Abstract
Recent studies on the obligate interaction between fig trees and their pollinating agaonid wasps have focused on population aspects and wasp–seed exploitation at the level of the inflorescence. Detailed studies on larval and gall development are required to more fully understand how resources are exploited and adaptations fine-tuned by each partner in nursery pollination mutualisms. We studied the larval development of the active pollinating fig wasp, Pegoscapus sp., and the galling process of individual flowers within the figs of its monoecious host, Ficus citrifolia, in Brazil. The pollinator development is strongly dependent on flower pollination. Figs entered by pollen-free wasps were in general more likely to abort. Retained, unpollinated figs had both higher larval mortality and a lower number of wasps. Pegoscapus sp. larvae are adapted to plant development, with two contrasting larval feeding strategies proceeding alongside gall development. The first two larval stages behave as ovary parasites. Later larval stages feed on hypertrophied endosperm. This indicates that a successful galling process relies on endosperm, and also reveals why pollination would be a prerequisite for the production of high-quality galls for this Pegoscapus species.
Similar content being viewed by others
References
Anstett MC (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
Anstett MC, Hossaert-McKey M, Kjellberg F (1997) Figs and fig pollinators: evolutionary conflicts in a coevoled mutualism. Trends Ecol Evol 12:94–99. doi:10.1016/S0169-5347(96)10064-1
Boucher DH, James S, Keeler KH (1982) The ecology of mutualism. Annu Rev Ecol Evol Syst 13:315–347. doi:10.1146/annurev.es.13.110182.001531
Bronstein JL, Alarcón R, Geber M (2006) The evolution of plant–insect mutualisms. New Phytol 172:412–428. doi:10.1111/j.1469-8137.2006.01864.x
Clausen CP (1962) Entomophagous Insects. Hafner Publishing Company, New York
Compton SG (1993) One way to be a fig. Afr Entomol 1:151–158
Condit IJ (1932) The structure and development of flowers in Ficus carica L. Hilgardia 6:443–481
Cunningham, DD (1889) On the phenomena of fertilization in Ficus Roxburghii, Appendix I. Annals of the Royal Botanical Garden, Calcuta, pp 13–51
Damiens D, Imbert E, Bressac C, Thibeaudeau C, Chevrier C (2001) Egg-laying, pre-imaginal growth, and mortality in Eupelmus orientalis and Dinarmus basalis, two solitary parasitoids of Callosobruchus maculatus. Entomol Exp Appl 99:97–105. doi:10.1023/A:1018954320519
Dufay M, Anstett MC (2003) Conflicts between plants and pollinators that reproduce within inflorescences: evolutionary variations on a theme. Oikos 100:3–14. doi:10.1034/j.1600-0706.2003.12053.x
Elias LG, Menezes AO, Pereira RAS (2008) Colonization sequence of non-pollinating fig wasps associated with Ficus citrifolia in Brazil. Symbiosis 45:107–111
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. doi:10.1111/j.1095-8312.2012.01851.x
Galil J, Eisikowitch D (1968) Flowering cycles and fruit types of Ficus sycomorus in Israel. New Phytol 67:745–758
Gerrits PO (1991) The application of glycol methacrylate in histotechnology; some fundamental principles. Department of Anatomy and Embryology. State University Groningen, Netherlands
Grandi G (1929) Studio Morfologico e Biologico Della Blastophaga psenes (L.). Boll Lab Ent R Ist Supr Agr Bologna 2:11–45
Harvey JA, Jervis MA, Gols R, Jiang N, Vet LEM (1999) Development of the parasitoid Cotesia rubecula (Hymenoptera: Braconidae) in Pieris rapae and Pieris brassicae (Lepidoptera: Pieridae): evidence for host regulation. J Insect Physiol 45:173–182. doi:16/S0022-1910(98)00113-9
Harvey JA, Bezemer TM, Elzinga JA, Strand MR (2004) Development of the solitary endoparasitoid Microplitis demolitor: host quality does not increase with host age and size. Ecol Entomol 29:35–43. doi:10.1111/j.0307-6946.2004.00568.x
Herre EA, West SA (1997) Conflict of interest in a mutualism: documenting the elusive fig wasp–seed trade–off. Proc Roy Soc Lond B 264:1501–1507. doi:10.1098/rspb.1997.0208
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
Jander KC, Herre EA (2010) Host sanctions and pollinator cheating in the fig tree–fig wasp mutualism. Proc Roy Soc Lond B 277:1481–1488. doi:10.1098/rspb.2009.2157
Jansen-Gonzalez S, Sarmiento CE (2008) A new species of high mountain Andean fig wasp (Hymenoptera: Agaonidae) with a detailed description of its life cycle. Symbiosis 45:135–141
Johansen DA (1940) Plant microtechnique. McGraw-Hill, New York
Johri BM, Konar RN (1956) The floral morphology and embryology of Ficus religiosa Linn. Phytomorphology 6:97–111
Joseph K (1958) Recherches sur les Chalcidiens Blastophaga psenes (L.) et Philothrypesis caricae (L.), du figuier (Ficus carica L.). Ann Sci Nat Zool 11:197–260
Joseph M (1984) Morphology, biology and behaviour of Ceratosolen fusciceps Mayr and its relationship with other fig wasp breeding in the receptacles of Ficus racemosa L. Doctoral thesis. University of Calicut, Kerala, India
Jousselin E, Kjellberg F (2001) The functional implications of active and passive pollination in dioecious figs. Ecol Lett 4:151–158. doi:10.1046/j.1461-0248.2001.00209.x
Jousselin E, Hossaert-Mckey M, Vernet D, Kjellberg F (2001) Egg deposition patterns of fig pollinating wasps: implications for studies on the stability of the mutualism. Ecol Entomol 26:602–608. doi:10.1046/j.1365-2311.2001.00368.x
Jousselin E, Hossaert-McKey M, Herre EA, Kjellberg F (2003) Why do fig wasps actively pollinate monoecious figs? Oecologia 134:381–387. doi:10.1007/s00442-002-1116-0
Jousselin E, Kjellberg F, Herre EA (2004) Flower specialization in a passively pollinated monoecious fig: a question of style and stigma? Int J Plant Sci 165:587–593. doi:10.1086/386558
Leclerc du Sablon M (1907) Sur la symbiose du Figuier et du Blastophage. C R Acad Sci Paris 20:756–757
Margulis L, Nealson KH (1989) Symbiosis as the source of evolutionary innovation. Endocytobiosis Cell Res 6:241–246
O’Brian TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373
Pellmyr O, Krenn HW (2002) Origin of a complex key innovation in an obligate insect–plant mutualism. Proc Natl Acad Sci USA 99:5498–5502. doi:10.1073/pnas.072588699
Renoult JP, Kjellberg F, Grout C, Santoni S, Khadari B (2009) Cyto-nuclear discordance in the phylogeny of Ficus section Galoglychia and host shifts in plant-pollinator associations. BMC Evol Biol 9:248. doi:10.1186/1471-2148-9-248
Stehr FW (1987) Immature insects. Kendall-Hunt Publishing Company, Dubuque
Tarachai Y, Compton SG, Trishonthi C (2008) The benefits of pollination for a fig wasp. Symbiosis 45:29–32
Verkerke W (1986) Anatomy of Ficus ottonifolia (Moraceae) syconia and its role in fig–fig wasp symbiosis. Proc K Ned Akad Wet Ser C Biol Med Sci 89:443–469
Verkerke W (1987) Syconial anatomy of Ficus asperifolia (Moraceae), a gynodioecious tropical fig. Proc K Ned Akad Wet Ser C Biol Med Sci 90:461–492
Verkerke W (1989) Structure and function of the fig. Experientia 45:612–622. doi:10.1007/BF01975678
Weiblen GD (2002) How to be a fig wasp. Annu Rev Entomol 47:299–330. doi:10.1146/annurev.ento.47.091201.145213
Acknowledgments
We thank Derek Dunn, Finn Kjellberg, Steve Compton and an anonymous referee for the critical review of the manuscript; and Dewey Litwiller for the English revision. We thank Viviane Leite and Edimárcio Campos for helping in material processing for the histological study. S.J.G. was supported by CAPES and FAPESP (#06/05465-8 and #09/10273-9). R.A.S.P. was supported by FAPESP (#04/10299-4) and CNPq (#302769/2008-0). S.P.T. was supported by CNPq (#301960/2009-7).
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Neal Williams.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jansen-González, S., Teixeira, S.P. & Pereira, R.A.S. Mutualism from the inside: coordinated development of plant and insect in an active pollinating fig wasp. Arthropod-Plant Interactions 6, 601–609 (2012). https://doi.org/10.1007/s11829-012-9203-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-012-9203-6