Skip to main content Accessibility help
×
Hostname: page-component-7c8c6479df-p566r Total loading time: 0 Render date: 2024-03-19T07:24:38.125Z Has data issue: false hasContentIssue false

Chapter Seven - Plant effects on herbivore–enemy interactions in natural systems

Published online by Cambridge University Press:  05 February 2013

Kailen A. Mooney
Affiliation:
Department of Ecology and Evolutionary Biology, University of California – Irvine
Michael S. Singer
Affiliation:
Department of Biology, Wesleyan University
Takayuki Ohgushi
Affiliation:
Kyoto University, Japan
Oswald Schmitz
Affiliation:
Yale University, Connecticut
Robert D. Holt
Affiliation:
University of Florida
Get access

Summary

Introduction

While it had long been recognized that herbivores are simultaneously influenced by natural enemies (Hairston et al. 1960) and plant defences (Fraenkel 1959), Price et al. (1980) were among the first to argue forcefully that these dual factors must be considered together. They argued that ‘[w]e cannot understand the plant–herbivore interaction without understanding the role of enemies. We cannot understand predator–prey interactions without understanding the role of plants’ (Price et al. 1980, p. 59). This holistic, tritrophic perspective conceptually unites theory from at least three areas of ecological and evolutionary research. First, this tritrophic perspective expands our view on plant defence from one based strictly on the direct defence, to one that also considers the indirect defence of plants by natural enemies (Janzen 1966; Turlings et al. 1990), as well as how natural enemies mediate the efficacy of direct defences (Moran and Hamilton 1980; Clancy and Price 1987; Williams 1999; Gassmann and Hare 2005). Second, this tritrophic perspective advances our understanding of the forces shaping the evolution of herbivore host plant choice and diet breadth by incorporating the interactive effects of host plant quality and risk of attack by natural enemies (Bernays 1998; Singer et al. 2004a, b). And third, this tritrophic perspective provides a mechanistic framework for understanding the ecological and evolutionary factors that determine the strength of the indirect effects natural enemies have on plant growth, i.e., trophic cascades (Mooney et al. 2010).

Tritrophic interactions have received considerable attention in agricultural systems, with numerous studies documenting the effects of crop traits on herbivores and their natural enemies (Hare 1992; Tumlinson et al. 1992; Vet and Dicke 1992; Bottrell et al. 1998; Turlings and Benrey 1998; Cortesaro et al. 2000; Hare 2002; Ode 2006). In contrast, comparatively little is known of the influences of plant traits on herbivore–enemy interactions from natural systems (e.g., Hare 1992, 2002). Our goals in this review are three-fold. First, where past reviews on this topic have focused on agricultural systems (e.g., Hare 1992, 2002), we give special attention to the evidence for plant variation in herbivore–enemy interactions from natural communities. Second, we position this topic within the framework of trait- and density-mediated indirect interactions. Finally, we consider the evolutionary and ecological implications of plant variation in herbivore–enemy interactions, and we do so with specific reference to the different mechanistic pathways by which such plant effects can occur.

Type
Chapter
Information
Trait-Mediated Indirect Interactions
Ecological and Evolutionary Perspectives
, pp. 107 - 130
Publisher: Cambridge University Press
Print publication year: 2012

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

Agrawal, A. A. 2003 Community genetics: new insights into community ecology by integrating population geneticsEcology 84 543CrossRefGoogle Scholar
Bailey, J. K.Wooley, S. C.Lindroth, R. L.Whitham, T. G. 2006 Importance of species interactions to community heritability: a genetic basis to trophic-level interactionsEcology Letters 9 78Google ScholarPubMed
Barbosa, P.Segarra, A. E.Gross, P. 2001 Differential parasitism of macrolepidopteran herbivores on two deciduous tree speciesEcology 82 698CrossRefGoogle Scholar
Bernays, E. A. 1998 Evolution of feeding behavior in insect herbivores: success seen as different ways to eat without being eatenBioScience 48 35CrossRefGoogle Scholar
Bottrell, D. G.Barbosa, P.Gould, F. 1998 Manipulating natural enemies by plant variety selection and modification: a realistic strategy?Annual Review of Entomology 43 347CrossRefGoogle ScholarPubMed
Brower, L. P.Zandt Brower, J.Corvino, J. M. 1967 Plant poisons in a terrestrial food chainProceedings of the National Academy of Sciences of the United States of America 57 893CrossRefGoogle Scholar
Bukovinszky, T.Veen, F. J. F.Jongema, Y.Dicke, M. 2008 Direct and indirect effects of resource quality on food web structureScience 319 804CrossRefGoogle ScholarPubMed
Clancy, K. M.Price, P. W. 1987 Rapid herbivore growth enhances enemy attack: sublethal plant defenses remain a paradoxEcology 68 733CrossRefGoogle Scholar
Coley, P. D.Bateman, M. L.Kursar, T. A. 2006 The effects of plant quality on caterpillar growth and defense against natural enemiesOikos 115 219CrossRefGoogle Scholar
Coley, P. D.Bryant, J. P.Chapin, F. S. 1985 Resource availability and plant antiherbivore defenseScience 230 895CrossRefGoogle ScholarPubMed
Cornelissen, T.Stiling, P. 2005 Sex-biased herbivory: a meta-analysis of the effects of gender on plant–herbivore interactionsOikos 111 488CrossRefGoogle Scholar
Cortesaro, A.Stapel, J.Lewis, W. 2000 Understanding and manipulating plant attributes to enhance biological controlBiological Control 17 35CrossRefGoogle Scholar
Crutsinger, G. M.Cadotte, M. W.Sanders, N. J. 2009 Plant genetics shapes inquiline community structure across spatial scalesEcology Letters 12 285CrossRefGoogle ScholarPubMed
Crutsinger, G. M.Collins, M. D.Fordyce, J. A. 2006 Plant genotypic diversity predicts community structure and governs an ecosystem processScience 313 966CrossRefGoogle ScholarPubMed
Feeny, P. P. 1976 Plant apparency and chemical defenseRecent Advances in Phytochemistry 10 1Google Scholar
Fine, P. V. A.Mesones, I.Coley, P. D. 2004 Herbivores promote habitat specialization by trees in Amazonian forestsScience 305 663CrossRefGoogle ScholarPubMed
Forkner, R. E.Hunter, M. D. 2000 What goes up must come down? Nutrient addition and predation pressure on oak herbivoresEcology 81 1588CrossRefGoogle Scholar
Fraenkel, G. S. 1959 Raison d’être of secondary plant substancesScience 129 1466CrossRefGoogle ScholarPubMed
Fritz, R. S.Nobel, J. 1990 Host plant variation in mortality of the leaf-folding sawfly on the arroyo willowEcological Entomology 15 25CrossRefGoogle Scholar
Fritz, R. S.Simms, E. L. 1992 Plant Resistance to Herbivores and Pathogens : Ecology, Evolution, and GeneticsChicago, IL:University of Chicago PressCrossRefGoogle Scholar
Fritz, R. S.McDonough, S. E.Rhoads, A. G. 1997 Effects of plant hybridization on herbivore-parasitoid interactionsOecologia 110 360CrossRefGoogle ScholarPubMed
Futuyma, D. J.Gould, F. 1979 Associations of plants and insects in a deciduous forestEcological Monographs 49 33CrossRefGoogle Scholar
Gassmann, A. J.Hare, J. D. 2005 Indirect cost of a defensive trait: variation in trichome type affects the natural enemies of herbivorous insects on Oecologia 144 62CrossRefGoogle Scholar
Gripenberg, S.Mayhew, P. J.Parnell, M.Roslin, T. 2010 A meta-analysis of preference-performance relationships in phytophagous insectsEcology Letters 13 383CrossRefGoogle ScholarPubMed
Gross, P.Price, P. W. 1988 Plant influences on parasitism of two leafminers: a test of enemy-free spaceEcology 69 1506CrossRefGoogle Scholar
Haggstrom, H.Larsson, S. 1995 Slow larval growth on a suboptimal willow results in high predation mortality in the leaf beetle Oecologia 104 308CrossRefGoogle ScholarPubMed
Hairston, N. G.Smith, F. E.Slobodkin, L. G. 1960 Community structure, population control, and competitionAmerican Naturalist 94 421CrossRefGoogle Scholar
Hare, J. D. 1992 Effects of plant variation on herbivore-natural enemy interactionsFritz, R. S.Simms, E. L.Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and GeneticsChicago, ILUniversity of Chicago Press278Google Scholar
Hare, J. D. 2002 Plant genetic variation in tritrophic interactionsTscharntke, T.Hawkins, B. A.Multitrophic Level InteractionsCambridgeCambridge University Press8CrossRefGoogle Scholar
Hedges, L. V.Gurevitch, J.Curtis, P. S. 1999 The meta-analysis of response ratios in experimental ecologyEcology 80 1150CrossRefGoogle Scholar
Helms, S. E.Connelly, S. J.Hunter, M. D. 2004 Effects of variation among plant species on the interaction between a herbivore and its parasitoidEcological Entomology 29 44CrossRefGoogle Scholar
Holmes, R. T.Robinson, S. K. 1981 Tree species preferences of foraging insectivorous birds in a northern hardwoods forestOecologia 48 31CrossRefGoogle Scholar
Holmes, R. T.Schultz, J. C.Nothnagle, P. 1979 Bird predation on forest insects: exclosure experimentScience 206 462CrossRefGoogle ScholarPubMed
Inouye, B.Stinchcombe, J. R. 2001 Relationships between ecological interaction modifications and diffuse coevolution: similarities, differences, and causal linksOikos 95 353CrossRefGoogle Scholar
Janzen, D. H. 1966 Coevolution of mutualism between ants and acacias in Central AmericaEvolution 20 249CrossRefGoogle ScholarPubMed
Johnson, M. T. J.Agrawal, A. A. 2005 Plant genotype and environment interact to shape a diverse arthropod community on evening primrose ()Ecology 86 874CrossRefGoogle Scholar
Johnson, M. T. J.Stinchcombe, J. R. 2007 An emerging synthesis between community ecology and evolutionary biologyTrends in Ecology and Evolution 22 250CrossRefGoogle ScholarPubMed
Kaplan, I.Lynch, M. E.Dively, G. P.Denno, R. F. 2007 Leafhopper-induced plant resistance enhances predation risk in a phytophagous beetleOecologia 152 665CrossRefGoogle Scholar
Kessler, A.Halitschke, R.Baldwin, I. T. 2004 Silencing the jasmonate cascade: induced plant defenses and insect populationsScience 305 665CrossRefGoogle ScholarPubMed
Lill, J. T.Marquis, R. J. 2001 The effects of leaf quality on herbivore performance and attack from natural enemiesOecologia 126 418CrossRefGoogle ScholarPubMed
Lill, J. T.Marquis, R. J.Ricklefs, R. E. 2002 Host plants influence parasitism of forest caterpillarsNature 417 170CrossRefGoogle ScholarPubMed
Linhart, Y. B.Keefover-Ring, K.Mooney, K. A.Breland, B.Thompson, J. D. 2005 A chemical polymorphism in a multitrophic setting: thyme monoterpene composition and food web structureAmerican Naturalist 166 517CrossRefGoogle Scholar
Marquis, R. J.Whelan, C. 1996 Plant morphology, and recruitment of the third trophic level: subtle and little-recognized defenses?Oikos 75 330CrossRefGoogle Scholar
Mooney, K. A.Agrawal, A. A. 2008 Plant genotype shapes ant-aphid interactions: Implications for community structure and indirect plant defenseAmerican Naturalist 168 E195CrossRefGoogle Scholar
Mooney, K. A.Halitschke, R.Kessler, A.Agrawal, A. A. 2010 Evolutionary trade-offs in plants mediate the strength of trophic cascadesScience 327 1642CrossRefGoogle ScholarPubMed
Mooney, K. A.Pratt, R. T.Singer, M. 2012
Moran, N.Hamilton, W. D. 1980 Low nutritive quality as defense against herbivoresJournal of Theoretical Biology 86 247CrossRefGoogle Scholar
Muller, M. S.McWilliams, S. R.Podlesak, D. 2006 Tri-trophic effects of plant defenses: chickadees consume caterpillars based on host leaf chemistryOikos 114 507CrossRefGoogle Scholar
Ness, J. H.Morris, W. F.Bronstein, J. L. 2009 For ant-protected plants, the best defense is a hungry offenseEcology 90 2823CrossRefGoogle ScholarPubMed
Ode, P. J. 2006 Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactionsAnnual Review of Entomology 51 163CrossRefGoogle ScholarPubMed
Polis, G. A.Strong, D. R. 1996 Food web complexity and community dynamicsAmerican Naturalist 147 813CrossRefGoogle Scholar
Price, P. W.Clancy, K. M. 1986 Interactions among three trophic levels: gall size and parasitoid attackEcology 67 1593CrossRefGoogle Scholar
Price, P. W.Bouton, C. E.Gross, P. 1980 Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemiesAnnual Review of Ecology and Systematics 11 41CrossRefGoogle Scholar
Robinson, S. K.Holmes, R. T. 1982 Foraging behavior of forest birds: the relationships among search tactics, diet, and habitat structureEcology 63 1918CrossRefGoogle Scholar
Rudgers, J. A. 2004 Enemies of herbivores can shape plant traits: selection in a facultative ant-plant mutualismEcology 85 192CrossRefGoogle Scholar
Schoonhoven, L. M.Loon, J. J. A. v.Dicke, M. 2005 Insect–Plant BiologyOxfordOxford University PressGoogle Scholar
Shuster, S. M.Lonsdorf, E. V.Wimp, G. M.Bailey, J. K.Whitham, T. G. 2006 Community heritability measures the evolutionary consequences of indirect genetic effects on community structureEvolution 60 991CrossRefGoogle ScholarPubMed
Singer, M. S.Carriere, Y.Theuring, C.Hartmann, T. 2004 Disentangling food quality from resistance against parasitoids: diet choice by a generalist caterpillarAmerican Naturalist 164 423CrossRefGoogle ScholarPubMed
Singer, M. C.Farkas, T. E.Skorik, C. M.Mooney, K. A. 2012
Singer, M. S.Rodrigues, D.Stireman, J. O.Carriere, Y. 2004 Roles of food quality and enemy-free space in host use by a generalist insect herbivoreEcology 85 2747CrossRefGoogle Scholar
Sipura, M. 1999 Tritrophic interactions: willows, herbivorous insects and insectivorous birdsOecologia 121 537CrossRefGoogle ScholarPubMed
Slanksy, F.Scriber, J. M. 1985 Food consumption and utilizationKerkut, G. A.Gilbert, L. I.Comprehensive Insect Physiology, Biochemistry, and PharmacologyOxfordPergamon Press87Google Scholar
Strauss, S. Y.Sahli, H.Conner, J. K. 2005 Toward a more trait-centered approach to diffuse (co)evolutionNew Phytologist 165 81CrossRefGoogle Scholar
Tumlinson, J. H.Turlings, T. C. J.Lewis, W. J. 1992 The semiochemical complexes that mediate insect parasitoid foragingAgricultural Zoology Reviews 5 221Google Scholar
Turlings, T. C. J.Benrey, B. 1998 Effects of plant metabolites on the behavior and development of parasitic waspsEcoscience 5 321CrossRefGoogle Scholar
Turlings, T. C. J.Tumlinson, J. H.Lewis, W. J. 1990 Exploitation of herbivore-induced plant odors by host-seeking parasitic waspsScience 250 1251CrossRefGoogle ScholarPubMed
Vet, L. E. M.Dicke, M. 1992 Ecology of infochemical use by natural enemies in a tritrophic contextAnnual Review of Entomology 37 141CrossRefGoogle Scholar
Weis, A. E.Abrahamson, W. G. 1986 Evolution of host-plant manipulation by gall makers: ecological and genetic factors in the –American Naturalist 127 681CrossRefGoogle Scholar
Whelan, C. J. 2001 Foliage structure influences foraging of insectivorous forest birds: an experimental studyEcology 82 219CrossRefGoogle Scholar
Whitham, T. G.Bailey, J. K.Schweitzer, J. A. 2006 A framework for community and ecosystem genetics: from genes to ecosystemsNature Reviews Genetics 7 510CrossRefGoogle ScholarPubMed
Whitham, T. G.Young, W. P.Martinsen, G. D. 2003 Community and ecosystem genetics: a consequence of the extended phenotypeEcology 84 559CrossRefGoogle Scholar
Williams, I. S. 1999 Slow-growth, high-mortality: a general hypothesis, or is it?Ecological Entomology 24 490CrossRefGoogle Scholar
Wimp, G. M.Whitham, T. G. 2001 Biodiversity consequences of predation and host plant hybridization on an aphid-ant mutualismEcology 82 440Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×