HOW TO BE A GOOD NON-POLLINATING FIG WASP: GALLING WASPS (Idarnes group flavicollis) DO NOT INTERFERE WITH THE FLORAL RECEPTIVITY
DOI:
https://doi.org/10.4257/oeco.2018.2204.06Keywords:
Agaonidae, brood-site pollination, mutualism, nursery pollination, plant-insect interactionAbstract
Mutualistic relationships are open to exploitation by non-cooperative species that can reduce the fitness of one or both cooperating partners. In addition to their obligate agaonid pollinators, a diverse community of non-pollinating fig wasps (NPFW) also uses the figs as a resource for the development of their broods. Some species of NPFW are gall makers and compete with the pollinators for the same pool of pistillate flowers. We experimentally demonstrated that the oviposition of the galling wasp Idarnes sp. group flavicollis at the beginning of anthesis does not interfere with stigma receptivity or the fig attractiveness of Ficus citrifolia. However, in situations of high Idarnes sp. infestation, the time window during which pollinators can enter the figs is shortened approximately by half. The enlargement of the Idarnes gall compresses the ostiole bracts, leading to an early closing of the fig ostiole, although the figs are still attractive. This negative effect on fig pollination seems to be more important in severely fragmented habitats where heliophilous fig tree species such as F. citrifolia are more abundant, favoring population of NPFWs, making over-infestation more frequent.
References
Abdurahiman, U. C., & Joseph, K. J. 1978. Cleptoparasitism of the fig wasps (Torymidae: Chalcidoidea) in Ficus hispida L. Entomon, 3(2), 181–186.
Bain, A., Harrison, R. D., & Schatz, B. 2014. How to be an ant on figs. Acta Oecologica, 57, 97–108. DOI: 10.1016/j.actao.2013.05.006
Berg, C. C., & Villavicencio, X. 2004. Taxonomic studies on Ficus (Moraceae) in the West Indies, extra-Amazonian Brazil and Bolivia. Bergen: Institutt for Biologi, Universitetet i Bergen: p. 132.
Borges, R. M. 2015. How to be a fig wasp parasite on the fig-fig wasp mutualism. Current Opinion in Insect Science, 8, 34–40. DOI: 10.1016/j.cois.2015.01.011
Borges, R. M., Bessière, J. M., & Ranganathan, Y. 2013. Diel variation in fig volatiles across syconium development: making sense of scents. Journal of Chemical Ecology, 39(5), 630–642. DOI: 10.1007/s10886-013-0280-5
Bronstein, J. L. 1999. Natural history of Anidarnes bicolor (Hymenoptera: Agaonidae), a galler of the Florida strangling fig (Ficus aurea). Florida Entomologist, 82(3), 454–461. DOI: 10.2307/3496871
Coelho, L. F. M., Ribeiro, M. C., & Pereira, R. A. S. 2014. Water availability determines the richness and density of fig trees within Brazilian semideciduous forest landscapes. Acta Oecologica, 57, 109–116. DOI: 10.1016/j.actao.2013.02.002
Compton, S. G., Holton, K. C., Rashbrook, V. K., van Noort, S., Vincent, S. L., & Ware, A. B. 1991. Studies of Ceratosolen galili, a non-pollinating agaonid fig wasp. Biotropica, 23(2), 188–194. DOI: 10.2307/2388305
Dafni, A., & Maués, M. M. 1998. A rapid and simple procedure to determine stigma receptivity. Sexual Plant Reproduction, 11(3), 177–180. DOI: 10.1007/s004970050138
Dunn, D. W., Jander, K. C., Lamas, A. G., & Pereira, R. A. S. 2015. Mortal combat and competition for oviposition sites in female pollinating fig wasps. Behavioral Ecology, 26(1), 262–268. DOI: 10.1093/beheco/aru191
Dunn, D. W., Yu, D. W., Ridley, J., & Cook, J. M. 2008. Longevity, early emergence and body size in a pollinating fig wasp - implications for stability in a fig-pollinator mutualism. Journal of Animal Ecology, 77(5), 927–935. DOI: 10.1111/j.1365-2656.2008.01416.x
Elias, L. G., Menezes Jr., A. O., & Pereira, R. A. S. 2008. Colonization sequence of non-pollinating fig wasps associated with Ficus citrifolia in Brazil. Symbiosis, 45(1), 107–111.
Elias, L. G., Ó, V. T., Farache, F. H. A., & Pereira, R. A. S. 2007. Efeito de vespas não-polinizadoras sobre o mutualismo Ficus – vespas de figos. Iheringia, Série Zoologia, 97(3), 253–256. DOI: 10.1590/S0073-47212007000300006
Elias, L. G., Teixeira, S. P., Kjellberg, F., & Pereira, R. A. S. 2012. Diversification in the use of resources by Idarnes species: bypassing functional constraints in the fig–fig wasp interaction. Biological Journal of the Linnean Society, 106(1), 114–122. DOI: 10.1111/j.1095-8312.2012.01851.x
Farache, F. H. A., Pereira, C. B., Koschnitzke, C., Barros, L. O., Souza, E. M. C., Felício, D. T., Gatti, F., Cardona, W., Rasplus, J. Y., & Pereira, R. A. S. The unknown followers: Discovery of a new species of Sycobia Walker (Hymenoptera: Epichrysomallinae) associated with Ficus benjamina L. (Moraceae) in the Neotropical region. Journal of Hymenoptera Research, in press.
Farache, F. H. A., Cruaud, A., Genson, G., Rasplus, J. Y., & Pereira, R. A. S. 2017. Taxonomic revision and molecular phylogenetics of the Idarnes incertus species-group (Hymenoptera, Agaonidae, Sycophaginae). Peerj, 5, e2842. DOI: 10.7717/peerj.2842
Figueiredo, R. A., & Motta Junior, J. C. 1993. Biology of Walkerella yashiroi (ISHII) (Hymenoptera, Chalcidoidea). Naturalia, 18, 27–32.
Galil, J., & Eisikowitch, D. 1968. On the pollination ecology of Ficus Sycomorus in east Africa. Ecology, 49(2), 259–269. DOI: 10.2307/1934454
Ghara, M., Ranganathan, Y., Krishnan, A., Gowda, V., & Borges, R. M. 2014. Divvying up an incubator: how parasitic and mutualistic fig wasps use space within their nursery microcosm. Arthropod-Plant Interactions, 8(3), 191–203. DOI: 10.1007/s11829-014-9300-9
Grison-Pigé, L., Hossaert-Mckey, M., Greeff, J. M., & Bessière, J. M. 2002. Fig volatile compounds - a first comparative study. Phytochemistry, 61(1), 61–71. DOI: 10.1016/S0031-9422(02)00213-3
Hossaert-Mckey, M., Soler, C., Schatz, B., & Proffit, M. 2010. Floral scents: their roles in nursery pollination mutualisms. Chemoecology, 20(2), 75–88. DOI: 10.1007/s00049-010-0043-5
Irwin, R. E., Bronstein, J. L., Manson, J. S., & Richardson, L. 2010. Nectar robbing: ecological and evolutionary perspectives. Annual Review of Ecology, Evolution, and Systematics, 41(1), 271–292. DOI: 10.1146/annurev.ecolsys.110308.120330
Jansen-González, S., Teixeira, S. P., Kjellberg, F., & Pereira, R. A. S. 2014. Same but different: larval development and gall-inducing process of a non-pollinating fig wasp compared to that of pollinating fig-wasps. Acta Oecologica, 57, 44–50. DOI: 10.1016/j.actao.2013.07.003
Jevanandam, N., Goh, A. G. R., & Corlett, R. T. 2013. Climate warming and the potential extinction of fig wasps, the obligate pollinators of figs. Biology Letters, 9(3), 1–4. DOI: 10.1098/rsbl.2013.0041
Khadari, B., Gibernau, M., Anstett, M. C., Kjellberg, F., & Hossaert-Mckey, M. 1995. When figs wait for pollinators: the length of fig receptivity. American Journal of Botany, 82(8), 992–999. DOI: 10.2307/2446228
Kjellberg, F., Doumesche, B., & Bronstein, J. L. 1988. Longevity of a fig wasp (Blastophaga psenes). Proceedings of The Koninklijke Nederlandse Akademie van Wetenschappen Series C: Biological and Medical Sciences, 91(2), 117–122.
Kjellberg, F., Jousselin, E., Hossaert-Mckey, & M., Rasplus, J. Y. 2005. Biology, ecology and evolution of fig-pollinating wasps (Chalcidoidea, Agaonidae). In: A. Raman, C. W. Schaefer & T. M. Withers (Eds.), Biology, ecology and evolution of gall-inducing arthropods. pp. 539–571. New Hampshire: Science publishers, Inc.
Pellmyr, O. 2002. Pollination by animals. In: C. M. Herrera & O. Pellmyr (Eds.), Plant-animal interactions: an evolutionary approach. pp. 157–184. Oxford: Wiley-Blackwell.
Pellmyr, O., Leebens-Mack, J., & Huth, C. J. 1996. Non-mutualistic yucca moths and their evolutionary consequences. Nature, 380(6570), 155–156. DOI: 10.1038/380155a0
Pereira, R. A. S., & Prado, A. P. 2005. Recognition of competitive asymmetries reduces the severity of fighting in male Idarnes fig wasps. Animal Behaviour, 70(2), 249–256. DOI: 10.1016/j.anbehav.2004.09.029
Pereira, R. A. S., & Prado, A. P. 2008. Mating strategies and aggressive combat in wingless neotropical fig wasp males. Brazilian Archives of Biology and Technology, 51(4), 753–760. DOI: 10.1590/S1516-89132008000400013
Pereira, R. A. S., Teixeira, S. P., & Kjellberg, F. 2007. An inquiline fig-wasp using seeds as a resource for small male production: a potential first step for the evolution of new feeding habits? Biological Journal of the Linnean Society, 92(1), 9–17. DOI: 10.1111/j.1095-8312.2007.00826.x
Price, P.W. 2002. Species interactions and the evolution of biodiversity. In: C. M. Herrera & O. Pellmyr (Eds.), Plant-animal interactions: an evolutionary approach. pp. 3–25. Oxford: Wiley-Blackwell.
Sapp, J. 1994. Evolution by association: a history of symbiosis. 1st ed. Oxford, UK: Oxford University Press: p. 272.
Souza, C. D., Pereira, R. A. S., Marinho, C. R., Kjellberg, F., & Teixeira, S. P. 2015. Diversity of fig glands is associated with nursery mutualism in fig trees. American Journal of Botany, 102(10), 1564–1577. DOI: 10.3732/ajb.1500279
Suleman, N., Raja, S., Zhang, Y., & Compton, S. G. 2011. Sexual differences in the attractiveness of figs to pollinators: females stay attractive for longer. Ecological Entomology, 36(4), 417–424. DOI: 10.1111/j.1365-2311.2011.01284.x
Tzeng, H. Y., Tseng, L. J., Ou, C. H., Lu, K. C., Lu, F. Y., & Chou, L. S. 2008. Confirmation of the parasitoid feeding habit in Sycoscapter, and their impact on pollinator abundance in Ficus formosana. Symbiosis, 45(1-3), 129–134.
Wang, R., Matthews, A., Ratcliffe, J., Barwell, L. J., Peng, Y. Q., Chou, L. S., Yu, H., Yang, H. W., & Compton, S. G. 2014. First record of an apparently rare fig wasp feeding strategy: obligate seed predation. Ecological Entomology, 39(4), 492–500. DOI: 10.1111/een.12122
Yu, D. W. 2001. Parasites of mutualisms. Biological Journal of the Linnean Society, 72(4), 529–546. DOI: 10.1111/j.1095-8312.2001.tb01336.x
Zhang, Y., Yang, D. R., Peng, Y. Q., & Compton, S. G. 2012. Costs of inflorescence longevity for an Asian fig tree and its pollinator. Evolutionary Ecology, 26(3), 513–527. DOI: 10.1007/s10682-011-9525-3