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

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Abstract

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.

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References

  • 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 106:20342–20347

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Berg CC (1989) Classification and distribution of Ficus. Experientia 45:605–611

    Article  Google Scholar 

  • 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 169:719–727

    Article  PubMed  Google Scholar 

  • Borges RM, Bessière JM, Hossaert-McKey M (2008) The chemical ecology of seed dispersal in monoecious and dioecious figs. Funct Ecol 22:484–493

    Article  Google Scholar 

  • Boucher DH, James S, Keeler KH (1982) The ecology of mutualism. Annu Rev Ecol Syst 13:315–347

    Article  Google Scholar 

  • Bronstein JL (1994) Our current understanding of mutualism. Q Rev Biol 69:31–51

    Article  Google Scholar 

  • Bronstein JL (2001) The exploitation of mutualisms. Ecol Lett 4:277–287

    Article  Google Scholar 

  • Bronstein JL (2009) The evolution of facilitation and mutualism. J Ecol 97:1160–1170

    Article  Google Scholar 

  • 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 34:1536–1544

    Article  PubMed  CAS  Google Scholar 

  • 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 23:941–950

    Article  Google Scholar 

  • Cook JM, Rasplus JY (2003) Mutualists with attitude: coevolving fig wasps and figs. Trends Ecol Evol 18:241–248

    Article  Google Scholar 

  • Dudareva N, Negre F, Nagegowda D, Orlova I (2006) Plant volatiles: recent advances and future perspectives. Crit Rev Plant Sci 25:417–440

    Article  CAS  Google Scholar 

  • 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 77:927–935

    Article  PubMed  Google Scholar 

  • Galil J, Eisikowitch D (1968) Flowering cycles and fruit types of Ficus sycomorus in Israel. New Phytol 67:745–758

    Article  Google Scholar 

  • Grison L, Edwards AA, Hossaert-McKey M (1999) Interspecies variation in floral fragrances emitted by tropical Ficus species. Phytochemistry 52:1293–1299

    Article  CAS  Google Scholar 

  • 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 15:551–558

    Article  Google Scholar 

  • 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 28:283–295

    Article  PubMed  Google Scholar 

  • Grison-Pigé L, Hossaert-McKey M, Greeff JM, Bessière JM (2002b) Fig volatile compounds—a first comparative study. Phytochemistry 61:61–71

    Article  PubMed  Google Scholar 

  • Härdle W, Simar L (2007) Applied multivariate statistical analysis. Springer, Heidelberg

    Google Scholar 

  • Harrison RD (2005) Figs and the diversity of tropical rainforests. Bioscience 55:1053–1064

    Article  Google Scholar 

  • Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53

    Article  PubMed  Google Scholar 

  • Hossaert-McKey M, Soler C, Schatz B, Proffit M (2010) Floral scents: their roles in nursery pollination mutualisms. Chemoecology 20:75–88

    Article  Google Scholar 

  • Janzen DH (1979) How to be a fig. Annu Rev Ecol Syst 10:13–51

    Article  Google Scholar 

  • Kessler D, Baldwin IT (2007) Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. Plant J 49:840–854

    Article  PubMed  CAS  Google Scholar 

  • Kjellberg F, Doumesche B, Bronstein JL (1988) Longevity of a fig wasp (Blastophaga psenes). Proc K Ned Akad Wet 91:117–122

    Google Scholar 

  • 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):6558–6565

    Article  PubMed  CAS  Google Scholar 

  • 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 75:771–777

    Article  Google Scholar 

  • 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 45:15–24

    CAS  Google Scholar 

  • 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 131:46–57

    Article  CAS  Google Scholar 

  • 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 126:531–534

    Article  Google Scholar 

  • Schiestl FP, Ayasse M, Paulus HF, Löfstedt C, Hansson BS, Ibarra F, Francke W (1999) Orchid pollination by sexual swindle. Nature 399:421–422

    Article  CAS  Google Scholar 

  • Song Q, Yang D, Zhang G, Yang C (2001) Volatiles from Ficus hispida and their attractiveness to fig wasps. J Chem Ecol 27:1929–1942

    Article  PubMed  CAS  Google Scholar 

  • Terry I, Walter GH, Moore C, Roemer R, Hull C (2007) Odor-mediated push-pull pollination in cycads. Science 318:70

    Article  PubMed  CAS  Google Scholar 

  • Van Noort S, Ware AB, Compton SG (1989) Pollinator-specific volatile attractants released from the figs of Ficus burtt-davyi. S Afr J Sci 85:323–324

    Google Scholar 

  • Ware AB, Compton SG (1994a) Responses of fig wasps to host-plant volatile cues. J Chem Ecol 20:785–802

    Article  CAS  Google Scholar 

  • Ware AB, Compton SG (1994b) Dispersal of adult female fig wasps. 1. Arrivals and departures. Entomol Exp Appl 73:221–229

    Article  Google Scholar 

  • Ware AB, Kaye PT, Compton SG, van Noort S (1993) Fig volatiles—their role in attracting pollinators and maintaining pollinator specificity. Plant Syst Evol 186:147–156

    Article  Google Scholar 

  • Wiebes JT (1979) Co-evolution of figs and their insect pollinators. Annu Rev Ecol Syst 10:1–12

    Article  Google Scholar 

  • 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 11:506–514

    Article  PubMed  CAS  Google Scholar 

  • Windsor DM, Morrison DW, Estribi MA, Leon BD (1989) Phenology of fruit and leaf production by ‘strangler’ figs on Barro Colorado Island, Panamá. Experientia 45:647–653

    Article  Google Scholar 

  • Zhang FP, Peng YQ, Guan JM, Yang DR (2008) A species of fig tree and three unrelated fig wasp pollinators. Evol Ecol Res 10:611–620

    Google Scholar 

  • 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 102:556–559

    Article  Google Scholar 

Download references

Acknowledgments

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).

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Correspondence to Darong Yang.

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Gu, D., Compton, S.G., Peng, Y. et al. ‘Push’ and ‘pull’ responses by fig wasps to volatiles released by their host figs. Chemoecology 22, 217–227 (2012). https://doi.org/10.1007/s00049-012-0108-8

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  • DOI: https://doi.org/10.1007/s00049-012-0108-8

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