Abstract
Herbivores and mycorrhizal fungi commonly occur together on host plants and thus are likely to interact in ways that could indirectly affect each other’s performance. In this chapter, we review the published studies on these interactions and their implications for plant, herbivore and fungal populations and communities. Six major patterns emerge from our review. First, in the majority of cases, aboveground herbivores reduce mycorrhizal colonization and alter mycorrhizal fungal community composition. Second, mycorrhizae also affect herbivores, but these effects are highly variable and range from positive to negative. Third, both of these interactions are conditional. For example, mycorrhizae are more likely to be affected by herbivores as the herbivory and/or the cumulative effects of environmental stress intensify. Under relatively benign conditions, herbivory may have no effect on mycorrhizae, but as plants are challenged, the impacts of herbivores on mycorrhizae can be great. Fourth, all mycorrhizae are not equal; the impacts of mycorrhizae on herbivores differ greatly between arbuscular mycorrhizal (AM) and ecto-mycorrhizal (EM) fungi and among species. Because different mycorrhizal species vary in their mutualistic effects on plants, such variation in impacts on herbivores should also be expected. Fifth, different types of herbivores are affected differently by mycorrhizae. Generalist herbivores appear to be affected more than specialists, and leaf chewers are more likely to be negatively affected, while sap feeders and their allies are more likely to be positively affected. Sixth, few studies have examined mycorrhizal effects on herbivores and herbivore effects on mycorrhizae in the same system. However, if interactions between aboveground herbivores and mycorrhizal fungi are similar to those observed between above- and belowground herbivores, they are likely to be highly asymmetrical with aboveground herbivores having greater negative effects on mycorrhizae than vice versa.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Allen MF, Richards JH, Busso CA (1989) Influence of clipping and soil water status on vesicular-arbuscular mycorrhiza of two semi-arid tussock grasses. Biol Fertil Soils 8: 285–289
Andersen CP, Rygiewicz PT (1991) Stress interactions and mycorrhizal plant response: understanding carbon allocation priorities. Environ Pollut 73: 217–244
Bayne HG, Brown MS, Bethlenfalvay GJ (1984) Defoliation effects on mycorrhizal colonization, nitrogen fixation and photosynthesis in the Glycine-Glomus-Rhizobium symbiosis. Physiol Plant 62: 576–580
Bethlenfalvay GJ, Dakessian S (1984) Grazing effects on mycorrhizal colonization and floristic composition of the vegetation on a semiarid range in northern Nevada. J Range Manage 37: 312–316
Bethlenfalvay GJ, Evans RA, Lesperance AL (1985) Mycorrhizal colonization of crested wheatgrass as influenced by grazing. Agron J 77: 233–236
Borowicz V (1997) A fungal root symbiont modifies plant resistance to an insect herbivore. Oecologia 112: 534–542
Mycorrhizae-Hervivore Interactions: Population and Community Consequences 317
Borowicz V, Fitter AH (1990) Effects of endomycorrhizal infection, artificial herbivory
and parental cross on growth of Lotus corniculatus L. Oecologia 82:402–407 Bronstein J (1994) Conditional outcomes in mutualistic interactions. Trends Ecol Evol 9:214–217
Brundrett M, Bougher N, Dell B, Grove T, Malajczuk N (1996) Working with mycorrhizas in forestry and agriculture. ACIAR Monogr 32, 374 pp
Chapin FS III (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11: 233–260
Choudhury D (1988) Herbivore induced changes in leaf-litter resource quality: a neglected aspect of herbivory in ecosystem nutrient dynamics. Oikos 51: 389–393
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18: 117–143
Cobb NS, Whitham TG (1993) Herbivore deme formation on individual trees: a test case. Oecologia 94: 496–502
Daft MJ, El-Giahmi AA (1978) Effect of arbuscular mycorrhiza on plant growth. VIII. Effect of defoliation and light on selected hosts. New Phytol 80: 365–372
Del Vecchio TA, Gehring CA, Cobb NS, Whitham TG (1993) Negative effects of scale insect herbivory on the ectomycorrhiza of juvenile pinyon pine. Ecology 74: 22972302
Denno RF, McClure MS, Ott JR (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu Rev Entomol 40: 297–332
Dungey HS, Potts BM, Whitham TG, Li H-F (2000) A genetic component to community structure. Evolution 54: 1938–1946
Findlay S, Carreiro M, Krischik V, Jones CG (1996) Effects of damage to living plants on leaf litter quality. Ecol Appl 6: 269–275
Fogel R (1979) Mycorrhiza and nutrient cycling in natural forest ecosystems. New Phytol 86: 199–212
Gange AC (2001) Species specific responses of a root-and shoot feeding insect to arbuscular mycorrhizal colonization of its host plant. New Phytologist (in press)
Gange AC, Bower E (1997) Interactions between insects and mycorrhizal fungi. In: Gange AC, Brown VK (eds) Multitrophic interactions in terrestrial systems. Blackwell, Oxford, pp 115–132
Gange AC, Nice HE (1997) Performance of the thistle gall fly, Urophora carduii, in rela tion to host plant nitrogen and mycorrhizal colonization. New Phytol 137: 335–343
Gange AC, West HM (1994) Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytol 128: 79–87
Gange AC, Brown VK, Sinclair GS (1994) Reduction of black vine weevil larval growth by vesicular-arbuscular mycorrhizal infection. Entomol Exp Appl 70: 115–119
Gange AC, Bower E, Brown VK (1999) Positive effects of an arbuscular mycorrhizal fungus on aphid life history traits. Oecologia 120: 123–131
Gardes M, Bruns TD (1996) ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhiza and rusts. Mol Ecol 2: 113–118
Gehring CA, Whitham TG (1991) Herbivore-driven mycorrhizal mutualism in insect
susceptible pinyon pine. Nature 353:556–557
Gehring CA, Whitham TG (1994a) Interactions between aboveground herbivores and the mycorrhizal mutualists of plants. Trends Ecol Evol 9: 251–255
Gehring CA, Whitham TG (1994b) Comparisons of ectomycorrhiza on pinyon pines (Pinus edulis; Pinaceae) across extremes of soil type and herbivory. Am J Bot 81: 15091516
Gehring CA, Whitham TG (1995) Duration of herbivore removal and environmental stress affect the ectomycorrhiza of pinyon pines. Ecology 76: 2118–2123
Gehring CA, Cobb NS, Whitham TG (1997) Three-way interactions among ecto-mycorrhizal mutualists, scale insects, and resistant and susceptible pinyons. Am Nat 149: 824–841
Gehring CA, Theimer TC, Whitham TG, Keim P (1998) Ecto-mycorrhizal fungal community structure of pinyon pines growing in two environmental extremes. Ecology 79: 1562–1572
Goverde M, van der Heijden MGA, Wiemken A, Sanders IR, Erhardt A (2000) Arbuscular mycorrhizal fungi influence life history traits of a lepidopteran butterfly. Oecologia 125: 362–369
Grier CC, Vogt DJ (1990) Effects of aphid honeydew on soil nitrogen availability and net primary production in an Alnus rubra plantation in western Washington. Oikos 57: 114–118
Grime JP, Mackey JML, Hillier SH, Read DJ (1987) Floristic diversity in a model system using experimental microcosms. Nature 328: 420–422
Helgason T, Daniell TJ, Husband R, Fitter AH,Young JPW (1998) Ploughing up the wood-wide web? Nature 394: 431
Holland JN, Weixin C, Crossley DA Jr (1996) Herbivore-induced changes in plant carbon allocation: assessment of below-ground C fluxes using carbon-14. Oecologia 107: 8794
Huntly N (1991) Herbivores and the dynamics of communities and ecosystems. Annu Rev Ecol Syst 22: 477–503
Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the parasitism-mutualism continuum. New Phytol 135: 575–585
Jones CG, Last FT (1991) Ectomycorrhiza and trees: implications for aboveground herbivory. In: Barbosa P, Krischik VA, Jones CG (eds) Microbial mediation of plant-herbivore interactions. Wiley, New York, pp 65–103
Kendrick B (1992) The fifth kingdom. Mycologue Publications, Waterloo
Klironomos JN, Kendrick B (1995) Relationships among microarthropods, fungi and their environment. Plant Soil 170: 183–197
Klironomos JN, Widden P, Deslandes I (1992) Feeding preferences of the collembolan Folsomia candida in relation to microfungal successions on decaying litter. Soil Biol Biochem 24: 685–692
Kolb TE, Dodds KA, Clancy KM (1999) Effect of western spruce budworm defoliation on the physiology and growth of potted Douglas-fir seedlings. For Sci 45: 280–291
Kruskal JB (1964) Multidimensional scaling by optimizing goodness of fit to a non-metric hypothesis. Psychometrika 29: 1–27
Llewellyn M (1972) The effects of the lime aphid, Eucallipterus tiliae L. (Aphididae) on the growth of the lime Tilia x vulgaris Hayne. J Appl Ecol 9: 261–282
MacFall JS, Slack SA, Iyer J (1991) Effects of Hebeloma arenosa on and phosphorous fertility on growth of red pine (Pinus resinosa) seedlings. Can J Bot 69: 372–379
Manninen A-M (1999) Susceptibility of Scots pine seedlings to specialist and generalist insect herbivores - importance of plant defense and mycorrhizal status. Natural and Environmental Sciences 100. PhD, Univ Kuopio, Kuopio Univ Publ C
Manninen A-M, Holopainen T, Holopainen JK (1998) Susceptibility of ecto-mycorrhizal and nonmycorrhizal Scots pine (Pinus sylvestris) seedlings to a generalist insect herbivore, Lygus rugulipennis, at two nitrogen availability levels. New Phytol 140: 55–63
Manninen A-M, Holopainen T, Holopainen JK (1999a) Performance of grey pine aphid, Schizolachnus pineti, on ecto-mycorrhizal and non-mycorrhizal Scots pine seedlings at different levels of nitrogen availability. Entomol Exp App19: 117–120
Manninen A-M, Holopainen T, Lyytikäinen-Saarenmaa P, Holopainen JK (1999b) The role of low level ozone exposure and mycorrhizas in chemical quality and insect herbivore performance on Scots pine seedlings. Global Change Biol 5: 1–11
Mycorrhizae-Hervivore Interactions: Population and Community Consequences 319
Markkola AM (1996) Effect of artificial defoliation on biomass allocation in ecto-mycorrhizal Pinus sylvestris seedlings. Can J For Res 26: 899–904
Marx DH, Hatch AB, Mendicino JF (1977) High soil fertility decreases sucrose content and susceptibility of loblolly pine roots to ecto-mycorrhizal infection by Pisolithus tinctorius. Can J Bot 55: 1569–1574
Masters GJ, Brown VK (1995) Host-plant mediated interactions between spatially separated herbivores: effects on community structure. In: Gange AC, Brown VK (eds) Multitrophic interactions in terrestrial system. Blackwell, Oxford, pp 217–237
Miller SL, Allen EB (1992) Mycorrhiza, nutrient translocation, and interactions between plants. In: Allen MF (ed) Mycorrhizal functioning: and integrative plant-fungal process. Routledge/Chapman and Hall, New York, pp 301–332
Minchin PR (1987a) An evaluation of the relative robustness of techniques for ecological ordination. Vegetatio 69: 89–107
Minchin PR (1987b) An evaluation of the relative robustness of techniques for ecological ordination. Vegetatio 71: 145–456
Naiman RJ, Melillo JM, Hobbie JE (1986) Ecosystem alteration of boreal forest streams by beaver (Castor canadensis). Ecology 67: 1254–1269
Pacovsky RS, Rabin LB, Montllor CB, Waiss AC Jr (1985) Host-plant resistance to insect pests altered by Glomus fasciculatum colonization. In: Molina R (ed) Proceedings of the 6th North American Conference on Mycorrhiza. Oregon State University, Corvallis, p 288
Paine RT (1966) Food web complexity and species diversity. Am Nat 100: 65–75
Pastor J, Naiman RJ (1992) Selective foraging and ecosystem processes in boreal forests. Am Nat 139: 690–705
Pastor J, Naiman RJ, Dewey B, McIness P (1988) Moose, microbes and the boreal forest. Bioscience 38: 770–777
Perry DA, Margolis H, Choquette C, Molina R, Trappe JM (1989) Ecto-mycorrhizal mediation of competition between coniferous tree species. New Phytol 112: 501–511
Power ME, Tilman D, Estes JA, Menge BA, Bond WJ, Mills LS, Daily G, Castilla JC, Lubchenco J, Paine RT (1996) Challenges in the quest for keystones. Bioscience 46: 609–620
Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62: 244–251
Rabin LB, Pacovsky RS (1985) Reduced larva growth of two lepidoptera ( Noctuidae) on excised leaves of soybean infected with a mycorrhizal fungus. J Econ Entomol 78: 1358–1363
Richards JH (1984) Root growth response to defoliation in two Agropyron bunchgrasses:
field observations with an improved root periscope. Oecologia 64:21–25
Ritchie ME, Tilman D, Knops JMH (1998) Herbivore effects on plant and nitrogen dynamics in oak savanna. Ecology 79: 165–177
Rossow LJ, Bryant JP, Kielland K (1997) Effects of above-ground browsing by mammals on mycorrhizal infection in an early successional taiga ecosystem. Oecologia 110: 94–98
Saikkonen K, Ahonen-Jonnarth U, Markkola AM, Helander M, Tuomi J, Roitto M, Ranta H (1999) Defoliation and mycorrhizal symbiosis: a functional balance between carbon sources and below-ground sinks. Ecol Lett 2: 19–26
Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, London Trent JD, Wallace LL, Svejcar TJ, Christiansen S (1988) Effect of grazing on growth, car bohydrate pools, and mycorrhiza in winter wheat. Can J Plant Sci 68:115–120
van der Meijden E (1996) Plant defence, an evolutionary dilemma: contrasting effects of (specialist and generalist) herbivores and natural enemies. Entomol Exp Appl 80:307–310 320 C.A. Gehring and T.G. Whitham
van der Heijden MGA, Boller T, Wiemken A, Sanders IR (1998a) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79: 2082–2091
van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998b) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69–72
Wall DH, Moore JC (1999) Interactions underground: Soil biodiversity, mutualism and ecosystem processes. Bioscience 49: 109–117
Wallace LL (1981) Growth, morphology and gas exchange of mycorrhizal and nonmycorrhizal Panicum coloratum L., a C4 grass species, under different clipping and fertilization regimes. Oecologia 49: 272–278
Waring GW, Cobb NS (1992) The impact of plant stress on herbivore population dynam ics. In: Bernays E (ed) Insect-plant interactions, vol 4. CRC, Boca Raton, pp 168–226
White TCR (1984) The abundance of invertebrate herbivores in relation to the availabil ity of nitrogen in stressed food plants. Oecologia 63: 90–105
Whitham TG, Mopper S (1985) Chronic herbivory: impacts on architecture and sex expression of pinyon pine. Science 228: 1089–1091
Wilson JB (1988) A review of evidence on the control of shoot:root ratio, in relation to models. Ann Bot 61: 433–449
Wimp GM, Whitham TG (2001) Biodiversity consequences of predation and host plant hybridization on an aphid-ant mutualism. Ecology 82: 440–452
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2002 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Gehring, C.A., Whitham, T.G. (2002). Mycorrhizae-Herbivore Interactions: Population and Community Consequences. In: van der Heijden, M.G.A., Sanders, I.R. (eds) Mycorrhizal Ecology. Ecological Studies, vol 157. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-38364-2_12
Download citation
DOI: https://doi.org/10.1007/978-3-540-38364-2_12
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-00204-8
Online ISBN: 978-3-540-38364-2
eBook Packages: Springer Book Archive