Civet pollination in Mucuna birdwoodiana (Fabaceae: Papilionoideae)

Abstract

Inferring pollinators from floral traits is problematic because many flowers do not conform to a prescribed phenotype by which they may be assigned to any one particular pollination ‘syndrome.’ This necessitates empirical investigation to confirm pollinator relationships. Mucuna birdwoodiana is thought to be fruit bat-pollinated on account of its malodorous, pale green, gullet-type flowers, but we sought to clarify its pollination system through direct examination. This study was conducted in Hong Kong. Flowers of this species undergo “explosive opening” during pollination. Bagging experiments were conducted to check the necessity of this mechanism to achieve fruit set. Floral visitors were recorded by video camera traps and nectar secretion patterns were surveyed. Flowers do not open automatically and unopened flowers do not fructify. Masked palm civets, Paguma larvata, and introduced Pallas’s squirrels, Callosciurus erythraeus styani, were observed opening flowers, and fruits were found to form on flowers opened by both species. Paguma larvata opened flowers more frequently and less destructively than C. e. styani. The nectar is sucrose-dominant with no variation in nectar volume nor sugar concentration throughout the day. Pollination success in M. birdwoodiana is dependent on flower-opening animals. The primary pollinator of M. birdwoodiana is P. larvata, not fruit bats as had been suggested by a suite of supposedly adaptive floral traits.

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References

  1. Agostini K, Sazima M, Sazima I (2006) Bird pollination of explosive flowers while foraging for nectar and caterpillars. Biotropica 38:674–678

    Article  Google Scholar 

  2. Agostini K, Sazima M, Galetto L (2011) Nectar production dynamics and sugar composition in two Mucuna species (Leguminosae, Faboideae) with different specialized pollinators. Naturwissenschaften 98:933–942

    Article  CAS  PubMed  Google Scholar 

  3. 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 15:317–327

    Article  CAS  PubMed  Google Scholar 

  4. Chen G, Zhang R, Dong K, Gong W, Ma Y (2012) Scented nectar of Mucuna sempervirens and its ecological function. Sheng Wu Duo Yang Xing 20:360–367 (in Chinese with English Abstract)

    CAS  Google Scholar 

  5. Corlett RT (1998) Frugivory and seed dispersal by vertebrates in the Oriental (Indomalayan) Region. Biol Rev 73:413–448

    Article  CAS  PubMed  Google Scholar 

  6. Corlett RT (2004) Flower visitors and pollination in the Oriental (Indomalayan) region. Biol Rev 79:497–532

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  8. Corlett RT (2007) What’s so special about Asian tropical forests? Curr Sci 93:1551–1557

    Google Scholar 

  9. Cotton PA (2001) The behavior and interactions of birds visiting Erythrina fusca flowers in the Colombian Amazon. Biotropica 33:662–669

    Article  Google Scholar 

  10. Cox PA, Elmqvist T, Pierson ED, Rainey WE (1991) Flying foxes as strong interactors in south pacific island ecosystems: A conservation hypothesis. Conserv Biol 5:448–454

    Article  Google Scholar 

  11. Duckworth JW, Timmins RJ, Molur S (2017) Callosciurus erythraeus. The IUCN red list of threatened species 2017. e.T3595A22254356. https://dx.doi.org/10.2305/IUCN.UK.2017-2.RLTS.T3595A22254356.en. Accessed 15 May 2018

  12. Dudgeon D, Corlett R (2004) The ecology and biodiversity of Hong Kong. Friends of Country Parks and Joint Publishing (HK) Co. Ltd., Hong Kong.

    Google Scholar 

  13. Fægri K, van der Pijl L (1979) The principles of pollination ecology, 3rd edn. Pergamon Press, Oxford

    Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  15. Goswami A, Friscia A (2010) Carnivoran evolution: new views on phylogeny, form and function. Cambridge University Press, Cambridge

    Google Scholar 

  16. Grand TI (1972) A mechanical interpretation of terminal branch feeding. J Mammal 53:198–201

    Article  Google Scholar 

  17. Hargreaves AL, Johnson SD, Nol E (2004) Do floral syndromes predict specialization in plant pollination systems? An experimental test in an “ornithophilous” African Protea. Oecologia 140:295–301

    Article  PubMed  Google Scholar 

  18. Ho C.-Y. (1994) The ecology of exotic squirrels (Sciuridae) in Hong Kong, with special reference to Callosciurus erythraeus thai (Kloss). Master’s Thesis, Hong Kong University, Hong Kong.

  19. Hong Kong Herbarium and South China Botanical Garden (2008) Flora of Hong Kong, Volume 2. Agriculture, Fisheries and Conservation Department, Government of the Hong Kong Special Administrative Region, Hong Kong SAR.

  20. Hopkins HCF, Hopkins MJG (1993) Rediscovery of Mucuna macropoda (Leguminosae: Papilionoideae), and its pollination by bats in Papua New Guinea. Kew Bull 48:297–305

    Article  Google Scholar 

  21. Janson CH, Terborgh J, Emmons LH (1981) Non-flying mammals as pollinating agents in the Amazonian forest. Biotropica 13:1–6

    Article  Google Scholar 

  22. Johnson CM, Pauw A (2014) Adaptation for rodent pollination in Leucospermum arenarium (Proteaceae) despite rapid pollen loss during grooming. Ann Bot 113:931–938

    Article  PubMed  PubMed Central  Google Scholar 

  23. Kay KM, Schemske DW (2003) Pollinator assemblages and visitation rates for 11 species of Neotropical Costus (Costaceae). Biotropica 35:198–207

    Google Scholar 

  24. Kobayashi S (2017) Mammal-dependent pollination system of Mucuna macrocarpa (Fabaceae). Ph.D. Thesis, University of the Ryukyus, Okinawa, Japan.

  25. Kobayashi S, Denda T, Mashiba S, Iwamoto T, Doi T, Izawa M (2015) Pollination partners of Mucuna macrocarpa (Fabaceae) at the northern limit of its range. Plant Species Biol 30:272–278

    Article  Google Scholar 

  26. Kobayashi S, Denda T, Liao C-C, Wu S-H, Lin Y-H, Izawa M (2017) Squirrel pollination of Mucuna macrocarpa (Fabaceae) in Taiwan. J Mammal 98:533–541

    Google Scholar 

  27. Kobayashi S, Denda T, Liao C-C, Lin Y-H, Liu W-T, Izawa M (2018a) Comparison of visitors and pollinators of Mucuna macrocarpa between urban and forest environments. Mammal Stud 43:219–228

    Article  Google Scholar 

  28. Kobayashi S, Denda T, Liao C-C, Lin Y-H, Wu S-H, Izawa M (2018b) Floral traits of mammal-pollinated Mucuna macrocarpa (Fabaceae): implications for generalist-like pollination systems. Eco Evol 8:8607–8615

    Article  Google Scholar 

  29. Kobayashi S, Denda T, Liao C-C, Placksanoi J, Waengsothorn S, Aryuthaka C, Pnaha S, Izawa M (2018c) Regional differences in mammalian pollinators of Mucuna macrocarpa (Leguminosae): a review. Trop Nat Hist 8:135–146

    Google Scholar 

  30. Kobayashi S, Hirose E, Denda T, Izawa M (2018d) Who can open the flower? Assessment of the flower opening force of mammal-pollinated Mucuna macrocarpa. Plant Species Biol 33:312–316

    Article  Google Scholar 

  31. Lack A (1977) Genets feeding on nectar of Maranthes polyandra in northern Ghana. Afr J Ecol 15:233–234

    Article  Google Scholar 

  32. Lau M (2004) Bat pollination in the climber Mucuna birdwoodiana. Porcupine 30:11–12.

    Google Scholar 

  33. Lau M (2012) Masked palm civet Paguma larvata apparently feeding on nectar of Mucuna birdwoodiana. Small Carnivore Conserv 47:79–81

    Google Scholar 

  34. Moura TM, Vatanparast M, Tozzi AMGA, Forest F, Wilmot-Dear CM, Simon MF, Mansano VF, Kajita T, Lewis GP (2016) A molecular phylogeny and new infrageneric classification of Mucuna Adans. (Leguminosae-Papilionoideae) including insights from morphology and hypotheses about biogeography. Int J Plant Sci 177:76–89

    Article  Google Scholar 

  35. Ollerton J, Alarcōn R, Waser NM, Price MV, Watts S, Cranmer L, Hingston A, Peter CI, Rotenberry J (2009) A global test of the pollination syndrome hypothesis. Ann Bot 103:1471–1480

    Article  PubMed  PubMed Central  Google Scholar 

  36. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326

    Article  Google Scholar 

  37. Parachnowitsch AL, Kessler A (2010) Pollinators exert natural selection on flower size and floral display in Penstemon digitalis. New Phytol 188:393–402

    Article  PubMed  Google Scholar 

  38. R Core Team R (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  39. Rabinowitz AR (1991) Behavior and movements of sympatric civet species in Huai Ka Khaeng Wildlife Sanctuary, Thailand. J Zool 223:281–298

    Article  Google Scholar 

  40. Rivera-Marchand B, Ackerman JD (2006) Bat pollination breakdown in the Caribbean columnar cactus Pilosocereus royenii. Biotropica 38:635–642

    Article  Google Scholar 

  41. Rosas-Guerrero V, Aguilar R, Martén-Rodríguez S, Ashworth L, Lopezaraiza-Mikel M, Bastida JM, Quesada M (2014) A quantitative review of pollination syndromes: do floral traits predict effective pollinators? Ecol Lett 17:388–400

    Article  PubMed  Google Scholar 

  42. Schrire BD (2005) Tribe Phaseoleae. In: Lewis G, Schrire BD, Mackinder B, Lock M (eds) Legumes of the World. Royal Botanic Gardens, Kew, London, pp 393–431

    Google Scholar 

  43. Shek C.-T. (2006) A field guide to the terrestrial mammals of Hong Kong. Agriculture, Fisheries and Conservation Department, Friends of the Country Parks and Cosmos Books Ltd., Hong Kong.

    Google Scholar 

  44. Steenhuisen ST, Balmer A, Zoeller K, Kuhn N, Midgley J, Hansen D, Johnson SD (2015) Carnivorous mammals feed on nectar of Protea species (Proteaceae) in South Africa and likely contribute to their pollination. Afr J Ecol 53:602–605

    Article  Google Scholar 

  45. Tandon R, Shivanna KR, Mohanram HY (2003) Reproductive biology of Butea monosperma (Fabaceae). Ann Bot 92:715–723

    Article  PubMed  PubMed Central  Google Scholar 

  46. Toyama C, Kobayashi S, Denda T, Nakamoto A, Izawa M (2012) Feeding behavior of the Orii’s flying-fox, Pteropus dasymallus inopinatus, on Mucuna macrocarpa and related explosive opening of petals, on Okinawajima Island in the Ryukyu Archipelago, Japan. Mammal Study 37:205–212

    Article  Google Scholar 

  47. van der Pijl L (1941) Flagelliflory and cauliflory as adaptations to bats in Mucuna and other plants. Ann Bot Gard Buitenzorg 51:83–93

    Google Scholar 

  48. van der Pijl L (1961) Ecological aspects of flower evolution. II. Zoophilous flower classes. Evolution 15:44–59

    Google Scholar 

  49. Wester P, Stanway R, Pauw, (2009) Mice pollinate the Pagoda Lily, Whiteheadia bifolia (Hyacinthaceae) —First field observations with photographic documentation of rodent pollination in South Africa. S Afr J Bot 75:713–719

    Article  Google Scholar 

  50. Willmer P (2011) Pollination and floral ecology. Princeton University Press, New Jersey

    Google Scholar 

  51. Wilmot-Dear CM (1984) A revision of Mucuna (Leguminosae-Phaseoleae) in China and Japan. Kew Bull 39:23–65

    Article  Google Scholar 

  52. Wilmot-Dear CM (1990) A revision of Mucuna (Leguminosae-Phaseoleae) in the Pacific. Kew Bull 45:1–35

    Article  Google Scholar 

  53. Wu ZY, Raven PH, Hong DY (2010) Flora of China. vol. 10 (Fabaceae). Science Press, Beijing, China and Missouri Botanical Garden Press, St. Louis.

  54. Yumoto T, Momose K, Nagamasu H (2000) A new pollination syndrome–squirrel pollination in a tropical rain forest in Lambir Hills National Park, Sarawak, Malaysia. Tropics 9:147–151

    Article  Google Scholar 

  55. Zhou YB, Zhang J, Slade E, Zhang L, Palomares F, Chen J, Wang XM, Zhang SY (2008) Dietary shifts in relation to fruit availability among masked palm civet (Paguma larvata) in central China. J Mammal 89:435–447

    Article  Google Scholar 

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Acknowledgements

We are grateful to Michael Lau for providing advice and to Kadoorie Farm and Botanic Garden for allowing us to conduct this study. We also thank Shinichi Gima (Center for Research Advancement and Collaboration, University of the Ryukyus) for running the HPLC analysis. This study was partly supported by JSPS KAKENHI (Grant No. 16H05771).

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Correspondence to Shun Kobayashi.

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Electronic supplementary material 1 (MP4 2569 kb) Video S1 Explosive opening behavior of masked palm civet (Paguma larvata) on Mucuna birdwoodiana flowers.

Electronic supplementary material 2 (MP4 9024 kb) Video S2 Explosive opening behavior of Pallas’s squirrel (Callosciurus erythraeus styani) on Mucuna birdwoodiana flowers.

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Kobayashi, S., Gale, S.W., Denda, T. et al. Civet pollination in Mucuna birdwoodiana (Fabaceae: Papilionoideae). Plant Ecol 220, 457–466 (2019). https://doi.org/10.1007/s11258-019-00927-y

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Keywords

  • Explosive opening
  • Mucuna
  • Non-flying mammal
  • Paguma larvata
  • Pollination
  • Tropical Asia