Abstract
The Ficus–their specific pollinating fig wasps (Chalcidoidea, Agaonidae) interaction presents a striking example of mutualism. Figs also shelter numerous non-pollinating fig wasps (NPFW) that exploit the fig–pollinator mutualism. Only a few NPFW species can enter figs to oviposit, they do not belong to the pollinating lineage Agaonidae. The internally ovipositing non-agaonid fig wasps can efficiently pollinate the Ficus species that were passively pollinated. However, there is no study to focus on the net effect of these internally ovipositing non-agaonid wasps in actively pollinated Ficus species. By collecting the data of fig wasp community and conducting controlled experiments, our results showed that internally ovipositing Diaziella bizarrea cannot effectively pollinate Ficus glaberrima, an actively pollinated monoecious fig tree. Furthermore, D. bizarrea failed to reproduce if they were introduced into figs without Eupristina sp., the regular pollinator, as all the figs aborted. Furthermore, although D. bizarrea had no effect on seed production in shared figs, it significantly reduced the number of Eupristina sp. progeny emerging from them. Thus, our experimental evidence shows that reproduction in Diaziella depends on the presence of agaonid pollinators, and whether internally ovipositing parasites can act as pollinators depends on the host fig’s pollination mode (active or passive). Overall, this study and others suggest a relatively limited mutualistic role for internally ovipositing fig wasps from non-pollinator (non-Agaonidae) lineages.
References
Compton SG (1990) A collapse of host specificity in some African fig wasps. S Afr J Sci 86:39–40
Compton SG, van Noort S (1992) Southern African fig wasp assemblages: host relationships and resource utilization. Proc K Ned Akad Wet 95:423–435
Compton SG, Ware AB (1992) Breakdown of pollinator specificity in an African fig tree. Biotropica 24:544–549
Compton SG, Holton KC, Rashbrook VK, van Noort S, Vincent S, Ware AB (1991) Studies of Ceratosolen galili, a non pollinating agaonid fig wasp (Hymenoptera, Agaonidae). Biotropica 23:188–194
Frank SA (1984) The behavior and morphology of the fig wasps Pegoscapus assuetus and P. jimenezi: descriptions and suggested behavioral characters for phylogenetic studies. Psyche 91:289–308
Galil J (1977) Fig biology. Endeavour 1:52–56
Galil J, Eisikowitch D (1969) On the pollination ecology of Ficus sycomorus in East Africa. Ecology 49:259–269
Galil J, Eisikowitch D (1970) The effect of Sycophaga sycomori L. on the structure and development of syconia in Ficus sycomorus. New Phytol 69:103–111
Galil J, Neeman G (1977) Pollen transfer and pollination in the common fig (Ficus carica L.). New Phytol 79:163–171
Haine ER, Martin J, Cook JM (2006) Deep mtDNA divergences indicate cryptic species in a fig-pollinating wasp. BMC Evol Biol 6:83
Harrison RD, Yamamura N (2003) A few more hypotheses for the evolution of dioecy in figs (Ficus, Moraceae). Oikos 100:628–635
Herre EA (1999) Laws governing species interactions? Encouragement and caution from figs and their associates. In: Keller L (ed) Levels of selection. Princeton University Press, Princeton, NJ, pp 209–235
Herre EA, Jander KC, Machado CA (2009) Evolutionary ecology of figs and their associates: ongoing progress and outstanding puzzles. Ann Rev Ecolog Syst 39:439–458
Janzen DH (1979) How many parents do the wasps from a fig have? Biotropica 11:127–129
Jousselin E, Rasplus JY, Kjellberg F (2001) Shift to mutualism in parasitic lineages of the fig/fig wasp interaction. Oikos 94:287–294
Jousselin E, Hossaert-McKey M, Herre EA, Kjellberg F (2003) Why do fig wasps actively pollinate monoecious figs? Oecologia 134:381–387
Jousselin E, Kjellberg F, Herre EA (2004) Flower specialisation and mutualism stability in a passively pollinated monoecious fig: a question of style and stigma. Int J Plant Sci 165:587–594
Kerdelhué C, Rasplus JY (1996) Non-pollinating afrotropical fig wasps affect the fig–pollinator mutualism in Ficus within the subgenus Sycomorus. Oikos 75:3–14
Kerdelhué C, Clainche IL, Rasplus JY (1999) Molecular phylogeny of the Ceratosolen species pollinating Ficus of the subgenus Sycomorus sensu stricto: biogeographical history and origins of the species-specificity breakdown cases. Mol Phylogenet Evol 11:401–414
Kjellberg F, Jousselin E, Bronstein JL, Patel A, Yokoyama J, Rasplus JY (2001) Pollination mode in fig wasps: the predictive power of correlated traits. Proc R Soc Lond Ser B 268:1113–1121
Machado CA, Jousselin E, Kjellberg F, Compton SG, Herre EA (2001) Phylogenetic relationships, historical biogeography and character evolution of fig pollinating wasps. Proc R Soc Lond Ser B 268:685–694
Machado CA, Robbins N, Gilbert MPT, Herre EA (2005) Critical review of host specificity and its coevolutionary implications in the fig/fig–wasp mutualism. Proc Nat Acad Sci USA 102:6558–6565
Michaloud G, Carriere S, Kobbi M (1996) Exceptions to the one: one relationship between African fig trees and their fig wasp pollinators: possible evolutionary scenarios. J Biogeogr 23:521–530
Molbo D, Machado CA, Sevenster JG, Keller L, Herre EA (2003) Cryptic species of fig-pollinating wasps: implications for the evolution of the fig–wasp mutualism, sex allocation, and precision of adaptation. Proc Nat Acad Sci USA 100:5867–5872
Peng YQ, Duan ZB, Yang DR, Rasplus JY (2008) Co-occurrence of two Eupristina species on Ficus altissima in Xishuangbanna, SW China. Symbiosis 45:9–14
Rasplus JY, Kerdelhué C, Le Clainche I, Mondor G (1998) Molecular phylogeny of fig wasps (Hymenoptera). Agaonidae are not monophyletic. Compte Rendu de l’Académie des Sciences de Paris 321:517–527
Su ZH, Iino H, Nakamura K, Serrato A, Oyama K (2008) Breakdown of the one-to-one rule in Mexican fig–wasp associations inferred by molecular phylogenetic analysis. Symbiosis 45:73–82
Tarachai Y, Compton SG, Trisonthi C (2008) The benefits of pollination for a fig wasp. Symbiosis 45:29–32
van Noort S, Compton SG (1996) Convergent evolution of agaonine and sycoecine (Agaonidae, Chalcidoidea) head shape in response to the constraints of host fig morphology. J Biogeogr 23:415–424
van Noort S, Peng YQ, Rasplus JY (2006) First record of the fig wasp genus Diaziella Grandi (Hymenoptera: Chalcidoidea: Pteromalidae: Sycoecinae) from the Asian mainland with description of two new species from China. Zootaxa 1337:39–59
Weiblen GD (2002) How to be fig wasp. Annu Rev Entomol 47:229–230
West SA, Herre EH (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 Ser B 258:67–72
West SA, Herre EA, Windsor DM, Green PRS (1996) The ecology and evolution of the New World non-pollinating fig wasp communities. J Biogeogr 23:447–458
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
Acknowledgements
We thank Zhang Jin-Yuan, Zhang Yuan and Wang Zhen-Ji for the assistance. This study was funded by the Chinese Natural Science Foundation (30571507, 30670358) and the Knowledge Innovation Program of the Chinese Academy of Sciences.
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Zhang, F., Peng, Y., Compton, S.G. et al. Host pollination mode and mutualist pollinator presence: net effect of internally ovipositing parasite in the fig–wasp mutualism. Naturwissenschaften 96, 543–549 (2009). https://doi.org/10.1007/s00114-008-0502-9
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DOI: https://doi.org/10.1007/s00114-008-0502-9