, Volume 22, Issue 4, pp 217–227 | Cite as

‘Push’ and ‘pull’ responses by fig wasps to volatiles released by their host figs

  • Ding Gu
  • Stephen G. Compton
  • Yanqiong Peng
  • Darong YangEmail author
Research Paper


In the specific mutualism between fig trees (Ficus) and their obligate pollinating fig wasps (Agaonidae), it is crucial that fig wasps can recognize the developmental stages of their host figs. However, the responses of fig wasps to volatiles released from figs during their developmental phases are less clearly understood and are the focus of this study. We extracted and identified the volatiles released from the figs of Ficus curtipes throughout their development. Using Y-tube choice experiments, we also compared the behavioural responses of the tree’s pollinator (Eupristina sp.) to figs at different developmental stages, and compared these results to those obtained by trapping fig wasps as they arrived at a tree with a developing fig crop. The chemical composition of the fig volatiles changed during fig development with the blends exhibiting clear segregation among figs at different developmental phases. Male phase figs had the most distinct blend. Fig wasp females were preferentially attracted to receptive figs, but figs at most other developmental phases were also attractive. Conversely, male phase figs had a repellent effect. These results were supported by the behaviour of the wasps under natural conditions, with small numbers of fig wasps arriving at the tree before and after receptive figs were present. These results indicate a more complex relationship between fig volatiles and fig wasp behaviour than previously realized, with volatiles mediating both the initial meeting of the mutualists to achieve pollination and egg laying and the subsequent departure of the next generation of fig wasps. This offers an explanation for the specialization and long-term coexistence of figs and fig wasps.


Agaonidae Behavioural response Chemical communication Ficus Mutualism Obligate pollinator 



We thank Zhen Yu for help in chemical analyses, and the two anonymous reviewers for suggestions and criticisms. Funding for this work was supported by the Chinese Natural Science Foundation (30970403 and 30970439).


  1. Ahmed S, Compton SG, Butlin RK, Gilmartin PM (2009) Wind-borne insects mediate directional pollen transfer between desert fig trees 160 kilometers apart. Proc Natl Acad Sci USA 106:20342–20347PubMedCrossRefGoogle Scholar
  2. Anstett MC, Hossaert-McKey M, McKey D (1997) Modeling the persistence of small populations of strongly interdependent species: figs and fig wasps. Conserv Biol 11:204–213CrossRefGoogle Scholar
  3. Berg CC (1989) Classification and distribution of Ficus. Experientia 45:605–611CrossRefGoogle Scholar
  4. Biere A, Honders SC (2006) Coping with third parties in a nursery pollination mutualism: Hadena bicruris avoids oviposition on pathogen-infected, less rewarding Silene latifolia. New Phytol 169:719–727PubMedCrossRefGoogle Scholar
  5. Borges RM, Bessière JM, Hossaert-McKey M (2008) The chemical ecology of seed dispersal in monoecious and dioecious figs. Funct Ecol 22:484–493CrossRefGoogle Scholar
  6. Boucher DH, James S, Keeler KH (1982) The ecology of mutualism. Annu Rev Ecol Syst 13:315–347CrossRefGoogle Scholar
  7. Bronstein JL (1994) Our current understanding of mutualism. Q Rev Biol 69:31–51CrossRefGoogle Scholar
  8. Bronstein JL (2001) The exploitation of mutualisms. Ecol Lett 4:277–287CrossRefGoogle Scholar
  9. Bronstein JL (2009) The evolution of facilitation and mutualism. J Ecol 97:1160–1170CrossRefGoogle Scholar
  10. Chen C, Song Q (2008) Responses of the pollinating wasp Ceratosolen solmsi marchali to odor variation between two floral stages of Ficus hispida. J Chem Ecol 34:1536–1544PubMedCrossRefGoogle Scholar
  11. Chen C, Song QS, Proffit M, Bessière JM, Li ZB, Hossaert-McKey M (2009) Private channel: a single unusual compound assures specific pollinator attraction in Ficus semicordata. Funct Ecol 23:941–950CrossRefGoogle Scholar
  12. Cook JM, Rasplus JY (2003) Mutualists with attitude: coevolving fig wasps and figs. Trends Ecol Evol 18:241–248CrossRefGoogle Scholar
  13. Dudareva N, Negre F, Nagegowda D, Orlova I (2006) Plant volatiles: recent advances and future perspectives. Crit Rev Plant Sci 25:417–440CrossRefGoogle Scholar
  14. Dunn DW, Yu DW, Ridley J, Cook JM (2008) Longevity, early emergence and body size in a pollinating fig wasp—implications for stability in a fig-pollinator mutualism. J Anim Ecol 77:927–935PubMedCrossRefGoogle Scholar
  15. Galil J, Eisikowitch D (1968) Flowering cycles and fruit types of Ficus sycomorus in Israel. New Phytol 67:745–758CrossRefGoogle Scholar
  16. Grison L, Edwards AA, Hossaert-McKey M (1999) Interspecies variation in floral fragrances emitted by tropical Ficus species. Phytochemistry 52:1293–1299CrossRefGoogle Scholar
  17. Grison-Pigé L, Bessière JM, Turlings TCJ, Kjellberg F, Roy J, Hossaert-McKey MM (2001) Limited intersex mimicry of floral odour in Ficus carica. Funct Ecol 15:551–558CrossRefGoogle Scholar
  18. Grison-Pigé L, Bessière JM, Hossaert-McKey M (2002a) Specific attraction of fig-pollinating wasps: role of volatile compounds released by tropical figs. J Chem Ecol 28:283–295PubMedCrossRefGoogle Scholar
  19. Grison-Pigé L, Hossaert-McKey M, Greeff JM, Bessière JM (2002b) Fig volatile compounds—a first comparative study. Phytochemistry 61:61–71PubMedCrossRefGoogle Scholar
  20. Härdle W, Simar L (2007) Applied multivariate statistical analysis. Springer, HeidelbergGoogle Scholar
  21. Harrison RD (2005) Figs and the diversity of tropical rainforests. Bioscience 55:1053–1064CrossRefGoogle Scholar
  22. Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53PubMedCrossRefGoogle Scholar
  23. Hossaert-McKey M, Soler C, Schatz B, Proffit M (2010) Floral scents: their roles in nursery pollination mutualisms. Chemoecology 20:75–88CrossRefGoogle Scholar
  24. Janzen DH (1979) How to be a fig. Annu Rev Ecol Syst 10:13–51CrossRefGoogle Scholar
  25. Kessler D, Baldwin IT (2007) Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. Plant J 49:840–854PubMedCrossRefGoogle Scholar
  26. Kjellberg F, Doumesche B, Bronstein JL (1988) Longevity of a fig wasp (Blastophaga psenes). Proc K Ned Akad Wet 91:117–122Google Scholar
  27. Machado CA, Robbins N, Gilbert MT, Herre EA (2005) Critical review of host specificity and its coevolutionary implications in the fig/fig-wasp mutualism. Proc Natl Acad Sci USA 102(Suppl 1):6558–6565PubMedCrossRefGoogle Scholar
  28. Proffit M, Johnson SD (2009) Specificity of the signal emitted by figs to attract their pollinating wasps: comparison of volatile organic compounds emitted by receptive syconia of Ficus sur and F. sycomorus in Southern Africa. S Afr J Bot 75:771–777CrossRefGoogle Scholar
  29. Proffit M, Schatz B, Bessière JM, Chen C, Soler C, Hossaert-McKey M (2008) Signalling receptivity: comparison of the emission of volatile compounds by figs of Ficus hispida before, during and after the phase of receptivity to pollinators. Symbiosis 45:15–24Google Scholar
  30. Proffit M, Chen C, Soler C, Bessière JM, Schatz B, Hossaert-McKey M (2009) Can chemical signals, responsible for mutualistic partner encounter, promote the specific exploitation of nursery pollination mutualisms?—The case of figs and fig wasps. Entomol Exp Appl 131:46–57CrossRefGoogle Scholar
  31. Schiestl FP, Ayasse M (2001) Post-pollination emission of a repellent compound in a sexually deceptive orchid: a new mechanism for maximising reproductive success? Oecologia 126:531–534CrossRefGoogle Scholar
  32. Schiestl FP, Ayasse M, Paulus HF, Löfstedt C, Hansson BS, Ibarra F, Francke W (1999) Orchid pollination by sexual swindle. Nature 399:421–422CrossRefGoogle Scholar
  33. Song Q, Yang D, Zhang G, Yang C (2001) Volatiles from Ficus hispida and their attractiveness to fig wasps. J Chem Ecol 27:1929–1942PubMedCrossRefGoogle Scholar
  34. Terry I, Walter GH, Moore C, Roemer R, Hull C (2007) Odor-mediated push-pull pollination in cycads. Science 318:70PubMedCrossRefGoogle Scholar
  35. Van Noort S, Ware AB, Compton SG (1989) Pollinator-specific volatile attractants released from the figs of Ficus burtt-davyi. S Afr J Sci 85:323–324Google Scholar
  36. Ware AB, Compton SG (1994a) Responses of fig wasps to host-plant volatile cues. J Chem Ecol 20:785–802CrossRefGoogle Scholar
  37. Ware AB, Compton SG (1994b) Dispersal of adult female fig wasps. 1. Arrivals and departures. Entomol Exp Appl 73:221–229CrossRefGoogle Scholar
  38. Ware AB, Kaye PT, Compton SG, van Noort S (1993) Fig volatiles—their role in attracting pollinators and maintaining pollinator specificity. Plant Syst Evol 186:147–156CrossRefGoogle Scholar
  39. Wiebes JT (1979) Co-evolution of figs and their insect pollinators. Annu Rev Ecol Syst 10:1–12CrossRefGoogle Scholar
  40. Wiemer AP, Moré M, Benitez-Vieyra S, Cocucci AA, Raguso RA, Sérsic AN (2009) A simple floral fragrance and unusual osmophore structure in Cyclopogon elatus (Orchidaceae). Plant Biol 11:506–514PubMedCrossRefGoogle Scholar
  41. Windsor DM, Morrison DW, Estribi MA, Leon BD (1989) Phenology of fruit and leaf production by ‘strangler’ figs on Barro Colorado Island, Panamá. Experientia 45:647–653CrossRefGoogle Scholar
  42. Zhang FP, Peng YQ, Guan JM, Yang DR (2008) A species of fig tree and three unrelated fig wasp pollinators. Evol Ecol Res 10:611–620Google Scholar
  43. Zhang FP, Peng YQ, Compton SG, Yang DR (2009) Floral characteristics of Ficus curtipes and the oviposition behavior of its pollinator fig wasp. Ann Entomol Soc Am 102:556–559CrossRefGoogle Scholar

Copyright information

© Springer Basel AG 2012

Authors and Affiliations

  • Ding Gu
    • 1
    • 2
  • Stephen G. Compton
    • 3
  • Yanqiong Peng
    • 1
  • Darong Yang
    • 1
    Email author
  1. 1.Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical GardenThe Chinese Academy of SciencesKunmingChina
  2. 2.Graduate School of the Chinese Academy of SciencesBeijingChina
  3. 3.Faculty of Biology SciencesUniversity of LeedsLeedsUK

Personalised recommendations