Divvying up an incubator: How parasitic and mutualistic fig wasps use space within their nursery microcosm

Abstract

Differential occupancy of space can lead to species coexistence. The fig–fig wasp pollination system hosts species-specific pollinating and parasitic wasps that develop within galls in a nursery comprising a closed inflorescence, the syconium. This microcosm affords excellent opportunities for investigating spatial partitioning since it harbours a closed community in which all wasp species are dependent on securing safe sites inside the syconium for their developing offspring while differing in life history, egg deposition strategies and oviposition times relative to nursery development. We determined ontogenetic changes in oviposition sites available to the seven-member fig wasp community of Ficus racemosa comprising pollinators, gallers and parasitoids. We used species distribution models (SDMs) for the first time at a microcosm scale to predict patterns of spatial occurrence of nursery occupants. SDMs gave high true-positive and low false-positive site occupancy rates for most occupants indicating species specificity in oviposition sites. The nursery microcosm itself changed with syconium development and sequential egg-laying by different wasp species. The number of sites occupied by offspring of the different wasp species was negatively related to the risk of syconium abortion by the plant host following oviposition. Since unpollinated syconia are usually aborted, parasitic wasps ovipositing into nurseries at the same time as the pollinator targeted many sites, suggesting response to lower risk of syconium abortion owing to reduced risk of pollination failure compared to those species ovipositing before pollination. Wasp life history and oviposition time relative to nursery development contributed to the co-existence of nursery occupants.

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References

  1. Al-Beidh S, Dunn DW, Power SA, Cook JM (2012) Parasites and mutualism function: measuring enemy-free space in a fig–pollinator symbiosis. Oikos 121:1833–1839. doi:10.1111/j.1600-0706.2011.20179.x

    Article  Google Scholar 

  2. Albrecht M, Gotelli NJ (2001) Spatial and temporal niche partitioning in grassland ants. Oecologia 126:134–141. doi:10.1007/s004420000494

    Article  Google Scholar 

  3. Anstett M-C (2001) Unbeatable strategy, constraint and coevolution, or how to resolve evolutionary conflicts: the case of the fig/wasp mutualism. Oikos 95:476–484. doi:10.1034/j.1600-0706.2001.950313.x

    Article  Google Scholar 

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

    Article  Google Scholar 

  5. Bailey R, Schönrogge K, Cook JM, Melika G, Csóka G, Thuróczy C, Stone GN (2009) Host niches and defensive extended phenotypes structure parasitoid wasp communities. PLoS Biol 7:e1000179. doi:10.1371/journal.pbio.1000179

    PubMed Central  PubMed  Article  Google Scholar 

  6. Bland JM, Altman DG (2000) The odds ratio. Brit Med J 320:1468. doi:10.1136/bmj.320.7247.1468

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  7. Brodeur J, Boivin G (2004) Functional ecology of immature parasitoids. Annu Rev Entomol 49:27–49. doi:10.1146/annurev.ento.49.061703.153618

    CAS  PubMed  Article  Google Scholar 

  8. Bronstein JL (1988) Mutualism, antagonism, and the fig–pollinator interaction. Ecology 69:1298–1302. doi:10.2307/1941287

    Article  Google Scholar 

  9. Bronstein JL (1991) The non pollinating wasp fauna of Ficus pertusa: exploitation of a mutualism? Oikos 61:175–186

    Article  Google Scholar 

  10. Bronstein JL (1992) Seed predators as mutualists: ecology and evolution of the fig/pollinator interaction. In: Bernays E (ed) Insect–plant interactions. CRC Press, Boca Raton, pp 1–44

    Google Scholar 

  11. Compton SG, Nefdt RJC (1988) Extra-long ovipositors in chalcid wasps: some examples and observations. Antenna 12:102–105

    Google Scholar 

  12. Compton SG, Rasplus J-Y, Ware AB (1994) African fig wasp parasitoid communities. In: Hawkins B, Sheehan W (eds) Parasitoid community ecology. Oxford University Press, Oxford, pp 343–368

    Google Scholar 

  13. Cook JM, Rasplus J-Y (2003) Mutualists with attitude: coevolving fig wasps and figs. Trends Ecol Evol 18:241–248. doi:10.1016/S0169-5347(03)00062-4

    Article  Google Scholar 

  14. Cruaud A, Jabbour-Zahab R, Genson G, Kjellberg F, Kobmoo N, van Noort S, Da-Rong Y, Yan-Qiong P, Ubaidillah R, Hanson PE, Santos-Mattos O, Farache FHA, Pereira RAS, Kerdelhué C, Rasplus J-Y (2011) Phylogeny and evolution of life-history strategies in the Sycophaginae non-pollinating fig wasps (Hymenoptera, Chalcidoidea). BMC Evol Biol 11:178. doi:10.1186/1471-2148-11-178

    PubMed Central  PubMed  Article  Google Scholar 

  15. Després L, Jaeger N (1999) Evolution of oviposition strategies and speciation in the globeflower flies Chiastocheta spp. (Anthomyiidae). J Evol Biol 12:822–831. doi:10.1046/j.1420-9101.1999.00088.x

    Article  Google Scholar 

  16. Dunn DW, Segar ST, Ridley J, Chan R, Crozier RH, Yu DW, Cook JM (2008) A role for parasites in stabilising the fig–pollinator mutualism. PLoS Biol 6:e59. doi:10.1371/journal.pbio.0060059

    PubMed Central  PubMed  Article  Google Scholar 

  17. Eggleton P, Belshaw R (1993) Comparison of dipteran, hymenopteran and coleopteran parasitoids: provisional phylogenetic explanations. Biol J Linn Soc 48:213–226. doi:10.1111/j.1095-8312.1993.tb00888.x

    Article  Google Scholar 

  18. Elias LG, Menezes AO Jr, Pereira RAS (2008) Colonization sequence of non-pollinating fig wasps associated with Ficus citrifolia in Brazil. Symbiosis 45:107–111

    Google Scholar 

  19. Elias LG, Teixeira SP, Kjellberg F, Pereira RAS (2012) Diversification in the use of resources by Idarnes species: bypassing functional constraints in the fig–fig wasp interaction. Biol J Linn Soc 106:114–122

    Article  Google Scholar 

  20. Elith J, Leathwick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annu Rev Ecol Evol Syst 40:677–697. doi:10.1146/annurev.ecolsys.110308.120159

    Article  Google Scholar 

  21. Fawcett T (2006) An introduction to ROC analysis. Pattern Recogn Lett 27:861–874. doi:10.1016/j.patrec.2005.10.010

    Article  Google Scholar 

  22. Galil J (1977) Fig biology. Endeavour 1:52–56

    Article  Google Scholar 

  23. Galil J, Eisikowitch D (1968) On the pollination ecology of Ficus sycomorus in East Africa. Ecology 49:259–269. doi:10.2307/1934454

    Article  Google Scholar 

  24. Gallet C, Ibanez S, Zinger L, Taravel FR, Trierweiler M, Jeacomine I, Després L (2007) Plant chemical defense induced by a seed-eating pollinator mutualist. J Chem Ecol 33:2078–2089. doi:10.1007/s10886-007-9362-6

    CAS  PubMed  Article  Google Scholar 

  25. Ganeshaiah KN, Kathuria P, Uma Shaanker R, Vasudeva R (1995) Evolution of style-length variability in figs and optimization of ovipositor length in their pollinator wasps: a coevolutionary model. J Genet 74:25–39. doi:10.1007/BF02924244

    Article  Google Scholar 

  26. Ganeshaiah KN, Kathuria P, Uma Shaanker R (1999) Does optimal packing of flowers in syconia shape style length variation in monoecious figs? Biotropica 31:312–320. doi:10.1111/j.1744-7429.1999.tb00143.x

    Article  Google Scholar 

  27. Ghara M, Borges RM (2010) Comparative life-history traits in a fig wasp community: implications for community structure. Ecol Entomol 35:139–148. doi:10.1111/j.1365-2311.2010.01176.x

    Article  Google Scholar 

  28. Ghara M, Kundanati L, Borges RM (2011) Nature’s Swiss army knives: ovipositor structure mirrors ecology in a multitrophic fig wasp community. PLoS ONE 6:e23642. doi:10.1371/journal.pone.0023642

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  29. Herberich E, Sikorski J, Hothorn T (2010) A robust procedure for comparing multiple means under heteroscedasticity in unbalanced designs. PLoS ONE 5:e9788. doi:10.1371/journal.pone.0009788

    PubMed Central  PubMed  Article  Google Scholar 

  30. Herre EA, Jandér KC, Machado CA (2008) Evolutionary ecology of figs and their associates: recent progress and outstanding puzzles. Annu Rev Ecol Evol Syst 39:439–458. doi:10.1146/annurev.ecolsys.37.091305.110232

    Article  Google Scholar 

  31. Holt RD, Lawton JL (1993) Apparent competition and enemy-free space in insect host-parasitoid communities. Am Nat 142:623–645. doi:10.1086/285561

    CAS  PubMed  Article  Google Scholar 

  32. Ibanez S, Gallet C, Dommanget F, Després L (2009) Plant chemical defence: a partner control mechanism stabilising plant–seed-eating pollinator mutualisms. BMC Evol Biol 9:261. doi:10.1186/1471-2148-9-261

    PubMed Central  PubMed  Article  Google Scholar 

  33. Jandér KC, Herre EA, Simms EL (2012) Precision of host sanctions in the fig tree–fig wasp mutualism: consequences for uncooperative symbionts. Ecol Lett 15:1362–1369. doi:10.1111/j.1461-0248.2012.01857.x

    Article  Google Scholar 

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

    Article  Google Scholar 

  35. Jeffries MJ, Lawton JH (1984) Enemy free space and the structure of ecological communities. Biol J Linn Soc 23:269–286. doi:10.1111/j.1095-8312.1984.tb00145.x

    Article  Google Scholar 

  36. Jones TS, Godfray HCJ, van Veen FJF (2009) Resource competition and shared natural enemies in experimental insect communities. Oecologia 159:627–635. doi:10.1007/s00442-008-1247-z

    PubMed  Article  Google Scholar 

  37. Jousselin E, Van Noort S, Berry V, Rasplus J-Y, Rønsted N, Erasmus JC, Greeff JM (2008) One fig to bind them all: host conservatism in a fig wasp community unraveled by cospeciation analyses among pollinating and nonpollinating fig wasps. Evolution 62:1777–1797. doi:10.1111/j.1558-5646.2008.00406.x

    PubMed  Article  Google Scholar 

  38. Kerdelhué C, Rasplus J-Y (1996) Non-pollinating Afrotropical fig wasps affect the fig–pollinator mutualism in Ficus within the subgenus Sycomorus. Oikos 75:3–14

    Article  Google Scholar 

  39. Kerdelhué C, Rossi JP, Rasplus J-Y (2000) Comparative community ecology studies on Old World figs and fig wasps. Ecology 81:2832–2849. doi:10.1890/0012-9658(2000)081

    Article  Google Scholar 

  40. Kronfeld-Schor N, Dayan T (2003) Partitioning of time as an ecological resource. Annu Rev Ecol Evol Syst 34:153–181. doi:10.1146/annurev.ecolsys.34.011802.132435

    Article  Google Scholar 

  41. Lachaise D, Tsacas L, Couturier G (1982) The Drosophilidae associated with tropical African figs. Evolution 36:141–151. doi:10.2307/2407976

    Article  Google Scholar 

  42. Nefdt RJC, Compton SG (1996) Regulation of seed and pollinator production in the fig–fig wasp mutualism. J Anim Ecol 65:170–182

    Article  Google Scholar 

  43. Osawa T, Mitsuhashi H, Uematsu Y, Ushimaru A (2011) Bagging GLM: improved generalized linear model for the analysis of zero-inflated data. Ecol Inform 6:270–275. doi:10.1016/j.ecoinf.2011.05.003

    Article  Google Scholar 

  44. Pellmyr O, Leebens-Mack J (2000) Reversal of mutualism as a mechanism for adaptive radiation in yucca moths. Am Nat 156:S62–S76. doi:10.1086/303416

    Article  Google Scholar 

  45. Pompanon F, Pettex E, Després L (2006) Patterns of resource exploitation in four coexisting globeflower fly species (Chiastocheta sp.). Acta Oecol 29:233–240. doi:10.1016/j.actao.2005.11.003

    Article  Google Scholar 

  46. Ranganathan Y (2012) Ants, figs, fig wasps: the chemical ecology of a multitrophic system. PhD dissertation, Indian Institute of Science

  47. Ranganathan Y, Ghara M, Borges RM (2010) Temporal associations in fig-wasp-ant interactions: diel and phenological patterns. Entomol Exp Appl 137:50–61. doi:10.1111/j.1570-7458.2010.01038.x

    Article  Google Scholar 

  48. Raxworthy CJ, Martinez-Meyer E, Horning N, Nussbaum RA, Schneider GE, Ortega-Huerta MA, Peterson AT (2003) Predicting distributions of known and unknown reptile species in Madagascar. Nature 426:837–841. doi:10.1038/nature02205

    CAS  PubMed  Article  Google Scholar 

  49. Schoener TW (1968) The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49:704–726. doi:10.2307/1935534

    Article  Google Scholar 

  50. Schoener TW (1974) Resource partitioning in ecological communities. Science 185:27–39. doi:10.1126/science.185.4145.27

    CAS  PubMed  Article  Google Scholar 

  51. van Veen FJF, Morris RJ, Godfray HCJ (2006) Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. Annu Rev Entomol 51:187–208. doi:10.1146/annurev.ento.51.110104.151120

    PubMed  Article  Google Scholar 

  52. Wang H, Ridley J, Dunn DW, Wang R, Cook JM, Yu DW (2012) Biased oviposition and biased survival together help resolve a fig–wasp conflict. Oikos. doi:10.1111/j.1600-0706.2012.20463.x

    Google Scholar 

  53. West SA, Herre EA (1994) The ecology of the New World fig-parasitizing wasps Idarnes and implications for the evolution of the fig-pollinator mutualism. Proc R Soc Lond B 258:67–72. doi:10.1098/rspb 1994.0143

    Article  Google Scholar 

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Acknowledgments

We thank the Ministry of Environment and Forests, Government of India, for supporting this research. We also thank Gautam Pramanik, Kanchan Jogdev, Santhosh Revadi, and Yathiraj Ganesh for help with collecting the samples. For assistance with data analysis we thank Meera Mane and Meghana Kulkarni. We are grateful to Takeshi Osawa for help with the bagging GLM analysis and for sending us the relevant R code, and to three anonymous reviewers and Alexander Bradley Duthie for insightful comments on the manuscript. We are especially thankful to Lakshy Katariya, Karpagam Chelliah, Venkatappa and Mary Sunitha for technical support.

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Correspondence to Renee M. Borges.

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Communicated by Handling Editor: Lars Chittka.

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Ghara, M., Ranganathan, Y., Krishnan, A. et al. Divvying up an incubator: How parasitic and mutualistic fig wasps use space within their nursery microcosm. Arthropod-Plant Interactions 8, 191–203 (2014). https://doi.org/10.1007/s11829-014-9300-9

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Keywords

  • Enemy-free space
  • Life history
  • Nursery pollination
  • Resource partitioning
  • Species distribution models