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Modification of galls of Diplolepis triforma (Hymenoptera: Cynipidae) by the parasitoids Eurytoma spongiosa (Hymenoptera: Eurytomidae) and Glyphomerus stigma (Hymenoptera: Torymidae)

Published online by Cambridge University Press:  02 April 2012

Jonathan J. Leggo
Affiliation:
Department of Biology, Laurentian University, Sudbury, Ontario, Canada P3E 2C6
Joseph D. Shorthouse*
Affiliation:
Department of Biology, Laurentian University, Sudbury, Ontario, Canada P3E 2C6
*
2Corresponding author (e-mail: [email protected]).

Abstract

Stem galls induced by the cynipid Diplolepis triforma Shorthouse and Ritchie are frequently inhabited by several species of parasitic chalcids and ichneumonids that consume inducers or other parasitoids. Two of these parasitoids, the eurytomid Eurytoma spongiosa Bugbee and the torymid Glyphomerus stigma (Fabr.), consume gall tissues after they have consumed their insect hosts and are considered entomophytophagous. Both are koinobiont ectoparasitoids. Eurytoma spongiosa oviposits within gall chambers and attacks larvae of the inducer throughout the summer season, from the early growth phase of the galls until the galls mature. If the inducer is killed by E. spongiosa in early summer, nutritive gall cells degenerate into vacuolate parenchyma and are consumed. If the inducer is killed later in the summer, when galls begin to mature, nutritive cells persist in the chambers for about 1 week before degenerating. Glyphomerus stigma kills and consumes inducer larvae when galls are maturing. New nutritive cells appear under the influence of G. stigma and are then consumed. The ability of entomophytophagous chalcids to promote the formation of gall cells provides insight into the derivation of the gall-inducing guild.

Résumé

Les galles sur les tiges provoquées par le cynipidé Diplolepis triforma Shorthouse et Ritchie sont souvent habitées par plusieurs espèces de chalcidés et d'ichneumonidés parasites qui se nourrissent des insectes galligènes et d'autres parasitoïdes. Deux de ces parasitoïdes, l'eurytomidé Eurytoma spongiosa Bugbee et le torymidé Glyphomerus stigma (Fabr.), se nourrissent de tissus de la galle après avoir consommé les insectes hôtes et sont considérés comme des entomophytophages. Les deux sont des ectoparasitoïdes coenobiontes. Eurytoma spongiosa pond dans les loges de la galle et attaque les larves de l'insecte galligène au cours de la saison estivale, depuis le début de la croissance jusqu'à la maturité de la galle. Si l'insecte galligène est tué par E. spongiosa au début de l'été, les cellules nourricières de la galle dégénèrent en parenchyme vacuolisé et sont consommées. Si l'hôte est tué plus tard en été au moment du début de la maturation de la galle, les cellules nourricières persistent dans les loges pour environ une semaine avant de dégénérer. Glyphomerus stigma tue les larves galligènes au moment de la maturation de la galle. De nouvelles cellules nourricières se développent sous l'influence de G. stigma et elles sont alors consommées. La capacité qu'ont les chalcoïdes entomophytophages de favoriser la formation de cellules dans la galle ouvre une perspective intéressante sur la dérivation de la guilde des insectes galligènes.

[Traduit par la Rédaction]

Type
Articles
Copyright
Copyright © Entomological Society of Canada 2006

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References

Askew, R.R. 1961. On the biology of the inhabitants of oak galls of Cynipidae (Hymenoptera) in Britain. Transactions of the Society of British Entomology, 14: 237268.Google Scholar
Askew, R.R., and Blasco-Zumeta, J. 1998. Insects associated with galls of a new species of Eurytomidae (Hymenoptera: Chalcidoidea) on Ephedra nebrodensis in Spain. Journal of Natural History, 32: 805821.CrossRefGoogle Scholar
Askew, R.R., and Shaw, M.R. 1986. Parasitoid communities: their size, structure and development. In Insect parasitoids. Edited by Waage, J. and Greathead, D.. Academic Press, London. pp. 225264.Google Scholar
Blair, K.G. 1945. Notes on the economy of the rose-galls formed by Rhodites (Hymenoptera, Cynipidae). Proceedings of the Royal Entomological Society of London Series A, General Entomology, 20: 2631.CrossRefGoogle Scholar
Bronner, R. 1977. Contribution à l'étude histochimique des tissus nourriciers des zoocécides. Marcellia, 40: 1134.Google Scholar
Bronner, R. 1992. The role of nutritive cells in the nutrition of cynipids and cecidomyiids. In Biology of insect-induced galls. Edited by Shorthouse, J.D. and Rohfritsch, O.. Oxford University Press, New York. pp. 118140.Google Scholar
Brooks, S.E., and Shorthouse, J.D. 1997. Biology of the rose stem galler Diplolepis nodulosa (Hymenoptera: Cynipidae) and its associated component community in central Ontario. The Canadian Entomologist, 129: 11211140.CrossRefGoogle Scholar
Brooks, S.E., and Shorthouse, J.D. 1998. Developmental morphology of stem galls of Diplolepis nodulosa (Hymenoptera: Cynipidae) and those modified by the inquiline Periclistus pirata (Hymenoptera: Cynipidae) on Rosa blanda (Rosaceae). Canadian Journal of Botany, 76: 365381.CrossRefGoogle Scholar
Bugbee, R.E. 1967. Revision of chalcid wasps of genus Eurytoma in America north of Mexico. Proceedings of the United States National Museum, 118(3533): 433552.CrossRefGoogle Scholar
Bugbee, R.E. 1975. A new species of the genus Eurytoma (Hymenoptera: Eurytomidae) from galls on Rubus and Chrysothalamnus. Journal of the Kansas Entomological Society, 48: 580584.Google Scholar
Bugbee, R.E. 1982. Six new species of Eurytoma and a parasite–host list of species described since 1967. Journal of the Kansas Entomological Society, 55: 159169.Google Scholar
Burks, B.D. 1971. A synopsis of the genera of the family Eurytomidae (Hymenoptera: Chalcidoidea). Transactions of the American Entomological Society, 97: 189.Google Scholar
Caltagirone, L.E. 1964. Notes on the biology, parasites, and inquilines of Pontania pacifica (Hymenoptera: Tenthredinidae), a leaf-gall incitant on Salix lasiolepis. Annals of the Entomological Society of America, 57: 279291.CrossRefGoogle Scholar
Csóka, G., Stone, G.N., and Melika, G. 2005. Biology, ecology, and evolution of gall-inducing Cynipidae. In Biology, ecology and evolution of gall-inducing arthropods. Vol. 2. Edited by Raman, A., Schaefer, C.W., and Withers, T.M.. Science Publishers, Inc., Enfield, New Hampshire. pp. 573–642.Google Scholar
Dennill, G.B. 1987. Establishment of the gall wasp Trichilogaster acaciaelongifoliae (Pteromalidae) for the biological control of Acacia longifolia in South Africa. Agriculture, Ecosystems and Environment, 19: 155168.CrossRefGoogle Scholar
Dreger-Jauffret, F., and Shorthouse, J.D. 1992. Diversity of gall-inducing insects and their galls. In Biology of insect-induced galls. Edited by Shorthouse, J.D. and Rohfritsch, O.. Oxford University Press, New York. pp. 833.Google Scholar
Fulmek, L. 1968. Parasitinsekten der insektengallen Europas. Beitrage zur Entomologie, 18: 719952.Google Scholar
Godfray, H.C.J. 1994. Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Princeton, New Jersey.CrossRefGoogle Scholar
Grissell, E.E. 1995. Toryminae (Hymenoptera: Chalcidoidea: Torymidae): a redefinition, generic classification, and annotated world catalog of species. In Memoirs on entomology, international. Vol. 2. Edited by Gupta, V.K.. Associated Publishers, Gainesville, Florida. pp. 1470.Google Scholar
Krombein, K.V., Hurd, P.D., Smith, D.R., and Burks, B.D. 1979. Catalogue of Hymenoptera in America north of Mexico. Smithsonian Institution Press, Washington, D.C.CrossRefGoogle Scholar
Lalonde, R.G., and Shorthouse, J.D. 2000. Using rose galls for field exercises in community ecology and island biogeography. The American Biology Teacher, 62: 436441.CrossRefGoogle Scholar
LaSalle, J. 2005. Biology of gall inducers and evolution of gall induction in Chalcidoidea (Hymenoptera: Eulophidae, Eurytomidae, Pteromalidae, Tanaostigmatidae, Torymidae). In Biology, ecology and evolution of gall-inducing arthropods. Vol. 2. Edited by Raman, A., Schaefer, C.W., and Withers, T.M.. Science Publishers, Inc., Enfield, New Hampshire. pp. 507537.Google Scholar
Leggo, J.J., and Shorthouse, J.D. 2006. Development of stem galls induced by Diplolepis triforma (Hymenoptera: Cynipidae) on Rosa acicularis (Rosaceae). The Canadian Entomologist, 138: 661680.CrossRefGoogle Scholar
Malyshev, S.I. 1968. Genesis of the Hymenoptera. Methuen and Co., London.CrossRefGoogle Scholar
Mani, M.S. 1964. Ecology of plant galls. Monographiae Biologicae. W. Junk, The Hague, the Netherlands.Google Scholar
Niblett, M. 1947. The species of Rhodites causing pea-galls on Rosa. II. Entomologist, 80: 121127.Google Scholar
Nieves-Aldrey, J.L., Vårdal, H., and Ronquist, F. 2005. Comparative morphology of terminal-instar larvae of Cynipoidea: phylogenetic implications. Zoologica Scripta, 34: 1536.CrossRefGoogle Scholar
Noble, N.S. 1940. Trichilogaster acaciae-longifoliae (Froggatt) (Hymenopt., Chalcidoidea), a wasp causing galling of the flower-buds of Acacia longifolia Willd., A. floribunda Sieber and A. sophorae. Transactions of the Royal Entomological Society of London, 90: 1338.CrossRefGoogle Scholar
O'Brien, T.P., and McCully, M.E. 1981. The study of plant structure: principles and selected methods. Termacarphi PTY, Melbourne, Australia.Google Scholar
Offman, S.T. 2004. Factors influencing structure of communities associated with galls induced by Diplolepis spinosa (Hymenoptera: Cynipidae) in northern Ontario. M.Sc. thesis, Laurentian University, Sudbury, Ontario.Google Scholar
Peck, O. 1963. A catalogue of the Nearctic Chalcidoidea (Insecta: Hymenoptera). The Canadian Entomologist, 30(Suppl.): 11092.Google Scholar
Price, P.W., Abrahamson, W.G., Hunter, M.D., and Melika, G. 2004. Using gall wasps on oaks to test broad ecological concepts. Conservation Biology, 18: 14051416.CrossRefGoogle Scholar
Quicke, D.L.J. 1997. Parasitic wasps. Chapman and Hall, London.Google Scholar
Randolph, S. 2005. The natural history of the rose bedeguar gall. The British Plant Gall Society. Prestige Typographics Ltd., Suffolk, United Kingdom.Google Scholar
Rohfritsch, O. 1971. Développement cécidien et rôle du parasite dans quelques galles d'arthropodes. Marcellia, 37: 233339.Google Scholar
Rohfritsch, O. 1992. Patterns in gall development. In Biology of insect-induced galls. Edited by Shorthouse, J.D. and Rohfritsch, O.. Oxford University Press, New York. pp. 6086.Google Scholar
Roininen, H., Price, P.W., and Tahvanainen, J. 1996. Bottom-up and top-down influences in the trophic system of a willow, a galling sawfly, parasitoids and inquilines. Oikos, 77: 4450.CrossRefGoogle Scholar
Ronquist, F. 1995. Phylogeny and early evolution of the Cynipoidea (Hymenoptera). Systematic Entomology, 20: 309335.CrossRefGoogle Scholar
Ronquist, F., and Liljeblad, J. 2001. Evolution of the gall wasp – host plant association. Evolution, 55: 25032522.Google ScholarPubMed
Roskam, J.C. 1992. Evolution of the gall-inducing guild. In Biology of insect-induced galls. Edited by Shorthouse, J.D. and Rohfritsch, O.. Oxford University Press, New York. pp. 3450.Google Scholar
Schröder, D. 1967. Diplolepis (= Rhodites) rosae (L.) (Hymenoptera: Cynipidae) and a review of its parasitoid complex in Europe. Commonwealth Institute of Biological Control Technical Bulletin No. 9: 93128.Google Scholar
Shorthouse, J.D. 1973. The insect community associated with rose galls of Diplolepis polita (Cynipidae, Hymenoptera). Quaestiones Entomologicae, 9: 5598.Google Scholar
Shorthouse, J.D. 1993. Adaptations of gall wasps of the genus Diplolepis (Hymenoptera: Cynipidae) and the role of gall anatomy in cynipid systematics. Memoirs of the Entomological Society of Canada, 165: 139163.CrossRefGoogle Scholar
Shorthouse, J.D. 1998. Role of Periclistus (Hymenoptera: Cynipidae) inquilines in leaf galls of Diplolepis (Hymenoptera: Cynipidae) on wild roses in Canada. In The biology of gall-inducing arthropods. US Forest Service General Technical Report NC-199. Edited by Csóka, G., Mattson, W.J., Stone, G.N., and Price, P.W.. US Department of Agriculture, Forest Service, North Central Forest Experiment Station, St. Paul, Minnesota. pp. 6181.Google Scholar
Shorthouse, J.D., and Leggo, J.J. 2002. Immature stages of the galler Diplolepis triforma (Hymenoptera: Cynipidae) with comments on the role of its prepupa. The Canadian Entomologist, 134: 433446.CrossRefGoogle Scholar
Stone, G.N., and Cook, J.M. 1998. The structure of cynipid oak galls: patterns in the evolution of an extended phenotype. Proceedings of the Royal Society of London, Series B: Biological Sciences, 265: 979988.CrossRefGoogle Scholar
Stone, G.N., and Schönrogge, K. 2003. The adaptive significance of insect gall morphology. Trends in Ecology and Evolution, 18: 512523.CrossRefGoogle Scholar
Stone, G.N., Schönrogge, K., Atkinson, R., Bellido, D., and Pujade-Villare, J. 2002. The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annual Review of Entomology, 47: 633668.CrossRefGoogle ScholarPubMed
Tormos, J., Asis, J.D., Gayubo, S.F., and Martin, M.A. 2004. Descriptions of the final instar of Eurytoma nodularis and E. heriadi (Hymenoptera: Eurytomidae). Florida Entomologist, 87: 278282.CrossRefGoogle Scholar
van Staden, J., Davey, J.E., and Noel, A.R.A. 1977. Gall formation in Erythrina latissima. Zeitschrift für Pflanzenphysiologie, 84: 283294.CrossRefGoogle Scholar
West, A., and Shorthouse, J.D. 1989. Initiation and development of the stem gall induced by Hemadas nubilipennis (Hymenoptera: Pteromalidae) on lowbush blueberry, Vaccinium angustifolium (Ericaceae). Canadian Journal of Botany, 67: 21872198.CrossRefGoogle Scholar
Wharton, R.A., and Hanson, P.E. 2005. Biology and evolution of braconid gall wasps (Hymenoptera). In Biology, ecology and evolution of gall-inducing arthropods. Vol. 2. Edited by Raman, A., Schaefer, C.W., and Withers, T.M.. Science Publishers, Inc., Enfield, New Hampshire. pp. 495505.Google Scholar
Wiebes-Rijks, A.A., and Shorthouse, J.D. 1992. Ecological relationships of insects inhabiting cynipid galls. In Biology of insect-induced galls. Edited by Shorthouse, J.D. and Rohfritsch, O.. Oxford University Press, New York. pp. 238257.Google Scholar
Williams, J.B., Shorthouse, J.D., and Lee, R.E. 2002. Extreme resistance to desiccation and microclimate-related differences in cold-hardiness of gall wasps (Hymenoptera: Cynipidae) overwintering on roses in southern Canada. The Journal of Experimental Biology, 205: 21152124.CrossRefGoogle ScholarPubMed
Zerova, M.D., and Fursov, V.N. 1991. The Palearctic species of Eurytoma (Hymenoptera: Eurytomidae) developing in stone fruits (Rosaceae: Prunoideae). Bulletin of Entomological Research, 81: 209219.CrossRefGoogle Scholar
Zerova, M.D., and Seryogina, L.Y. 1999. A review of Palearctic species of the genus Glyphomerus (Hymenoptera, Torymidae) with description of two new species. Entomological Review, 79: 977981.Google Scholar
Zuchlinski, J.A. 1979. Interactions among the inhabitants of a Diplolepis (Hymenoptera: Cynipidae) bud gall on Rosa acicularis (Rosaceae) in northern Ontario. M.Sc. thesis, Laurentian University, Sudbury, Ontario.Google Scholar