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Specialist versus generalist insect herbivores and plant defense

2012; Elsevier BV; Volume: 17; Issue: 5 Linguagem: Inglês

10.1016/j.tplants.2012.02.006

1878-4372

Jared G. Ali, Anurag A. Agrawal,

Plant Parasitism and Resistance

There has been a long-standing hypothesis that specialist and generalist insects interact with plants in distinct ways. Although many tests exist, they typically compare only one species of each, they sometimes confound specialization and feeding guild, and often do not link chemical or transcriptional measures of the plant to actual resistance. In this review, we synthesize current data on whether specialists and generalists actually differ, with special attention to comparisons of their differential elicitation of plant responses. Although we find few consistencies in plant induction by specialists versus generalists, feeding guilds are predictive of differential plant responses. We outline a novel set of predictions based on current coevolutionary hypotheses and make methodological suggestions for improved comparisons of specialists and generalists. There has been a long-standing hypothesis that specialist and generalist insects interact with plants in distinct ways. Although many tests exist, they typically compare only one species of each, they sometimes confound specialization and feeding guild, and often do not link chemical or transcriptional measures of the plant to actual resistance. In this review, we synthesize current data on whether specialists and generalists actually differ, with special attention to comparisons of their differential elicitation of plant responses. Although we find few consistencies in plant induction by specialists versus generalists, feeding guilds are predictive of differential plant responses. We outline a novel set of predictions based on current coevolutionary hypotheses and make methodological suggestions for improved comparisons of specialists and generalists. ‘Jack of all trades is master of none’. Here lies the theoretical basis for why ecologists and plant scientists have long argued that specialist insect herbivores, as compared with generalists, will have distinct and predictable interactions with their host plants (Box 1). With specialization, it was proposed that alongside the loss of ability to use many host plants, herbivores would gain the ability to tolerate plant defenses, manipulate hosts to their benefit and evolve ways to reduce predation and parasitism [1Krieger R.I. et al.Detoxication enzymes in the guts of caterpillars: an evolutionary answer to plant defenses?.Science. 1971; 172: 579-580Crossref PubMed Scopus (228) Google Scholar, 2Whittaker R.H. Feeny P.P. Allelochemics: chemical interactions between species.Science. 1971; 171: 757-770Crossref PubMed Scopus (820) Google Scholar]. This powerful and seductive hypothesis has been a mainstay of coevolutionary studies for over 40 years, and yet little resolution has been reached on certain predictions. In particular, we argue below that ecologists and plant scientists have been too quick to position the specialist–generalist dichotomy as a paradigm, and often uncritically. Below we evaluate the current evidence and provide a roadmap for future studies.Box 1Who's who on the diet breadth continuum?Insect herbivores have been conventionally grouped into categories based on their degree of dietary specialization. When limited to only one or a few closely related plant taxa, often a single genus, herbivores are considered monophagous (or highly specialized). Insect herbivores that feed on several plant species, usually within one botanical family, are designated oligophagous. Finally, polyphagous (or highly generalized) species are insects that feed on species in more than one plant family. Although these terms are helpful for generalizing broad groups of herbivores into simpler categories, their basis is drawn on fairly arbitrary observations and may lead to inherit limitations in their use. Nonetheless, some groups of herbivores, such as aphids, leaf hoppers and leaf miners are dominated (>75%) by monophages [71Schoonhoven L.M. et al.Insect-Plant Biology. Oxford University Press, 2005Google Scholar]. Across all herbivorous insects, it is estimated that 75%) by monophages [71Schoonhoven L.M. et al.Insect-Plant Biology. Oxford University Press, 2005Google Scholar]. Across all herbivorous insects, it is estimated that <10% feed on plants in more than three different plant families [72Bernays E.A. Graham M. On the evolution of host specificity in phytophagous arthropods.Ecology. 1988; 69: 886-892Crossref Google Scholar]. The distribution of feeding on one plant species to a diversity of plants is truly a graded continuum. We also recognize that polyphagous individuals can show preferences over their distribution of hosts, where herbivores may be more limited than we predict. Here we have adopted the terms specialists and generalists to focus on the extremes, usually meaning species that consume a few related species to species in several plant families, respectively. Nonetheless, the comparison is a relative one and the specific contrast of a specialist and generalist should be explained as fully as possible for each case. There have been several specific predictions made about the specialist–generalist paradigm. First, specialists should be less impacted by a given plant defense compared with a generalist [2Whittaker R.H. Feeny P.P. Allelochemics: chemical interactions between species.Science. 1971; 171: 757-770Crossref PubMed Scopus (820) Google Scholar] (Figure 1). In addition to being less affected by particular defense traits, some specialist herbivores have even evolved the capacity to use these same traits in host finding or protection from predators (sequestration or fecal shields). Second, generalists should have ‘general’ mechanisms to tolerate an array of plant defenses and also possess mechanisms to manipulate plants via highly conserved plant pathways [1Krieger R.I. et al.Detoxication enzymes in the guts of caterpillars: an evolutionary answer to plant defenses?.Science. 1971; 172: 579-580Crossref PubMed Scopus (228) Google Scholar, 2Whittaker R.H. Feeny P.P. Allelochemics: chemical interactions between species.Science. 1971; 171: 757-770Crossref PubMed Scopus (820) Google Scholar]. The notion behind this prediction is that although generalists do not master any one defense, many aspects of plant defense can be overcome because plants possess a common evolutionary history leading to shared physiological features in core signal transduction chains [e.g. jasmonate (JA) signaling] [3Katsir L. et al.Jasmonate signaling: a conserved mechanism of hormone sensing.Curr. Opin. Plant Biol. 2008; 11: 428-435Crossref PubMed Scopus (282) Google Scholar]. Third, upon damage, induced plant responses to specialists will be distinct compared with responses to generalists. This general prediction is complicated by coevolution: are observed plant responses adaptive for the plant or manipulated by herbivores? The perspective from which we view the interaction distinctly shapes our predictions (Figure 2).Figure 2Three herbivore strategies (a–c) and their expected relationships with plant toxins. Sequestering specialists benefit from the toxins at intermediate levels (via protection from predation) and nonsequestering specialists are tolerant of toxins at low levels; however, in both cases toxins eventually impose a cost. From the perspective of the insect, induction should maximize their own growth, and across all herbivore strategies induction should be low (either intermediate, minimal or suppressed (a–c), respectively). From the perspective of the plant, maximizing defense, induction responses can be more variable and alternative strategies (i.e. indirect defense via induction of volatile organic compounds) might be the most effective defense against specialists. We note that there are special cases that might not fit this model; for example, some generalists benefit from feeding on toxic plants, even if they do not sequester the toxins [59Cornelius M.L. Bernays E.A. The effect of plant chemistry on the acceptability of caterpillar prey to the argentine ant iridomyrmex humilis (hymenoptera: formicidae).J. Insect Behav. 1995; 8: 579-593Crossref Scopus (28) Google Scholar].View Large Image Figure ViewerDownload (PPT) Although we will touch on the first prediction above, the focus of our review is on the latter two: how and why specialists and generalists might elicit differential plant responses (or manipulate the plants in different ways). Since the origin of the specialist–generalist paradigm, there have been hundreds of studies of insect tolerance and detoxification of plant defense [4Cornell H. Hawkins B. Herbivore responses to plant secondary compounds: a test of phytochemical coevolution theory.Am. Nat. 2003; 161: 507-522Crossref PubMed Scopus (188) Google Scholar]. However, it is only in the past 20 years that plant biologists have realized that induced responses are a crucial component of plant defense, and ideas about how specialists and generalists differ in this regard are continuing to develop. In addition, modern studies that span bioassays of insect preference and performance, plant production of hormonal signals and defensive secondary metabolites, and transcriptional responses have the potential to aid us in making rapid progress in understanding how and why specialists and generalist herbivores differ. The notion that specialists are immune to the defenses of the host plant is widespread but incorrect. Cases where specialist herbivores are negatively impacted by defense compounds include: parsnip webworms (Depressaria pastinacella) eating furanocoumarins [5Berenbaum M. et al.Chemical barriers to adaptation by a specialist herbivore.Oecologia. 1989; 80: 501-506Crossref Scopus (58) Google Scholar], buckeye caterpillars (Junonia coenia) ingesting iridoid glycosides [6Adler L.S. et al.Genetic variation in defensive chemistry in Plantago lanceolata (Plantaginaceae) and its effect on the specialist herbivore Junonia coenia (Nymphalidae).Oecologia. 1995; 101: 75-85Crossref Scopus (106) Google Scholar], monarch caterpillars (Danaus plexippus) on cardenolide-containing sandhill milkweed (Asclepias humistrata) [7Zalucki M.P. et al.Detrimental effects of latex and cardiac glycosides on survival and growth of first-instar monarch butterfly larvae Danaus plexippus feeding on the sandhill milkweed Asclepias humistrata.Ecol. Entomol. 2001; 26: 212-224Crossref Scopus (134) Google Scholar], cabbage white caterpillars (Pieris rapae) being poisoned by isothiocyanates [8Agrawal A.A. Kurashige N.S. A role for isothiocyanates in plant resistance against the specialist herbivore Pieris rapae.J. Chem. Ecol. 2003; 29: 1403-1415Crossref PubMed Scopus (270) Google Scholar] and tobacco hornworms (Manduca sexta) fed artificial diets containing nicotine [9Harvey J.A. et al.Effects of dietary nicotine on the development of an insect herbivore, its parasitoid and secondary hyperparasitoid over four trophic levels.Ecol. Entomol. 2007; 32: 15-23Crossref Scopus (59) Google Scholar]. In nearly all of these cases, the specialists do have physiological adaptations to cope with the plant defenses, which allow greater tolerance than most generalists. Indeed, on average, specialist herbivores are less negatively impacted by defense compounds than generalists [4Cornell H. Hawkins B. Herbivore responses to plant secondary compounds: a test of phytochemical coevolution theory.Am. Nat. 2003; 161: 507-522Crossref PubMed Scopus (188) Google Scholar] (Figure 1). Our main message is that tolerance of specialist insects to low levels of toxins is to be expected; however, at higher levels of defense, few insects are immune to the deleterious effects of plant toxins. It is unclear whether certain classes of plant defense are more effective against generalists or specialists. A study 35 years ago suggested that although toxins could be overcome by specialists, digestibility reducers are likely to be effective against all attackers [10Feeny P. Plant apparency and chemical defense.Recent Adv. Phytochem. 1976; 10: 1-40Google Scholar]. Others have argued that indirect defense (i.e. attracting enemies of herbivores) is likely to be more difficult to overcome compared with direct defense (e.g. digestibility reducers and toxins) [11Kahl J. et al.Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore.Planta. 2000; 210: 336-342Crossref PubMed Scopus (276) Google Scholar]. Although most plants produce all of these classes of defense, both generalists and specialists can overcome some digestibility reducers, although it is unclear how common this is [12Bernays E.A. Diet-induced head allometry among foliage-chewing insects and its importance for graminivores.Science. 1986; 231: 495-497Crossref PubMed Scopus (134) Google Scholar, 13Broadway R.M. Are insects resistant to plant proteinase inhibitors?.J. Insect Physiol. 1995; 41: 107-116Crossref Scopus (230) Google Scholar, 14Gruden K. et al.The cysteine protease activity of Colorado potato beetle (Leptinotarsa decemlineata Say) guts, which is insensitive to potato protease inhibitors, is inhibited by thyroglobulin type-1 domain inhibitors.Insect Biochem. Mol. 1998; 28: 549-560Crossref PubMed Scopus (74) Google Scholar]. In addition, some generalists possess remarkable abilities to consume highly toxic host plants [15Hartmann T. et al.Acquisition, transformation and maintenance of plant pyrrolizidine alkaloids by the polyphagous arctiid Grammia geneura.Insect Biochem. Mol. 2005; 35: 1083-1099Crossref PubMed Scopus (45) Google Scholar, 16Dussourd D.E. Denno R.F. Host range of generalist caterpillars: trenching permits feeding on plants with secretory canals.Ecology (Tempe). 1994; 75: 69-78Crossref Scopus (79) Google Scholar, 17Pelser P.B. et al.Frequent gain and loss of pyrrolizidine alkaloids in the evolution of Senecio section Jacobaea (Asteraceae).Phytochemistry. 2005; 66: 1285-1295Crossref PubMed Scopus (86) Google Scholar]. Thus, based on the literature and the commonly used experimental designs, few conclusions can be reached about the relative impact of different classes of plant defense on specialists and generalists. A hypothesis that grew out of the specialist–generalist paradigm is that specialist herbivores will cause distinct induction of plant defenses compared with those induced by generalists [18Bowers M. Stamp N. Effects of plant-age, genotype, and herbivory on Plantago performance and chemistry.Ecology. 1993; 74: 1778-1791Crossref Scopus (188) Google Scholar, 19Agrawal A.A. Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars.Oikos. 2000; 89: 493-500Crossref Scopus (210) Google Scholar, 20Poelman E.H. et al.Performance of specialist and generalist herbivores feeding on cabbage cultivars is not explained by glucosinolate profiles.Entomol. Exp. Appl. 2008; 127: 218-228Crossref Scopus (85) Google Scholar]. Nonetheless, there have been few explicit predictions in the literature about how and why specialists will differ from generalists with regard to elicitation of induced defenses. Given that generalists are typically more sensitive to plant toxins than specialists, from the perspective of the insect, one prediction is that generalists should suppress induced plant responses, whereas specialists should only minimize the induction of high levels of defense (Figure 2). From the perspective of the plant, the predicted responses are less consistent: induction of direct defenses could be variable against specialists (Figure 2), but induction of indirect defenses [e.g. extrafloral nectar and parasite-attracting volatile organic compounds (VOCs)] should be strong if the specialist is not sequestering. Nonetheless, it is presumably adaptive for plants to respond, as strongly as possible, to most generalists (Figure 2). Experiments comparing phenotypic or transcriptional responses to both specialist and generalist herbivores often include only one specialist and one generalist species, making rigorous conclusions impossible; in addition, many studies compare specialist and generalist species from different feeding guilds [21van Poecke R.M.P. et al.Attraction of the specialist parasitoid Cotesia rubecula to Arabidopsis thaliana infested by host or non-host herbivore species.Entomol. Exp. Appl. 2003; 107: 229-236Crossref Scopus (52) Google Scholar, 22Mewis I. et al.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. 2006; 67: 2450-2462Crossref PubMed Scopus (229) Google Scholar, 23Sutter R. Muller C. Mining for treatment-specific and general changes in target compounds and metabolic fingerprints in response to herbivory and phytohormones in Plantago lanceolata.New Phytol. 2011; 191: 1069-1082Crossref PubMed Scopus (38) Google Scholar]. We found 20 studies comparing the phenotypic or transcriptional responses of a plant to both specialist and generalist herbivores using one feeding guild (Table 1). Although we interpret these results in light of the predictions in Figure 2, we recommend caution because nearly every result can be interpreted in an adaptive context, because what is beneficial for the plant and beneficial for the insect herbivore can be different. In addition, we assumed that the authors were careful to match the amount and timing of damage by the two herbivores; we highly recommend that future studies explicitly address this issue (Box 2).Table 1Comparison of plant defensive response to at least one specialist and one generalist insect herbivore from the same feeding guildPlantGeneralistSpecialistMeasure of plant responseResultsaColor-coding reflects consistency with the hypotheses in Figure 2 (green = consistent, but only two species are compared). Yellow indicates no consistent pattern and red indicates that the level of specialization was not predictive of plant responses.(Brassicaceae)A. thaliana(Aphididae)Myzus persicae(Aphididae)Brevicoryne brassicaeTranscriptional responses, glucosinolates (GS)The generalist caused slightly more changes in gene expression than did the specialist (sequesterer). General stress-responsive genes and octadecanoid and indole GS synthesis genes were similarly induced by generalist and specialist 22Mewis I. et al.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. 2006; 67: 2450-2462Crossref PubMed Scopus (229) Google Scholar, 32Kusnierczyk A. et al.Transcriptional responses of Arabidopsis thaliana ecotypes with different glucosinolate profiles after attack by polyphagous Myzus persicae and oligophagous Brevicoryne brassicae.J. Exp. Bot. 2007; 58: 2537-2552Crossref PubMed Scopus (125) Google Scholar. The specialist induced a lower GS response than did the generalist 26Bidart-Bouzat M.G. Kliebenstein D. An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores.Oecologia. 2011; 167: 677-689Crossref PubMed Scopus (90) Google Scholar.(Brassicaceae)Brassica oleraceae(Aphididae)M. persicae(Aphididae)B. brassicaeGSInduction pattern by the two species depended on water status of the plant 58Winz R.A. Baldwin I.T. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. IV. Insect-induced ethylene reduces jasmonate-induced nicotine accumulation by regulating putrescine N-methyltransferase transcripts.Plant Physiol. 2001; 125: 2189-2202Crossref PubMed Scopus (200) Google Scholar.(Brassicaceae)A. thaliana(Noctuidae)Spodoptera exigua(Piridae)Pieris rapaeTranscriptional response, GSExpression of GS genes was similar for generalist and specialist, but GS levels only showed an increase in response to S. exigua. Mean aliphatic GS levels were equal. P. rapae caused a higher increase in indolyl GS content 22Mewis I. et al.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. 2006; 67: 2450-2462Crossref PubMed Scopus (229) Google Scholar.(Brassicaceae)A. thaliana(Noctuidae)S. littoralis(Piridae)P. rapaeTranscriptional responseTranscription profiles were indistinguishable 24Reymond P. et al.A conserved transcript pattern in response to a specialist and a generalist herbivore.Plant Cell. 2004; 16: 3132-3147Crossref PubMed Scopus (430) Google Scholar.(Brassicaceae)A. thaliana(Noctuidae)S. exigua(Piridae)P. rapae(Plutellidae)P. xylostellaParasitoid specificity for herbivore induced plant volatiles (HIPVs)Parasitoid attracted to damaged plants over controls for both generalists and specialists. Parasitoids only discriminate between induction by insects in different guilds 21van Poecke R.M.P. et al.Attraction of the specialist parasitoid Cotesia rubecula to Arabidopsis thaliana infested by host or non-host herbivore species.Entomol. Exp. Appl. 2003; 107: 229-236Crossref Scopus (52) Google Scholar.(Brassicaceae)A. thaliana(Noctuidae)T. ni,S. exigua(Piridae)P. rapae,(Plutellidae)P. xylostellaTranscriptional responses, GSTranscriptional responses and GS were not consistently influenced by degree of insect specialization 26Bidart-Bouzat M.G. Kliebenstein D. An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores.Oecologia. 2011; 167: 677-689Crossref PubMed Scopus (90) Google Scholar.(Brassicaceae)Brassica nigra(Noctuidae)Mamestra brassicae(Piridae)P. rapae,(Plutellidae)Plutella xylostellaGSIndole GS was significantly higher after feeding by P. rapae and M. brassicae than after P. xylostella feeding 60Poelman E.H. et al.Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field.Mol. Ecol. 2008; 17: 3352-3365Crossref PubMed Scopus (195) Google Scholar.(Brassicaceae)B. nigra(Noctuidae)Trichoplusia ni(Piridae)P. rapaeFoliar trichomes, sinigrin, foliar nitrogenDifferential induction by specialist versus generalist led to increased trichomes, but the effect reversed on different leaf positions 61Traw M.B. Dawson T.E. Differential induction of trichomes by three herbivores of black mustard.Oecologia. 2002; 131: 526-532Crossref Scopus (129) Google Scholar.(Brassicaceae)Boechera divaricarpa(Noctuidae)T. ni(Plutellidae)P. xylostellaTranscriptional responseSpecialist induced SA- and ethylene-associated genes, whereas generalist induced JA and ET genes 36Vogel H. et al.Different transcript patterns in response to specialist and generalist herbivores in the wild Arabidopsis relative Boechera divaricarpa.PLoS ONE. 2007; 2: e1081Crossref PubMed Scopus (38) Google Scholar. The specialist might be well adapted, but the plant defends against the generalist.(Brassicaceae)Raphanus sativus(Noctuidae)T. ni,S. exigua(Piridae)P. rapae,(Plutellidae)P. xylostellaInduced resistance, herbivore performanceVariation in induction was found, but it was not associated with insect specialization. P. xylostella and S. exigua induced resistance to all, whereas P. rapae only induced resistance to P. rapae and S. exigua. T. ni did not induce resistance 19Agrawal A.A. Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars.Oikos. 2000; 89: 493-500Crossref Scopus (210) Google Scholar.(Brassicaceae)Sinapis alba(Noctuidae)S. frugiperda(Tenthredinidae)Athalia rosaeGS, myrosinase (MYR)Specialist (sequesterer) and mechanical wounding induced GS and MYR threefold, whereas generalist induced only GS (twofold) 37Travers-Martin N. Mueller C. Matching plant defence syndromes with performance and preference of a specialist herbivore.Funct. Ecol. 2008; 22: 1033-1043Crossref Scopus (64) Google Scholar – generalist might be adaptively suppressing defense.(Lauraceae)Lindera benzoin(Noctuidae)S. exigua(Geometridae)Epimecis hortariaPeroxidase activity (POD), C/N ratio, protein content, insect bioassaysPOD activity was more strongly induced by generalist than specialist (no difference in bioassay) 62Mooney E.H. et al.Differential induced response to generalist and specialist herbivores by Lindera benzoin (Lauraceae) in sun and shade.Oikos. 2009; 118: 1181-1189Crossref Scopus (27) Google Scholar – plant might be adaptively defending against generalist.(Plantaginaceae)Plantago lanceolata(Nymphalidae)Junonia ceonia(Erebidae)Spilosoma congraIridoid GS (IrGS), protein, foliar nitrogenHigher IrGS induced by specialist (sequesterer) compared with generalist 63Stamp N.E. Bowers M.D. Effects of cages, plant age and the mechanical clipping on plantain chemistry.Oecologia (Berlin). 1994; 99: 66-71Crossref Scopus (32) Google Scholar – plant might be adaptively defending against generalist.PoaceaeZea mays(Chrysomelidae)Diabrotica balteata(Chrysomelidae)Diabrotica virgifera virgiferaParasitoid specificity for herbivore induced plant volatilesNatural enemies preferred roots attacked by specialist over roots damaged by generalist. The specialist induced significantly more (E)-β-caryophyllene than the generalist.(Solanacae)Nicotiana attenuata(Noctuidae)S. exigua(Sphingidae)Manduca sextaPhytohormonesSpecialist induced JA/ET burst, generalist induced SA 64Diezel C. et al.Different Lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling.Plant Physiol. 2009; 150: 1576-1586Crossref PubMed Scopus (257) Google Scholar – might be adaptive for generalists to suppress resistance by activating SA.(Solanacae)N. attenuata(Noctuidae)Heliothis virescens,S. exigua(Sphingidae)M. sextaTranscriptional responseDespite large overlap, the plant response to the generalists was more similar than the response to the specialist. This was correlated to FACs/oral secretions. Both generalists were noctuids and downregulated a large number of similar genes 54Voelckel C. Baldwin I.T. Generalist and specialist lepidopteran larvae elicit different transcriptional responses in Nicotiana attenuata, which correlate with larval FAC profiles.Ecol. Lett. 2004; 7: 770-775Crossref Scopus (91) Google Scholar.(Solanacae)N. attenuata(Noctuidae)T. ni,S. littoralis(Sphingidae)M. sextaPhytohormonesM. sexta induced a JA and SA response, whereas S. littoralis and T. ni induced stronger SA responses 33Heidel A. Baldwin I. Microarray analysis of salicylic acid- and jasmonic acid-signalling in responses of Nicotiana attenuata to attack by insects from multiple feeding guilds.Plant Cell Environ. 2004; 27: 1362-1373Crossref Scopus (186) Google Scholar.(Solanacae)N. tabacum(Noctuidae)Helicoverpa armigera(Noctuidae)Helicoverpa assultaLipoxygenase (LOX), proteinase inhibitors (PIs), nicotine, peroxidase (POD), polyphenol oxidase (PPO)Both herbivores induced a similar defensive response, but response intensity of plants was different: specialist induced a lower PPO response and more intensive nicotine and POD response than generalist (JA, LOX and PIs were not different) 65Zong N. Wang C.-Z. Larval feeding induced defensive responses in tobacco: comparison of two sibling species of Helicoverpa with different diet breadths.Planta. 2007; 226: 215-224Crossref PubMed Scopus (24) Google Scholar.a Color-coding reflects consistency with the hypotheses in Figure 2 (green = consistent, but only two species are compared). Yellow indicates no consistent pattern and red indicates that the level of specialization was not predictive of plant responses. Open table in a new tab Box 2Testing for differences in induced plant defense among specialist and generalist herbivoresIf the goal is to test the hypothesis that specialists elicit differential plant resistance compared with generalists, we recommend the following experimental design (Figure I). Ideally, a comparison of more than two species is necessary because any two species will differ in a myriad of ways. We suggest a minimum of comparin