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Development of stem galls induced by Diplolepis triforma (Hymenoptera: Cynipidae) on Rosa acicularis (Rosaceae)

Published online by Cambridge University Press:  02 April 2012

Jonathan J. Leggo  and
Joseph D. Shorthouse
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: jshorthouse@laurentian.ca).
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Abstract

The cynipid Diplolepis triforma Shorthouse and Ritchie induces a fusiform, multi chambered stem gall from leaf buds on Rosa acicularis Lindl. in central and western Canada. Galls at all stages of development were fixed and sectioned using botanical histological techniques to illustrate, for the first time, the unique host-modifying abilities of gall-inducing cynipids that distinguish them from other phytophagous insects. Key events in gall ontogeny, whereby D. triforma gains control and redirects the development of attacked host tissues to provide larvae with shelter and food, include proliferation of cytoplasmically dense parenchymatous cells within the strands of the procambium at the point of egg contact, appearance of nutritive cells when larvae first begin to feed, formation of new xylem and phloem extending from un affected vascular bundles to the larval chambers, formation of several layers of nutritive cells during the period of larval feeding, and formation of sclerenchyma cells around each larval chamber. The role of these tissues in galler biology is explained.

Résumé

Le cynips Diplolepis triforma Shorthouse et Ritchie provoque la formation de galles fusiformes à logettes multiples à partir des bourgeons foliaires sur les tiges de Rosa acicularis Lindl. dans le centre et l'ouest du Canada. Nous avons fixé et sectionné à l'aide de techniques histologiques botaniques des galles à tous les stades de leur développement afin d'illustrer, pour la première fois, les capacités exceptionnelles des cynips cécidogènes pour modifier leur hôte, ce qui les distingue des autres insectes phytophages. Les étapes importantes de la cécidogenèse, par lesquelles D. triforma prend le contrôle des tissus de l'hôte attaqué et en dévie le développement pour procurer le gîte et la nourriture à ses larves, inclut la prolifération de cellules parenchymateuses à cytoplasme dense au milieu des bandes de procambium au point de contact de l'oeuf, l'apparition de cellules nourricières au moment où les larves commencent à s'alimenter, l'élaboration de nouveaux tissus de xylème et phloème s'étendant des faisceaux vasculaires non affectés vers les logettes des larves, la formation de plusieurs couches de cellules nourricières durant la période d'alimentation des larves et l'apparition de cellules sclérenchymateuses autour de chaque logette larvaire. Nous expliquons le rôle de ces tissus dans les biologie des insectes cécidogènes.

[Traduit par la Rédaction]

Type
Articles
Information
The Canadian Entomologist , Volume 138 , Issue 5 , October 2006 , pp. 661 - 680
Copyright
Copyright © Entomological Society of Canada 2006

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References

Adler, H. 1877. Beiträge zur Naturgeschichte der Cynipiden. Deutsche Entomologische Zeitschrift, 21: 209–247.Google Scholar
Aloni, R. 1987. Differentiation of vascular tissues. Annual Review of Plant Physiology, 38: 179–204.CrossRefGoogle Scholar
Aloni, R. 2001. Foliar and axial aspects of vascular differentiation: Hypotheses and evidence. Journal of Plant Growth Regulation, 20: 22–34.CrossRefGoogle Scholar
Aloni, R., Katz, D.A., and Wool, D. 1989. Effect of the gall-forming aphid Slavum wertheimae on the differentiation of xylem in branches of Pistacia atlantica. Annals of Botany, 63: 373–375.CrossRefGoogle Scholar
Askew, R.R. 1984. The biology of gall wasps. In Biology of gall insects. Edited by Ananthakrishnan, T.N.. Oxford and IBN, New Delhi, India. pp. 223–271.Google Scholar
Berleth, T., and Sachs, T. 2001. Plant morphogenesis: long-distance coordination and local patterning. Current Opinion in Plant Biology, 4: 57–62.CrossRefGoogle ScholarPubMed
Beyerinck, M.W. 1882. Beobachtungen über die ersten Entwicklungsphasen einiger Cynipidengallen. Natuurkundige Verhandelingen Koninklijke Akademie van Wetenschappen, 22: 1–198.Google Scholar
Bronner, R. 1977. Contribution à l'étude histochimique des tissus nourriciers des zoocécides. Marcellia, 40: 1–134.Google Scholar
Bronner, R. 1985. Anatomy of the ovipositor and oviposition behavior of the gall wasp Diplolepis rosae (Hymenoptera: Cynipidae). The Canadian Entomologist, 117: 849–858.CrossRefGoogle 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. 118–140.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: 1121–1140.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: 365–381.CrossRefGoogle Scholar
Cornell, H.V. 1983. The secondary chemistry and complex morphology of galls formed by the Cynipinae (Hymenoptera): why and how? The American Midland Naturalist, 110: 225–234.CrossRefGoogle Scholar
Crepsi, B.J., and Worobey, M. 1998. Comparative analysis of gall morphology in Australian gall thrips: the evolution of extended phenotypes. Evolution, 52: 1686–1698.Google 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
Dawkins, R. 1982. The extended phenotype. Oxford University Press, Oxford.Google Scholar
DeClerck, R.A., and Shorthouse, J.D. 1985. Tissue preference and damage by Fenusa pusilla and Messa nana (Hymenoptera: Tenthredinidae), leaf mining sawflies on white birch (Betula papyrifera). The Canadian Entomologist, 117: 351–362.CrossRefGoogle Scholar
Dengler, N.G. 2001. Regulation of vascular development. Journal of Plant Growth Regulation, 20: 1–13.CrossRefGoogle Scholar
Fourcroy, M., and Braun, C. 1967. Observations sur la galle de l'Aulax glechomae L. sur Glechoma hederacea L. II. Histologie et rôle physiologique de la coque sclérifiée. Marcellia, 34: 3–30.Google Scholar
Harper, L.J., Schönrogge, K., Lim, K.Y., Francis, P., and Lichtenstein, C.P. 2004. Cynipid galls: insect-induced modifications of plant development create novel plant organs. Plant, Cell and Environment, 27: 327–335.CrossRefGoogle Scholar
Harris, P., and Shorthouse, J.D. 1996. Effectiveness of gall inducers in weed biological control. The Canadian Entomologist, 128: 1021–1055.CrossRefGoogle Scholar
Houard, C. 1903. Recherches anatomiques sur les galles de tiges: Pleurocécidies. Bulletin Scientifique de France et Belgique, 38: 140–419.Google Scholar
Hough, J.S. 1953. Studies on the common spangle gall of oak. I. The developmental history. New Phytologist, 52: 149–177.CrossRefGoogle Scholar
Jankiewicz, L.S., Plich, H., and Antoszewsji, R. 1969. Preliminary studies on the translocation of 14C-labelled assimilates and 32PO3-4 towards the gall evoked by Cynips (Diplolepis) quercus-folii L on oak leaves. Marcellia, 36: 163–174.Google Scholar
Jensen, W.A. 1962. Botanical histochemistry. W.H. Freeman, San Francisco, California.Google Scholar
Kostoff, D., and Kendall, J. 1929. Studies on the structure and development of certain cynipid galls. Biological Bulletin, 56: 402–459.CrossRefGoogle Scholar
Küster, E. 1911. Die gallen der pflanzen. S. Hirzel, Leipzig, Germany.Google 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: 436–441.CrossRefGoogle Scholar
LeBlanc, D.A., and Lacroix, C.R. 2001. Developmental potential of galls induced by Diplolepis rosaefolii (Hymenoptera: Cynipidae) on the leaves of Rosa virginiana and the influence of Periclistus species on the Diplolepis rosaefolii galls. International Journal of Plant Sciences, 162: 29–46.CrossRefGoogle Scholar
Lewis, W.H. 1959. A monograph of the genus Rosa in North America. I. R. acicularis. Brittonia, 11: 1–24.CrossRefGoogle Scholar
Magnus, W. 1914. Die Entstehung der Pflanzengallen verursacht durch Hymenopteren. G. Fischer, Jena, Germany.Google Scholar
Mauseth, J.D. 1988. Plant anatomy. Benjamin/Cummings, Menlo Park, California.Google Scholar
Meyer, J. 1969. Irrigation vasculaire dans les galles. Memoires de la Societé Botanique de France. pp. 75–97.Google Scholar
Meyer, J. 1987. Plant galls and gall inducers. Gebrüder Borntraeger, Berlin, Germany.Google Scholar
Meyer, J., and Maresquelle, H.J. 1983. Anatomie des Galles. Gebrüder Borntraeger, Berlin, Germany.Google Scholar
Nuismer, S.L., and Thompson, J.N. 2001. Plant polyploidy and non-uniform effects on insect herbivores. Proceedings of the Royal Society of London, Series B: Biological Sciences, 268: 1937–1940.CrossRefGoogle ScholarPubMed
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
Plantard, O., Shorthouse, J.D., and Rasplu, J.-Y. 1998. Molecular phylogeny of the genus Diplolepis (Hymenoptera: Cynipidae). 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. 247–260.Google Scholar
Price, P.W., Fernandes, G.W., and Waring, G.L. 1987. Adaptive nature of insect galls. Environmental Entomology, 16: 15–24.CrossRefGoogle Scholar
Rickards, J.C., and Shorthouse, J.D. 1989. Overwintering strategy of the stem-gall inducer Diplolepis spinosa (Hymenoptera: Cynipidae) in central Ontario. Canadian Journal of Zoology, 67: 2232–2237.CrossRefGoogle Scholar
Rohfritsch, O. 1971. Développement cécidien et rôle du parasite dans quelques galles d'arthropodes. Marcellia, 37: 233–339.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. 60–86.Google Scholar
Rohfritsch, O., and Shorthouse, J.D. 1982. Insect galls. In Molecular biology of plant tumors. Edited by Kahl, G. and Schell, J.S.. Academic Press, New York. pp. 131–152.CrossRefGoogle Scholar
Ronquist, F., and Liljeblad, J. 2001. Evolution of the gall wasp — host plant association. Evolution, 55: 2503–2522.Google ScholarPubMed
Roth, P. 1949. Beitäge zur biologie der gallwespen. Naturforschende Gesellschaft, Basel, 60: 104–178.Google Scholar
Sachs, R. 2000. Integrating cellular and organismic aspects of vascular differentiation. Plant Cell Physiology, 41: 649–656.CrossRefGoogle ScholarPubMed
Salt, R.W. 1961. Principles of insect cold-hardiness. Annual Review of Entomology, 6: 55–74.CrossRefGoogle Scholar
Sass, J.E. 1958. Botanical microtechnique. Iowa University Press, Ames, Iowa.CrossRefGoogle Scholar
Savidge, R.A. 2001. Intrinsic regulation of cambial growth. Journal of Plant Growth Regulation, 20: 52–77.CrossRefGoogle Scholar
Shorthouse, J.D. 1973. The insect community associated with rose galls of Diplolepis polita (Cynipidae: Hymenoptera). Quaestiones entomologicae, 9: 55–98.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: 139–163.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. 61–81.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: 433–446.CrossRefGoogle Scholar
Shorthouse, J.D., and Ritchie, A.J. 1984. Description and biology of a new species of Diplolepis Fourcroy (Hymenoptera: Cynipidae) inducing galls on the stems of Rosa acicularis. The Canadian Entomologist, 116: 1623–1636.CrossRefGoogle Scholar
Shorthouse, J.D., and Rohfritsch, O. 1992. Biology of insect galls. Oxford University Press, New York.Google Scholar
Shorthouse, J.D., Leggo, J.J., Sliva, M.D., and Lalonde, R.G. 2005. Has egg location influenced the radiation of Diplolepis (Hymenoptera: Cynipidae) gall wasps on wild roses? Basic and Applied Ecology, 6: 423–434.CrossRefGoogle Scholar
St. John, M.G., and Shorthouse, J.D. 2000. Allocation patterns of organic nitrogen and mineral nutrients within stem galls of Diplolepis spinosa and Diplolepis triforma (Hymenoptera: Cynipidae) on wild roses (Rosaceae). The Canadian Entomologist, 132: 635–648.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: 979–988.CrossRefGoogle Scholar
Stone, G.N., and Schönrogge, K. 2003. The adaptive significance of insect gall morphology. Trends in Ecology and Evolution, 18: 512–523.CrossRefGoogle Scholar
Stone, G.N., Schönrogge, K., Atkinson, R.J., Bellido, D., and Pujade-Villar, J. 2002. The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annual Review of Entomology, 47: 633–668.CrossRefGoogle ScholarPubMed
Strong, D.R., Lawton, J.H., and Southwood, R. 1984. Insects on plants: community patterns and mechanisms. Blackwell Scientific Publications, Oxford.Google Scholar
Turner, J.S. 2000. The extended organism; the physiology of animal-built structures. Harvard University Press, Cambridge, Massachusetts.Google Scholar
Weidel, F. 1911. Beiträge zur entwicklungsgeschichte und vergleichenden anatomie der zynipidengallen der eiche. Flora, 102: 279–334.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.. Biology of insect-induced galls. Oxford University Press, New York. pp. 238–257.Google Scholar
Williams, J., Shorthouse, J.D., and Lee, R.E. Jr., 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: 2115–2124.CrossRefGoogle ScholarPubMed
Wool, D., Aloni, R., Ben-Zvi, O., and Wollberg, M. 1999. A galling aphid furnishes its home with a built-in pipeline to the host food supply. Entomologia Experimentalis et Applicata, 91: 183–186.CrossRefGoogle Scholar
Zeh, D.W., Zeh, J.A., and Smith, R.L. 1989. Ovipositors, amnions and eggshell architecture in the diversification of terrestrial arthropods. The Quarterly Review of Biology, 64: 147–168.CrossRefGoogle Scholar