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The enemy hypothesis: correlates of gall morphology with parasitoid attack rates in two closely related rose cynipid galls

  • Z. László (a1) and B. Tóthmérész (a2)

We tested the enemy hypothesis for gall morphology on a model system comprising two Diplolepis rose gall wasp species and their associated parasitoids. The enemy hypothesis predicts both that gall traits will influence parasitoid attack rates within species, and that galls with contrasting morphologies will support different parasitoid communities. This hypothesis is supported by studies at both intraspecific and broader taxonomic levels (i.e. between genera), but patterns remain to be explored in closely related species. Our aims were to explore the relationships between aspects of gall morphology (number of larval chambers, overall gall size and thickness of the gall wall) in each of Diplolepis mayri and D. rosae, and to explore correlations between these traits and both the presence/absence (=incidence) and attack rates imposed by parasitoids. We found in both galls that chamber number is positively correlated with gall size. In galls of D. mayri, parasitoid incidence was negatively correlated with thickness of the wall of the larval chamber, but there was no significant correlation between parasitoid attack rates and overall gall size. In D. rosae galls, parasitoid incidence was positively correlated with chamber wall thickness, but parasitoid attack rates were negatively correlated with gall size, suggesting that selection may favour the induction of galls containing more larval chambers. These results confirm that gall extended phenotypes can significantly influence enemy attack rates, consistent with the ‘enemy hypothesis’. Further, differences in gall morphology between the two Diplolepis species may underlie differences in their associated parasitoid communities – further research is required to test this hypothesis.

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Abrahamson, W.G. & Weis, A.E. (1997) Evolutionary Ecology Across Three Trophic Levels: Goldenrods, Gallmakers and Natural Enemies. Princeton, New Jersey, Princeton University Press.
Askew, R.R. (1961) On the biology of the inhabitants of oak galls of Cynipidae (Hymenoptera) in Britain. Transactions of the Society for British Entomology 14, 237268.
Askew, R.R. (1984) The biology of gallwasps. pp. 223271 in Ananthakrishnan, T.N. (Ed.) The Biology of Galling Insects. New Delhi, India, Oxford & IBH Publishing.
Askew, R.R., Gómez, J.F., Hernández Nieves, M. & Nieves-Aldrey, J.L. (2006) Catalogue of parasitoids and inquilines in galls of Aylacini, Diplolepidini and Pediaspidini (Hym., Cynipidae) in the West Palaearctic. Zootaxa 1301, 160.
Atkinson, R.J., McVean, G.A.T. & Stone, G.N. (2002) Use of population genetic data to infer oviposition behaviour: species-specific patterns in four oak gallwasps (Hymenoptera: Cynipidae). Proceedings of the Royal Society B – Biological Sciences 269, 383390.
Atkinson, R.J., Brown, G.S. & Stone, G.N. (2003) Skewed sex ratios and multiple founding in galls of the oak apple gallwasp Biorhiza pallida (Hymenoptera: Cynipidae). Ecological Entomology 28, 1424.
Bailey, R., Schönrogge, K., Cook, J.M., Melika, G., Csóka, G., Thuróczy, C., & Stone, G.N. (2009) Host niches and defensive extended phenotypes structure parasitoid wasp communities. PLoS Biology 7: e1000179. doi:10.1371/journal.pbio.1000179.
Cooper, W.R. & Rieske, L.K. (2009) Woody stem galls interact with foliage to affect community associations. Environmental Entomology 38, 417424.
Cooper, W.R. & Rieske, L.K. (2010) Gall structure affects ecological associations of Dryocosmus kuriphilus (Hymenoptera: Cynipidae). Environmental Entomology 39, 787797.
Cornell, H.V. (1983) The secondary chemistry and complex morphology of galls formed by the Cynipinae. Why and how? American Midland Naturalist 110, 225234.
Crespi, B.J., Carmean, D.A. & Chapman, T.W. (1997) Ecology and evolution of galling thrips and their allies. Annual Review of Entomology 42, 5171.
Demeter, A., Vámosi, J., Peregovits, L. & Topál, G. (1994) An image-capture and data-collection system for morphometric analysis. pp. 359369 in Marcus, L.F., Corti, M., Loy, A., Naylor, G.J.P. & Slice, D.E. (Eds) Advances in Morphometrics, NATO ASI Series A. New York, Plenum Press.
Eady, R.D. & Quinlan, J. (1963) Handbooks for the Identification of British Insects. Vol. VIII. Part 1 (a). Hymenoptera: Cynipoidea. Key to families and subfamilies and Cynipinae (including galls). London, Royal Entomological Society of London.
Erdős, J. (1960) Magyarország Allatvilága. XII. Kötet. Hymenoptera II. 3. Füzet. Fémfürkészek II. Chalcidoidea II. Torymidae, Eurytomidae, Agaonidae, Cleonymidae, Eupelmidae. Fauna Hungariae 52, Budapest.
Freese, G. & Zwolfer, H. (1996) The problem of optimal clutch size in a tritrophic system: the oviposition strategy of the thistle gallfly Urophora cardui (Diptera, Tephritidae). Oecologia 108, 293302.
Frenzel, M., Eber, S., Klotz, S. & Brandl, R. (2000) Ecological comparisons across geographical distributions: the thistle gall fly Urophora cardui (Diptera: Tephritidae) on two different Cirsium hosts. European Journal of Entomology 97, 183189.
Gauld, I.D. & Mitchell, P.A. (1977) Handbooks for the Identification of British Insects. Vol. VII. Part 2 (b). Ichneumonidae. Orthopelmatinae & Anomaloninae. London, Royal Entomological Society of London.
Gómez, J.F., Hernández Nieves, M., Garrido Torres, A.M., Askew, R.R. & Nieves-Aldrey, J.L. (2006) Los Chalcidoidea (Hymenoptera) asociados con agallas de cinípidos (Hymenoptera, Cynipidae) en la Comunidad de Madrid. Graellsia 62, 293331.
Graham, M.W.R. de V. (1969) The Pteromalidae of north-western Europe (Hymenoptera: Chalcidoidea). Bulletin of the British Museum (Natural History) (Entomology) Supplement 16.
Graham, M.W.R. de V. (1987) A reclassification of the European Tetrastichinae (Hymenoptera: Eulophidae), with a revision of certain genera. Bulletin of the British Museum (Natural History) (Entomology) 55, 1392.
Graham, M.W.R. de V. & Gijswijt, M.J. (1998) Revision of the European species of Torymus Dalman (s. lat.) (Hymenoptera: Torymidae). Zoologische Verhandelingen, Leiden 317, 1202.
Ito, M. & Hijii, N. (2002) Factors affecting refuge from parasitoid attack in a cynipid wasp, Aphelonyx glanduliferae . Population Ecology 44, 2332.
Ito, M. & Hijii, N. (2004) Roles of gall morphology in determining potential fecundity and avoidance of parasitoid attack in Aphelonyx glanduliferae . Journal of Forest Research 9, 93100.
Kaartinen, R., Stone, G.N., Hearn, J., Lohse, K. & Roslin, T. (2010) Revealing secret liaisons: DNA bar-coding changes our understanding of food webs. Ecological Entomology 35, 623638.
Kato, K. & Hijii, N. (1993) Optimal clutch size of the chestnut gall-wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae). Researches Population Ecology 35, 114.
Kohnen, A., Wissemann, V. & Brandl, R. (2011) No host-associated differentiation in the gall wasp Diplolepis rosae (Hymenoptera: Cynipidae) on three dog rose species. Biological Journal of the Linnean Society 102, 369377.
László, Z., & Tóthmérész, B. (2006) Inquiline effects on a multilocular gall community. Acta Zoologica Academiae Scientiarum Hungaricae 52, 373383.
László, Z. & Tóthmérész, B. (2008) Optimal clutch size of the gall wasp Diplolepis rosae (Hymenoptera: Cynipidae). Entomologica Fennica 19, 168175.
László, Z. & Tóthmérész, B. (2011) Parasitism, phenology and sex ratio in galls of Diplolepis rosae . Entomologica Romanica 16, 3338.
Nieves-Aldrey, J.L. (1983) Contribución al conocimiento de la fauna de himenópteros inquilinos y parásitos en las agallas de Diplolepis mayri (Schlechtendal) y Diplolepis eglanteriae (Hartig) (Hym., Cynipidae). Graellsia 39, 93102.
Nieves-Aldrey, J.L. & Askew, R.R. (2002) Calcidoideos (Hym: Chalcidoidea) asociados a agallas de Aylacini y Diplolepidini (Hym: Cynipidae) en España. Boletín de la Asociación Española de Entomología 26, 1137.
Nordlander, G. (1973) Parasitic wasps in galls of Diplolepis rosae (L.) and D. mayri Schlechtd. (Hymenoptera: Cynipidae) (Hym.: Ichneumonoidea, Chalcidoidea, Cynipoidea). Entomologisk Tidskrift 94, 148176.
Plantard, O. & Hochberg, M.E. (1998) Factors affecting parasitism in the oak-galler Neuroterus quercusbaccarum (Hymenoptera: Cynipidae). Oikos 81, 289298.
Price, P.W. & Clancy, K.M. (1986) Interactions among three trophic levels: gall size and parasitoid attack. Ecology 67, 15931600.
Price, P.W., Fernandes, G.W. & Waring, G.L. (1987) Adaptive nature of insect galls. Environmental Entomology 16, 1524.
R Development Core Team (2011) R: A language and environment for statistical computing. R foundation for Statistical Computing, Vienna, Austria. Available at:
Rohfritsch, O. (1992) Patterns in gall development. pp. 6087 in Shorthouse, J.D., Rohfritsch, O. (Eds) Biology of Insect-induced Galls. New York, Oxford University Press.
Schröder, D. (1967) Diplolepis (=Rhodites) rosae (L.) (Hym.: Cynipidae) and a review of its parasite complex in Europe. Technical Bulletin of the Commonwealth Institute of Biological Control 9, 93131.
Schönrogge, K., Stone, G.N. & Crawley, M.J. (1996) Alien herbivores and native parasitoids: rapid developments and structure of the parasitoid and inquiline complex in an invading gall wasp Andricus quercuscalicis (Hymenoptera: Cynipidae). Ecological Entomology 21, 7180.
Shorthouse, J.D. (2010) Galls induced by cynipid wasps of the genus Diplolepis (Hymenoptera: Cynipidae) on the roses of Canada's grasslands. pp. 251279 in Shorthouse, J.D., Floate, K.D. (Eds) Arthropods of Canadian Grasslands, Vol 1. Ottawa, Ontario, Biological survey of Canada.
Stille, B. (1984) The effect of host plant and parasitoids on the reproductive success of the parthenogenetic gall wasp Diplolepis rosae; (Hymenoptera, Cynipidae). Oecologia 63, 364369.
Stone, G.N. & Cook, J.M. (1998) The structure of cynipid oak galls: patterns in the evolution of an extended phenotype. Proceedings of the Royal Society B – Biological Sciences 265, 979988.
Stone, G.N. & Schönrogge, K. (2003) The adaptive significance of insect gall morphology. Trends Ecology and Evolution 18, 512522.
Stone, G.N., Schönrogge, K., Atkinson, R.J., Bellido, D. & Pujade-Villar, J. (2002) The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annual Review of Entomology 47, 633668.
Stone, G.N., Lohse, K., Nicholls, J.A., Fuentes-Utrilla, P., Sinclair, F., Schönrogge, K., Csóka, G., Melika, G., Nieves-Aldrey, J.-L., Pujade-Villar, J., Tavakoli, M., Askew, R.R. & Hickerson, M.J. (2012) Reconstructing community assembly in time and space reveals enemy escape in a western palaearctic insect community. Current Biology 22, 16.
Washburn, J.O. & Cornell, H.V. (1981) Parasitoids, patches, and phenology: their possible role in the local extinction of a cynipid gall wasp population. Ecology 62, 15971607.
Weis, A.E., Abrahamson, W.G. & McCrea, K.D. (1985) Host gall size and oviposition success by the parasitoid Eurytoma gigantea . Ecological Entomology 10, 341348.
Wiebes-Rijks, A.A. & Shorthouse, J.D. (1992) Ecological relationships of insects inhabiting cynipid galls. pp. 238257 in Shorthouse, J.D., Rohfritsch, O. (Eds) Biology of Insect-induced Galls. New York, Oxford University Press.
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