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Plant and herbivore ontogeny interact to shape the preference, performance and chemical defense of a specialist herbivore

  • Special Topic: From Plants to Herbivores
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Abstract

The amount of damage that herbivorous insects impose on plants varies as a function of plant ontogenetic trajectories in tissue quality and defenses, and the herbivores’ own developmental trajectories in body size, mandible shape and detoxification enzymes, among others. However, little is known about how host plant and herbivore ontogeny interact. Using four ontogenetic stages of Plantago lanceolata (Plantaginaceae) and three to five larval stages of the specialist caterpillar Junonia coenia (Nymphalidae), we evaluated how ontogenies in both of these trophic levels shape: (i) caterpillar feeding choice, (ii) performance, and (iii) sequestration of plant allelochemicals. Plant physical (leaf toughness) and chemical (iridoid glycosides) defenses increased, while nutritional quality (water and nitrogen content) decreased, as plants aged. These plant ontogenetic trajectories strongly altered the behavior and physiology of this specialist herbivore, but the magnitude of the response varied with larval stage. In feeding experiments, while first instar larvae showed little preference among plant stages, older larvae significantly preferred juvenile over reproductive stages. In turn, larval consumption increased and digestive efficiency decreased, potentially explaining their decrease in relative growth rate, as larvae and host plant aged, but differences were greater for younger than older caterpillars. Finally, sequestration of plant allelochemicals increased through plant and larval development; however, the major differences due to diet occurred earlier during larval development. Our results highlight that changes in plant ontogeny most strongly influence early herbivore instars, emphasizing the need to consider the developmental stage of both trophic levels to better understand temporal variation in herbivore damage.

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References

  • Adler LS, Schmitt J, Bowers MD (1995) Genetic variation in defensive chemistry in Plantago lanceolata (Plantaginaceae) and its effect on the specialist herbivore Junonia coenia (Nymphalidae). Oecologia 101:75–85

    Article  PubMed  Google Scholar 

  • Barrett ELB, Hunt J, Moore AJ, Moore PJ (2009) Separate and combined effects of nutrition during juvenile and sexual development on female life-history trajectories: the thrifty phenotype in a cockroach. Proc R Soc B 276:3257–3264

    Article  PubMed  PubMed Central  Google Scholar 

  • Barton KE (2007) Early ontogenetic patterns in chemical defense in Plantago (Plantaginaceae): genetic variation and trade-offs. Am J Bot 94:56–66

    Article  PubMed  CAS  Google Scholar 

  • Barton BT (2010) Climate warming and predation risk during herbivore ontogeny. Ecology 91:2811–2818

    Article  PubMed  Google Scholar 

  • Barton KE, Koricheva J (2010) The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am Nat 175:481–493

    Article  PubMed  Google Scholar 

  • Beara IN, Lesjak MM, Orčić DZ, Simin NĐ, Četojević-Simin DD, Božin BN, Mimica-Dukić NM (2012) Comparative analysis of phenolic profile, antioxidant, anti-inflammatory and cytotoxic activity of two closely-related Plantain species: Plantago altissima L. and Plantago lanceolata L. LWT Food Sci Technol 47:64–70

    Article  CAS  Google Scholar 

  • Behmer ST (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54:165–187

    Article  PubMed  CAS  Google Scholar 

  • Bernays EA (1991) Evolution of insect morphology in relation to plants. Philos Trans R Soc B 333:257–264

    Article  Google Scholar 

  • Blüthgen N, Metzner A (2007) Contrasting leaf age preferences of specialist and generalist stick insects (Phasmida). Oikos 116:1853–1862

    Article  Google Scholar 

  • Boege K (2005) Herbivore attack in Casearia nitida influenced by plant ontogenetic variation in foliage quality and plant architecture. Oecologia 143:117–125

    Article  PubMed  Google Scholar 

  • Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. TREE 20:441–448

    PubMed  Google Scholar 

  • Bowers MD (1991) Iridoid glycosides. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites. Academic Press Inc., San Diego, pp 297–326

    Chapter  Google Scholar 

  • Bowers MD, Collinge SK (1992) Fate of iridoid glycosides in different life stages of the Buckeye, Junonia coenia (Lepidoptera, Nymphalidae). J Chem Ecol 18:817–831

    Article  PubMed  CAS  Google Scholar 

  • Bowers MD, Stamp NE (1993) Effects of plant-age, genotype, and herbivory on Plantago performance and chemistry. Ecology 74:1778–1791

    Article  Google Scholar 

  • Bowler K, Terblanche JS (2008) Insect thermal tolerance: what is the role of ontogeny, ageing and senescence? Biol Rev 83:339–355

    Article  PubMed  Google Scholar 

  • Brock JP, Kaufman K (2003) Butterflies of North America. Houghton Miffin Company, Massachusetts

    Google Scholar 

  • Bukovinszky T, Poelman EH, Gols R, Prekatsakis G, Vet LEM, Harvey JA, Dicke M (2009) Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism. Oecologia 160:299–308

    Article  PubMed  Google Scholar 

  • Camara MD (1997) Physiological mechanisms underlying the costs of chemical defence in Junonia coenia Hubner (Nymphalidae): a gravimetric and quantitative genetic analysis. Evol Ecol 11:451–469

    Article  Google Scholar 

  • Campos WG, Teixeira NC, Valim JOS, Guedes RNC, Oliveira MGA (2016) Bottom-up mechanisms generate the same temporal pattern of attack by a specialist and a generalist caterpillar on short-lived plants. Environ Entomol 2016:1–9

    Google Scholar 

  • Cavers PB, Bassett IJ, Crompton CW (1980) The biology of Canadian weeds. 47. Plantago lanceolata L. Can J Plant Sci 60:1269–1282

    Article  Google Scholar 

  • Chiang LC, Ng LT, Chiang W, Chang MY, Lin CC (2003) Immunomodulatory activities of flavonoids, monoterpenoids, triterpenoids, iridoid glycosides and phenolic compounds of plantago species. Planta Med 69:600–604

    Article  PubMed  CAS  Google Scholar 

  • Choong MF (1996) What makes a leaf tough and how this affects the pattern of Castanopsis fissa leaf consumption by caterpillars. Funct Ecol 10:668–674

    Article  Google Scholar 

  • Clarke AR, Zalucki MP (2000) Foraging and vein-cutting behaviour of Euploea core corinna (W. S. Macleay) (Lepidoptera: Nymphalidae) caterpillars feeding on latex-bearing leaves. Austr J Entomol 39:283–290

    Article  Google Scholar 

  • Clissold FJ, Sanson GD, Read J, Simpson SJ (2009) Gross vs. net income: how plant toughness affects performance of an insect herbivore. Ecology 90:3393–3405

    Article  PubMed  Google Scholar 

  • Costa JT (1993) Larval ontogeny and survivorship of eastern tent caterpillar colonies. J Res Lepidop 32:89–98

    Google Scholar 

  • de la Fuente MA (2002) Variation in plant antiherbivore defenses: causes and consequences. PhD dissertation, University of Colorado, Boulder

  • de la Fuente MA, Dyer LA, Bowers MD (1995) The iridoid glycoside, catalpol, as a deterrent to the predator Camponotus floridanus (Formicidae). Chemoecology 5:13–18

    Google Scholar 

  • Dmitriew C, Rowe L (2011) The effects of larval nutrition on reproductive performance in a food-limited adult environment. PLoS ONE 6(3):e17399. https://doi.org/10.1371/journal.pone.0017399

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dobler S, Petschenka G, Pankoke H (2011) Coping with toxic plant compounds—the insect’s perspective on iridoid glycosides and cardenolides. Phytochemistry 72:1593–1604

    Article  PubMed  CAS  Google Scholar 

  • Dyer LA, Bowers MD (1996) The importance of sequestered iridoid glycosides as a defense against an ant predator. J Chem Ecol 22:1527–1539

    Article  PubMed  CAS  Google Scholar 

  • Dyer LA, Floyd T (1993) Determinants of predation on phytophagous insects—the importance of diet breadth. Oecologia 96:575–582

    Article  PubMed  Google Scholar 

  • Fonseca CR, Fleck T, Fernandes GW (2006) Processes driving ontogenetic succession of galls in a canopy. Biotropica 38:514–521

    Article  Google Scholar 

  • Fuchs A, Bowers MD (2004) Patterns of iridoid glycoside production and induction in Plantago lanceolata and the importance of plant age. J Chem Ecol 30:1723–1741

    Article  PubMed  CAS  Google Scholar 

  • Gaston KJ, Reavey D, Valladares GR (1991) Changes in feeding habit as caterpillars grow. Ecol Entomol 16:339–344

    Article  Google Scholar 

  • Goodger JQD, Heskes AM, Woodrow IE (2013) Contrasting ontogenetic trajectories for phenolic and terpenoid defences in Eucalyptus froggattii. Ann Bot 112:651–659

    Article  PubMed  PubMed Central  Google Scholar 

  • Graves SD, Shapiro AM (2003) Exotics as host plants of the California butterfly fauna. Biol Conserv 110:413–433

    Article  Google Scholar 

  • Gripenberg S, Mayhew PJ, Parnell M, Roslin T (2010) A meta-analysis of preference–performance relationships in phytophagous insects. Ecol Letters 13:383–393

    Article  Google Scholar 

  • Hammer TJ, McMillan WO, Fierer N (2014) Metamorphosis of a butterfly-associated bacterial community. PLoS ONE 9:e86995

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hanley ME, Lamont BB, Fairbanks MM, Rafferty CM (2007) Plant structural traits and their role in anti-herbivore defence. PPEES 8:157–178

    Google Scholar 

  • Hanley ME, Girling RD, Felix AE, Olliff ED, Newland PL, Poppy GM (2013) Olfactory selection of Plantago lanceolata by snails declines with seedling age. Ann Bot 112:671–676

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hawkins BA, Cornell HV, Hochberg ME (1997) Predators, parasitoids, and pathogens as mortality agents in phytophagous insect populations. Ecology 78:2145–2152

    Article  Google Scholar 

  • Hochuli DF (1996) The ecology of plant/insect interactions: implications of digestive strategy for feeding by phytophagous insects. Oikos 75:133–141

    Article  Google Scholar 

  • Hochuli DF (2001) Insect herbivory and ontogeny: how do growth and development influence feeding behaviour, morphology and host use? Austral Ecol 26:563–570

    Article  Google Scholar 

  • Jamieson MA, Bowers MD (2010) Iridoid glycoside variation in the invasive plant Dalmatian Toadflax, Linaria dalmatica (Plantaginaceae), and sequestration by the biological control agent, Calophasia lunula. J Chem Ecol 36:70–79

    Article  PubMed  CAS  Google Scholar 

  • Johnson M-L, Zalucki MP (2005) Foraging behaviour of Helicoverpa armigera first instar larvae on crop plants of different developmental stages. J App Entomol 129:239–245

    Article  Google Scholar 

  • Johnson M-L, Zalucki MP (2007) Feeding and foraging behaviour of a generalist caterpillar: are third instars just bigger versions of firsts? Bull Entomol Res 97:81–88

    Article  PubMed  Google Scholar 

  • Johnston PR, Rolff J (2015) Host and symbiont jointly control gut microbiota during complete metamorphosis. PLoS Pathog 11:e1005246

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jones BC, Despland E (2006) Effects of synchronization with host plant phenology occur early in the larval development of a spring folivore. Can J Zool 84:628–633

    Article  Google Scholar 

  • Klockars GK, Bowers MD, Cooney B (1993) Leaf variation in iridoid glycoside content of Plantago lanceolata (Plantaginaceae) and oviposition of the buckeye, Junonia coenia (Nymphalidae). Chemoecology 4:72–78

    Article  CAS  Google Scholar 

  • Kos M, Broekgaarden C, Kabouw P, Lenferink KO, Poelman EH, Vet LEM, Dicke M, van Loon JJA (2011) Relative importance of plant-mediated bottom-up and top-down forces on herbivore abundance on Brassica oleracea. Funct Ecol 25:1113–1124

    Article  Google Scholar 

  • Lampert EC, Bowers MD (2015) Incompatibility between plant-derived defensive chemistry and immune response of two Sphingid herbivores. J Chem Ecol 41:85–92

    Article  PubMed  CAS  Google Scholar 

  • Langellotto GA, Denno RF (2004) Responses of invertebrate natural enemies to complex-structured habitats: a meta-analytical synthesis. Oecologia 139:1–10

    Article  PubMed  Google Scholar 

  • Laurentz M, Reudler JH, Mappes J, Friman V, Ikonen S, Lindstedt C (2012) Diet quality can play a critical role in defense efficacy against parasitoids and pathogens in the Glanville Fritillary (Melitaea cinxia). J Chem Ecol 38(1):116–125

    Article  PubMed  CAS  Google Scholar 

  • Llandres AL, Marques GM, Maino JL, Kooijman SALM, Kearney MR, Casas J (2015) A dynamic energy budget for the whole life-cycle of holometabolous insects. Ecol Monogr 85:353–371

    Article  Google Scholar 

  • Maino JL, Kearney MR (2015) Ontogenetic and interspecific scaling of consumption in insects. Oikos 124:1564–1570

    Article  Google Scholar 

  • Mattson WJ (1980) Herbivory in relation to plant nitrogen-content. Annu Rev Ecol Syst 11:119–161

    Article  Google Scholar 

  • McArthur C, Loney PE, Davies NW, Jordan GJ (2010) Early ontogenetic trajectories vary among defence chemicals in seedlings of a fast-growing eucalypt. Austral Ecol 35:157–166

    Article  Google Scholar 

  • Milla R, Reich PB, Niinemets U, Castro-Diez P (2008) Environmental and developmental controls on specific leaf area are little modified by leaf allometry. Funct Ecol 22:565–576

    Article  Google Scholar 

  • Mittapalli O, Neal JJ, Shukle RH (2007) Tissue and life stage specificity of glutathione S-transferase expression in the Hessian fly, Mayetiola destructor: implications for resistance to host allelochemicals. J Insect Sci 7:1–13

    Article  PubMed  Google Scholar 

  • Murphy SM, Stoepler TM, Grenis K, Lill JT (2014) Host ontogeny determines parasitoid use of a forest caterpillar. Entomol Exper Appl 150:217–225

    Article  Google Scholar 

  • Ochoa-Lopez S, Villamil N, Zedillo-Avelleyra P, Boege K (2015) Plant defence as a complex and changing phenotype throughout ontogeny. Ann Bot 116:797–806

    Article  PubMed  PubMed Central  Google Scholar 

  • Pankoke H, Buschmann T, Müller C (2013) Role of plant β-glucosidases in the dual defense system of iridoid glycosides and their hydrolyzing enzymes in Plantago lanceolata and Plantago major. Phytochemistry 94:99–107

    Article  PubMed  CAS  Google Scholar 

  • Pinault L, Thurston G, Quiring D (2009) Interaction of foliage and larval age influences preference and performance of a geometrid caterpillar. Can J Entomol 141:136–144

    Article  Google Scholar 

  • Prudic KL, Oliver JC, Bowers MD (2005) Soil nutrient effects on oviposition preference, larval performance, and chemical defense of a specialist insect herbivore. Oecologia 143:578–587

    Article  PubMed  Google Scholar 

  • Quintero C, Bowers MD (2011) Plant induced defenses depend more on plant age than previous history of damage: implications for plant-herbivore interactions. J Chem Ecol 37:992–1001

    Article  PubMed  CAS  Google Scholar 

  • Quintero C, Bowers MD (2012) Changes in plant chemical defenses and nutritional quality as a function of ontogeny in Plantago lanceolata (Plantaginaceae). Oecologia 168:471–481

    Article  PubMed  Google Scholar 

  • Quintero C, Barton KE, Boege K (2013) The ontogeny of plant indirect defenses. PPEES 15:245–254

    Google Scholar 

  • Quintero C, Lampert EC, Bowers MD (2014) Time is of the essence: direct and indirect effects of plant ontogenetic trajectories on higher trophic levels. Ecology 95:2589–2602

    Article  Google Scholar 

  • Rantala MJ, Roff DA (2005) An analysis of trade-offs in immune function, body size and development time in the Mediterranean field cricket, Gryllus bimaculatus. Fun Ecol 19:323–330

    Article  Google Scholar 

  • Raubenheimer D, Simpson SJ (1992) Analysis of covariance—an alternative to nutritional indexes. Entomol Exper Appl 62:221–231

    Article  Google Scholar 

  • Raubenheimer D, Simpson SJ (1999) Integrating nutrition: a geometrical approach. Entomol Exper Appl 91:67–82

    Article  Google Scholar 

  • Remmel T, Davison J, Tammaru T (2011) Quantifying predation on folivorous insect larvae: the perspective of life-history evolution. Biol J Linn Soc 104:1–18

    Article  Google Scholar 

  • Reudler JH, Lindstedt C, Pakkanen H, Lehtinen I, Mappes J (2015) Costs and benefits of plant allelochemicals in herbivore diet in a multi enemy world. Oecologia 179:1147–1158

    Article  PubMed  CAS  Google Scholar 

  • Richards LA, Lampert EC, Bowers MD, Dodson CD, Smilanich AM, Dyer LA (2012) Synergistic effects of iridoid glycosides on the survival, development and immune response of a specialist caterpillar, Junonia coenia (Nymphalidae). J Chem Ecol 38:1276–1284

    Article  PubMed  CAS  Google Scholar 

  • Ronsted N, Gobel E, Franzyk H, Jensen SR, Olsen CE (2000) Chemotaxonomy of Plantago. Iridoid glucosides and caffeoyl phenylethanoid glycosides. Phytochemistry 55:337–348

    Article  PubMed  CAS  Google Scholar 

  • Saastamoinen M, Hirai N, van Nouhuys S (2013) Direct and trans-generational responses to food deprivation during development in the Glanville fritillary butterfly. Oecologia 171:93–104

    Article  PubMed  CAS  Google Scholar 

  • Santana AFK, Zucoloto FS (2011) Influence of previous experience on the preference, food utilization and performance of Ascia monuste orseis wild larvae (Godart) (Lepidoptera: Pieridae) for three different hosts. Neo Entomol 40:631–638

    CAS  Google Scholar 

  • Schäpers A, Nylin S, Carlsson MA, Janz N (2015) Specialist and generalist oviposition strategies in butterflies: maternal care or precocious young? Oecologia 180:335–343

    Article  PubMed  Google Scholar 

  • Schippers P, Olff H (2000) Biomass partitioning, architecture and turnover of six herbaceous species from habitats with different nutrient supply. Plant Ecol 149:219–231

    Article  Google Scholar 

  • Schwartzberg EG, Jamieson MA, Raffa KF, Reich PB, Montgomery RA, Lindroth RL (2014) Simulated climate warming alters phenological synchrony between an outbreak insect herbivore and host trees. Oecologia 175:1041–1049

    Article  PubMed  Google Scholar 

  • Scriber JM, Slansky F (1981) The nutritional ecology of immature insects. Ann Rev Entomol 26:183–211

    Article  Google Scholar 

  • Shefferson RP, Roach DA (2010) Longitudinal analysis of Plantago: adaptive benefits of iteroparity in a short-lived, herbaceous perennial. Ecology 91:441–447

    Article  PubMed  PubMed Central  Google Scholar 

  • Smilanich AM, Dyer LA, Chambers JQ, Bowers MD (2009) Immunological cost of chemical defence and the evolution of herbivore diet breadth. Ecol Lett 12:612–621

    Article  PubMed  Google Scholar 

  • Stamp NE (2001) Effects of prey quantity and quality on predatory wasps. Ecol Entomol 26:292–301

    Article  Google Scholar 

  • Stockoff BA (1993) Ontogenetic change in dietary selection for protein and lipid by gypsy-moth larvae. J Insect Physiol 39:677–686

    Article  Google Scholar 

  • Strohmeyer HH, Stamp NE, Jarzomski CM, Bowers MD (1998) Prey species and prey diet affect growth of invertebrate predators. Ecol Entomol 23:68–79

    Article  Google Scholar 

  • Sutter R, Müller C (2011) Mining for treatment-specific and general changes in target compounds and metabolic fingerprints in response to herbivory and phytohormones in Plantago lanceolata. New Phytol 191:1069–1082

    Article  PubMed  CAS  Google Scholar 

  • Taborsky B (2006) The influence of juvenile and adult environments on life-history trajectories. Proc R Soc B 273:741–750

    Article  PubMed  Google Scholar 

  • Thaler JS, Griffin CAM (2008) Relative importance of consumptive and non-consumptive effects of predators on prey and plant damage: the influence of herbivore ontogeny. Entomol Exper Appl 128:34–40

    Article  Google Scholar 

  • Thaler JS, McArt SH, Kaplan I (2012) Compensatory mechanisms for ameliorating the fundamental trade-off between predator avoidance and foraging. PNAS 109:12075–12080

    Article  PubMed  PubMed Central  Google Scholar 

  • Theodoratus DH, Bowers MD (1999) Effects of sequestered iridoid glycosides on prey choice of the prairie wolf spider, Lycosa carolinensis. J Chem Ecol 25:283–295

    Article  CAS  Google Scholar 

  • Travers-Martin N, Müller C (2008) Matching plant defence syndromes with performance and preference of a specialist herbivore. Funct Ecol 22:1033–1043

    Article  Google Scholar 

  • Van Bael SA, Brawn JD, Robinson SK (2003) Birds defend trees from herbivores in a Neotropical forest canopy. PNAS 100:8304–8307

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van Dam NM, Hermenau U, Baldwin IT (2001) Instar-specific sensitivity of specialist Manduca sexta larvae to induced defences in their host plant Nicotiana attenuata. Ecol Entomol 26:578–586

    Article  Google Scholar 

  • Waldbauer GP (1968) The consumption and utilization of food by insects. Adv Insect Physiol 5:229–289

    Article  Google Scholar 

  • Woods HA (2013) Ontogenetic changes in the body temperature of an insect herbivore. Funct Ecol 27:1322–1331

    Article  Google Scholar 

  • Yang LH, Rudolf VHW (2010) Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecol Lett 13:1–10

    Article  PubMed  CAS  Google Scholar 

  • Zalucki MP, Clarke AR, Malcolm SB (2002) Ecology and behavior of first instar larval Lepidoptera. Annu Rev Entomol 47:361–393

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank C. Müller and two anonymous reviewers for valuable comments and suggestions that improved the quality of the manuscript. In addition, we gratefully acknowledge E. Lynch, S. McNamara, A. Gonzalez, L. Mulder, M. P. Belazis, and A. Russell for greenhouse and laboratory assistance. Funding for this project was provided by the Department of Ecology and Evolutionary Biology and the Undergraduate Research Opportunity Program, at the University of Colorado, and National Science Foundation grants DEB 0614883 and 0909717. CQ is a member of the Carrera del Investigador Científico of the National Research Council of Argentina (CONICET).

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  1. Laboratorio Ecotono, INIBIOMA, CONICET-Universidad Nacional del Comahue, Quintral 1250, Bariloche, Argentina

    Carolina Quintero

  2. Department of Ecology and Evolutionary Biology and University of Colorado Museum, University of Colorado, Campus Box 334, Boulder, CO, 80309-0260, USA

    Carolina Quintero & M. Deane Bowers

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  1. Carolina Quintero
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CQ and MDB conceived and designed the experiments. CQ performed the experiments, analyzed the data, and wrote the manuscript; MDB provided editorial advice.

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Correspondence to Carolina Quintero.

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Communicated by Caroline Müller.

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Quintero, C., Bowers, M.D. Plant and herbivore ontogeny interact to shape the preference, performance and chemical defense of a specialist herbivore. Oecologia 187, 401–412 (2018). https://doi.org/10.1007/s00442-018-4068-8

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