Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-24T13:09:00.934Z Has data issue: false hasContentIssue false

Interactions between galling insects and leaf-feeding insects: the role of plant phenolic compounds and their possible interference with herbivores

Published online by Cambridge University Press:  01 May 2008

Enrique Pascual-Alvarado
Affiliation:
Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Michoacán, México
Pablo Cuevas-Reyes*
Affiliation:
Laboratorio de Ecología de Interacciones Bióticas, Facultad de Biología, Universidad Michoacana de San Nicolás de Hidalgo, Ciudad Universitaria, Morelia, Michoacán, México
Mauricio Quesada
Affiliation:
Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Michoacán, México
Ken Oyama
Affiliation:
Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Michoacán, México
*
1Corresponding author. Email: [email protected]

Abstract:

The objective of this study was to determine the effects of gall induction on leaf phenolic compounds and their indirect effects on the subsequent attack of folivorous insects in Achatocarpus gracilis, Cordia alliodora, Guapira macrocarpa, Guettarda elliptica and Ruprechtia fusca that occur in both hillside and riparian sites at Chamela-Cuixmala tropical dry forest in western Mexico. There are differences in soil water content between riparian and hillside sites where trees in the first are mainly evergreen and deciduous in the second. A few tree species occur in both sites and their intraspecific phenological response is also different between sites. In this case, trees of a given species that occur in riparian sites will be evergreen whereas trees on hillsides of the same species will be deciduous. Four plant species had significantly greater total phenol concentrations in galled than ungalled leaves in both deciduous hillside and riparian sites. In three plant species associated with galls, host total phenol concentrations were significantly greater in short than in tall plants. The frequency and amount of folivore damage were greater in leaves without galls than leaves with galls in these four plant species. These results indicate that galling insect species may directly affect leaf phenolic concentrations and indirectly may affect the incidence and consumption of folivorous insects in tropical plant species. This may have important consequences on the preference of leaves by folivorous insects that might be excluded by galling insect species in this dry tropical system.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ABRAHAMSON, W. G. & WEIS, A. E. 1986. Evolutionary ecology of arthropod gall makers. Pp. 235258 in Slansky, F. & Rodriguez, J. G. (eds.). Nutritional ecology of insects, mites, spiders, and related invertebrates. Wiley-Interscience, New York.Google Scholar
ABRAHAMSON, W. G., MCCREA, K. D., WHITWELL, A. J. & VERNIER, L. A. 1991. The role of phenolic compounds in goldenrod ball resistance and formation. Biochemical Systematics and Ecology 19;615622.CrossRefGoogle Scholar
ANANTHAKRISHNAN, T. N. 1984. Adaptative strategies in cecidogenous insects. Pp. 19 in Ananthakrishan, T. N. (ed.). The biology of gall insects. Oxford University Press and IBH, New Delhi.Google Scholar
ASKEW, R. R. 1984. The biology of gall-wasps. Pp. 223271 in Ananthakrishan, T. N. (ed.). The biology of gall insects. Oxford and IBH, New Delhi.Google Scholar
BENNET, R. N. & WALLS-GROVE, R. M. 1994. Secondary metabolites in plant defence mechanisms. New Phytologist 127;617633.CrossRefGoogle Scholar
BIRCH, M. L., BREWER, J. & ROHFRITSCH, O. 1992. Biology of Dasineura affinis (Cecidomyiidae) and influence of its gall on Viola odorata. Pp. 171184 in Shorthouse, J. D. & Rohfritsch, O. (eds.). Biology of insect-induced galls. Oxford University Press, New York.Google Scholar
BULLOCK, S. H. 1985. Breeding systems in the flora of tropical deciduous forest in Mexico. Biotropica 4:287301.CrossRefGoogle Scholar
BULLOCK, S. H. & SOLÍS-MAGALLANES, J. A. 1990. Phenology of canopy trees of a tropical deciduous forest in Mexico. Biotropica 22:2235.CrossRefGoogle Scholar
CORNELL, H. V. 1983. The secondary chemistry and complex morphology of galls formed by Cynipinae (Hymenoptera): why and how? American Midland Naturalist 110:225234.CrossRefGoogle Scholar
CUEVAS-REYES, P., SIEBE, C., MARTÍNEZ-RAMOS, M. & OYAMA, K. 2003. Species richness of gall-forming insects in a tropical rain forest: correlations with plant diversity and soil fertility. Biodiversity and Conservation 3:411422.CrossRefGoogle Scholar
CUEVAS-REYES, P., QUESADA, M., HANSON, P., DIRZO, R. & OYAMA, K. 2004a. Diversity of gall-forming insects in a Mexican tropical dry forest: the importance of plant species richness, life forms, host plant age and plant density. Journal of Ecology 92:707716.CrossRefGoogle Scholar
CUEVAS-REYES, P., SIEBE, C. & OYAMA, K. 2004b. Spatial patterns of herbivory by gall-forming insects: a test to the soil fertility hypothesis in a Mexican tropical dry forest. Oikos 107:181189.CrossRefGoogle Scholar
CUEVAS-REYES, P., QUESADA, M. & OYAMA, K. 2006. Abundance and leaf damage caused by gall-inducing insects in a Mexican tropical dry forest. Biotropica 38:107115.CrossRefGoogle Scholar
DICKE, M. 2000. Chemical ecology of host-plant selection by herbivorous arthropods: a multitrophic perspective. Biochemical Systematics and Ecology 28:601617.CrossRefGoogle ScholarPubMed
DREGER-JAUFFRET, J. D. & SHORTHOUSE, J. D. 1992. Diversity of gall-inducing insects and their galls. Pp. 834 in Shorthouse, J. D. & Rohfritsch, O. (eds.). Biology of insect-induced galls. Oxford University Press, Oxford.Google Scholar
FERNANDES, G. W. & PRICE, P. W. 1992. The adaptative significance of insect gall distributions: survivorship of species in xeric and mesic habitats. Oecologia 90:1420.CrossRefGoogle ScholarPubMed
FILIP, V., DIRZO, R., MAASS, J. M. & SARUKHÁN, J. 1995. Within-and among-year variation in the levels of herbivory on the foliage of trees from a Mexican tropical deciduous forest. Biotropica 27:7886.CrossRefGoogle Scholar
FISHER, A. E. I., HARTLEY, S. E. & YOUNG, M. 2000. Direct and indirect competitive effects of foliage feeding guilds on the performance of the birch leaf-miner Eriocrania. Journal of Animal Ecology 69:165176.CrossRefGoogle Scholar
FOSS, L. K. & RIESKE, L. K. 2004. Stem galls affects oak foliage with potential consequences for herbivory. Ecological Entomology 29:273280.CrossRefGoogle Scholar
FRANKIE, G. W., BAKER, H. G. & OPLER, P. A. 1974. Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. Journal of Ecology 62:881899.CrossRefGoogle Scholar
GENTRY, A. H. 1982. Patterns of Neotropical plant species diversity. Evolutionary Biology 15:154.Google Scholar
GENTRY, A. H. 1988. Changes in plant community diversity and floristic composition on environmental and geographical gradients. Annals of the Missouri Botanical Garden 75:134.CrossRefGoogle Scholar
HARBORNE, J. B. 1988. Introduction to ecological biochemistry. Academic Press, London. 243 pp.Google Scholar
HARBORNE, J. B. & GRAYER, R. J. 1993. Flavonoids and insects. Pp. 589618 in Harborne, J. B. (ed.). The flavonoids: advances in research. Chapman and Hall, London.CrossRefGoogle Scholar
HARTLEY, S. E. 1998. The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall-former. Oecologia 113:492501.CrossRefGoogle ScholarPubMed
HARTLEY, S. E. 1999. Are gall insects large rhizobia? Oikos 84:333342.CrossRefGoogle Scholar
HARTLEY, S. E. & JONES, C. G. 1997. Plant chemistry and herbivory, or why the world is green. Pp. 284324 in Crawley, M. J. (eds). Plant ecology. Blackwell Science, Oxford.Google Scholar
HARTLEY, S. E. & LAWTON, J. H. 1992. Host-plant manipulation by gall-insects: a test of the nutrition hypothesis. Journal of Animal Ecology 61:113119.CrossRefGoogle Scholar
KARBAN, R. & BALDWIN, I. T. 1997. Induced responses to herbivory. University of Chicago Press, Chicago. 301 pp.CrossRefGoogle Scholar
KOLEHMAINEN, J., ROININEN, H., JULKUNEN-TIITTO, R. & TAHVANAINEN, J. 1994. Importance of phenolic glucosides in host selection of shoot galling sawfly, Euura amerinae, on Salix pentandra. Journal of Chemical Ecology 20:24552466.CrossRefGoogle Scholar
LANGENHEIM, J. H. & STUBBLEBINE, W. H. 1983. Variation in leaf resin between parent tree and progeny in Hymenaea: implications for herbivory in the humid tropics. Biochemical Systematic and Ecology 11:97106.CrossRefGoogle Scholar
LARSON, K. C. & WHITHAM, T. G. 1991. Manipulation of food resources by a gall-forming aphid: the physiology of sink-source interactions. Oecologia 88:1521.CrossRefGoogle ScholarPubMed
LIEBERMAN, D. 1982. Seasonality and phenology in dry tropical forest in Ghana. Journal of Ecology 70:791806.CrossRefGoogle Scholar
LITTELL, R. C., FREUD, R. J. & SPECTOR, P. H. 1991. SAS system for linear models. SAS Institute, Cary, North Carolina. 329 pp.Google Scholar
LOTT, E., BULLOCK, S. H. & SOLIS-MAGALLANES, J. A. 1987. Floristic diversity and structure of upland and arroyo forest in coastal Jalisco. Biotropica 19:228235.CrossRefGoogle Scholar
MOOPER, S. & SIMBERLOFF, D. 1995. Differential herbivory in an oak population: the role of plant phenology and insect performance. Ecology 76:12331241.CrossRefGoogle Scholar
NYMAN, T. & JULKUNEN-TITTO, R. 2000. Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proceedings of the National Academy of Sciences, USA 97:1318413187.CrossRefGoogle ScholarPubMed
OPLER, P. A., FRANKIE, G. H. & BAKER, H. G. 1980. Comparative phenological studies of tree let and shrubs species in tropical wet and dry forests in the lowlands of Costa Rica. Journal of Animal Ecology 68:167188.CrossRefGoogle Scholar
PRICE, P. W., ROININEN, H. & TAHVANAINEN, J. 1987. Plant age and attack by the bud galler, Euura mucronata. Oecologia 73:334337.CrossRefGoogle ScholarPubMed
REICH, P. B. & BORCHERT, R. 1984. Water stress and tree phenology in a tropical dry forest in the lowlands of Costa Rica. Journal of Ecology 72:6174.CrossRefGoogle Scholar
ROININEN, H., PRICE, P. W., JULKUNEN-TIITTO, R., TAHVANAINEN, J. & IKONEN, A. 1999. Oviposition stimulant for a gall-inducing sawfly, Euura lasiolepis, on willow is a phenolic glucoside. Journal of Chemical Ecology 25:943953.CrossRefGoogle Scholar
RZEDOWSKI, J. 1978. Vegetación de México. Editorial Limusa, México. 432 pp.Google Scholar
SCHULTZ, B. B. 1992. Insect herbivores as potential causes of mortality and adaptation in gall-forming insects. Oecologia 90:297299.CrossRefGoogle Scholar
SHORTHOUSE, J. D. 1986. Significance of nutritive cells in insect galls. Proceedings of the Entomological Society of Washington 88:368375.Google Scholar
STONE, G. N. & SCHÖNROGGE, K. 2003. The adaptive significance of insect gall morphology. Trends in Ecology and Evolution 18:512522.CrossRefGoogle Scholar
STOKES, M. E., DAVIS, C. S. & KOCH, G. G. 2000. Categorical data analysis using the SAS system. (Second edition). SAS Institute, Cary. 626 pp.Google Scholar
TALLAMY, D. W. & RAUPP, M. J. 1991. Phytochemical induction by herbivores. John Wiley & Sons, New York. 280 pp.Google Scholar
TAPER, M. L. & CASE, T. J. 1987. Interactions between oak tannins and parasite community structure: unexpected benefits of tannins to cynipid gall-wasps. Oecologia 71:254261.CrossRefGoogle ScholarPubMed
TAYLOR, L. R. 1986. Synoptic dynamics, migration and the Rothamsted insect survey. Journal of Animal Ecology 55:138.CrossRefGoogle Scholar
TJIA, B. & HOUSTON, D. B. 1975. Phenolic constituents of Norway spruce resistant or susceptible to the eastern spruce gall aphid. Forest Science 21:180184.Google Scholar
VEREECKE, D., MESSENS, E., KLARSKOV, K., DE BRUYN, A., VAN MONTAGU, M. & GOETHALS, K. 1997. Patterns of phenolic compounds in leafy galls of tobacco. Planta 201:342348.CrossRefGoogle ScholarPubMed
VAN SCHAIK, C. P., TERBORGH, J. W. & WRIGHT, S. J. 1993. The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annual Review in Ecology and Systematics 24:353377.CrossRefGoogle Scholar
WARING, G. L. & PRICE, P. W. 1990. Plant water stress and gall formation (Cecidomyiidae: Asphondylia spp.) on creosote bush. Ecological Entomology 15:8795.CrossRefGoogle Scholar
WATERMAN, P. G. & MOLE, S. 1994. Analysis of phenolic plant metabolites. Blackwell Scientific Publications, Oxford. 238 pp.Google Scholar
WEIS, A. E., WALTON, R. & CREGO, C. L. 1988. Reactive plant tissue sites and the population biology of gall makers. Annual Review of Entomology 33:467486.CrossRefGoogle Scholar
WESTPHAL, E., BRONNER, R. & LE RET, M. 1981. Changes in leaves of susceptible and resistance Solanum dulcamara infested by the gall mite Eriophyes cladophthirus (Acarina, Eriphyoidea). Canadian Journal of Botany 59:875882.CrossRefGoogle Scholar
YUKAWA, J. 2000. Synchronization of gallers with host plant phenology. Population Ecology 42:105113.CrossRefGoogle Scholar
ZUCKER, W. V. 1982. How aphids choose leaves: the role of phenolics in host selection by a galling aphid. Ecology 63:972981.CrossRefGoogle Scholar