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ISRN Zoology  2012 

Spatial Stratification of Internally and Externally Non-Pollinating Fig Wasps and Their Effects on Pollinator and Seed Abundance in Ficus burkei

DOI: 10.5402/2012/908560

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Fig trees (Ficus spp.) are pollinated by tiny wasps that enter their enclosed inflorescences (syconia). The wasp larvae also consume some fig ovules, which negatively affects seed production. Within syconia, pollinator larvae mature mostly in the inner ovules whereas seeds develop mostly in outer ovules—a stratification pattern that enables mutualism persistence. Pollinators may prefer inner ovules because they provide enemy-free space from externally ovipositing parasitic wasps. In some Australasian Ficus, this results in spatial segregation of pollinator and parasite offspring within syconia, with parasites occurring in shorter ovules than pollinators. Australian figs lack non-pollinating fig wasps (NPFW) that enter syconia to oviposit, but these occur in Africa and Asia, and may affect mutualist reproduction via parasitism or seed predation. We studied the African fig, F. burkei, and found a similar general spatial pattern of pollinators and NPFWs within syconia as in Australasian figs. However, larvae of the NPFW Philocaenus barbarus, which enters syconia, occurred in inner ovules. Philocaenus barbarus reduced pollinator abundance but not seed production, because its larvae replaced pollinators in their favoured inner ovules. Our data support a widespread role for NPFWs in contributing to factors preventing host overexploitation in fig-pollinator mutualisms. 1. Introduction Mutualisms are reciprocally beneficial interspecific interactions [1, 2], and a well-known system is that between fig trees (Ficus spp.) and their agaonid wasp pollinators [3–6]. In return for pollination, the wasps gall some fig ovules, which are then eaten by the larvae. About half (300+) of Ficus species are monoecious, where both male flowers and ovules are present in the same syconium (enclosed inflorescence or “fig”). Within monoecious syconia, ovules are highly variable in length [7–10]. Long (inner) ovules have short styles and mature near the centre of the syconium, whereas short (outer), long-styled ovules mature nearer the outer wall (see Figure 1). Female pollinating wasps (foundresses) lay their eggs by inserting their ovipositors down the flower styles. At maturation, wasp galls are clustered at the syconium’s centre [4, 6, 9–13] with seeds at the outer wall. This spatial stratification of pollinating wasps and seeds enables mutualism stability, although the mechanisms preventing the wasps from galling all ovules are unclear. Figure 1: Variation in style and pedicel length in female flowers of monoecious Ficus (adapted from Dunn et al. [ 13]). Mechanisms proposed to


[1]  S. A. West, A. S. Griffin, and A. Gardner, “Evolutionary explanations for cooperation,” Current Biology, vol. 17, no. 16, pp. R661–R672, 2007.
[2]  S. A. West, A. S. Griffin, and A. Gardner, “Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection,” Journal of Evolutionary Biology, vol. 20, no. 2, pp. 415–432, 2007.
[3]  D. H. Janzen, “How to be a fig,” Annual Review of Ecology and Systematics, vol. 10, pp. 13–51, 1979.
[4]  G. D. Weiblen, “How to be a fig wasp,” Annual Review of Entomology, vol. 47, pp. 299–330, 2002.
[5]  J. M. Cook and J. Y. Rasplus, “Mutualists with attitude: coevolving fig wasps and figs,” Trends in Ecology and Evolution, vol. 18, no. 5, pp. 241–248, 2003.
[6]  E. A. Herre, K. C. Jandér, and C. A. Machado, “Evolutionary ecology of figs and their associates: recent progress and outstanding puzzles,” Annual Review of Ecology, Evolution, and Systematics, vol. 39, pp. 439–458, 2008.
[7]  K. N. Ganeshaiah, P. Kathuria, and R. Uma Shaanker, “Does optimal packing of flowers in syconia shape style length variation in monoecious figs?” Biotropica, vol. 31, no. 2, pp. 312–320, 1999.
[8]  K. N. Ganeshaiah, P. Kathuria, R. Uma Shaanker, and R. Vasudeva, “Evolution of style-length variability in figs and optimization of ovipositor length in their pollinator wasps: a coevolutionary model,” Journal of Genetics, vol. 74, no. 1-2, pp. 25–39, 1995.
[9]  E. Jousselin, J. Y. Rasplus, and F. Kjellberg, “Shift to mutualism in parasitic lineages of the fig/fig wasp interaction,” Oikos, vol. 94, no. 2, pp. 287–294, 2001.
[10]  E. Jousselin, F. Kjellberg, and E. A. Herre, “Flower specialization in a passively pollinated monoecious fig: a question of style and stigma?” International Journal of Plant Sciences, vol. 165, no. 4, pp. 587–593, 2004.
[11]  R. J. C. Nefdt and S. G. Compton, “Regulation of seed and pollinator production in the fig-fig wasp mutualism,” Journal of Animal Ecology, vol. 65, no. 2, pp. 170–182, 1996.
[12]  D. W. Yu, J. Ridley, E. Jousselin et al., “Oviposition strategies, host coercion and the stable exploitation of figs by wasps,” Proceedings of the Royal Society B, vol. 271, no. 1544, pp. 1185–1195, 2004.
[13]  D. W. Dunn, S. T. Segar, J. Ridley et al., “A role for parasites in stabilising the fig-pollinator mutualism,” PLoS Biology, vol. 6, no. 3, article e59, pp. 1–7, 2008.
[14]  S. A. West and E. A. Herre, “The ecology of the New World fig-parasitizing wasps Idarnes and implications for the evolution of the fog-pollinator mutualism,” Proceedings of the Royal Society B, vol. 258, no. 1351, pp. 67–72, 1994.
[15]  D. W. Dunn, D. W. Yu, J. Ridley, and J. M. Cook, “Longevity, early emergence and body size in a pollinating fig wasp—implications for stability in a fig-pollinator mutualism,” Journal of Animal Ecology, vol. 77, no. 5, pp. 927–935, 2008.
[16]  R. W. Wang, J. Ridley, B. F. Sun et al., “Interference competition and high temperatures reduce the virulence of fig wasps and stabilize a fig-wasp mutualism,” PLoS ONE, vol. 4, no. 11, article e7802, 2009.
[17]  J. L. Bronstein, “The exploitation of mutualisms,” Ecology Letters, vol. 4, no. 3, pp. 277–287, 2001.
[18]  D. W. Yu, “Parasites of mutualisms,” Biological Journal of the Linnean Society, vol. 72, no. 4, pp. 529–546, 2001.
[19]  S. G. Compton and S. van Noort, “Southern African fig wasps (Hymenoptera: Chalcidoidea): resource utilisation and host relationships,” Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, vol. 95, pp. 423–435, 1992.
[20]  F. P. Zhang, Y. Q. Peng, J. M. Guan, and D. R. Yang, “A species of fig tree and three unrelated fig wasp pollinators,” Evolutionary Ecology Research, vol. 10, no. 4, pp. 611–620, 2008.
[21]  F. Zhang, Y. Peng, S. G. Compton, Y. Zhao, and D. Yang, “Host pollination mode and mutualist pollinator presence: net effect of internally ovipositing parasite in the fig-wasp mutualism,” Naturwissenschaften, vol. 96, no. 4, pp. 543–549, 2009.
[22]  E. Jousselin, M. Hossaert-Mckey, D. Vernet, and F. Kjellberg, “Egg deposition patterns of fig pollinating wasps: implications for studies on the stability of the mutualism,” Ecological Entomology, vol. 26, no. 6, pp. 602–608, 2001.
[23]  L. E. Newton and A. Lomo, “The pollination of F. vogelii in Ghana,” Botanical Journal of the Linnean Society, vol. 78, no. 1, pp. 21–30, 1979.
[24]  S. G. Compton, K. C. Holton, V. K. Rashbrook, S. Van Noort, S. L. Vincent, and A. B. Ware, “Studies of Ceratosolen galili, a non-pollinating agaonid fig wasp,” Biotropica, vol. 23, no. 2, pp. 188–194, 1991.
[25]  N. R?nsted, G. Salvo, and V. Savolainen, “Biogeographical and phylogenetic origins of African fig species (Ficus section Galoglychia),” Molecular Phylogenetics and Evolution, vol. 43, no. 1, pp. 190–201, 2007.
[26]  C. C. Berg and J. T. Wiebes, “African fig trees and fig wasps,” Koninklijke Nederlandse Akademie van Wetenschappen, vol. 89, pp. 1–298, 1992.
[27]  Z. Bou?ek, A. Watsham, and J. T. Wiebes, “The fig wasp fauna of the receptacles of Ficus thonningii (Hymenoptera, Chalcidoidea),” Tijdschrift voor Entomologie, vol. 124, pp. 149–233, 1981.
[28]  J. Galil and D. Eisikowitch, “On the pollination ecology of Ficus Sycomorus,” Ecology, vol. 49, pp. 259–269, 1968.
[29]  C. Kerdelhué, M. E. Hochberg, and J. Y. Rasplus, “Active pollination of Ficus sur by two sympatric fig wasp species in West Africa,” Biotropica, vol. 29, no. 1, pp. 69–75, 1997.
[30]  S. A. West, E. A. Herre, D. M. Windsor, and P. R. S. Green, “The ecology and evolution of the New World non-pollinating fig wasp communities,” Journal of Biogeography, vol. 23, no. 4, pp. 447–458, 1996.
[31]  R Development Core Team, A Language and Environment for Statistical Computing, R foundation for Statistical Computing, Vienna, Austria, 2005.
[32]  M. J. Crawley, Statistics: An Introduction Using R, John Wiley, New York, NY, USA, 2005.
[33]  J. M. Cook and S. A. Power, “Effects of within-tree flowering asynchrony on the dynamics of seed and wasp production in an Australian fig species,” Journal of Biogeography, vol. 23, no. 4, pp. 487–493, 1996.
[34]  J. L. Bronstein, “The non-pollinating wasp fauna of Ficus pertusa: exploitation of a mutualism?” Oikos, vol. 61, no. 2, pp. 175–186, 1991.
[35]  K. C. Jander and E. A. Herre, “Host sanctions and pollinator cheating in the fig tree-fig wasp mutualism,” Proceedings of the Royal Society of London Series B, vol. 277, pp. 1481–1488, 2010.
[36]  E. A. Herre and S. A. West, “Conflict of interest in a mutualism: documenting the elusive fig wasp-seed trade-off,” Proceedings of the Royal Society B, vol. 264, no. 1387, pp. 1501–1507, 1997.
[37]  E. Jousselin, M. Hossaert-McKey, E. A. Herre, and F. Kjellberg, “Why do fig wasps actively pollinate monoecious figs?” Oecologia, vol. 134, no. 3, pp. 381–387, 2003.
[38]  W. A. Marussich and C. A. Machado, “Host-specificity and coevolution among pollinating and non-pollinating New World fig wasps,” Molecular Ecology, vol. 16, no. 9, pp. 1925–1946, 2007.
[39]  N. R?nsted, G. D. Weiblen, J. M. Cook, N. Salamin, C. A. Machado, and V. Savolainen, “60 million years of co-divergence in the fig-wasp symbiosis,” Proceedings of the Royal Society B, vol. 272, no. 1581, pp. 2593–2599, 2005.
[40]  J. L. Bronstein, D. Vernet, and M. Hossaert-McKey, “Do fig wasps interfere with each other during oviposition?” Entomologia Experimentalis et Applicata, vol. 87, no. 3, pp. 321–324, 1998.
[41]  J. C. Moore and J. M. Greeff, “Resource defence in female pollinating fig wasps: two's a contest, three's a crowd,” Animal Behaviour, vol. 66, no. 6, pp. 1101–1107, 2003.


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