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ALLOCATION PATTERNS OF ORGANIC NITROGEN AND MINERAL NUTRIENTS WITHIN STEM GALLS OF DIPLOLEPIS SPINOSA AND DIPLOLEPIS TRIFORMA (HYMENOPTERA: CYNIPIDAE) ON WILD ROSES (ROSACEAE)

Published online by Cambridge University Press:  31 May 2012

Mark G. St John
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
*
2 Author to whom all corresponding should be addressed (E-mail: jshortho@nickel.laurentian.ca).

Abstract

Concentrations of organic N and minerals Ca, Fe, K, Mg, Na, P, and S in tissues of galls induced by Diplolepis spinosa (Ashmead) and Diplolepis triforma Shorthouse and Ritchie in growth and maturation phases were compared with those in ungalled tissues of host roses and tissues distal to galls to increase our understanding of nutritional relationships between gall wasps and their host plants (Rosa blanda Aiton and Rosa acicularis Lindley, respectively). Concentrations of N and most mineral nutrients were lower in galls than in ungalled tissues, and tissues distal to galls, suggesting that cynipids regulate rather than concentrate nutrients within their galls. Concentrations of mineral nutrients within the larvae of both species of inducers, and their parasitoids, were determined for galls in the maturation phase. Absolute amounts of most minerals in gall tissues were positively correlated with the number of inhabitants, indicating that control of translocation of nutrients to galls occurs on a per inducer basis. Concentrations of nutrients in mature larvae of parasitoids were the same as concentrations in mature larvae of inducers, which explains why parasitism of gall inducers had no influence on the concentrations or amounts of nutrients in galls. Galls of D. triforma had greater concentrations of N and most mineral nutrients than did galls of D. spinosa. Likewise, larvae of D. triforma, and the parasitoids feeding on D. triforma, had greater concentrations of N and mineral nutrients than did larvae of D. spinosa and its parasitoids. Galls of both species had different concentrations of nutrients compared with ungalled tissues and tissues distal to the galls. Galls of both species also had seasonal decreases in concentrations of nutrients. Parasitoids of each species of inducer were generally similar in mineral composition to their hosts.

Résumé

Nous avons comparé les concentrations d’azote (N) organique et des minéraux Ca, Fe, K, Mg, Na, P et S dans les tissus des galles de Diplolepis spinosa (Ashmead) et de Diplolepis triforma Shorthouse et Ritchie durant les phases de croissance et de maturation, avec celles de tissus d’églantiers sains et de tissus situés au-delà des galles, dans le but de mieux comprendre les relations entre ces cynips gallicoles et leurs hôtes respectifs, les églantiers Rosa blanda Aiton et Rosa acicularis Lindsey. Les concentrations de N et de la plupart des minéraux étaient plus faibles dans les galles que dans le tissus sains ou les tissus en position distale par rapport aux galles, ce qui semble indiquer que ces cynips sont capables de contrôler, mais non de concentrer les éléments nutritifs dans leurs galles. Les concentrations de nutriments minéraux chez les larves des deux espèces de guêpes gallicoles et chez leurs parasitoïdes ont été déterminées dans les galles en phase de maturation. Les quantités absolues de la plupart des minéraux dans les tissus des galles étaient en corrélation positive avec le nombre d’insectes habitant la galle, ce qui indique que le transport des nutriments vers les galles est dû à l’action individuelle des guêpes gallicoles. Les concentrations de nutriments dans les larves à maturité des parasitoïdes étaient les mêmes que celles trouvées dans les larves à maturité des guêpes gallicoles, ce qui explique pourquoi le parasitisme des guêpes gallicoles n’a pas d’influence sur les concentrations ou sur les quantités de nutriments dans les galles. Les galles de D. triforma contenaient de plus grandes concentrations de N et de la plupart des minéraux que les galles de D. spinosa. De même, les larves de D. trifoma et les parasitoïdes qui s’en nourrissent avaient de plus grandes concentrations de N et de minéraux que les larves de D. spinosa et leurs parasitoïdes. Les galles des deux espèces avaient des concentrations de nutriments différentes de celles des tissus sains ou de tissus situés au-delà des galles. Les galles des deux espèces ont subi des diminutions saisonnières de leurs concentrations de nutriments. Les parasitoïdes de chacune des espèces de guêpe gallicole avaient généralement une composition minérale semblable à celle de leur hôte.

[Traduit par la Rédaction]

Type
Articles
Copyright
Copyright © Entomological Society of Canada 2000

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References

Abrahamson, W.G., McCrea, K.D. 1986. Nutrient and biomass allocation in Solidago altissima: effects of two stem gallmakers, fertilization, and ramet isolation. Oecologia 68: 174–80Google Scholar
Abrahamson, W.G., Weis, A.E. 1987. Nutritional ecology of arthropod gall makers. pp. 235–58 in Slansky, F. Jr., Rodriguez, J.G. (Eds.), Nutritional ecology of insects, mites, spiders, and related invertebrates. New York: John Wiley and SonsGoogle Scholar
Abrahamson, W.G., Weis, A.E. 1997. Evolutionary ecology across three trophic levels: goldenrods, gallmakers, and natural enemies. Princeton: Princeton University PressGoogle Scholar
Anderson, P.C., Mizell, R.F. 1987. Physiological effects of galls induced by Phylloxera notabilis (Homoptera: Phyloxeridae) on pecan foliage. Environmental Entomology 16: 264–8CrossRefGoogle Scholar
Askew, R.R. 1984. The biology of gall wasps. pp. 223–71 in Ananthakrishnan, T.N. (Ed.), Biology of gall insects. New Delhi: Oxford-IBHGoogle Scholar
Askew, R.R., Shaw, M.R. 1986. Parasitoid communities: their size, structure and development. pp. 225–64 in Waage, J., Greathead, D. (Eds.), Insect parasitoids. London: Academic PressGoogle Scholar
Bagatto, G., Shorthouse, J.D. 1994 a. Mineral nutrition of galls induced by Diplolepis spinosa (Hymenoptera: Cynipidae) on wild and domestic roses in central Canada. pp. 405–28 in Williams, M.A.J. (Ed.), Plant galls: organisms, interactions, populations. Systematics Association, Special Volume Number 9. Oxford: Clarendon PressGoogle Scholar
Bagatto, G., Shorthouse, J.D. 1994 b. Mineral concentrations within cells of galls induced by Hemadas nubilipennis (Hymenoptera: Pteromalidae) on lowbush blueberry: evidence from cryoanalytical scanning electron microscopy. Canadian Journal of Botany 72: 1387–90CrossRefGoogle Scholar
Bagatto, G., Shorthouse, J.D. 1997. Accumulation of mineral nutrients by the galler Hemadas nubilipennis (Hymenoptera: Pteromalidae) and its parasitoids on lowbush blueberry: implications for feeding behaviour. pp. 159–68 in Raman, A. (Ed.), Ecology and evolution of plant-feeding insects in natural and man made environments. New Delhi: International Scientific PublicationsGoogle Scholar
Bagatto, G., Zmijowskyj, T.J., Shorthouse, J.D. 1991. Galls induced by Diplolepis spinosa influence distribution of mineral nutrients in the shrub rose. HortScience 26: 1283–4CrossRefGoogle Scholar
Bagatto, G., Paquette, L.C., Shorthouse, J.D. 1996. Influence of galls of Phanacis taraxici on carbon partitioning within common dandelion, Taraxacum officinale. Entomologia Experimentalis et Applicata 79: 111–7CrossRefGoogle Scholar
Bazzaz, F.A., Grace, J. 1997. Plant resource allocation. San Diego: Academic PressGoogle Scholar
Brewer, J.W., Bishop, J.N., Skuhravy, V. 1987. Levels of foliar chemicals in insect-induced galls (Dipt., Cecidomyiidae). Zeitschrift fuer Angewandte Entomologie 104: 503–10Google Scholar
Bronner, R. 1992. The role of nutritive cells in the nutrition of cynipids and cecidomyiids. pp. 118–40 in Shorthouse, J.D., Rohfritsch, O. (Eds.), Biology of insect-induced galls. New York: Oxford University PressGoogle Scholar
Brooks, S.E., 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: 1121–40Google Scholar
Brooks, S.E., 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: 365–81CrossRefGoogle Scholar
Clifford, P.E. 1992. Understanding the source-sink concept of phloem translocation. Journal of Biological Education 26: 112–6Google Scholar
Fay, P.A., Hartnett, D.C. 1991. Constraints on growth and allocation patterns of Silphium integrifolium (Asteraceae) caused by a cynipid gall wasp. Oecologia 88: 243–50Google Scholar
Fernandes, M.S., Rossiello, R.O.P. 1995. Mineral nitrogen in plant physiology and plant nutrition. Critical Reviews in Plant Sciences 14: 111–48Google Scholar
Fourcroy, M., Braun, C. 1967. Observations sur la galle de l'Aulax glecomas L. sur Glechoma hederacea L. II. Histologie et rôle physiologique de la coque sclérifié. Marcellia 34: 340Google Scholar
Harper, J.L. 1977. Population biology of plants. New York: Academic PressGoogle Scholar
Harris, P., Shorthouse, J.D. 1996. Effectiveness of gall inducers in weed biological control. The Canadian Entomologist 128: 1021–55Google Scholar
Hartley, S.E. 1990. What are galls for? Tests of the nutrition hypothesis. pp. 265–74 in Jermy, T., Szentesi, A., Dezso, G., Horvath, J. (Eds.), Proceedings of the 7th International Symposium on Insect Galls. Budapest: Hungarian Academy of SciencesGoogle Scholar
Hartley, S.E. 1998. The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall-former? Oecologia 113: 492501Google Scholar
Hartley, S.E., Lawton, J.H. 1992. Host-plant manipulation by gall-insects: a test of the nutrition hypothesis. Journal of Animal Ecology 61: 113–19Google Scholar
Ho, L.C. 1988. Metabolism and compartmentation of imported sugars in sink organs in regulation to sink strength. Annual Review of Plant Physiology and Plant Molecular Biology 39: 355–78Google Scholar
House, H.L. 1965. Insect nutrition. pp. 796813in Rockstein, M. (Ed.), The physiology of Insecta Volume II. New York: Academic PressGoogle Scholar
Jones, J.B., Wolf, B., Mills, H.A. 1991. Plant analysis handbook. Athens, Georgia: Micro-Macro Publishing, Inc.Google Scholar
Kaitaniemi, P., Honkanen, T. 1996. Simulating source–sink control of carbon and nutrient translocation in a modular plant. Ecological Modelling 88: 227–40Google Scholar
Larson, K.C., Whitham, T.G. 1991. Manipulation of food resources by a gall-forming aphid: the physiology of sink–source interactions. Oecologia 88: 1521CrossRefGoogle ScholarPubMed
Larson, K.C., Whitham, T.G. 1997. Competition between gall aphids and natural plant sinks: plant architecture affects resistance to galling. Oecologia 109: 575–82Google Scholar
Marschner, H. 1983. General introduction to the mineral nutrition of plants. pp. 560in Lauchli, A., Bieleski, R.L. (Eds.), Inorganic plant nutrition. New York: Springer-VerlagGoogle Scholar
Mattson, W.J. 1980. Herbivory in relation to plant nitrogen content. Annual Review of Ecology and Systematics 11: 119–61Google Scholar
Mattson, W.J., Scriber, J.M. 1987. Nutritional ecology of insect folivores of woody plants: nitrogen, water, fiber, and mineral considerations. pp. 105–46 in Slansky, F. Jr., Rodriguez, J.G. (Eds.), Nutritional ecology of insects, mites, spiders, and related invertebrates. New York: John Wiley and SonsGoogle Scholar
McCrea, K.D., Abrahamson, W.G., Weis, A.E. 1985. Goldenrod ball gall effects on Solidago altissima: 14C translocation and growth. Ecology 66: 1902–7Google Scholar
Mehra, A., Farrago, M.E. 1994. Metal ions and plant nutrition. pp. 3166in Farrago, M.E. (Ed.), Plants and the chemical elements: biochemistry, uptake, tolerance and toxicity. New York: VCHGoogle Scholar
Meyer, J., Maresquelle, H.J. 1983. Anatomie des galles. Stuttgart: Gebrüder BorntraegerGoogle Scholar
Norman, G.R., Streiner, D.L. 1994. Biostatistics: the bare essentials. Mosby: St. LouisGoogle Scholar
Paclt, J., Hassler, J. 1967. Concentration of nitrogen in some plant galls. Phyton 12: 173–6Google Scholar
Paquette, L.C., Bagatto, G., Shorthouse, J.D. 1993. Distribution of mineral nutrients within the leaves of common dandelion (Taraxacum officinale) galled by Phanacis taraxaci (Hymenoptera: Cynipidae). Canadian Journal of Botany 71: 1026–31CrossRefGoogle Scholar
Price, P.W., Fernandes, G.W., Waring, G.L. 1987. Adaptive nature of insect galls. Environmental Entomology 16: 1524Google Scholar
Rohfritsch, O. 1992. Patterns in gall development. pp. 6086in Shorthouse, J.D., Rohfritsch, O. (Eds.), Biology of insect-induced galls. New York: Oxford University PressGoogle Scholar
Schoonhoven, L.M., Jenny, T., van Loon, J.J.A. 1998. Insect–plant biology: from physiology to evolution. London: Chapman and HallGoogle Scholar
Shorthouse, J.D. 1988. Occurrence of two gall wasps of the genus Diplolepis (Hymenoptera: Cynipidae) on the domestic shrub rose, Rosa rugosa Thunb. (Rosaseae). The Canadian Entomologist 120: 727–37Google Scholar
Shorthouse, J.D. 1993. Adaptations of gall wasps of the genus Diplolepis (Hymenoptera: Cynipidae) and the role of gall anatomy in cynipid systematics. pp. 139–63 in Ball, G.E., Danks, H.V. (Eds.), Systematics and entomology: diversity, distribution, adaptation, and application. Memoirs of the Entomological Society of Canada 165Google Scholar
Shorthouse, J.D., 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: 1623–36Google Scholar
Shorthouse, J.D., Rohfritsch, O. (Editors). 1992. Biology of insect-induced galls. New York: Oxford University PressGoogle Scholar
Skuhravy, V., Skuhravá, M., Brewer, J.W. 1980. Evaluation of plant damage by three species of gall midge (Diptera: Cecidomyiidae). Zeitschrift fuer Angewandte Entomologie 90: 184–90Google Scholar
Slansky, F., Feeny, P. 1977. Stabilization of the rate of nitrogen accumulation by larvae of the cabbage butterfly on wild and cultivated food plants. Ecological Monographs 47: 209–28Google Scholar
Thompson, K., Stewart, A.J.A. 1981. The measurement and meaning of reproductive effort in plants. American Naturalist 177: 205–11Google Scholar
Welch, R.M. 1995. Micronutrient nutrition of plants. Critical Reviews in Plant Sciences 14: 4982Google Scholar
White, T.C.R. 1993. The inadequate environment: nitrogen and the abundance of animals. Heidelberg: Springer-VerlagGoogle Scholar
Wiebes-Rijks, A.A., Shorthouse, J.D. 1992. Ecological relationships of insects inhabiting cynipid galls. pp. 238–57 in Shorthouse, J.D., Rohfritsch, O. (Eds.), Biology of insect-induced galls. New York: Oxford University PressGoogle Scholar
Williams, M.A.J. (Editor). 1994. Plant galls: organisms, interactions, populations. Systematics Association, Special Volume Number 9. Oxford: Clarendon PressGoogle Scholar