Community-wide effects of below-ground rhizobia on above-ground arthropods

Ecological Entomology

Volumn 36, Issue 1, 2011, Pages 43-51

  Katayama, Noboru ^a   Zhang, Zhi Qi ^a   Ohgushi, Takayuki ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Above and below ground interactions; Bottom up effects; Community structure; Glycine max; Rhizobia

Indexed keywords

ARTHROPOD; BELOWGROUND BIOMASS; BOTTOM-UP CONTROL; COMMUNITY STRUCTURE; GROWTH RATE; HERBIVORE; HOST PLANT; NUTRIENT UPTAKE; PREDATOR; RHIZOBACTERIUM; RHIZOSPHERE; SOYBEAN; SPECIES DIVERSITY; SPECIES RICHNESS; SYMBIOSIS; TAXONOMY; TROPHIC LEVEL;

ARTHROPODA; BACTERIA (MICROORGANISMS); GLYCINE MAX; RHIZOBIACEAE;

EID: 78650942211     PISSN: 03076946     EISSN: 13652311     Source Type: Journal    
DOI: 10.1111/j.1365-2311.2010.01242.x     Document Type: Article

References (68)

1. Bascompte, J. & Jordano, P. (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annual Review of Ecology, Evolution, and Systematics, 38, 567-593.
2. Cardinale, B.J., Weis, J.J., Forbes, A.E., Tilmon, K.J. & Ives, A.R. (2006) Biodiversity as both a cause and consequence of resource availability: a study of reciprocal causality in a predator-prey system. Journal of Animal Ecology, 75, 497-505.
3. Chaneton, E.J. & Omacini, M. (2007) Bottom-up cascades induced by fungal endophytes in multitrophic systems. Ecological Communities: Plant Mediation in Indirect Interaction Webs (ed. by T. Ohgushi, T. P. Craig and P. W. Price ), pp. 164-187. Cambridge University Press, Cambridge, U.K.
4. Crutsinger, G.M., Reynolds, W.N., Classen, A.T. & Sanders, N.J. (2008) Disparate effects of plant genotypic diversity on foliage and litter arthropod communities. Oecologia, 158, 65-75.
5. Denno, R.F., Finke, D.L. & Langellotto, G.A. (2005) Direct and indirect effects of vegetation structure and habitat complexity on predator-prey and predator-predator interactions. Ecology Predator-Prey Interactions (ed. by P. Barbosa and I. Castellanos ), pp. 211-239. Oxford University Press, Oxford, U.K.
6. Dudt, J.F. & Shure, D.J. (1994) The influence of light and nutrients on foliar phenolics and insect herbivory. Ecology, 75, 86-98.
7. Feeny, P. (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology, 51, 565-581.
8. Finke, D.L. & Denno, R.F. (2004) Predator diversity dampens trophic cascades. Nature, 429, 407-410.
9. Finkes, L.K., Cady, A.B., Mulroy, J.C., Clay, K. & Rudgers, J.A. (2006) Plant-fungus mutualism affects spider composition in successional fields. Ecology Letters, 9, 347-356.
10. Fonseca, C.R., Prado, P.I., Almeida-Neto, M., Kubota, U. & Lewinsohn, T.M. (2005) Flower-heads, herbivores, and their parasitoids: food web structure along a fertility gradient. Ecological Entomology, 30, 36-46.
11. Forkner, R.E. & Hunter, M.D. (2000) What goes up must come down? Nutrient addition and predation pressure on oak herbivores. Ecology, 81, 1588-1600.
12. Forkner, R.E., Marquis, R.J. & Lill, J.T. (2004) Feeny revisited: condensed tannins as anti-herbivore defences in leaf-chewing herbivore communities of Quercus. Ecological Entomology, 29, 174-187.
13. Gange, A.C. (2007) Insect-mycorrhizal interactions: patterns, processes and consequences. Ecological Communities: Plant Mediation in Indirect Interaction Webs (ed. by T. Ohgushi, T. P. Craig and P. W. Price ), pp. 124-144. Cambridge University Press, Cambridge, U.K.
14. Gange, A.C. & West, H.M. (1994) Interaction between arbuscular-mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytologist, 128, 79-87.
15. Gange, A.C., Stagg, P.G. & Ward, L.K. (2002) Arbuscular mycorrhizal fungi affect phytophagous insect specialism. Ecology Letters, 5, 11-15.
16. Gange, A.C., Brown, V.K. & Aplin, D.M. (2003) Multitrophic links between arbuscular mycorrhizal fungi and insect parasitoids. Ecology Letters, 6, 1051-1055.
17. Gotelli, N.J. & Colwell, R.K. (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters, 4, 379-391.
18. Gotelli, N.J. & Entsminger, G.L. (2004) EcoSim: Null Models Software for Ecology, Version 7. Acquired Intelligence Inc. & Kesey-Bear., Jericho, Vermont. URL [accessed in 2010].
19. Haddad, N.M., Haarstad, J. & Tilman, D. (2000) The effects of long-term nitrogen loading on grassland insect communities. Oecologia, 124, 73-84.
20. Haddad, N.M., Crutsinger, G.M., Gross, K., Haarstad, J., Knops, J.M. & Tilman, D. (2009) Plant species loss decreases arthropod diversity and shifts trophic structure. Ecology Letters, 12, 1029-1039.
21. Hairston, N.G., Smith, F.E. & Slobodkin, L.B. (1960) Community structure, population control and competition. American Naturalist, 94, 421-425.
22. Hartley, S.E. & Gange, A.C. (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annual Review of Entomology, 54, 323-342.
23. van der Heijden, M.G.A., Bardgett, R.D. & van Straalen, N.M. (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters, 11, 296-310.
24. Hunter, M.D. & Price, P.W. (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural community. Ecology, 73, 724-732.
25. Hunter, M.D., Ohgushi, T. & Price, P.W. (1992) Effects of Resource Distribution on Animal-Plant Interactions. Academic Press, San Diego, California.
26. Ings, T.C., Montoya, J.M., Bascompte, J., Blüthgen, N., Brown, L., Dormann, C.F. et al. (2009) Ecological networks - beyond food webs. Journal of Animal Ecology, 78, 253-269.
27. Ives, A.R., Kareiva, P. & Perry, R. (1993) Response of a predator to variation in prey density at 3 hierarchical scales - lady beetles feeding on aphids. Ecology, 74, 1929-1938.
28. Jani, A.J., Faeth, S.H. & Gardner, D. (2010) Asexual endophytes and associated alkaloids alter arthropod community structure and increase herbivore abundances on a native grass. Ecology Letters, 13, 106-117.
29. Johnson, M.T.J. & Agrawal, A.A. (2005) Plant genotype and environment interact to shape a diverse arthropod community on evening primrose (Oenothera biennis). Ecology, 86, 874-885.
30. Kaplan, I. & Denno, R.F. (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecology Letters, 10, 977-994.
31. Katayama, N., Nishida, T., Zhang, Z.Q. & Ohgushi, T. (2010) Belowground microbial symbiont enhances plant susceptibility to a spider mite through change in soybean leaf quality. Population Ecology, 52, 499-506.
32. Kempel, A., Brandl, R. & Schädler, M. (2009) Symbiotic soil microorganisms as players in aboveground plant-herbivore interactions - the role of rhizobia. Oikos, 118, 634-640.
33. Kempel, A., Schmidt, A.K., Brandl, R. & Schädler, M. (2010) Support from the underground: induced plant resistance depends on arbuscular mycorrhizal fungi. Functional Ecology, 24, 293-300.
34. Knops, J.M.H., Tilman, D., Haddad, N.M., Naeem, S., Mitchell, C.E., Haarstad, J. et al. (1999) Effects of plant species richness on invasion dynamics, disease outbreaks, insect abundance and diversity. Ecology Letters, 2, 286-293.
35. Koricheva, J., Gange, A.C. & Jones, T. (2009) Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology, 90, 2088-2097.
36. Langellotto, G.A. & Denno, R.F. (2004) Responses of invertebrate natural enemies to complex-structured habitats: a meta-analytical synthesis. Oecologia, 139, 1-10.
37. Larson, K.C. & Berry, R.E. (1984) Influence of peppermint phenolics and monoterpenes on two spotted spider mite (Acari: Tetranychidae). Environmental Entomology, 13, 282-285.
38. Lawton, J.H. & Strong, D.R. Jr (1981) Community patterns and competition in folivorous insects. American Naturalist, 118, 317-338.
39. Mathews, A., Carroll, B.J. & Gresshoff, P.M. (1987) Characterization of non-nodulating mutants of soybean [Glycine max (L.) Merr]: Bradyrhizobium effects and absence of root hair curling. Journal of Plant Physiology, 131, 349-361.
40. Mattson, W.J. & Scriber, J.M. (1987) Nutritional ecology of insect folivores of woody plants: nitrogen, water, fiber, and mineral considerations. Nutritional Ecology of Insects, Mites, Spiders, and Related Invertebrates (ed. by F. Slansky and J. G. Rodrigues ), pp. 105-146. John Wiley and Sons, New York, New York.
41. Miklashevichs, E., Röhrig, H., Schell, J. & Schmidt, J. (2001) Perception and signal transduction of rhizobial NOD factors. Critical Review in Plant Sciences, 20, 373-394.
42. Nakamura, M., Kagata, H. & Ohgushi, T. (2006) Trunk cutting initiates bottom-up cascades in a tri-trophic system: sprouting increases biodiversity of herbivorous and predaceous arthropods on willows. Oikos, 113, 259-268.
43. Nishida, T., Katayama, N., Izumi, N. & Ohgushi, T. (2010) Arbuscular mycorrhizal fungi species-specifically affect induced plant responses to a spider mite. Population Ecology, 52, 507-515.
44. Ohgushi, T. (1992) Resource limitation on insect herbivore populations. Effects of Resource Distribution on Animal-Plant Interactions (ed. by M. D. Hunter, T. Ohgushi and P. W. Price ), pp. 199-241. Academic Press, San Diego, California.
45. Ohgushi, T. (2005) Indirect interaction webs: herbivore-induced effects through trait change in plants. Annual Review of Ecology, Evolution, and Systematics, 36, 81-105.
46. Ohgushi, T. (2008) Herbivore-induced indirect interaction webs on terrestrial plants: the importance of non-trophic, indirect, and facilitative interactions. Entomologia Experimentalis et Applicata, 128, 217-229.
47. Ohgushi, T., Craig, T.P. & Price, P.W. (2007) Ecological Communities: Plant Mediation in Indirect Interaction Webs. Cambridge University Press, Cambridge, U.K.
48. Omacini, M., Chaneton, E.J., Ghersa, C.M. & Muller, C.B. (2001) Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature, 409, 78-81.
49. Price, P.W. & Hunter, M.D. (2005) Long-term population dynamics of a sawfly show strong bottom-up effects. Journal of Animal Ecology, 74, 917-925.
50. van Rhijn, P. & Vanderleyden, J. (1995) The rhizobium-plant symbiosis. Microbiological Reviews, 59, 124-142.
51. Rudgers, J.A. & Clay, K. (2008) An invasive plant-fungal mutualism reduces arthropod diversity. Ecology Letters, 11, 831-840.
52. Schmitz, O., Hamback, P.A. & Beckerman, A.P. (2000) Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. American Naturalist, 155, 141-153.
53. Siemann, E. (1998) Experimental tests of effects of plant productivity and diversity on grassland arthropod diversity. Ecology, 79, 2057-2070.
54. Simpson, E.H. (1949) Measurement of diversity. Nature, 163, 688.
55. Smith, S.E. & Read, D.J. (1997) Mycorrhizal Symbiosis, 2nd edn. Academic Press, San Diego, California.
56. Smith, B. & Wilson, J.B. (1996) A consumer's guide to evenness indices. Oikos, 76, 70-82.
57. Strong, D.R. Jr, Lawton, J.H. & Southwood, T.R.E. (1984) Insects on Plants: Community Patterns and Mechanisms. Blackwell Scientific, Oxford, U.K.
58. Suganuma, N., Kanada, H. & Yanagimoto, N. (1991) Detection of polypeptides involved in early stages of nodulation in soybean roots. Plant and Cell Physiology, 32, 1259-1266.
59. Utsumi, S. & Ohgushi, T. (2009) Community-wide impacts of herbivore-induced plant regrowth on arthropods in a multi-willow species system. Oikos, 118, 1805-1815.
60. Utsumi, S., Nakamura, M. & Ohgushi, T. (2009) Community consequences of herbivore-induced bottom-up trophic cascades: the importance of resource heterogeneity. Journal of Animal Ecology, 78, 953-963.
61. Van der Putten, W.H., Vet, L.E.M., Harvey, J.A. & Wackers, F.L. (2001) Linking above- and belowground multi-trophic interactions of plants, herbivores, pathogens and their antagonists. Trends in Ecology & Evolution, 16, 547-554.
62. Van Zandt, P.A. & Agrawal, A.A. (2004) Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology, 85, 2616-2629.
63. Wardle, D.A. (2002) Communities and Ecosystems: Linking the Aboveground and Belowground Components. Princeton University Press, Princeton, New Jersey.
64. White, T.C.R. (1993) The Inadequate Environment: Nitrogen and the Abundance of Animals. Springer, Berlin, Germany.
65. Whitham, T.G., Morrow, P.A. & Potts, B.M. (1994) Plant hybrid zones as centers of biodiversity: the herbivore community of two endemic Tasmanian eucalypts. Oecologia, 97, 481-490.
66. Whitham, T.G., Young, W.P., Martinsen, G.D., Gehring, C.A., Schweitzer, J.A., Shuster, S.M. et al. (2003) Community and ecosystem genetics: a consequence of the extended phenotype. Ecology, 84, 559-573.
67. Whitham, T.G., Bailey, J.K., Schweitzer, J.A., Shuster, S.M., Bangert, R.K., LeRoy, C.J. et al. (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nature Reviews Genetics, 7, 510-523.
68. Williams, L.F. & Lynch, D.L. (1954) Inheritance of a non-nodulating character in the soybean. Agronomy Journal, 46, 28-29.