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Bees are supplementary pollinators of self-compatible chiropterophilous durian

Published online by Cambridge University Press:  28 January 2018

Kanuengnit Wayo
Affiliation:
Department of Biology, Faculty of Science, Prince of Songkla University, Hatyai, Songkhla 90112, Thailand
Chama Phankaew
Affiliation:
Department of Entomology, Faculty of Agriculture, Kasetsart University, Chatuchuk, Bangkok 10900, Thailand
Alyssa B. Stewart
Affiliation:
Department of Plant Science, Faculty of Science, Mahidol University, Bangkok 10400, Thailand
Sara Bumrungsri*
Affiliation:
Department of Biology, Faculty of Science, Prince of Songkla University, Hatyai, Songkhla 90112, Thailand

Abstract:

Nocturnally foraging insects may be supplementary pollinators to chiropterophilous plant species when bats are scarce. Given that insects are much smaller than bats, they may be more effective at transferring pollen for plant species with similar stamen and pistil lengths, such as the ‘Monthong’ durian cultivar. The present study clarifies the role of insects in pollinating the ‘Monthong’ cultivar by examining the floral biology, conducting pollination treatments on 19 trees and observing floral visitors in southern Thailand. Stigmas were receptive by 17h00, and over 50% of ‘Monthong’ anthers had dehisced by 17h30. Several bee species began foraging on flowers during the late afternoon, and the giant honey bee (Apis dorsata) continued to visit throughout the night. Our results show that at 4 wk after pollination, the highest fruit set occurred from hand-crossed pollination (13.5%), followed by open pollination (5.5%), insect pollination (3.3%) and automatic autogamy (2.0%), indicating that this cultivar is highly self-incompatible. Moreover, insects appear to be important pollinators of ‘Monthong’ durian in areas where nectar bats visit infrequently. One bee species in particular, Apis dorsata, commonly foraged on flowers at dusk and appears to be the most effective insect pollinator of durian. Our findings highlight that nocturnally foraging bees are capable of securing pollination for night-blooming plant taxa, even those typically considered to be bat-pollinated.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

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References

LITERATURE CITED

ACHARYA, P. R., RACEY, P. A., SOTTHIBANDHU, S. & BUMRUNGSRI, S. 2015. Feeding behavior of the dawn bat (Eonycteris spelaea) promotes cross pollination of economically important plants in Southeast Asia. Journal of Pollination Ecology 15:4450.CrossRefGoogle Scholar
AZIZ, S. A., CLEMENTS, G. R., MCCONKEY, K. R., SRITONGCHUAY, T., PATHIL, S., YAZID, A., HAFIZI, M. N., 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). Ecology and Evolution 7:86708684.CrossRefGoogle ScholarPubMed
BAWA, K. S. 1990. Plant–pollinator interactions in tropical rain forests. Annual Review of Ecology and Systematics 21:399422.CrossRefGoogle Scholar
BAWA, K. S., PERRY, D. R. & BEACH, J. H. 1985. Reproductive biology of tropical lowland rain forest trees. I. Sexual systems and incompatibility mechanisms. American Journal of Botany 72:331345.CrossRefGoogle Scholar
BOONGIRD, S. 1992. Biological studies of stingless bee, Trigona laeviceps Smith and its role in pollination of durian, Durio zibethinus L. cultivar Chanee. Ph.D dissertation, Kasetsart University, Thailand. 89 pp.Google Scholar
BREWBAKER, J. L. & KWACK, B. H. 1963. The essential role of calcium ion in pollen germination and pollen tube growth. American Journal of Botany 50:859865.CrossRefGoogle Scholar
BUMRUNGSRI, S., SRIPAORAYA, E., CHONGSIRI, T., SRIDITH, K. & RACEY, P. A. 2009. The pollination ecology of durian (Durio zibethinus, Bombacaceae) in southern Thailand. Journal of Tropical Ecology 25:8592.CrossRefGoogle Scholar
BUMRUNGSRI, S., DUNCAN, L., COLIN, H., SRIPAORAYA, E., KITPIPAT, K. & RACEY, P. A. 2013. The dawn bat, Eonycteris spelaea Dobson (Chiroptera: Pteropodidae) feeds mainly on pollen of economically important food plant in Thailand. Acta Chiropterologica 15:95104.CrossRefGoogle Scholar
CHATTAVONGSIN, R. & SIRIPHANICH, J. 1990. The relationship between fruit-stem stiffness and maturity of ‘Monthong’ durians, Durio zibethinus L. International Society for Horticultural Science Symposium on Tropical Fruit in International Trade. Wageningen. Acta Horticulturae 269:217222.CrossRefGoogle Scholar
COOK, S. A. & STANLEY, R. G. 1960. Tetrazolium chloride as an indicator of pine pollen germinability. Silvae Genetica 9:134136.Google Scholar
CRANE, E. 1991. Apis species of tropical Asia as pollinators and some rearing methods for them. Acta Horticulture 288:2948.CrossRefGoogle Scholar
EDWARDS, J., SMITH, G. P. & MCENTEE, M. H. F. 2015. Long-term time-lapse video provides near complete records of floral visitation. Journal of Pollination Ecology 16:91100.CrossRefGoogle Scholar
HONSHO, C., YONEMORI, K. & SUGIURA, A. 2004a. Durian floral differentiation and flowering habit. Journal of the American Society for Horticultural Science 129:4245.CrossRefGoogle Scholar
HONSHO, C., YONEMORI, K., SOMSRI, S., SUBHADRABANDHU, S. & SUGIURA, A. 2004b. Marked improvement of fruit set in Thai durian by artificial cross-pollination. Scientia Horticulturae 101:399406.CrossRefGoogle Scholar
HONSHO, C., SOMSRI, S., TAKUYA, T., YAMASHITA, K., YAPWATTANAPHUN, C. & YONEMORI, K. 2007a. Characterization of male reproductive organs in durian; anther dehiscence and pollen longevity. Journal of the Japanese Society for Horticultural Science 76:120124.CrossRefGoogle Scholar
HONSHO, C., SOMSRI, S., TETSUMURA, T., YAMASHITA, K. & YONEMORI, K. 2007b. Effective pollination period in durian (Durio zibethinus Murr.) and the factors regulating it. Scientia Horticulturae 111:193196.CrossRefGoogle Scholar
KEARNS, C. A. & INOUYE, D. W. 1993. Techniques for pollination biologists. The University Press of Colorado, Niwot. 583 pp.Google Scholar
KLEIN, A. M., VAISSIERE, B.E., CANE, J.H., STEFFAN-DEWENTER, I., CUNNINGHAM, S.A., KREMEN, C. & TSCHARNTKE, T. 2007. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society of London B: Biological Sciences 274:303313.Google ScholarPubMed
KOZAI, N., CHUSRI, O., CHUTINANTHAKUN, T., TONGTAO, S., HIGUCHI, H. & OGATA, T. 2014. Pollination and subsequent ovule development through fruit set in ‘Chanee’, ‘Monthong’, and ‘Kradumthong’ durian. Tropical Agriculture and Development 58:5865.Google Scholar
KREMEN, C., WILLIAMS, N. M. & THORP, R.W. 2002. Crop pollination from native bees at risk from agricultural intensification. Proceedings of the National Academy of Sciences USA 99:1681216816.CrossRefGoogle ScholarPubMed
LASSEN, K. M., OUEDRAOGO, M., DUPONT, Y. L., KJAER, E. D. & NIELSEN, L. R. 2017. Honey bees ensure the pollination of Parkia biglobosa in absence of bats. Journal of Pollination Ecology 20:2234.CrossRefGoogle Scholar
LIM, T. K. & LUDERS, L. 1998. Durian flowering, pollination and incompatibility studies. Annals of Applied Biology 132:151165.CrossRefGoogle Scholar
LO, K. H., CHEN, I. Z. & CHANG, T. L. 2007. Pollen-tube growth behavior in ‘Chanee’ and ‘Monthong’ durians (Durio zibethinus L.) after selfing and reciprocal crossing. Journal of Horticultural Science and Biotechnology 82:824828.CrossRefGoogle Scholar
MORTON, J. 1987. Durian. Pp. 287291 in Morton, J. F. (ed.). Fruits of warm climates. Florida Flair Books, Miami.Google Scholar
OLLERTON, J., WINFREE, R. & TARRANT, S. 2011. How many flowering plants are pollinated by animals? Oikos 120:321326.CrossRefGoogle Scholar
PAULL, R. E. & KETSA, S. 2011. Durian: postharvest quality-maintenance guidelines. University of Hawaii at Manoa, College of Tropical Agriculture and Human Resources. Fruit, Nut, and Beverage Crops Publication F_N-27.Google Scholar
POTTS, S. G., BIESMEIJER, J. C., KREMEN, C., NEUMANN, P., SCHWEIGER, O. & KUNIN, W. E. 2010. Global pollinator declines: trends, impacts and drivers. Trends in Ecology and Evolution 25:345353.CrossRefGoogle ScholarPubMed
SALAKPETCH, S. 2005. Durian (Durio zibethinus L.) flowering, fruit set and pruning. Pp. 1726 in Nagao, M. A. (ed.). Fifteenth Annual International Tropical Fruit Conference Proceedings. Hawaii Tropical Fruit Growers, Hawaii.Google Scholar
SALAKPETCH, S., CHANDRAPARNNIK, S. & HIRANPRADIT, H. 1992. Pollen grains and pollination in durian, Durio zibethinus Murr. Acta Horticulturae 321:636640.CrossRefGoogle Scholar
SOEPADMO, E. & EOW, B. K. 1976. The reproductive biology of Durio zibethinus Murr. Gardens’ Bulletin, Singapore 29:2533.Google Scholar
SOMSRI, S. 2008. Durian: Southeast Asia's king of fruits. Chronica Horticulturae 48:1922.Google Scholar
SRITHONGCHUAY, T., BUMRUNGSRI, S. & SRIPAO-RAYA, E. 2008. The pollination ecology of the late-successional tree, Oroxylum indicum (Bignoniaceae) in Thailand. Journal of Tropical Ecology 24:477484.CrossRefGoogle Scholar
SRITONGCHUAY, T., KREMEN, C., & BUMRUNGSRI, S. 2016. Effects of forest and cave proximity on fruit set of tree crops in tropical orchards in Southern Thailand. Journal of Tropical Ecology 32:269279.CrossRefGoogle Scholar
STEWART, A. B. & DUDASH, M. R. 2016. Differential pollen placement on an Old World nectar bat increases pollination efficiency. Annals of Botany 117:145152.CrossRefGoogle Scholar
STEWART, A. B. & DUDASH, M. R. 2017. Flower-visiting bat species contribute unequally toward agricultural pollination ecosystem services in southern Thailand. Biotropica 49:239248.CrossRefGoogle Scholar
SUBHADRABANDHU, S. & KETSA, S. 2001. Durian – king of tropical fruit. CABI, Wallingford. 204 pp.CrossRefGoogle Scholar
SUWANNAPONG, G., BENBOW, M. E. & NIEH, J. C. 2012. Biology of Thai honeybees: natural history and threats. Pp. 198 in Florio, R. M. (ed.). Bees: biology, threats and colonies. Nova Science Publishers, New York.Google Scholar
THOMSON, J. D. & BARRETT, S. C. H. 1981.Temporal variation of gender in Aralia hispida Vent. (Araliaceae). Evolution 35:10941107.CrossRefGoogle ScholarPubMed
WILLIAMS, R. R. 1965. The effect of summer nitrogen applications on the quality of apple blossom. Journal of Horticultural Science 40:3141.CrossRefGoogle Scholar
WONGSIRI, S., CHANCHAO, C., DEOWANISH, S., AEMPRAPA, S., CHAIYAWONG, T., PETERSEN, S. & LEEPITAKRAT, S. 2000. Honey bee diversity and beekeeping in Thailand. Bee World 81:2029.CrossRefGoogle Scholar
ZEISLER, M. 1938. Uber die Abgrenzung der eigentlichen Narbenflache mit Hilfe von Reaktionen. Beihefte zum Botanisches Zentralblatt A. 58:308318.Google Scholar