2). The majority of the fruits observed in this study, however, were yellow, green, and orange. All the leaves were green in colour.

Odour

Eleven species of fruits produced an odour that could be detected when the fruits were held close to the nose of a human observer in the field. Nevertheless, the odour emitted by different species of fruits was markedly different (Table 2).

Growth form

Of the 14 species of food plants exploited by P. giganteus, 10 were tall trees and four were small trees. Shrubs and herbs were not included among the bat food sources in this study (Table 2).

Discussion and Conclusion

Of the 14 species of plants eaten by Pteropus giganteus, four species, namely Ficus racemosa, F. virens, Terminalia catappa, and Musa sapientum, were available to bats throughout the year; other plant species that had a long fruiting season were Psidium guajava, Mangifera indica, and Ziziphus jujuba. Therefore, these plant species may be important for maintaining the population of P. giganteus. Some of the food plants are agricultural (or those used by humans): Syzygium jambos, Psidium guajava, Tamarindus indica, Mangifera indica, Ziziphus jujuba, and Musa sapientum. There is, however, no known negative interaction between fruit bats and fruit-growers in the study area. In this study, bats consumed fruits of a variety of different colours displayed openly by plants so that they are easily accessed by bats in flight. Fruits also tended to have distinct odours as well. Many samples of faeces contained seeds which are dispersed by bats (Image 3). In contrast, seeds in some rejecta pellets, such as F. virens (Image 4), were parasitized by fig wasps and were no longer viable. Some fruits were observed in both faeces and rejecta under the day roost. Kunz & Diaz (1996) suggested that one of the consequences of seed dispersal by bats is that the survival and growth of trees from such seeds may ultimately provide roost trees for other bats. In addition to dispersing seeds over a wide area, the concentration of seeds deposited beneath roosting sites may give rise to a clumped distribution of seedlings. Pteropus giganteus often defecate or drop seeds during flight, which potentially disperses seeds over a large area each night (Oleksy et al. 2017). Dietary studies can provide the concept of dietary importance to the conservation of P. giganteus. In the present study, most plants in the diet of P. giganteus were from the forests of Pyay environs and this together with the fact that forests are critically important for the diet of P. giganteus may indicate the role of forest in maintaining the population of this species. The information in this study suggests that there exists a considerable potential for future research on the management and conservation strategies of fruit bats.

Table 1. Food resources exploited by Pteropus giganteus in the Municipal Office Compound in Pyay Township, Myanmar.

	Plant species	Food type	Food resources
			F	R	C
1.	Albizzia lebbek Benth	Fruit/ leaf	-	+	+
2.	Bombax ceiba L.	Fruit/ flower	-	+	+
3.	Ficus racemosa L.	Fruit	+	+	-
4.	F. virens Aiton	Fruit/ leaf	+	+	-
5.	Syzygium jambos (L.) Alston	Fruit	+	+	-
6.	Psidium guajava L.	Fruit	+	+	-
7.	Tamarindus indica L.	Fruit/ leaf	-	+	+
8.	Mangifera indica	Fruit	+	+	-
9.	Ziziphus jujuba Lam	Fruit	-	+	+
10.	Terminalia catappa L.	Fruit	-	+	+
11.	Musa sapientum L.	Fruit	-	+	+
12.	Mimusops elengi Roxb	Fruit	+	+	-
13.	Morinda angustifolia Roxb	Fruit	-	+	+
14.	Calophyllum inophyllum L.	Fruit	-	+	+

F - Feces collected below day roosts | R - Rejecta and large seeds | C - Food items carried into day roosts by bats | + Available | - Not available.

Table 2. Characteristics of food resources exploited by Pteropus giganteus in the Municipal Office Compound in Pyay Township, Myanmar.

	Family	Plant species	Growth form	Food colour	Odour
1.	Mimosaceae	Albizzia lebbek Benth	T	Green	Y
2.	Bombacaceae	Bombax ceiba L.	T	Orange	N
3.	Moraceae	Ficus racemosa L.	T	Mauve	Y
4.	Moraceae	Ficus virens Aiton	T	Brownish	Y
5.	Myrtaceae	Syzygium jambos (L.) Alston	T	Dark purple	N
6.	Myrtaceae	Psidium guajava L.	ST	Greenish-yellow	Y
7.	Caesalpiniaceae	Tamarindus indica L.	T	Reddish-brown	Y
8.	Anacardiaceae	Mongifera indica	T	Yellow	Y
9.	Rhamnaceae	Ziziphus jujuba Lam	ST	Reddish	Y
10.	Combretaceae	Terminalia catappa L.	T	Pinkish	Y
11.	Musaceae	Musa sapientum L.	ST	Yellow	Y
12.	Sapotaceae	Mimusops elengi Roxb	T	Orange	Y
13.	Rubiaceae	Morinda angustifolia Roxb	ST	Creamy	Y
14.	Clusiaceae	Calophyllum inophyllum L.	T	Green	N

T - Tree | ST - Small tree | Y - Yes | N - No. Plant growth form follows Kress et al. (2003).

For figure & images – click here

References

Aziz, S.A., K.J. Olival, S. Bumrungsri, G.C. Richards & P.A. Racey (2015). The conflict between fruit bats and fruit growers: species, legislation and mitigation, pp377–426. In: Voigt, C.C. & T. Kingston (eds.). Bats in the Anthropocene: Conservation of Bats in a Changing World. Springer, New York, ix+606pp. https://doi.org/10.1007/978-3-319-25220-9

Banack, S.A. (1998). Diet selection and resource use by flying foxes (genus Pteropus). Ecology 79(76): 1949–1967. https://doi.org/10.2307/176701

Clulow, S. & A.T. Blundell (2011). Deliberate insectivory by the fruit bat Pteropus poliocephalus by aerial hunting. Acta Chiropterologica 13: 201–205.

Dumont, E.R. & A.R. Irvine (1998). Old World bat fruits: diversity and implications for pteropodid ecology. Bat Research News 39: 166.

Fleming, T.H. (1988). The Short-Tailed Fruit Bat. In: Kunz, T.H. & M.B. Fenton (eds.). Bat Ecology. The University of Chicago Press, Chicago and London, 798pp.

Fleming, T.H. & W.J. Kress (2011). A brief history of fruit and frugivores. Acta Oecologica 37: 521–530.

Fujita, M.S. & M.D. Tuttle (1991). Flying foxes (Chiroptera, Pteropodidae)—threatened animals of key ecological and economic importance. Conservation Biology 5(4): 455–463.

Kress, W.J., R.A. Defilipps, E. Farr & Yin Yin Kyi (2003). A Checklist of the Trees, Shrubs, Herbs and Climbers of Myanmar. Contributions from the United States National Herbarium, Vol. 45. Smithsonian Institution, Washington, DC, 590pp.

Kunz, T.H. & C.A. Diaz (1996). Folivory in fruit-eating bats, with new evidence from Artibeus jamaicensis (Chiroptera: Phyllostomidae). Biotropica 27: 106–120.

Lobova, T.A., C.K. Geiselman & S.A. Mori (2009). Seed dispersal by bats in the Neotropics. Memoirs of the New York Botanical Garden 101.

Marshall, A.G. (1983). Bats, flowers and fruit: evolutionary relationships in the Old World. Biological Journal of the Linnean Society 20: 115–135.

McConkey, K.R. & D.R. Drake (2006). Flying foxes cease to function as seed dispersers long before they become rare. Ecology 87(2): 271–276.

Mickleburgh, S., P.A. Racey & A.M. Huston (eds.) (1992). Old World Fruit Bat Action Plan. International Union for Conservation of Nature and Natural Resources, Gland, Switzerland.

Moe Moe Aung (2013). Autecology of Pteropus giganteus in Myanmar. Lambert Academic Publishing House, Germany, 84pp.

Nyhagen, D.F., S.D.Turnbull & J.M. Olesen (2005). An investigation into the role of the Mauritian Flying Fox, Pteropus niger, in forest regeneration. Biological Conservation 122: 491–497.

Oleksy, R., P.A. Racey & G. Jones (2015). High-resolution GPS tracking reveals habitat selection and the potential for long-distance seed dispersal by Madagascan Flying Foxes Pteropus rufus. Global Ecology and Conservation 3: 678–692.

Oleksy, R., L. Giuggioli, T.J. McKetterick, P.A. Racey & G. Jones (2017). Flying foxes create extensive seed shadows and enhance germination success of pioneer plant species in deforested Madagascan landscapes. PLoS ONE 12(9): e0184023.

Scanlon, A.T., S. Petit & L.D.S. Sternberg (2013). Insectivory in Fijian Flying Foxes (Pteropodidae). Australian Journal of Zoology 61: 342–349.

Shanahan, M., S. So, S.G. Gompton & R. Gorlett (2001). Fig-eating by vertebrate frugivores: a global review. Biological Reviews 76(4): 529–572.

Simmons, N. (2005). Chiroptera, pp312–529. In: Wilson, D.E. & D.A.M. Reeder (eds.). Mammal Species of the World—A Taxonomic and Geographic Reference - 3rd Edition. Johns Hopkins University Press, Baltimore, 2,142pp.

Stier, S. & T. Mildenstein (2005). Dietary habitat of the world’s largest bats: the Philippine flying foxes, Acerodon jubatus and Pteropus vampyrus lanensis. Journal of Mammalogy 86(4): 719–728.

Tan, K.H., A. Zubaid & T.H. Kunz (1998). Food habits of Cynopterus brachyotis (Muller) (Chiroptera: Pteropodidae) in Peninsular Malaysia. Journal of Tropical Ecology 14: 299–307.

Thomas, D.W. (1984). Fruit intake and energy budgets of frugivorous bats. Physiological Zoology 57: 457–467.

Whitaker, R.J.,  & S.J. Jones (1994).  The role of frugivorous bats and birds in the rebuilding of a tropical forest ecosystem, Krakatau, Indonesia. Journal of Biogeography 21: 245–258.