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Eco-evolutionary dynamics in herbivorous insect communities mediated by induced plant responses

  • Special Feature: Review
  • Linking Genome to Ecosystem
  • Published:
Population Ecology

Abstract

It is increasingly recognized that the ecology of communities and evolution of species within communities are interdependent, and researchers have been paying attention to this rapidly emerging field of research, i.e., through studies on eco-evolutionary dynamics. Most of the studies on eco-evolutionary dynamics have been concerned with direct trophic interactions. However, community ecologists have shown that trait-mediated indirect effects play an important role in shaping the structure of natural communities. In particular, in terrestrial plant–insect systems, indirect effects mediated through herbivore-induced plant responses are common and have a great impact on the structure of herbivore communities. This review describes eco-evolutionary dynamics in herbivorous insect communities, and specifically focuses on the key role of herbivore-induced plant responses in eco-evolutionary dynamics. First, I review studies on the evolution of herbivore traits relevant to plant induction and discuss evolution in a community context mediated by induced plant responses. Second, I highlight how intraspecific genetic variation or evolution in herbivore traits can influence herbivore community structure. Finally, I propose the hypothetical model that induced plant responses supports eco-evolutionary feedback in herbivore communities. In this review, I argue that the application of the indirect interaction web approaches into studies on eco-evolutionary will provide profound insights into understanding of mechanisms of the generation and maintenance of biodiversity.

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References

  • Abrams PA (2000) The evolution of predator–prey interactions: theory and evidence. Annu Rev Ecol Syst 31:79–105

    Google Scholar 

  • Abrams PA, Menge BA, Mittelbach GG, Spiller DA, Yodzis P (1996) The role of indirect effects in food webs. In: Polis GA, Winemiller KO (eds) Food webs: integration of patterns and dynamics. Chapman & Hall, New York, pp 371–395

    Google Scholar 

  • Agrawal AA (1998) Induced responses to herbivory and increased plant performance. Science 279:1201–1202

    CAS  PubMed  Google Scholar 

  • Agrawal AA (2000) Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars. Oikos 89:493–500

    Google Scholar 

  • Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321–326

    CAS  PubMed  Google Scholar 

  • Agrawal AA (2005) Future directions in the study of induced plant responses to herbivory. Entomol Exp Appl 115:97–105

    Google Scholar 

  • Agrawal AA, Karban R, Colfer RG (2000) How leaf domatia and induced plant resistance affect herbivores, natural enemies and plant performance. Oikos 89:70–80

    Google Scholar 

  • Anderson P, Agrell J (2005) Within-plant variation in induced defence in developing leaves of cotton plants. Oecologia 144:427–434

    CAS  PubMed  Google Scholar 

  • Ando Y, Ohgushi T (2008) Ant- and plant-mediated indirect effects induced by aphid colonization on herbivorous insects on tall goldenrod. Popul Ecol 50:181–189

    Google Scholar 

  • Antonovics J (1992) Toward community genetics. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. University of Chicago Press, Chicago, pp 426–449

    Google Scholar 

  • Arimura G, Huber DPW, Bohlmann J (2004) Forest tent caterpillars (Malacosoma disstria) induce local and systemic diurnal emissions of terpenoid volatiles in hybrid poplar (Populus trichocarpa × deltoides): cDNA cloning, functional characterization, and patterns of gene expression of (−)-germacrene d synthase, PtdTPS1. Plant J 37:603–616

    CAS  PubMed  Google Scholar 

  • Barbour RC, O’Reilly-Wapstra JM, De Little DW, Jordan GJ, Steane DA, Humphreys JR, Bailey JK, Whitham TG, Potts BM (2009) A geographic mosaic of genetic variation within a foundation tree species and its community-level consequences. Ecology 90:1762–1772

    PubMed  Google Scholar 

  • Benkman CW, Holimon WC, Smith JW (2001) The influence of a competitor on the geographic mosaic of coevolution between crossbills and lodgepole pine. Evolution 55:282–294

    CAS  PubMed  Google Scholar 

  • Bezemer TM, Wagenaar R, Van Dam NM, Wäckers FL (2003) Interactions between above- and belowground insect herbivores as mediated by the plant defense system. Oikos 101:555–562

    Google Scholar 

  • Bonte D, De Roissart A, Vandegehuchte ML, Ballhorn DJ, Van Leeuwen T, de la Peña E (2010) Local adaptation of aboveground herbivores towards plant phenotypes induced by soil biota. Plos One 5:e11174. doi:10.1371/journal.pone.0011174

    PubMed  Google Scholar 

  • Broadway RM (1995) Are insects resistant to plant proteinase inhibitors? J Insect Physiol 41:107–116

    CAS  Google Scholar 

  • Broadway RM (1997) Dietary regulation of serine proteinases that are resistant to serine proteinase inhibitors. J Insect Physiol 43:855–874

    CAS  PubMed  Google Scholar 

  • Bultman TL, Bell G, Martin WD (2004) A fungal endophyte mediates reversal of wound-induced resistance and constrains tolerance in a grass. Ecology 85:679–685

    Google Scholar 

  • Carroll SP, Hendry AP, Reznick DN, Fox CW (2007) Evolution on ecological time-scales. Funct Ecol 21:387–393

    Google Scholar 

  • Chambers JLE, Berenbaum MR, Zangerl AR (2007) Benefits of trenching behavior in the context of an inducible defense. Chemoecology 17:125–130

    CAS  Google Scholar 

  • Darwin CR (1859) On the origin of species by means of natural selection or the preservation favored races in the struggle for life. John Murray, London

    Google Scholar 

  • Denno RF, Kaplan I (2007) Plant-mediated interactions in herbivorous insects: mechanisms, symmetry, and challenging the paradigms of competition past. In: Ohgushi T, Craig TP, Price PW (eds) Ecological communities: plant mediation in indirect interaction webs. Cambridge University Press, Cambridge, pp 19–50

    Google Scholar 

  • Denno RF, McClure MS, Ott JR (1995) Interspecific interactions in phytophagous insets: competition reexamined and resurrected. Annu Rev Entomol 40:297–331

    CAS  Google Scholar 

  • Denno RF, Peterson MA, Gratton C, Cheng J, Langellotto GA, Huberty AF, Finke DL (2000) Feeding-induced changes in plant quality mediate interspecific competition between sap-feeding herbivores. Ecology 81:1814–1827

    Google Scholar 

  • Després L, David J-P, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22:298–307

    PubMed  Google Scholar 

  • Dicke M, Hilker M (2003) Induced plant defenses: from molecular biology to evolutionary ecology. Basic Appl Ecol 4:3–14

    CAS  Google Scholar 

  • Dicke M, de Boer JG, Höfte M, Rocha-Granados MC (2003) Mixed blends of herbivore-induced plant volatiles and foraging success of carnivorous arthropods. Oikos 101:38–48

    Google Scholar 

  • Dicke M, van Loon JJA, Soler R (2009) Chemical complexity of volatiles from plants induced by multiple attack. Nat Chem Biol 5:317–324

    CAS  PubMed  Google Scholar 

  • Dussourd DE (1993) Foraging with finesse: caterpillar adaptations for circumventing plant defenses. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constraints on foraging. Chapman & Hall, London, pp 92–131

    Google Scholar 

  • English-Loeb GM, Karban R, Hougen-Eitzman D (1993) Direct and indirect competition between spider mites feeding on grapes. Ecol Appl 3:699–707

    Google Scholar 

  • Espinosa EG, Fornoni J (2006) Host tolerance does not impose selection on natural enemies. New Phytol 170:609–614

    PubMed  Google Scholar 

  • Faeth SH (1986) Indirect interactions between temporally separated herbivores mediated by the host plant. Ecology 67:479–494

    Google Scholar 

  • Fordyce JA (2006) The evolutionary consequences of ecological interactions mediated through phenotypic plasticity. J Exp Biol 209:2377–2383

    PubMed  Google Scholar 

  • Fussmann GF, Ellner SP, Hairston NG (2003) Evolution as a critical component of plankton dynamics. Proc R Soc Lond B 270:1015–1022

    Google Scholar 

  • Fussmann GF, Loreau M, Abrams PA (2007) Eco-evolutionary dynamics of communities and ecosystems. Funct Ecol 21:465–477

    Google Scholar 

  • Gatehouse JA (2002) Plant resistance towards insect herbivores: a dynamic interaction. New Phytol 156:145–169

    CAS  Google Scholar 

  • Gould R (1988) Genetics of pairwise and multispecies plant–herbivore coevolution. In: Spencer KC (ed) Chemical mediation of coevolution. Academic Press, San Diego, pp 13–55

    Google Scholar 

  • Hairston NG, Ellner SP, Geber MA, Yoshida T, Fox JA (2005) Rapid evolution and the convergence of ecological and evolutionary time. Ecol Lett 8:1114–1127

    Google Scholar 

  • Haloin JR, Strauss SY (2008) Interplay between ecological communities and evolution: review of feedbacks from microevolutionary to macroevolutionary scales. Ann NY Acad Sci 1133:87–125

    PubMed  Google Scholar 

  • Harmon LJ, Matthews B, Des Roches S, Chase JM, Shurin JB, Schluter D (2009) Evolutionary diversification in stickleback affects ecosystem functioning. Nature 458:1167–1170

    CAS  PubMed  Google Scholar 

  • Helmus MR, Dussourd DE (2005) Glues or poisons: which triggers vein cutting by monarch caterpillars? Chemoecology 15:45–49

    CAS  Google Scholar 

  • Hougen-Eitzman D, Karban R (1995) Mechanisms of interspecific competition that result in successful control of Pacific mites following inoculations of Willamette mites on grapevines. Oecologia 103:157–161

    Google Scholar 

  • Huhta A-P, Lennartsson T, Tuomi J, Rautio P, Laine K (2000) Tolerance of Gentianella campestris in relation to damage intensity: an interplay between apical dominance and herbivory. Evol Ecol 14:373–392

    Google Scholar 

  • Inouye B, Stinchcombe JR (2001) Relationships between ecological interaction modifications and diffuse coevolution: similarities, differences, and causal links. Oikos 95:353–360

    Google Scholar 

  • Iwao K, Rausher MD (1997) Evolution of plant resistance to multiple herbivores: quantifying diffuse coevolution. Am Nat 149:316–335

    Google Scholar 

  • Johnson MTJ (2010) The contribution of evening primrose (Oenothera biennis) to a modern synthesis of evolutionary ecology. Popul Ecol. doi:10.1007/s10144-010-0250-5

  • Johnson MTJ, Stinchcombe JR (2007) An emerging synthesis between community ecology and evolutionary biology. Trends Ecol Evol 22:250–257

    PubMed  Google Scholar 

  • Johnson MTJ, Vellend M, Stinchcombe JR (2009) Evolution in plant populations as a driver of ecological changes in arthropod communities. Philos Trans R Soc Lond B 364:1593–1605

    Google Scholar 

  • Johnson SN, Mayhew PJ, Douglas AE, Hartley SE (2002) Insects as leaf engineers: can leaf-miners alter leaf structure for birch aphids? Funct Ecol 16:575–584

    Google Scholar 

  • Jones LE, Becks L, Ellner SP, Hairston NG, Yoshida T, Fussman GF (2009) Rapid contemporary evolution and clonal food web dynamics. Philos Trans R Soc Lond B 364:1579–1591

    Google Scholar 

  • Kant MR, Sabelis MW, Haring MA, Schuurink RC (2008) Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences. Proc R Soc Lond B 275:443–452

    CAS  Google Scholar 

  • Kaplan I, Denno RF (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol Lett 10:977–994

    PubMed  Google Scholar 

  • Karban R (1986) Interspecific competition between folivorous insects on Erigeron glaucus. Ecology 67:1063–1072

    Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago

    Google Scholar 

  • Kessler A, Halitschke R, Baldwin IT (2004) Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305:665–668

    CAS  PubMed  Google Scholar 

  • Lankau RA, Strauss SY (2008) Community complexity drives patterns of natural selection on a chemical defense of Brassica nigra. Am Nat 171:150–161

    PubMed  Google Scholar 

  • Li X, Schuler MA, Berenbaum MR (2002) Jasmonate and salicylate induce expression of herbivore cytochrome P450 genes. Nature 419:712–715

    CAS  PubMed  Google Scholar 

  • Long JD, Hamilton RS, Mitchell JL (2007) Asymmetric competition via induced resistance: specialist herbivores indirectly suppress generalist preference and populations. Ecology 88:1232–1240

    PubMed  Google Scholar 

  • Martinsen GD, Driebe EM, Whitham TG (1998) Indirect interactions mediated by changing plant chemistry: beaver browsing benefits beetles. Ecology 79:192–200

    Google Scholar 

  • Mattiacci L, Rudelli S, Rocca BA, Genini S, Dorn S (2001) Systemically-induced response of cabbage plants against a specialist herbivore, Pieris brassicae. Chemoecology 11:167–173

    Google Scholar 

  • McCloud ES, Tallamy DW, Halaweish FT (1995) Squash beetle trenching behavior: avoidance of cucurbitacin induction or mucilaginous plant sap? Ecol Entomol 20:51–59

    Google Scholar 

  • McNaughton SJ (1983) Compensatory plant growth as a response to herbivory. Oikos 40:329–336

    Google Scholar 

  • Molis M, Enge A, Karsten U (2010) Grazing impact of, and indirect interactions between mesograzers associated with kelp (Laminaria digitata). J Phycol 46:76–84

    Google Scholar 

  • Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy JB, Felton GW (2002) Herbivory: caterpillar saliva beats plant defences. Nature 416:599–600

    CAS  PubMed  Google Scholar 

  • Nakamura M, Miyamoto Y, Ohgushi T (2003) Gall initiation enhances the availability of food resources for herbivorous insects. Funct Ecol 17:851–857

    Google Scholar 

  • Núñez-Farfán J, Fornoni J, Valverde PL (2007) The evolution of resistance and tolerance to herbivores. Annu Rev Ecol Evol Syst 38:541–566

    Google Scholar 

  • Odling-Smee FJ, Laland KN, Feldman MW (2003) Niche construction: the neglected process in evolution. Princeton University Press, Princeton

    Google Scholar 

  • Ohgushi T (2005) Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Evol Syst 36:81–105

    Google Scholar 

  • Ohgushi T (2008) Herbivore-induced indirect interaction webs on terrestrial plants: the importance of non-trophic, indirect, and facilitative interactions. Entomol Exp Appl 128:217–229

    Google Scholar 

  • Ohgushi T, Craig TP, Price PW (2007) Ecological communities: plant mediation in indirect interaction webs. Cambridge University Press, Cambridge

    Google Scholar 

  • Palkovacs EP, Post DM (2008) Eco-evolutionary interactions between predators and prey: can predator-induced changes to prey communities feed back to shape predator foraging traits? Evol Ecol Res 10:699–720

    Google Scholar 

  • Palkovacs EP, Post DM (2009) Experimental evidence that phenotypic divergence in predators drives community divergence in prey. Ecology 90:300–305

    PubMed  Google Scholar 

  • Palkovacs EP, Marshall MC, Lamphere BA, Lynch BR, Weese DJ, Fraser DF, Reznick DN, Pringle CM, Kinnison MT (2009) Experimental evaluation of evolution and coevolution as agents of ecosystem change in Trinidadian streams. Philos Trans R Soc Lond B 364:1617–1628

    Google Scholar 

  • Poelman EH, van Loon JJA, van Dam NM, Vet LEM, Dicke M (2010) Herbivore-induced plant responses in Brassica oleracea prevail over effects of constitutive resistance and result in enhanced herbivore attack. Ecol Entomol 35:240–247

    Google Scholar 

  • Polis GA, Winemiller KO (1996) Food webs: integration of patterns and dynamics. Chapman & Hall, New York

    Google Scholar 

  • Post DM, Palkovacs EP (2009) Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play. Philos Trans R Soc Lond B 364:1629–1640

    Google Scholar 

  • Post DM, Palkovacs EP, Schielke EG, Dodson SI (2008) Intraspecific variation in a predator affects community structure and cascading trophic interactions. Ecology 89:2019–2032

    PubMed  Google Scholar 

  • Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86:501–509

    Google Scholar 

  • Rasmann S, Turlings TCJ (2007) Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies. Ecol Lett 10:926–936

    PubMed  Google Scholar 

  • Raupp MJ, Denno RF (1984) The suitability of damaged willow leaves as food for the leaf beetle, Plagiodera versicolora. Ecol Entomol 9:443–448

    Google Scholar 

  • Raupp MJ, Sadof CS (1991) Responses of leaf beetles to injury-related changes in their salicaceous hosts. In: Tallamy DW, Raupp MJ (eds) Phytochemical induction by herbivores. Wiley, New York, pp 183–203

    Google Scholar 

  • Rodriguez-Saona C, Crafts-Brandner SJ, Cañas LA (2003) Volatile emissions triggered by multiple herbivore damage: beet armyworm and whitefly feeding on cotton plants. J Chem Ecol 29:2539–2550

    CAS  PubMed  Google Scholar 

  • Rodriguez-Saona C, Chalmers JA, Raj S, Thaler JS (2005) Induced plant responses to multiple damagers: differential effects on an herbivore and its parasitoid. Oecologia 143:566–577

    PubMed  Google Scholar 

  • Roslin T, Syrjälä H, Roland J, Harrison PJ, Fownes S, Matter SF (2008) Caterpillars on the run—induced defences create spatial patterns in host plant damage. Ecography 31:335–347

    Google Scholar 

  • Rundle HD, Vamosi SM, Schluter D (2003) Experimental test of predation’s effect on divergent selection during character displacement in sticklebacks. Proc Natl Acad Sci USA 100:14943–14948

    CAS  PubMed  Google Scholar 

  • Schmitz OJ (1998) Direct and indirect effects of predation and predation risk in old-field interaction webs. Am Nat 151:327–342

    CAS  PubMed  Google Scholar 

  • Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163

    Google Scholar 

  • Siepielski AM, Benkman CW (2004) Interactions among moths, crossbills, squirrels, and lodgepole pine in a geographic selection mosaic. Evolution 58:95–101

    PubMed  Google Scholar 

  • Stinchcombe JR (2002) Can tolerance traits impose selection on herbivores? Evol Ecol 16:595–602

    Google Scholar 

  • Stinchcombe JR, Rausher MD (2002) The evolution of tolerance to deer herbivory: modifications caused by the abundance of insect herbivores. Proc R Soc Lond B 269:1241–1246

    Google Scholar 

  • Stout MJ, Workman KV, Bostock RM, Duffey SS (1998) Specificity of induced resistance in the tomato, Lycopersicon esculentum. Oecologia 113:74–81

    Google Scholar 

  • Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant–animal interactions. Annu Rev Ecol Evol Syst 35:435–466

    Google Scholar 

  • Strauss SY, Sahli H, Conner JK (2005) Toward a more trait-centered approach to diffuse (co)evolution. New Phytol 165:81–89

    PubMed  Google Scholar 

  • Takabayashi J, Shimoda T, Dicke M, Ashihara W, Takafuji A (2000) Induced response of tomato plants to injury by green and red strains of Tetranychus urticae. Exp Appl Acarol 24:377–383

    CAS  PubMed  Google Scholar 

  • Thompson JN (1994) The coevolutionary process. University of Chicago Press, Chicago

    Google Scholar 

  • Thompson JN (1998) Rapid evolution as an ecological process. Trends Ecol Evol 13:329–332

    CAS  PubMed  Google Scholar 

  • Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago

    Google Scholar 

  • Tscharntke T (1989) Attack by a stem-boring moth increases susceptibility of Phragmites australis to gall-making by a midge: mechanisms and effects on midge population dynamics. Oikos 54:93–100

    Google Scholar 

  • Underwood N (2000) Density dependence in induced plant resistance to herbivore damage: threshold, strength and genetic variation. Oikos 89:295–300

    Google Scholar 

  • Utsumi S, Ohgushi T (2007) Plant regrowth response to a stem-boring insect: a swift moth–willow system. Popul Ecol 49:241–248

    Google Scholar 

  • Utsumi S, Ohgushi T (2008) Host plant variation in plant-mediated indirect effects: moth boring-induced susceptibility of willows to a specialist leaf beetle. Ecol Entomol 33:250–260

    Google Scholar 

  • 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

    Google Scholar 

  • Utsumi S, Ando Y, Ohgushi T (2009a) Evolution of feeding preference in a leaf beetle: the importance of phenotypic plasticity of a host plant. Ecol Lett 12:920–929

    PubMed  Google Scholar 

  • Utsumi S, Nakamura M, Ohgushi T (2009b) Community consequences of herbivore-induced bottom-up trophic cascades: the importance of resource heterogeneity. J Anim Ecol 78:953–963

    PubMed  Google Scholar 

  • Utsumi S, Ando Y, Miki T (2010) Linkages among trait-mediated indirect effects: a new framework for the indirect interaction web. Popul Ecol 52:485–497

    Google Scholar 

  • van Straalen NM, Roelofs D (2006) An introduction to ecological genomics. Oxford University Press, New York

    Google Scholar 

  • Van Zandt PA, Agrawal AA (2004) Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85:2616–2629

    Google Scholar 

  • Voelckel C, Baldwin IT (2004) Herbivore-induced plant vaccination. Part II. Array-studies reveal the transience of herbivore-specific transcriptional imprints and a distinct imprint from stress combinations. Plant J 38:650–663

    CAS  PubMed  Google Scholar 

  • Wallin KF, Raffa KF (2001) Effects of folivory on subcortical plant defenses: can defense theories predict interguild processes? Ecology 82:1387–1400

    Google Scholar 

  • Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100

    Google Scholar 

  • Whitham TG, Bailey JK, Schweitzer JA, Shuster SM, Bangert RK, LeRoy CJ, Lonsdorf EV, Allan GJ, DiFazio SP, Potts BM, Fischer DG, Gehring CA, Lindroth RL, Marks JC, Hart SC, Wimp GM, Wooley SC (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7:510–523

    CAS  PubMed  Google Scholar 

  • Whitham TG, DiFazio SP, Schweitzer JA, Shuster SM, Allan GJ, Bailey JK, Woolbright SA (2008) Extending genomics to natural communities and ecosystems. Science 320:492–495

    CAS  PubMed  Google Scholar 

  • Yoshida T, Jones LE, Ellner SP, Fussmann GF, Hairston NG (2003) Rapid evolution drives ecological dynamics in a predator–prey system. Nature 424:303–306

    CAS  PubMed  Google Scholar 

  • Yoshida T, Ellner SP, Jones LE, Bohannan BJM, Lenski RE, Hairston NG (2007) Cryptic population dynamics: rapid evolution masks trophic interactions. Plos Biol 5:1868–1879

    CAS  Google Scholar 

  • Zhang P-J, Zheng S-J, van Loon JJA, Boland W, David A, Mumm R, Dicke M (2009) Whiteflies interfere with indirect plant defense against spider mites in lima bean. Proc Natl Acad Sci USA 106:21202–21207

    CAS  PubMed  Google Scholar 

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Acknowledgments

I am grateful to Takayuki Ohgushi for providing me the opportunity to talk in the symposium in the 25th annual meeting of the Society of Population Ecology and write this manuscript. I also thank two anonymous reviewers and Yoshino Ando for valuable comments to an earlier draft. This work was partly supported by Global COE program (A06) to Kyoto University and a Grant-in Aid for a Research Fellow of the Japan Society of the Promotion of Science (no. 22-9260) to Shunsuke Utsumi.

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  1. Department of General Systems Studies, University of Tokyo, 3-8-1 Komaba, Meguro, Tokyo, 153-8902, Japan

    Shunsuke Utsumi

  2. Department of Biology, University of Eastern Finland, POB 111, Joensuu, 80101, Finland

    Shunsuke Utsumi

  3. Center for Ecological Research, Kyoto University, Otsu, Shiga, 520-2113, Japan

    Shunsuke Utsumi

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Correspondence to Shunsuke Utsumi.

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This manuscript was submitted for the special feature based on the symposium in Kyoto, held on 18th October 2009.

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Utsumi, S. Eco-evolutionary dynamics in herbivorous insect communities mediated by induced plant responses. Popul Ecol 53, 23–34 (2011). https://doi.org/10.1007/s10144-010-0253-2

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