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Variation in reproductive output of Ficus superba despite aseasonal reproduction

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Abstract

Studies of Ficus reproductive phenology have focused on documenting its seasonality and dependence on meteorological factors. While there have been reports that duration of receptivity of syconia can be prolonged in response to pollinator limitation, the effect of pollination rate on the duration of phenological phases over a year has not been examined. Percentage of unpollinated syconia, number of foundresses per pollinated syconium, duration of receptivity, frequency of single-sex broods, crop size, frequency of parasitisation, persistence of ripe syconia, and mass abscission were recorded for Ficus superba at the crop level. Percentage of unpollinated syconia is significantly negatively correlated with the number of foundresses per syconium, and positively correlated with the duration of receptivity, and the persistence of ripe syconia. Despite the absence of sesonality in reproduction, the occurrences of receptive syconia and ripe syconia showed unimodal and bimodal peaks, respectively, owing to prolongment of these phases. This is attributable to meteorological factors, which are hypothesized to influence pollinator dispersal, or population dynamics, and thus pollination rate. This highlights the overlooked significance of pollinator, and possibly frugivore phenology in accounting for Ficus reproduction, and suggests that while reproduction may be aseasonal, reproductive potential may not be. Furthermore, crop size was shown to affect the number of foundresses per syconium, duration of receptivity, and persistence of ripe syconia. Possible adaptive value of producing crops of different sizes is discussed.

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References

  1. Ansett MC, Bronstein JL, Hossaert-McKey M (1996) Resource allocation: a conflict in fig/fig wasp mutualism? J Evol Biol 9:417–428. doi:10.1046/j.1420-9101.1996.9040417.x

  2. Anstett MC, Gibernau M, Hossaert-McKey M (1998) Partial avoidance of female inflorescences of a dioecious fig by their mutualistic pollinating wasps. Proc R Soc Lond Biol Sci 265:45–50. doi:10.1098/rspb.1998.0262

  3. Anstett MC, Hossaert-McKey M, McKey D (1997) Modeling the persistence of small populations of strongly interdependent species: figs and fig wasps. Conserv Biol 11:204–213. doi:10.1046/j.1523-1739.1997.95436.x

  4. Anstett MC, Kjellberg F, Bronstein JL (1996) Waiting for wasps: consequences for pollination dynamics of Ficus pertusa L. J Biogeogr 23:459–466. doi:10.1111/j.1365-2699.1996.tb00007.x

  5. Anstett MC, Michaloud G, Kjellberg F (1995) Critical population size for fig/wasp mutualism in a seasonal environment: effect and evolution of the duration of female receptivity. Oecologia 103:453–461. doi:10.1007/BF00328683

  6. Batschelet E (1981) Circular statistics in biology. In: Sibson R, Cohen JE (eds) Mathematics in biology. Academic Press, London

  7. Berg CC, Corner EJH (2005) Moraceae: Ficeae. In: Nooteboom HP (ed) Flora Malesiana, series I, part 2, vol 17. The National Herbarium Nederland, Leiden, pp 610–614

  8. Borchert R (1983) Phenology and control of flowering in tropical trees. Biotropica 15:81–89. doi:10.2307/2387949

  9. Borchert R (1998) Responses of tropical trees to rainfall seasonality and its long-term changes. Clim Change 39:381–393. doi:10.1023/A:1005383020063

  10. Boucek Z (1988) Australasian Chalcidoidea (Hymenoptera): a biosystematic revision of genera of fourteen families, with a reclassification of species. C.A.B. International, Wallingford, Oxon

  11. Bronstein JL (1987) Maintenance of species-specificity in a neotropical fig-pollinator wasp mutualism. Oikos 48:39–46. doi:10.2307/3565686

  12. Bronstein JL (1988) Limits to fruit production in a monoecious fig: consequences of an obligate mutualism. Ecology 69:207–214. doi:10.2307/1943176

  13. Bronstein JL (1989) A mutualism at the edge of its range. Experientia 45:622–639. doi:10.1007/BF01975679

  14. Bronstein JL, Hoffmann K (1996) Spatial and temporal variation in frugivory at a neotropical fig, Ficus pertusa. Oikos 49:261–268. doi:10.2307/3565760

  15. Bronstein JL, Hossaert-McKey M (1995) Hurricane Andrew and a Florida fig pollination mutualism: resilience of an obligate interaction. Biotropica 27:373–381. doi:10.2307/2388922

  16. Bronstein JL, Patel A (1992) Causes and consequences of within-tree phenological patterns in the Florida strangling fig, Ficus aurea (Moraceae). Am J Bot 79:41–48. doi:10.2307/2445195

  17. Chapman CA, Chapman LJ, Zanne AE, Poulsen JR, Clark CJ (2005) A 12-year phenological record of fruiting: Implications for frugivore populations and indicators of climate change. In: Dew JL, Boubli JP (eds) Tropical fruits and frugivores: the search for strong interactors. Springer, The Netherlands, pp 75–92

  18. Chia LS, Foong SF (1991) Climate and weather. In: Chia LS, Rahman A, Tay DBH (eds) The biophysical environment of Singapore. Singapore University Press, Singapore, pp 13–49

  19. Compton SG, Ellwood MDF, Davis AJ, Welch K (2000) The flight heights of chalcid wasps (Hymenoptera, Chalcidoidea) in lowland Bornean rain forest: fig wasps are high fliers. Biotropica 32:522–525

  20. Corlett RT, Boudville V, Seet K (1990) Seed and wasp production in five fig species (Ficus, Moraceae). Malay Nat J 44:97–102

  21. Corlett RT, Lafrankie JV Jr (1998) Potential impacts of climate change on tropical asian forests through an influence on phenology. Clim Change 39:439–453. doi:10.1023/A:1005328124567

  22. Fenner M (1998) The phenology of growth and reproduction in plants. Perspect Plant Ecol Evol Syst 1:78–91. doi:10.1078/1433-8319-00053

  23. Foo SL (2002) Singapore facts and pictures 2002. Ministry of Information, Communications and the Arts, Singapore

  24. Galil J, Eisikowitch D (1968) Flowering cycles and fruit types of Ficus sycomorus in Israel. New Phytol 67:745–758. doi:10.1111/j.1469-8137.1968.tb05497.x

  25. Harrison RD (2000) Repercussions of El Niño: Drought causes extinction and breakdown of mutualism in Borneo. Proc Proc R Soc Lond Biol Sci 267:911–915. doi:10.1098/rspb.2000.1089

  26. Harrison RD, Yamamura N (2003) A few more hypotheses for the evolution of dioecy in figs (Ficus, Moraceae). Oikos 100:628–635. doi:10.1034/j.1600-0706.2003.11829.x

  27. Harrison RD, Yamamura N, Inoue T (2000) Phenology of a common roadside fig in Sarawak. Ecol Res 15:47–61. doi:10.1046/j.1440-1703.2000.00319.x

  28. Herre EA (1989) Coevolution of reproductive characteristics in 12 species of new world figs and their pollinator wasps. Experientia 14:637–647. doi:10.1007/BF01975680

  29. Herre EA (1996) An overview of studies on a community of Panamanian figs. J Biogeogr 23:593–607. doi:10.1111/j.1365-2699.1996.tb00020.x

  30. Hossaert-McKey M, Gibernau M, Frey JE (1994) Chemosensory attraction of fig wasps to substances produced by receptive figs. Entomol Exp Appl 70:185–191. doi:10.1007/BF02380526

  31. IPCC (2007) Climate change 2007: The physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA

  32. Janzen DH (1979a) How to be a fig? Annu Rev Ecol Syst 10:13–51. doi:10.1146/annurev.es.10.110179.000305

  33. Janzen DH (1979b) How many babies do figs pay for babies? Biotropica 11:48–50. doi:10.2307/2388172

  34. Khadari B, Gibernau M, Ansett MC, Kjellberg F, Hossaert-McKey M (1995) When figs wait for pollinators: the length of fig receptivity. Am J Bot 82:992–999. doi:10.2307/2446228

  35. Kjellberg F, Doumesche B, Bronstein JL (1988) Longevity of a fig wasp. In: Proceedings of the Koninklijke Nederlandse Akademie Wetenschappen series C, vol 91(2), pp 117–122

  36. Kjellberg F, Maurice S (1989) Seasonality in the reproductive phenology of Ficus: its evolution and consequences. Experientia 45:653–660. doi:10.1007/BF01975682

  37. Korine C, Kalko EKV EA, Herre EA (2000) Fruit characteristics and factors affecting fruit removal in a Panamanian community of stranglers. Oecologia 123:560–568. doi:10.1007/PL00008861

  38. Lambert FR, Marshall AG (1991) Keystone characteristics of bird dispersed Ficus in a Malaysian lowland rain forest. J Ecol 79:793–809. doi:10.2307/2260668

  39. Leighton M, Leighton DR (1983) Vertebrate responses to fruiting seasonality within a Bornean rain forest. In: Sutton SL, Whitmore TC, Chadwick AC (eds) Tropical rain forest: ecology and management. Blackwell, Oxford, pp 181–196

  40. Milton K (1991) Leaf change and fruit production in six neotropical Moraceae species. J Ecol 79:1–26. doi:10.2307/2260781

  41. Milton K, Windsor DM, Morrison DW, Estribi MA (1982) Fruiting phenologies of two Neotropical Ficus species. Ecology 63:752–762. doi:10.2307/1936796

  42. Nason JD, Herre EA, Hamrick JL (1998) The breeding structure of a tropical keystone plant resource. Nature 391:685–687. doi:10.1038/35607

  43. Pereira RAS, Rodrigues E, de Oliveira Menezes A Jr (2007) Phenological patterns of Ficus citrifolia (Moraceae) in a seasonal humid-subtropical region in southern Brazil. Plant Ecol 188:265–275. doi:10.1007/s11258-006-9161-0

  44. Ragusa-Netto J (2002) Fruiting phenology and consumption by birds in Ficus calyptroceras (Miq.) Miq. (Moraceae). Braz J Biol 62:339–346

  45. Shanahan M, So S, Compton SG, Corlett R (2001) Fig-eating by vertebrate frugivores: a global review. Biol Rev Camb Philos Soc 76:529–572

  46. Smith CM, Bronstein JL (1996) Site variation in reproductive synchrony in three neotropical figs. J Biogeogr 23:477–486. doi:10.1111/j.1365-2699.1996.tb00009.x

  47. Terborgh J (1986) Keystone plant resources in the tropical forest. In: Soulé ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer Associates, Sunderland, Massachusetts, U.S.A., pp 330–344

  48. Tweheyo M, Lye KA (2003) Phenology of figs in Budongo forest Uganda and its importance for chimpanzee diet. Afr J Ecol 41:306–316. doi:10.1111/j.1365-2028.2003.00475.x

  49. Wang RW, Yang CY, Zhao GF, Yang JX (2005) Fragmentation effects on diversity of wasp community and its impact on fig/fig wasp interaction in Ficus racemosa L. J Integr Plant Biol 47:20–26

  50. Ware AB, Compton SG (1994a) Dispersal of adult female fig wasps 1. Arrivals and departures. Entomol Exp Appl 73:221–229. doi:10.1007/BF02382473

  51. Ware AB, Compton SG (1994b) Dispersal of adult female fig wasps 2. Movement between trees. Entomol Exp Appl 73:231–238. doi:10.1007/BF02382474

  52. Ware AB, Kaye PT, Compton SG, van Noort S (1993) Fig volatiles: their roles in attracting pollinators and maintaining pollinator specificity. Plant Syst Evol 186:147–156. doi:10.1007/BF00940794

  53. West SA, Herre EA, Compton SG, Godfray HCJ, Cook JM (1997) A comparative study of virginity in fig wasps. Anim Behav 54:437–450. doi:10.1006/anbe.1996.0494

  54. Wiebes JT (1994) The Indo-Australian Agaoninae (pollinators of figs). Verhandelingen der Koninklijke Nederlandse akademie van wetenschappen. Afdeling natuurkunde. Tweede Reeks, Deel 92. North-Holland, Amsterdam

  55. Windsor DM, Morrison DW, Estribi MA, de Leon B (1989) Phenology of fruit and leaf production by ‘strangler’ figs on Barro Colorado Island, Panama. Experientia 45:647–653. doi:10.1007/BF01975681

  56. Yang D, Peng Y, Zhao T, Wang Q, Xu L (2005) Relationship between activity of Ceratosolen fusciceps and seasonal changes of the seed number of Ficus raceomsa. Scientia Silvae Sinicae 41:25–29

  57. Yang D, Wang R, Song Q, Zhang G, Zhao T (2000) Rule of seasonal changes of the Ceratosolen sp. in the tropical rainforest of Xishuangbanna, China. For Res 13:477–484

  58. Zhang G, Song Q, Yang D (2006) Phenology of Ficus racemosa in Xishuangbanna, southwest China. Biotropica 38:334–341. doi:10.1111/j.1744-7429.2006.00150.x

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Acknowledgements

We would like to thank Dr Rhett D. Harrison for sharing his expertise in identifying the fig wasps, and to express our gratitude to Dr Richard T. Corlett and Dr Von Bing Yap for having provided useful criticisms and suggestions. Ms Sharon Sim also deserves thanks for the generous field assistance rendered. We would also like to thank anonymous reviewers for making specific suggestions to allow us to improve the clarity and content of the manuscript.

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Correspondence to Chow Khoon Yeo.

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Yeo, C.K., Tan, H.T.W. Variation in reproductive output of Ficus superba despite aseasonal reproduction. Plant Ecol 205, 235 (2009). https://doi.org/10.1007/s11258-009-9613-4

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Keywords

  • Crop size
  • Fig phenology
  • Pollination rate
  • Reproduction
  • Seasonality