Skip to main content

Advertisement

Log in

Diet, ecological role and potential ecosystem services of the fruit bat, Cynopterus brachyotis, in a tropical city

  • Published:
Urban Ecosystems Aims and scope Submit manuscript

Abstract

Urbanisation is happening at an unprecedented pace, affecting ecological interactions between frugivores and plants by altering the species composition of plant communities. Cynopterus brachyotis, a bat common in cities, is known to provide important ecosystem services, such as seed dispersal. Studying its diet offers insights into how ecological roles of bats in tropical landscapes could be affected by urbanisation. We documented the diet of C. brachyotis in Singapore, and tested the hypothesis that urbanisation decreases dietary breadth and proportion of native plants in its diet. We collected droppings of C. brachyotis at nine sites, and used morphological and molecular methods to identify plant species they contained. We evaluated whether species richness, proportion of native species and composition of plants in diet varied according to various urbanisation metrics. We recorded 33 plant species belonging to 25 genera and 21 families. Ten are native, 17 are exotic, and six are indeterminate. Twelve have never been reported in diets of C. brachyotis anywhere. Contrary to our hypotheses, urbanisation was not associated with reduced dietary breadth or declining reliance on native plants. Our results suggest urban C. brachyotis have a generalist approach to foraging and can readily exploit exotic plants as food. Because urbanisation does not affect dietary breadth or the proportion of native species they eat, these bats potentially continue to play important ecological roles by dispersing seeds of native plants even in the most urbanised sites, which is important in aiding succession in degraded landscapes. However, they may equally disperse exotic species they have exploited.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

All DNA sequence data associated with this project are archived in the BOLD public project ‘JCSDB Seeds dispersed by Cynopterus in Singapore’ and available at http://www.boldsystems.org/.

References

  • Aziz SA, Clements GR, McConkey KR, Sritongchuay T, Pathil S, Abu Yazid MNH, Campos-Arceiz A, Forget PM, Bumrungsri S (2017a) Pollination by the locally endangered island flying fox (Pteropus hypomelanus) enhances fruit production of the economically important durian (Durio zibethinus). Ecol Evol 7(21):8670–8684. https://doi.org/10.1002/ece3.3213

    Article  PubMed  PubMed Central  Google Scholar 

  • Aziz SA, Clements GR, Peng LY, Campos-Arceiz A, McConkey KR, Forget PM, Gan HM (2017b) Elucidating the diet of the island flying fox (Pteropus hypomelanus) in peninsular Malaysia through Illumina next-generation sequencing. PeerJ 5:e3176

    PubMed  PubMed Central  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48

    Google Scholar 

  • Brook BW, Sodhi NS, Ng PKL (2003) Catastrophic extinctions follow deforestation in Singapore. Nature 424(6947):420–423

  • Bumrungsri S (2002) The foraging ecology of the short-nosed fruit bat, Cynopterus brachyotis (Muller, 1838), in lowland dry evergreen rain forest, Southeast Thailand. University of Aberdeen, Dissertation

    Google Scholar 

  • Carlo TA, Collazo JA, Groom MJ (2003) Avian fruit preferences across a Puerto Rican forested landscape: pattern consistency and implications for seed removal. Oecologia 134(1):119–131

    PubMed  Google Scholar 

  • Chai ZJY (2016) Features of anthropogenic roosts used by bats in Singapore. National University of Singapore, Dissertation

    Google Scholar 

  • Chattopadhyay B, Garg KM, Mendenhall IH, Rheindt FE (2019) Historic DNA reveals Anthropocene threat to a tropical urban fruit bat. Curr Biol 29(24):R1299–R1300

    CAS  PubMed  Google Scholar 

  • Chen SF, Shen TJ, Lee HC, Wu HW, Zeng WT, Lu DJ, Lin HC (2017) Preference of an insular flying fox for seed figs enhances seed dispersal of dioecious species. Biotropica 49(4):511–520

    Google Scholar 

  • Cheptou PO, Carrue O, Rouifed S, Cantarel A (2008) Rapid evolution of seed dispersal in an urban environment in the weed Crepis sancta. Proc Natl Acad Sci U S A 105(10):3796–3799

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chong KY, Tan HTW, Corlett RT (2009) A checklist of the total vascular plant flora of Singapore: native, naturalised and cultivated species. Raffles Museum of Biodiversity Research, Singapore

    Google Scholar 

  • Chong KY, Tan HTW, Corlett RT (2011) A summary of the total vascular plant flora of Singapore. Gard Bull Singapore 63:197–204

    Google Scholar 

  • Chua M, Lim KKP (2011) Fruit bats. In: Ng PKL, Corlett RT, Tan HTW (eds) Singapore biodiversity: an encyclopedia of the natural environment and sustainable development, 1st edn. Editions Didier Millet, Singapore, pp 318–319

    Google Scholar 

  • Cilliers SS, Siebert SJ (2008) Urban flora and vegetation: patterns and processes. In: Niemela J (ed) Urban ecology: patterns, processes, and applications, 1st edn., Oxford University Press, New York, pp 148–158

  • Clare EL (2014) Molecular detection of trophic interactions: emerging trends, distinct advantages, significant considerations and conservation applications. Evol Appl 7(9):1144–1157

    PubMed  PubMed Central  Google Scholar 

  • Corlett RT (1992) The ecological transformation of Singapore, 1819-1990. J Biogeogr 19(4):411–420

    Google Scholar 

  • Corlett RT (1997) The vegetation in the nature reserves of Singapore. Gard Bull Singapore 49(2):147–159

    Google Scholar 

  • Corlett RT (2005) Interactions between birds, fruit bats and exotic plants in urban Hong Kong, South China. Urban Ecosyst 8(3–4):275–283

    Google Scholar 

  • Corlett RT (2011a) Terrestrial ecosystems. In: Ng PKL, Corlett RT, Tan HTW (eds) Singapore biodiversity: an encyclopedia of the natural environment and sustainable development, 1st edn. Editions Didier Millet, Singapore, pp 44–49

  • Corlett RT (2011b) Urban biodiversity. In: Ng PKL, Corlett RT, Tan HTW (eds) Singapore biodiversity: an encyclopedia of the natural environment and sustainable development, 1st edn. Editions Didier Millet, Singapore, pp 88–95

  • Corlett RT, Hau BCH (2000). Seed dispersal and forest restoration. For Restor Wildl Conserv 317–325

  • Corner EJH (1988). Wayside trees of Malaya, 3rd edn. The Malayan Nature Society, Kuala Lumpur

  • Dormann CF, Gruber B, Fruend J (2008) Introducing the bipartite package: analysing ecological networks. R News 8(2):8–11

    Google Scholar 

  • Dumont ER, Weiblen GD, Winkelmann JR (2004) Preference of fig wasps and fruit bats for figs of functionally dioecious Ficus pungens. J Trop Ecol 20(2):233–238

    Google Scholar 

  • Elangovan V, Marimuthu G, Kunz TH (2001) Temporal patterns of resource use by the short-nosed fruit bat, Cynopterus sphinx (Megachiroptera: Pteropodidae). J Mammal 82(1):161–165

    Google Scholar 

  • ESRI (2017). ArcGIS Pro. CA: Environmental Systems Research Institute

  • Fleming TH (1982). Foraging strategies of plant-visiting bats. In: Kunz TH (ed), Ecology of bats, 1st edn. Plenum Publishing Corporation, New York, pp 287–325

  • Fletcher C, Akbar Z, Kunz TH (2012) Fruit diet of frugivorous bats (Cynopterus brachyotis and Cynopterus horsfieldii) in tropical hill forests of peninsular Malaysia. Mamm 76(3):389–397

    Google Scholar 

  • Fujita MS, Tuttle MD (1991) Flying foxes (Chiroptera: Pteropodidae): threatened animals of key ecological and economic importance. Conserv Biol 5(4):455–463

    Google Scholar 

  • Haase D, Larondelle N, Andersson E, Artmann M, Borgström S, Breuste J, Gomez-Baggethun E, Gren Å, Hamstead Z, Hansen R, Kabisch N, Kremer P, Langemeyer J, Rall EL, McPhearson T, Pauleit S, Qureshi S, Schwarz N, Voigt A, Wurster D, Elmqvist T (2014) A quantitative review of urban ecosystem service assessments: concepts, models, and implementation. AMBIO 43(4):413–433

    PubMed  PubMed Central  Google Scholar 

  • Hobbs RJ, Arico S, Aronson J, Baron JS, Bridgewater P, Cramer VA, Epstein PR, Ewel JJ, Klink CA, Lugo AE, Norton D, Ojima D, Richardson DM, Sanderson EW, Valladares F, Vila M, Zamora R, Zobel M (2006) Novel ecosystems: theoretical and management aspects of the new ecological world order. Glob Ecol Biogeogr 15(1):1–7

    Google Scholar 

  • Hodgkison R, Balding ST, Zubaid A, Kunz TH (2003) Fruit bats (Chiroptera: Pteropodidae) as seed dispersers and pollinators in a lowland Malaysian rain forest. Biotropica 35(4):491–502

    Google Scholar 

  • Hodgkison R, Balding ST, Zubaid A, Kunz TH (2004) Temporal variation in the relative abundance of fruit bats (Megachiroptera: Pteropodidae) in relation to the availability of food in a lowland Malaysian rain forest. Biotropica 36(4):522–533

    Google Scholar 

  • Ingle NR (2003) Seed dispersal by wind, birds, and bats between Philippine montane rainforest and successional vegetation. Oecologia 134(2):251–261

    PubMed  Google Scholar 

  • Janzen DH (1981) Enterolobium cyclocarpum seed passage rate and survival in horses, Costa Rican Pleistocene seed dispersal agents. Ecology 62(3):593–601

    Google Scholar 

  • Jordaan LA, Johnson SD, Downs CT (2012) Wahlberg’s epauletted fruit bat (Epomophorus wahlbergi) as a potential dispersal agent for fleshy-fruited invasive alien plants: effects of handling behaviour on seed germination. Biol Invasions 14(5):959–968

    Google Scholar 

  • Jung K, Threlfall CG (2016). Urbanisation and its effects on bats—a global meta-analysis. In: Voigt CC, Kingston T (eds), bats in the anthropocene: conservation of bats in a changing world, 1st edn. Springer international publishing, pp 13–33

  • Kasada M, Matsuba M, Miyashita T (2017) Human interest meets biodiversity hotspots: a new systematic approach for urban ecosystem conservation. PLoS One 12(2):e0172670

    PubMed  PubMed Central  Google Scholar 

  • Kingston T (2010) Research priorities for bat conservation in Southeast Asia: a consensus approach. Biodivers Conserv 19(2):471–484

    Google Scholar 

  • Kress WJ (2017) Plant DNA barcodes: applications today and in the future. J Syst Evol 55(4):291–307

    Google Scholar 

  • Kress WJ, Erickson DL (2007) A two-locus global DNA barcode for land plants: the coding rbcL gene complements the non-coding trnH-psbA spacer region. PLoS One 2(6):e508

    PubMed  PubMed Central  Google Scholar 

  • Kunz TH (1982) Roosting ecology. In: Kunz TH (ed), Ecology of bats, 1st edn. Plenum Publishing Corporation, New York, pp 1–55

  • Kunz TH, de Torrez EB, Bauer D, Lobova T, Fleming TH (2011) Ecosystem services provided by bats. Ann N Y Acad Sci 1223:1–38

    PubMed  Google Scholar 

  • Lane DJW, Kingston T, Lee BPYH (2006) Dramatic decline in bat species richness in Singapore, with implications for Southeast Asia. Biol Conserv 131(4):584–593

    Google Scholar 

  • Leong TM, Chan KW (2011) Bats in Singapore – ecological roles and conservation needs. Nature Conservation for a Sustainable Singapore, Proc Nat Soc, Singap, pp 41–64

    Google Scholar 

  • Lewis SE (1995) Roost fidelity of bats: a review. J Mammal 76(2):481–496

    Google Scholar 

  • Lim VC, Clare EL, Littlefair JE, Ramli R, Bhassu S, Wilson JJ (2018a) Impact of urbanisation and agriculture on the diet of fruit bats. Urban Ecosyst 21(1):61–70

    Google Scholar 

  • Lim VC, Ramli R, Bhassu S, Wilson JJ (2018b) Pollination implications of the diverse diet of tropical nectar-feeding bats roosting in an urban cave. PeerJ 6:e4572

    PubMed  PubMed Central  Google Scholar 

  • Lok AFSL, Chong KY, Tan KX, Tan HTW (2010) A checklist of the spontaneous exotic vascular plant flora of Singapore. Cosmos 6(01):57–83

    Google Scholar 

  • Marshall AG (1985) Old World phytophagous bats and their food plants: a survey. Zool J Linnean Soc 83:351–369

    Google Scholar 

  • Mathieu E (1918) Notes on Cola trees in the economic garden, Singapore. Straits Settlements Bot Gard Bull 2:74–86

    Google Scholar 

  • McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127(3):247–260

    Google Scholar 

  • McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst 11(2):161–176

    Google Scholar 

  • Mohd-Azlan J, Alek Tuen A, Abd Rahman MR (2010) Preliminary assessment of activity pattern and diet of the lesser dog faced fruit bat Cynopterus brachyotis in a Dipterocarp forest, Sarawak, Borneo. Trop Ecol 51(2):297

    Google Scholar 

  • Nghiem LTP, Tan HTW, Corlett RT (2015) Invasive trees in Singapore: are they a threat to native forests? Trop Conserv Sci 8(1):201–214

    Google Scholar 

  • Nielsen JM, Clare EL, Hayden B, Brett MT, Kratina P (2017) Diet tracing in ecology: method comparison and selection. Methods Ecol Evol 9(2):1–14

    Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M et al (2018) Vegan: community ecology package. R package version 2:4–6 https://cran.r-project.org/package=vegan

    Google Scholar 

  • Phua PB, Corlett RT (1989) Seed dispersal by the lesser short-nosed fruit bat (Cynopterus brachyotis, Pteropodidae, Megachiroptera). Malay Nat J 42:251–256

    Google Scholar 

  • R Core Team (2017). R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.r-project.org/. Accessed 9 February 2019

  • Rao AN, Wee YC (1989). Singapore trees, 1st edn. Singapore Institute of Biology, Singapore

  • Ratti C, Seiferling I, Li X, Ghaeli N, So W (2016). Exploring the green canopy in cities around the world. Massachusetts Institute of Technology Senseable City Lab. http://senseable.mit.edu/treepedia. Accessed 20 January 2019

  • Schupp EW, Jordano P, Gómez JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytol 188(2):333–353

    PubMed  Google Scholar 

  • Seto KC, Güneralp B, Hutyra LR (2012) Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proc Natl Acad Sci U S A 109(40):16083–16088

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shackleton CM, Ruwanza S, Sanni GS, Bennett S, De Lacy P, Modipa R, Mtati N, Sachikonye M, Thondhlana G (2016) Unpacking Pandora’s box: understanding and categorising ecosystem disservices for environmental management and human wellbeing. Ecosyst 19(4):587–600

    Google Scholar 

  • Sheherazade Y, Pradana DH, Tsang SM (2017) The role of fruit bats in plant community changes in an urban forest in Indonesia. Raffles Bull Zool 65:497–505

    Google Scholar 

  • Shilton LA, Altringham JD, Compton SG, Whittaker RJ (1999) Old World fruit bats can be long-distance seed dispersers through extended retention of viable seeds in the gut. Proc R Soc B 266(1416):219–223

    PubMed Central  Google Scholar 

  • Singapore Land Authority [SLA] (2019) Total land area of Singapore (as at 31 Dec). Singapore Land Authority. https://www.sla.gov.sg/Press-Room/Statistics. Accessed 9 February 2019

  • Sritongchuay T, Gale GA, Stewart A, Kerdkaew T, Bumrungsri S (2014) Seed rain in abandoned clearings in a lowland evergreen rain forest in southern Thailand. Trop Conserv Sci 7(3):572–585

    Google Scholar 

  • Stewart AB, Sritongchuay T, Teartisup P, Kaewsomboon S, Bumrungsri S (2018) Habitat and landscape factors influence pollinators in a tropical megacity, Bangkok, Thailand. PeerJ 6:e5335

    PubMed  PubMed Central  Google Scholar 

  • Tan HTW (2011a). Tembusu. In: Ng PKL, Corlett RT, Tan HTW (eds) Singapore biodiversity: an encyclopedia of the natural environment and sustainable development, 1st edn. Editions Didier Millet, Singapore, p 477

  • Tan HTW (2011b). Tiup tiup. In: Ng PKL, Corlett RT, Tan HTW (eds) Singapore biodiversity: an encyclopedia of the natural environment and sustainable development, 1st edn. Editions Didier Millet, Singapore, pp 48

  • Tan KH, Zubaid A, Kunz TH (1998) Food habits of Cynopterus brachyotis (Muller) in peninsular Malaysia. J Trop Ecol 14(3):299–307

    Google Scholar 

  • Tan HTW, Ibrahim A, Tan K (2008) A new record of Piper aduncum L. (Piperaceae) in Singapore. Nat Singapore 1:55–59

    Google Scholar 

  • Tang ZH, Mukherjee A, Sheng LX, Cao M, Liang B, Corlett RT, Zhang SY (2007) Effect of ingestion by two frugivorous bat species on the seed germination of Ficus racemosa and F. hispida (Moraceae). J Trop Ecol 23(1):125–127

    Google Scholar 

  • Thomas DW (1988) Analysis of the diets of plant-visiting bats. In: Kunz TH (ed) Ecological and behavioral methods for the study of bats, 1st edn. Smithsonian Institution Press. Washington, DC, pp 211–220

    Google Scholar 

  • United Nations [UN] (2018). World urbanisation prospects: the 2018 revision. United Nations, Department of Economic and Social Affairs, Population Division. https://population.un.org/wup/Country-Profiles/. Accessed 20 January 2019

  • Utzurrum RCB (1995) Feeding ecology of Philippine fruit bats: patterns of resource use and seed dispersal. Symp Zool Soc Lond 67:63–77

    Google Scholar 

  • Utzurrum RCB, Hideman PD (1991) Differential ingestion of viable vs nonviable ficus seeds by fruit bats. Biotropica 23(3):311–312

    Google Scholar 

  • Vaz AS, Kueffer C, Kull CA, Richardson DM, Vicente JR, Kühn I, Schröter M, Hauck J, Bonn A, Honrado JP (2017) Integrating ecosystem services and disservices: insights from plant invasions. Ecosyst Serv 23:94–107

    Google Scholar 

  • Vendan SE, Kaleeswaran B (2011) Plant dispersal by Indian flying fox Pteropus giganteus in Madurai region, India. Elixir Bio Div 30:1810–1813

    Google Scholar 

  • Voigt CC, Kelm DH, Bradley BJ, Ortmann S (2009) Dietary analysis of plant-visiting bats. In: Kunz TH, Parsons S (eds) Ecological and behavioral methods for the study of bats, 2nd edn. The John Hopkins University Press, Baltimore, pp 593–609

  • Voigt FA, Farwig N, Johnson SD (2011) Interactions between the invasive tree Melia azedarach (Meliaceae) and native frugivores in South Africa. J Trop Ecol 27(4):355–363

    Google Scholar 

  • Voigt CC, Phelps KL, Aguirre LF, Corrie Schoeman M, Vanitharani J, Zubaid A (2015). Bats and buildings: the conservation of synanthropic bats. In: Voigt CC, Kingston T (eds), bats in the anthropocene: conservation of bats in a changing world, 1st edn. Springer international publishing, pp 427–462

  • von Döhren P, Haase D (2015) Ecosystem disservices research: a review of the state of the art with a focus on cities. Ecol Indic 52:490–497

    Google Scholar 

  • Williams NSG, McDonnell MJ, Phelan GK, Keim LD, Van Der Ree R (2006) Range expansion due to urbanization: increased food resources attract Grey-headed flying-foxes (Pteropus poliocephalus) to Melbourne. Austral Ecol 31(2):190–198

    Google Scholar 

  • Yao H, Song J, Liu C, Luo K, Han J, Li Y, Pang X, Xu H, Zhu Y, Xiao P, Chen S (2010) Use of ITS2 region as the universal DNA barcode for plants and animals. PLoS One 5(10):e13102

    PubMed  PubMed Central  Google Scholar 

  • Yee ATK, Corlett RT, Liew SC, Tan HTW (2011) The vegetation of Singapore ― an updated map. Gard Bull Singapore 63(1&2):205–212

    Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge Wildlife Reserves Singapore Conservation Fund for funding the molecular aspect of this study, and the Department of Biological Sciences at National University of Singapore (University) for funding the rest. We thank: E. Velautham for help with seedling identification; V. C. Lim for advice on dietary analyses; University field assistants and laboratory technicians for logistical support; National Parks Board for access to field sites.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joanna L. Coleman.

Electronic supplementary material

ESM 1

(DOCX 328 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chan, A.A.Q., Aziz, S.A., Clare, E.L. et al. Diet, ecological role and potential ecosystem services of the fruit bat, Cynopterus brachyotis, in a tropical city. Urban Ecosyst 24, 251–263 (2021). https://doi.org/10.1007/s11252-020-01034-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11252-020-01034-x

Keywords

Navigation