Abstract
Plants have diverse ways of responding to damage by herbivores, such as changes in allelochemistry, physiology, morphology, growth, and phenology. These responses form the mechanistic basis for trait-mediated indirect interactions (TMIIs) between organisms on the plants. There is a growing appreciation that such TMIIs form complex networks (i.e., indirect interaction webs) in terrestrial plant-associated arthropod communities. Almost all previous studies have had the same framework: examining trait-mediated indirect effects within a single interactive unit consisting of one initiator of herbivore, a host plant as a mediator, and one receiver [trait-mediated indirect interaction unit (TMIU)]. However, this framework is too simple to understand the dynamics of the indirect interaction web. Recent studies suggest that there is a wide variety of interactions among TMIUs within a community, which may largely affect the outcomes of indirect effects in each unit. Here, we review recent advance in studies of trait-mediated indirect effects in plant-associated arthropod communities and explore the mechanisms of linkages among TMIUs. Then, we argue the importance of examining linkages among TMIUs as a new framework for future studies on the indirect interaction web. Finally, we propose the hypothesis that linkages among TMIUs contribute to the maintenance of biodiversity.
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References
Abrams PA (1995) Implications of dynamically variable traits for identifying, classifying, and measuring direct and indirect effects in ecological communities. Am Nat 146:112–134
Agrawal AA (1999) Induced responses to herbivory in wild radish: effects on several herbivores and plant fitness. Ecology 80:1713–1723
Agrawal AA (2000) Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars. Oikos 89:493–500
Agrawal AA (2005) Future directions in the study of induced plant responses to herbivory. Entomol Exp Appl 115:97–105
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
Bailey JK, Whitham TG (2002) Interactions among fire, aspen, and elk affect insect diversity: reversal of a community response. Ecology 83:1701–1712
Baldwin IT (1991) Damage-induced alkaloids in wild tobacco. In: Tallamy DW, Raupp MJ (eds) Phytochemical induction by herbivores. Wiley, New York, pp 47–69
Baldwin IT, Schmelz EA (1994) Constraints on an induced defense: the role of leaf area. Oecologia 97:424–430
Beckerman AP, Uriate M, Schmitz OJ (1997) Experimental evidence for a behavior-mediated trophic cascade in a terrestrial food chain. Proc Natl Acad Sci USA 94:10735–10738
Bergelson J, Fowler S, Hartley S (1986) The effects of foliage damage on casebearing moth larvae, Coleophora serratella, feeding on birch. Ecol Entomol 11:241–250
Berlow EL, Neutel A-M, Cohen JE, De Ruiter PC, Evenman B, Emmerson M, Fox JW, Jansen VAA, Jones JI, Kokkoris GD, Logofet DO, McKane AJ, Montoya JM, Petchey O (2004) Interaction strengths in food webs: issues and opportunities. J Anim Ecol 73:585–598
Bezemer TM, Van Dam NM (2005) Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol Evol 20:617–624
Bezemer TM, Wagenaar R, Van Dam NM, Wäckers FL (2003) Interactions between above- and belowground insect herbivores as mediated by the defense system. Oikos 101:555–562
Bolker B, Holyoak M, Křivan V, Rowe L, Schmitz O (2003) Connecting theoretical and empirical studies of trait-mediated indirect interactions. Ecology 84:1101–1114
Cipollini D, Enright S, Traw MB, Bergelson J (2004) Salicylic acid inhibits jasmonic acid-induced resistance Arabidopsis thaliana to Spodoptera exigua. Mol Ecol 13:1643–1653
Creel S, Winnie J, Maxwell B, Hamlin K, Creel M (2005) Elk alter habitat selection as an antipredator response to wolves. Ecology 86:3387–3397
Cronin JT, Haynes KJ, Dillemuth F (2004) Spider effects on planthopper mortality, dispersal, and spatial population dynamics. Ecology 85:2134–2143
Davis MA, Gordon MP, Smit BA (1991) Assimilate movement dictates remote sites of wound-induced gene expression in popular leaves. Proc Natl Acad Sci USA 88:2393–2396
de Boer JG, Hordijk CA, Posthumus MA, Dicke M (2008) Prey and non-prey arthropods sharing a host plant: effects on induced volatile emission and predator attraction. J Chem Ecol 34:281–290
De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573
De Vos M, Van Zaanen W, Koornneef A, Korzelius JP, Dicke M, Van Loon LC, Pieterse CMJ (2006) Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiol 142:352–363
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
Denno RF, Peterson MA (1995) Density-dependent dispersal and its consequences for population dynamics. In: Cappuccino N, Price PW (eds) Population dynamics: new approaches and synthesis. Academic Press, San Diego, pp 113–130
Denno RF, McClure MS, Ott JR (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu Rev Entomol 40:297–331
Denno RF, Gratton C, Peterson MA, Gratton C, Cheng J, Langelloto GA, Huberty AF, Finke DL (2000) Feeding-induced changes in plant quality mediate interspecific competition between sap-feeding herbivores. Ecology 81:1814–1827
Dicke M (1999) Evolution of induced indirect defense of plants. In: Tollrian R, Harvell CE (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, pp 62–88
Dicke M, Van Loon JJA, Soler R (2009) Chemical complexity of volatile from plants induced by multiple attack. Nat Chem Biol 5:317–324
Edwards PJ, Wratten SD (1983) Wound induced defenses in plants, and their consequences for patterns of insect grazing. Oecologia 59:88–93
Faeth SH (1986) Indirect interactions between temporally separated herbivores mediated by the host plant. Ecology 67:479–494
Felton GW, Korth KL, Bi JL, Wesley SV, Huhman DV, Mathews MC, Murphy JB, Lamb C, Dixon RA (1999) Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory. Curr Biol 9:317–320
Fortin D, Beyer HL, Boyce MS, Smith DS, Duchesne T, Mao JS (2005) Elk movements: behavior shapes a trophic cascade in Yellowstone National Park. Ecology 86:1320–1330
Garay-Narváez L, Ramos-Jiliberto R (2009) Induced defenses within food webs: the role of community trade-offs, delayed responses, and defense specificity. Ecol Complex 6:383–391
Gols R, Roosjen M, Dijkman H, Dicke M (2003) Induction of direct and indirect plant responses by jasmonic acid, low spider mites densities, or a combination of jasmonic acid treatment and spider mite infection. J Chem Ecol 29:2651–2666
Griffin CAM, Thaler JS (2006) Insect predators affect plant resistance via density- and trait-mediated indirect interactions. Ecol Lett 9:338–346
Halaj J, Ross DW, Moldenke AR (2000) Importance of habitat structure to the arthropod food-web in Douglas-fir canopies. Oikos 90:139–152
Heil M (2010) Plastic defence expression in plants. Evol Ecol 24:555–569
Heil M, Bueno JCS (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104:5467–5472
Heil M, Koch T, Hilpert A, Fiala B, Boland W, Linsenmair KE (2001) Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid. Proc Natl Acad Sci USA 98:1083–1088
Huhta A-P, Lennartsson T, Tuomi J, Raustio 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
Inbar M, Doostdar H, Mayer RT (1999) Effects of sessile whitefly nymphs (Homoptera: Aleyrodidae) on leaf-chewing larvae (Lepidoptera: Noctuidae). Environ Entomol 28:353–357
James DG, Grasswitz TR (2005) Synthetic herbivore-induced plant volatiles increase filed captures of parasitic wasps. Biol Control 50:871–880
Kaitaniemi P, Vehvilläinen H, Ruohomäki K (2004) Movement and disappearance of mountain birch defoliators are influenced by the interactive effects of plant architecture and induced resistance. Ecol Entomol 29:437–446
Kant MR, Ament K, Sabelis MW, Haring MA, Schuurink RC (2004) Differential timing of spider mite-induced direct and indirect defenses in tomato plants. Plant Physiol 135:483–495
Kaplan I, Denno RF (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol Lett 10:977–994
Kaplan I, Lynch ME, Dively GP, Denno RF (2007) Leafhopper-induced plant resistance enhances predation risk in a phytophagous beetle. Oecologia 152:665–675
Kaplan I, Halitschke R, Kessler A, Rehill BJ, Sardanelli S, Denno RF (2008) Physiological integration of roots and shoots in plant defense strategies links above- and belowground herbivory. Ecol Lett 11:841–851
Kaplan I, Srdanelli S, Denno RF (2009) Field evidence for indirect interactions between foliar-feeding insect and root-feeding nematode communities on Nicotiana tabacum. Ecol Entomol 34:262–270
Karban R, Baldwin IT (1997) Induced response to herbivory. University of Chicago Press, Chicago
Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144
Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328
Kessler A, Baldwin IT (2004) Herbivore-induced plant vaccination. Part I. The orchestration of plant defenses in nature and their fitness consequences in the wild tobacco Nicotiana attenuata. Plant J 38:639–649
Kessler A, Halitschke R (2007) Specificity and complexity: the impact of herbivore-induced plant responses on arthropod community structure. Curr Opin Plant Biol 10:409–414
Kiefer IW, Slusarenko AJ (2003) The pattern of systemic acquired resistance induction within the Arabidopsis rosette in relation to the pattern of translocation. Plant Physiol 132:840–847
Kondoh M (2003) Foraging adaptation and the relationship between food-web complexity and stability. Science 299:1388–1391
Kondoh M (2007) Anti-predator defence and the complexity-stability relationship of food webs. Proc R Soc B 274:1617–1624
Krause SC, Raffa KF (1995) Defoliation intensity and larval age interact to affect sawfly performance on previously injured Pinus resinosa. Oecologia 102:24–30
Lynch ME, Kaplan I, Dively GP, Denno RF (2006) Host-plant-mediated competition via induced resistance: interactions between pest herbivores on potatoes. Ecol Appl 16:855–864
Martinsen GD, Driebe EM, Whitham TG (1998) Indirect interactions mediated by changing plant chemistry: beaver browsing benefits beetles. Ecology 79:192–200
Martinsen GD, Floate KD, Waltz AM, Wimp GM, Whitham TG (2000) Positive interactions between leafrollers and other arthropods enhance biodiversity on hybrid cottonwoods. Oecologia 123:82–89
Masters GJ, Jones TH, Rogers M (2001) Host-plant mediated effects of root herbivory on insect seed predators and their parasitoids. Oecologia 127:246–250
McNaughton SJ (1983) Compensatory plant growth as a response to herbivory. Oikos 40:329–336
Messina FJ (1981) Plant protection as a consequence of an ant-membracid mutualism: interactions on goldenrod (Solidago sp.). Ecology 62:1433–1440
Mewis I, Tokuhisa JG, Schultz JC, Appel HM, Ulrichs C, Gershenzon J (2006) Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways. Phytochemistry 67:2450–2462
Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692
Moran NA, Whitham TG (1990) Interspecific competition between root-feeding and leaf-galling aphids mediated by host-plant resistance. Ecology 71:1050–1058
Nakamura M, Miyamoto Y, Ohgushi T (2003) Gall initiation enhance the availability of food resources for herbivorous insects. Funct Ecol 17:851–857
Ohgushi T (2005) Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Evol Syst 36:81–105
Ohgushi T, Craig TP, Price PW (2007) Ecological communities: plant mediation in indirect interaction webs. Cambridge University Press, Cambridge
Orians CM (2005) Herbivores, vascular pathways, and systemic induction: facts and artifacts. J Chem Ecol 31:2231–2242
Orians CM, Jones CG (2001) Plants as resource mosaics: a functional model for predicting patterns of within-plant resource heterogeneity to consumers based on vascular architecture and local environmental variability. Oikos 94:493–504
Orians CM, Pomerleau J, Ricco R (2000) Vascular architecture generates fine scale variation in the systemic induction of proteinase inhibitors in tomato. J Chem Ecol 26:471–485
Orre GUS, Wratten SD, Jonsson M, Hale RJ (2010) Effects of an herbivore-induced plant volatile on arthropods from three trophic levels in brassicas. Biol Control 53:62–67
Paige KN (1992) Overcompensation in response to mammalian herbivory: from mutualistic to antagonistic interactions. Ecology 73:2076–2085
Pallini A, Janssen A, Sabelis MW (1997) Odour-mediated responses of phytophagous mites to conspecific and heterospecific competitors. Oecologia 110:179–185
Paul ND, Hatcher PE, Taylor JE (2000) Coping with multiple enemies: an integration of molecular and ecological perspectives. Trends Plant Sci 5:220–225
Poelman EH, Van Loon JJA, Dicke M (2008a) Consequences of variation in plant defense for biodiversity at higher trophic levels. Trends Plant Sci 13:534–541
Poelman EH, Broekgaarden C, Van Loon JJA, Dicke M (2008b) Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Mol Ecol 17:3352–3365
Poveda K, Steffan-Dewenter I, Scheu S, Tscharntke T (2007) Plant-mediated interactions between below- and aboveground processes: decomposition, herbivory, parasitism, and pollination. In: Ohgushi T, Craig TP, Price PW (eds) Ecological communities: plant mediation in indirect interaction webs. Cambridge University Press, Cambridge, pp 147–163
Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology 86:501–509
Preston CA, Lewandowski C, Enyedi AJ, Baldwin IT (1999) Tobacco mosaic virus inoculation inhibits wound-induced jasmonic acid-mediated responses within but not between plants. Planta 209:87–95
Raffa KF, Berryman AA (1987) Interacting selective pressures in conifer-bark beetle systems: a basis for reciprocal adaptations? Am Nat 129:234–262
Ramos-Jiliberto R, Mena-Lorca J, Flores JD, Morales-Álvarez W (2008) Role of inducible defenses in the stability of a tritrophic system. Ecol Complex 5:183–192
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
Raupp MJ, Sadof CS (1989) Behavioral responses of a leaf beetle to injury-related changes in its salicaceous host. Oecologia 80:154–157
Rhodes JD, Thain JF, Wildon DC (1999) Evidence for physically distinct systemic signaling pathways in the wounded tomato plant. Ann Bot Lond 84:109–116
Rieske LK, Raffa KF (1998) Interactions among insect herbivore guilds: influence of thrips bud injury of foliar chemistry and suitability to gypsy moths. J Chem Ecol 24:501–523
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
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
Roland J, Myers JH (1987) Improved insect performance from host-plant defoliation: winter moth on oak and apple. Ecol Entomol 12:409–414
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
Rothley KD, Schmitz OJ, Cohon JL (1997) Foraging to balance conflicting demands: novel insights from grasshoppers under predation risk. Behav Ecol 8:551–559
Rudgers JA, Hodgen JG, White JW (2003) Behavioral mechanisms underlie an ant-plant mutualism. Oecologia 135:51–59
Sandström J, Telang A, Moran NA (2000) Nutritional enhancement of host plants by aphids—a comparison of three aphid species on grasses. J Insect Physiol 46:33–40
Schittko U, Baldwin IT (2003) Constraints to herbivore-induced systemic responses: bidirectional signaling along orthostichies in Nicotiana attenuata. J Chem Ecol 29:763–770
Schmitz OJ (1998) Direct and indirect effects of predation and predation risk in old-field interaction webs. Am Nat 151:327–342
Schmitz OJ (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163
Schmitz OJ, Beckerman A, O’Brien KM (1997) Behaviourally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388–1399
Shulaev V, Leon J, Raskin I (1995) Is salicylic acid a translocated signal of systemic acquired resistance in tobacco? Plant Cell 7:1691–1701
Silkstone BE (1987) The consequences of leaf damage for subsequent insect grazing on birch (Betula spp.): a field experiment. Oecologia 74:149–152
Stamp NE, Bowers MD (1996) Consequences for plantain chemistry and growth when herbivores are attacked by predators. Ecology 77:535–549
Stout MJ, Workman KV, Bostock RM, Duffey SS (1998a) Specificity of induced resistance in the tomato, Lycopersicon esculentum. Oecologia 113:74–81
Stout MJ, Workman KV, Bostock RM, Duffey SS (1998b) Stimulation and attenuation of induced resistance by elicitors and inhibitors of chemical induction in tomato (Lycopersicon esculentum). Entomol Exp Appl 86:267–279
Thaler JS (1999) Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399:686–688
Thaler JS (2002) Effect of jasmonate-induced plant responses on the natural enemies of herbivores. J Anim Ecol 71:141–150
Thaler JS, Bostock RM (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogens and insects. Ecology 85:48–58
Thaler JS, Fidantsef AL, Duffey SS, Bostok RM (1999) Trade-offs in plant defense against pathogens and herbivores: a field demonstration of chemical elicitors of induced resistance. J Chem Ecol 25:1597–1609
Thaler JS, Fidantsef AL, Bostock RM (2002a) Antagonism between jasmonate- and salicylate-mediated induced plant resistance: effects of concentration and timing of elicitation on defense-related proteins, herbivore, and pathogen performance in tomato. J Chem Ecol 28:1131–1159
Thaler JS, Karban R, Ullman DE, Boege K, Bostock RM (2002b) Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites. Oecologia 131:227–235
Travers-Martin N, Müller C (2007) Specificity of induction responses in Sinapis alba L. and their effects on a specialist herbivore. J Chem Ecol 33:1582–1597
Traw MB, Dawson TE (2002) Differential induction of trichomes by three herbivores of black mustard. Oecologia 131:526–532
Underwood N (2000) Density dependence in induced plant resistance to herbivore damage: threshold, strength and genetic variation. Oikos 89:295–300
Underwood N, Anderson K, Inouye BD (2005) Induced vs. constitutive resistance and the spatial distribution of insect herbivores among plants. Ecology 86:594–602
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
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
Utsumi S, Nakamura M, Ohgushi T (2009) Community consequences of herbivore-induced bottom-up trophic cascades: the importance of resource heterogeneity. J Anim Ecol 78:953–963
Van Dam NM, Hadwich K, Baldwin IT (2000) Induced responses in Nicotiana attenuata affect behavior and growth of the specialist herbivore Manduca sexta. Oecologia 122:371–379
Van Zandt PA, Agrawal AA (2004a) Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85:2616–2629
Van Zandt PA, Agrawal AA (2004b) Specificity of induced plant responses to specialist herbivores of the common milkweed Asclepias Syriaca. Oikos 104:401–409
Viswanathan DV, Thaler JS (2004) Plant vascular architecture and within-plant spatial patterns in resource quality following herbivory. J Chem Ecol 30:531–543
Viswanathan DV, Narwani AJT, Thaler JS (2005) Specificity in induced plant responses shapes patterns of herbivore occurrence on Solanum dulcamara. Ecology 86:886–896
Viswanathan DV, Lifchits OA, Thaler JS (2007) Consequences of sequential attack for resistance to herbivores when plants have specific induced responses. Oikos 116:1389–1399
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
von Dahl CC, Havecker M, Schögl R, Baldwin IT (2006) Caterpillar-elicited methanol emission: a new signal in plant-herbivore interactions? Plant J 46:948–960
Wallin KF, Raffa KF (2001) Effects of folivory on subcortical plant defense: can defense theories predict interguild processes? Ecology 82:1387–1400
Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216
Watson MA, Casper BB (1984) Morphogenetic constraints on patterns of carbon distribution in plants. Annu Rev Ecol Syst 15:233–258
Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100
Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875
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
Zheng S-J, van Dijk JP, Bruinsma M, Dicke M (2007) Sensitivity and speed of induced defense of cabbage (Brassica leracea L.): dynamics of BoLox expression patterns during insect and pathogen attack. Mol Plant Microbe Interact 20:1332–1345
Acknowledgments
We thank T. Ohgushi, E. Nakajima, and anonymous reviewers for valuable comments on an earlier draft. We also thank O. Kishida, T. Namba, and M. Kondoh for their helpful comments on this study. This study was partly supported by the Global COE program A06 to Kyoto University and a Grant-in-Aid for a Research Fellow of the Japan Society for the Promotion of Science for Young Scientists (no. 22-9260) to S. Utsumi.
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Utsumi, S., Ando, Y. & Miki, T. Linkages among trait-mediated indirect effects: a new framework for the indirect interaction web. Popul Ecol 52, 485–497 (2010). https://doi.org/10.1007/s10144-010-0237-2
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DOI: https://doi.org/10.1007/s10144-010-0237-2