Skip to main content
Springer Nature Link
Log in

The role of pteropodid bats in pollination of durian (Durio zibethinus) in managed orchards in suburban habitat of Thailand

  • Published:
Urban Ecosystems Aims and scope Submit manuscript

Abstract

Pollination specialists are increasingly threatened worldwide, especially in intensively-managed durian orchards where loss of pollinators may lead to reduced fruit production. In tropical plant communities where plant species attract multiple species of pollinators, specialists may have advantages over generalists. The present study examined the pollination ecology of durian (Durio zibethinus) in intensively and non-intensively managed orchards in suburban habitats of Nakhon Nayok and Chanthaburi provinces, respectively, in Thailand. Manual-pollination yielded the greatest fruit set 60 d after pollination, followed by open pollination (mostly by pteropodid bats), and insect pollination, while non-pollinated flowers had no fruit set. Eonycteris spelaea was the major bat pollinator in both provinces. Bats found in suburban habitat of Nakhon Nayok were mostly Eonycteris spelaea (67%). Pollen of at least five plant species was found on Eonycteris spelaea fur, including Musa sp., Oroxylum indicum, Durio zibethinus, Bombax valetonii and an unknown species. Pollen of only two species, Oroxylum indicum and Musa sp., was observed on Cynopterus sphinx fur. The non-intensive orchards in Nakhon Nayok, where mixed-species gardens are maintained under more naturalistic conditions, might offer higher fruit set on average. Such conditions might maintain higher bats capture rate of natural pollinators and reduce the risk of pollination failure in comparison with intensively-managed durian orchards.

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

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

References

  • Acharya PR, Racey PA, Sothibandhu S, Bumrungsri S (2015a) Feeding behaviour of the dawn bat (Eonycteris spelaea) promotes cross pollination of economically important plants in Southeast Asia. J Pollinat Ecol 15:44–50

    Google Scholar 

  • Acharya PR, Racey PA, Sothibandhu S, Bumrungsri S (2015b) Home-range and foraging areas of the dawn bat Eonycteris spelaea in agricultural areas of Thailand. Acta Chiropterol 17:301–319

    Google Scholar 

  • Akaike H (1973) Information theory as an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Second international symposium on information theory. Akademiai Kiado, Budapest, pp 267–281

    Google Scholar 

  • Allen-Wardell G, Bernhardt P, Bitner R, Burquez A, Buchmann S, Cane J, Cox PA, Dalton V, Feinsinger P, Ingram M, Inouye D, Jones CE, Kennedy K, Kevan P, Koopowitz H, Medellin R, Medellin-Morales S, Nabhan GP, Pavlik B, Tepedino V, Torchio P, Walker S (1998) The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Conserv Biol 12:8–17

    Google Scholar 

  • Amorim FW, Galetto L, Sazima M (2013) Beyond the pollination syndrome: nectar ecology and the role of diurnal and nocturnal pollinators in the reproductive success of Inga sessilis (Fabaceae). Plant Biol 15:317e327

    Google Scholar 

  • Aziz SA, Clements GR, McConkey KR, Sritongchuay T, Pathil S, Yazid MNHA, Campos-Arceiz A, Forget P-M, Bumrungsri S (2017) Pollination by the locally endangered island flying fox (Pteropus hypomelanus) enhances fruit production of the economically important durian (Durio zibethinus). Ecol Evol 7:8670–8684

    PubMed  PubMed Central  Google Scholar 

  • Bayat S, Geiser F, Kristiansen P, Wilson SC (2014) Organic contaminants in bats: trends and new issues. Environ Int 63:40–52

    CAS  PubMed  Google Scholar 

  • Brandt K, Glemnitz M, Schröder B (2017) The impact of crop parameters and surrounding habitats on different pollinator group abundance on agricultural fields. Agric Ecosyst Environ 243:55–66

    Google Scholar 

  • Bumrungsri S, Harbit A, Benzie C, Carmouche K, Sridith K, Racey P (2008) The pollination ecology of two species of Parkia (Mimosaceae) in southern Thailand. J Trop Ecol 24:467–475

    Google Scholar 

  • Bumrungsri S, Sripaoraya E, Chongsiri T, Sridith K, Racey PA (2009) The pollination ecology of durian (Durio zibethinus, Bombacaceae) in southern Thailand. J Trop Ecol 25:85–92

    Google Scholar 

  • Bumrungsri S, Duncan L, Colin H, Sripaoraya E, Kitpipat K, Racey PA (2013) The dawn bat, Eonycteris spelaea Dobson (Chiroptera: Pteropodidae) feeds mainly on pollen of economically important food plant in Thailand. Acta Chiropterol 15:95–104

    Google Scholar 

  • Cadenasso ML, Pickett ST, Schwarz K (2007) Spatial heterogeneity in urban ecosystems: Reconceptualized land cover and a framework for classification. Front Ecol Environ 5:80–88

    Google Scholar 

  • Chakraborty S, Srinivasulu C, Srinivasulu B, Pradhan MS, Nameer PO (2004) Checklist of insectivores (Mammalia: Insectivora) of South Asia. Zoo Print J 19(2):1361–1371

    Google Scholar 

  • de Araújo MLVS, Bernard E (2016) Green remnants are hotspots for bat activity in a large Brazilian urban area. Urban Ecosyst 19:287–296

    Google Scholar 

  • Department of Agriculture (2001a) Analysis of agroecosystem - east. Ministry of Agriculture and Cooperatives, Chonburi

    Google Scholar 

  • Department of Agriculture (2001b) Analysis of agroecosystem – central and west. Chumchonsahakonkankaset Press, Bangkok

    Google Scholar 

  • Development Core Team R (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Fenster CB, Armbruster WS, Thomson JD, Wilson P, Dudash MR (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35:375–403

    Google Scholar 

  • Fleming TH, Cullen G, Kress WJ (2009) The evolution of bat pollination: a phylogenetic perspective. Ann Bot 104:1017–1043

    PubMed  PubMed Central  Google Scholar 

  • Francis CM (2008) A guide to the mammals of Southeast Asia. New Holland Publishers United Ltd, UK

    Google Scholar 

  • Giam X, Olden JD (2016) Quantifying variable importance in a multimodel inference framework. Methods Ecol Evol 7:388–397

    Google Scholar 

  • Johnson SD, Steiner KE (2000) Generalization versus specialization in plant pollination systems. Trends Ecol Evol 15:140–143

    CAS  PubMed  Google Scholar 

  • Johnson JB, Gates JE, Ford WM (2008) Distribution and activity of bats at local and landscape scales within a rural-urban gradient. Urban Ecosyst 11:227–242

    Google Scholar 

  • Keven PG, Phillips TP (2011) The economic impact of pollinator declines: an approach to assessing the consequences. Conserv Ecol 5:1–19

    Google Scholar 

  • Kremen C, Ricketts T (2000) Global perspectives on pollination disruptions. Conserv Biol 14:1226–1228

    Google Scholar 

  • Lekagul B, McNeely JA (1977) Mammals of Thailand. Association for the Conservation of Wildlife, Bangkok

    Google Scholar 

  • Li H, Wilkins KT (2014) Patch or mosaic: bat activity responds to fine-scale urban heterogeneity in a medium-size city in the United States. Urban Ecosyst 17:1073–1031

    Google Scholar 

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

    Google Scholar 

  • MacSwiney MCG, Bolívar-Cimé B, Alfaro-Bates R, Ortíz-Díaz JJ, Clarke FM, Racey PA (2017) Pollen movement by the bat Artibeus jamaicensis (Chiroptera) in an agricultural landscape in the Yucatan Peninsula, Mexico. Mamm Res 62:189–193

    Google Scholar 

  • Maldonada MB, Lomáscolo SB, Vázquez DP (2013) The importance of pollinator generalization and abundance for the reproductive success of a generalist plant. PLoS One 10:e75482

    Google Scholar 

  • Manipphan N (2006) Durian cultivation and propagation king of fruits. Phetkarat press, Bangkok

    Google Scholar 

  • Marimuthu G, Rajan KE, Koilraj AJ, Isaac SS, Balasingh J (1998) Observations on the foraging behavior of a tent-roosting Megachiropteran bat Cynopterus sphinx. Biotrop 30:321–324

    Google Scholar 

  • Marténez-Rodríguez E, Aronne G (2000) Pollination failure in mediterranean Ruscus aculeatus L. Bot J Linn Soc 134:443–452

    Google Scholar 

  • Martén-Rodríguez S, Fenster CB (2008) Pollination ecology and breeding systems of five Gesneria species from Puerto Rico. Ann Bot 102:23–30

    PubMed  PubMed Central  Google Scholar 

  • McAney C, Sheil C, Sullivan C, Fairley J (1991) The analysis of bats droppings. Mammal Society, Occasional Publication No. 14, London

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

    Google Scholar 

  • Medellín RA, Equihua M, Amin MA (2000) Bat diversity and abundance as indicators of disturbance in neotropical rainforests. Conserv Biol 14:1666–1675

    Google Scholar 

  • Menz MHM, Phillips RD, Winfree R, Kremen C, Aizen MA, Johnson SD, Dixon KW (2011) Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms. Trends Plant Sci 16:4–12

    CAS  PubMed  Google Scholar 

  • Molur S, Marimuthu G, Srinivasulu C, Mistry S, Hutson AM, Bates PJJ, Walker S, Priya KP, Priya ARB (2002) Status of South Asian Chiroptera: Conservation assessment and management plan (CAMP) Workshop Report, Zoo Outreach Organisation, CBSG South Asia and WILD, Coimbatore

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Google Scholar 

  • Phusiri S (1986) Durian. Trang Agriculture College, Trang

  • Pokterng S, Kengpol A (2010) The forecasting of durian production quantity for consumption in domestic and international markets. Asian Inter J Sci Technol Product Manufact Engineer 3(3):7–18

    Google Scholar 

  • Queiroz JA, Quirino ZGM, Lopes AV, Machado IC (2016) Vertebrate mixed pollination system in Encholirium spectabile: a bromeliad pollinated by bats, opossum and hummingbirds in a tropical dry forest. J Arid Environ 125:21–30

    Google Scholar 

  • Rathcke BJ (2000) Hurricane causes resource and pollination limitation of fruit set in a bird-pollinated shrub. Ecol 81(7):1951–1958

    Google Scholar 

  • Ratto F, Simmons BI, Spake R, Zamora-Gutierrez V, MacDonald MA, Merriman JC, Tremlett CJ, Poppy GM, Peh KS-H, Dicks LV (2018) Global importance of vertebrate pollinators for plant reproductive success: a meta-analysis. Front Ecol Environ 16(2):82–90

    Google Scholar 

  • Russo D, Ancillotto L (2015) Sensitivity of bats to urbanization: a review. Mamm Biol 80:205–212

    Google Scholar 

  • Sikes RS, Gannon WL, Animal Care, Use Committee of the American Society of Mammalogists (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 92:235–253

    Google Scholar 

  • Srinivasulu C, Srinivasulu B (2002) Greater short-nosed fruit bat (Cynopterus sphinx) foraging and damage in vineyards in India. Acta Chirop 4(2):167–171

    Google Scholar 

  • Srithongchuay T, Bumrungsri S (2016) Specialized and facultative nectar-feeding bats have different effects on pollination networks in mixed fruit orchards, in southern Thailand. J Pollinat Ecol 19(14):98–103

    Google Scholar 

  • Srithongchuay T, Bumrungsri S, Sripao-Raya E (2008) The pollination ecology of the late-successional tree, Oroxylum indicum (Bignoniaceae) in Thailand. J Trop Ecol 24:477–484

    Google Scholar 

  • Srithongchuay T, Kremen C, Bumrungsri S (2016) Effects of forest and cave proximity on fruit set of tree crops in tropical orchards in Southern Thailand. J Trop Ecol 32(4):269–279

    Google Scholar 

  • Stebbins GL (1970) Adaptive radiation of reproductive characteristics in angiosperms I: pollination mechanisms. Annu Rev Ecol Syst 1:307–326

    Google Scholar 

  • Stewart AB, Dudash MR (2016) Field evidence of strong differential pollen placement by Old World bat-pollinated plants. Ann Bot 119:73–79

    PubMed  PubMed Central  Google Scholar 

  • Stewart AB, Dudash MR (2017) Flower-visiting bat species contribute unequally toward agricultural pollination ecosystem services in southern Thailand. Biotropica 49(2):239–248

    Google Scholar 

  • Storz JF, Kunz TH (1999) Cynopterus sphinx. Mamm Species 613:1–8

    Google Scholar 

  • Stroo A (2000) Pollen morphological evolution in bat pollinated plants. Plant Syst Evol 222:225–242

    Google Scholar 

  • Von Helversen O, Winkler L, Bestmann HJ (2000) Sulphur-containing “perfumes” attract flower-visiting bats. J Comp Physiol 186(2):143–153

    Google Scholar 

  • Wayo K, Phankaew C, Stewart AB, Bumrungsri S (2018) Bees are supplementary pollinators of self-compatible chiropterophilous durian. J Trop Ecol 34(1):41–52

    Google Scholar 

  • Yumoto T (2000) Bird-pollination of three Durio species (Bombacaceae) in a tropical rainforest in Sarawak, Malaysia. Am J Bot 87(8):1181–1188

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank durian orchard owners in both Nakhon Nayok and Chanthaburi provinces who helped us. Our appreciation and thanks to Prof. Warren Y. Brockelman, Institute of Molecular Biosciences, Mahidol University, for editing the manuscript. This research was supported and approved by the Committee on Animal Ethics, Mahidol University.

Role of the funding source

Funding sources did not play a role in the study design; collection, analysis or interpretation of data; the writing of the manuscript; or the decision to submit the manuscript for publication.

Author information

Authors and Affiliations

  1. Wildlife and Plant Research Center, Faculty of Environment and Resource Studies, Mahidol University, Salaya, 73170, Thailand

    Rattanawat Chaiyarat & Preeyaporn Koedrith

  2. Office of Natural Resources and Environmental Policy and Planning, Bangkok, 10400, Thailand

    Wannipa Boonma

Authors
  1. Rattanawat Chaiyarat
    View author publications

    Search author on:PubMed Google Scholar

  2. Wannipa Boonma
    View author publications

    Search author on:PubMed Google Scholar

  3. Preeyaporn Koedrith
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Rattanawat Chaiyarat.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chaiyarat, R., Boonma, W. & Koedrith, P. The role of pteropodid bats in pollination of durian (Durio zibethinus) in managed orchards in suburban habitat of Thailand. Urban Ecosyst 23, 97–106 (2020). https://doi.org/10.1007/s11252-019-00919-w

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11252-019-00919-w

Keywords