Abstract
Studies on plant-defensive chemistry have mainly focused on plants in direct interaction with aboveground and occasionally belowground herbivores and pathogens. Here we investigate whether decomposers and the spatial distribution of organic residues in soil affect plant-defensive chemistry. Litter concentrated in a patch (vs. homogeneously mixed into the soil) led to an increase in the aucubin content in shoots of Plantago lanceolata. Earthworms increased total phytosterol content of shoots, but only when the litter was mixed homogeneously into the soil. The phytosterol content increased and aphid reproduction decreased with increasing N concentration of the shoots. This study documents for the first time that earthworms and the spatial distribution of litter may change plant-defensive chemistry against herbivores.
Similar content being viewed by others
REFERENCES
Alphei, J., Bonkowski, M., and Scheu, S. 1996. Protozoa, Nematoda and Lumbricidae in the rhizophere of Hordelymus europaeus (Poaceae): Faunal interactions, response of microorganisms and effects on plant growth. Oecologia 106:111–126.
Bodnaryk, R. P., Luo, M., and Kudryk, L. 1997. Effects of modifying the phytosterol profile of canola, Brassica napus L., on growth, development, and survival of the bertha armyworm, Mamestra configurata Walker (Lepidoptera: Noctuidae), the flea beetle, Phyllotreta cruciferae (Goeze) (Coleoptera: Chrysomelidae) and the aphids, Lipaphis erysimi (Kaltenbach) and Myzus persicae (Sulzer) (Homoptera: Aphididae). Can. J. Plant Sci. 77:677–683.
Bowers, M. D. and Puttick, G. M. 1988. Response of generalist and specialist insects to qualitative allelochemical variation. J. Chem. Ecol. 14:319–334.
Brussaard, L. 1999. On the mechanisms of interactions between earthworms and plants. Pedobiologia 43:880–885.
Campell, B. C. and Nes, W. D. 1983. A reappraisal of sterol biosynthesis and metabolism in aphids. J. Insect Physiol. 29:149–156.
Darrow, K. and Bowers, M. D. 1999. Effects of herbivore damage and nutrient level on induction of iridoid glycosides in Plantago lanceolata. J. Chem. Ecol. 25: 1427–1440.
Douglas, A. E. 1998. Nutritional interactions in insect-microbial symbiosis: Aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 43:17–37.
Dugassa-Gobena, D., Von Alten, H., and SchÖnbeck, F. 1996. Effects of arbuscular mycorrhiza (AM) on health of Linum usitatissimum L. infected by fungal pathogens. Plant Soil 185:173–182.
Fajer, E. D., Bowers, M. D., and Bazzaz, F. A. 1992. The effects of nutrients and enriched CO2 environments on production of carbon-based allelochemicals in Plantago: A test of the carbon/nutrient balance hypothesis. Am. Nat. 140:707–723.
Gange, A. and West, H. M. 1994. Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytol. 128:79–87.
Gardner, D. R. and Stermitz, F. R. 1988. Host plant utilization and iridoid glycoside sequestration by Euphydryas anicia (Lepidoptera: Nymphalidae). J. Chem. Ecol. 14:2147–2168.
Haimi, J., Huhta, V., and Boucelham, M. 1992. Growth increase of birch seedlings under the influence of earthworms—A laboratory study. Soil Biol. Biochem. 14:1525–1528.
Hutchings, M. J. and De Kroon, H. 1994. Foraging in plants: The role of morphological plasticity in resource acquisition. Adv. Ecol. Res. 25:159–238.
Ishikawa, H. 1989. Biochemical and molecular aspects of the aphid endocytobiosis, pp. 123–143, in W. Schwemmler and G. Gassner (eds.). Insect Endocytobiosis: Morphology, Physiology, Genetics, Evolution. CRC Press, Boca Raton, FL.
Jarzomski, C. M., Stamp, N. E., and Bowers, M. D. 2000. Effects of plant phenology, nutrients and herbivory on growth and defensive chemistry of plantain, Plantago lanceolata. Oikos 88:371–379.
Karban, R. and Baldwin, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago.
Lehrer, A. T., Dugassa-Gobena, D., Vidal, S., and Seifert, K. 2000. Transport of resistance-inducing sterols in phloem sap of Barley. Z. Naturforsch. 55c:948–952.
Newton, A. C. 1989. Measuring the sterol content of barley leaves infected with powdery mildew as a means of assessing partial resistance of Erysiphe graminis fr.sp. hordei. Plant Pathol. 38:534–540.
Puttick, G. M. and Bowers, M. D. 1988. The effect of qualitative and quantitative variation in allelochemicals on a generalist insect: Iridoid glycosides and the southern armyworm. J. Chem. Ecol. 14:319–334.
Reineking, A., Langel, R., and Schikowski, J. 1993. 15N, 13C-on-line measurements with an elemental analyser (Carlo Erba, NA 1500), a modified trapping box and a gas isotope mass spectrometer (Finnigan, MAT 251). Isotopenpraxis Environ. Health Stud. 29:169–174.
Robinson, D. 1994. The responses of plants to non-uniform supplies of nutrients. New Phytol. 127:635–674.
Scheu, S. 2003. Effects of earthworms on plant growth: Patterns and perspectives. Pedobiologia 47:846–856.
Scheu, S., Theenhaus, A., and Jones, T. H. 1999. Links between the detritivore and the herbivore system: Effects of earthworms and Collembola on plant growth and aphid development. Oecologia 119:541–551.
Stamp, N. E. and Bowers, M. D. 2000. Do enemies of herbivores influence plant growth and chemistry? Evidence from a seminatural experiment. J. Chem. Ecol. 26:2367–2386.
Svoboda, J. A., Feldlaufer, M. F., and Weirich, G. F. 1994. Evolutionary aspects of steroid utilization in insects, pp. 126–139, in W. D. Nes (ed.). Isopentenoids and Other Natural Products. Evolution and Function. ACS Symposium Series, American Chemical Society, Washington, DC.
Van Dam, N. M., Harvey, J. A., WÄckers, F. L., Bezemer, T. M., Van Der Putten, W. H., and Vet, L. E. M. 2003. Interactions between aboveground and belowground induced responses against phytophages. Basic Appl. Ecol. 4:63–77.
Vidal, S. and Dugassa-Gobena, D. 1999. Wirkungsmechanismen von antagonistischen Wechselbeziehungen zwischen Organismen verschiedener trophischer Ebenen: Nutzungsmöglichkeiten im Pflanzenschutz. Ergeb. landwirtschaft. Forsch. Justus-Liebig-Universität 14:49–69.
Wolters, V. and Stickan, W. 1991. Resource allocation of beech seedlings (Fagus sylvatica L.)—Relationship to earthworm activity and soil conditions. Oecologia 88:125–131.
Wurst, S. and Jones, T. H. 2003. Indirect effects of earthworms (Aporrectodea caliginosa) on an above-ground tritrophic interaction. Pedobiologia 47:91–97.
Wurst, S., Langel, R., Reineking, A., Bonkowski, M., and Scheu, S. 2003. Effects of earthworms and organic litter distribution on plant performance and aphid reproduction. Oecologia 137:90–96.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Wurst, S., Dugassa-Gobena, D. & Scheu, S. Earthworms and Litter Distribution Affect Plant-Defensive Chemistry. J Chem Ecol 30, 691–701 (2004). https://doi.org/10.1023/B:JOEC.0000028425.43869.b8
Issue Date:
DOI: https://doi.org/10.1023/B:JOEC.0000028425.43869.b8