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Induced plant responses to multiple damagers: differential effects on an herbivore and its parasitoid

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Abstract

Herbivore-induced plants responses can affect the preference and performance of herbivores and their natural enemies. These responses may vary depending on the identity and number of herbivore species feeding on the plant so that when herbivores from different guilds feed on plants, the interactions between plants, herbivores, and natural enemies may be disrupted. Tomato plants were damaged either by the caterpillar Spodoptera exigua, or the aphid Macrosiphum euphorbiae, or damaged by both herbivores, or undamaged controls. We measured the preference and performance of S. exigua and its parasitoid Cotesia marginiventris, and activity of proteinase inhibitors (PI) as an indicator of induced resistance. Compared to undamaged plants, caterpillar damage reduced the number of eggs laid by S. exigua adults, reduced growth, consumption, and survival of larval S. exigua and C. marginiventris, and increased activity of PIs 43%; but did not increase attraction of C. marginiventris. While pupal mass of S. exigua was not affected, the pupal mass of C. marginiventris decreased on caterpillar-damaged plants compared to controls. In contrast, plants damaged by aphids were preferred for oviposition by S. exigua, and had increased larval consumption and survival, compared to controls. Aphid feeding did not affect the preference or performance of C. marginiventris, or PI activity, compared to controls. While oviposition was deterred on caterpillar-damaged plants, plants damaged by both herbivores received the same amount of oviposition as controls. The attraction of C. marginiventris to plants damaged by caterpillars and aphids was increased compared to controls. However, plants damaged by both herbivores had similar PI activity, larval growth and survival of S. exigua and C. marginiventris, as plants singly damaged by caterpillars. Overall, the preference component for both the herbivore and parasitoid was more strongly affected by damage due to multiple herbivores than the performance component.

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References

  • Barbosa P, Gross P, Kemper J (1991) Influence of plant allelochemicals on the tobacco hornworm and its parasitoid Cotesia congregata. Ecology 72:1567–1575

    Article  CAS  Google Scholar 

  • Benrey B, Denno R (1997) The slow-growth-high-mortality hypothesis: a test using the cabbage butterfly. Ecology 78:987–999

    Google Scholar 

  • Bernays EA, Chapman RF (1994) Host-plant selection by phytophagous insects. Chapman and Hall, New York

    Google Scholar 

  • Bernays E, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892

    Article  Google Scholar 

  • Boland W, Hopke J, Piel J (1998) Induction of plant volatile biosynthesis by jasmonates. In: Schreier P, Herderich M, Humpf H, Schwab W (eds) Natural product analysis: chromatography, spectroscopy, biological testing. Vieweg, Germany, pp 255–269

    Google Scholar 

  • Cardoza YJ, Alborn HT, Tumlinson JH (2002) In vivo volatile emissions from peanut plants induced by simultaneous fungal infection and insect damage. J Chem Ecol 28:161–174

    Article  PubMed  CAS  Google Scholar 

  • Cardoza YJ, Lait CG, Schmelz EA, Huang J, Tumlinson JH (2003a) Fungus-induced biochemical changes in peanut plants and their effect on development of beet armyworm, Spodoptera exigua Hübner (Lepidoptera: Noctuidae) larvae. Environ Entomol 32:220–228

    CAS  Google Scholar 

  • Cardoza YJ, Teal PEA, Tumlinson JH (2003b) Effect of peanut plant fungal infection on oviposition preference by Spodoptera exigua and on host-searching behavior by Cotesia marginiventris. Environ Entomol 32:970–976

    Article  Google Scholar 

  • De Moraes CM, Mescher MC, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580

    Article  PubMed  CAS  Google Scholar 

  • Dicke M (2000) Chemical ecology of host-plant selection by herbivorous arthropods: a multitrophic perspective. Biochem Syst Ecol 28:601–617

    Article  PubMed  CAS  Google Scholar 

  • Doares SH, Narváez-Vásquez J, Conconi A, Ryan CA (1995) Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol 108:1741–1746

    PubMed  CAS  Google Scholar 

  • Farmer EE, Ryan CA (1990) Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Nat Acad Sci USA 87:7713–7716

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Fidantsef AL, Stout MJ, Thaler JS, Duffey SS, Bostock RM (1999) Signal interactions in pathogen and insect attack: expression of lipoxygenase, proteinase inhibitor II, and pathogenesis-related protein P4 in the tomato, Lycopersicon esculentum. Physiol Mol Plant Pathol 54:97–114

    Article  CAS  Google Scholar 

  • Fordyce JA, Shapiro AM (2003) Another perspective on the slow-growth/high mortality hypothesis: chilling effects on swallowtail larvae. Ecology 84:263–268

    Article  Google Scholar 

  • Godfray HCJ (1994) Parasitoids—behavioral and evolutionary ecology. Princeton University Press, New Jersey

    Google Scholar 

  • Gols R, Posthumus MA, Dicke M (1999) Jasmonic acid induces the production of gerbera volatiles that attract the biological control agent Phytoseiulus persimilis. Entomol Exp Appl 93:77–86

    Article  CAS  Google Scholar 

  • Guerrieri E, Poppy GM, Powell W, Tremblay E, Pennacchio F (1999) Induction and systemic release of herbivore-induced plant volatiles mediating in-flight orientation of Aphidius ervi. J Chem Ecol 25:1247–1261

    Article  CAS  Google Scholar 

  • Hare JD (2002) Plant genetic variation in tritrophic interactions. In: Tscharntke T, Hawkins BA (eds) Multitrophic level interactions. Cambridge University Press, Cambridge, pp 8–43

    Google Scholar 

  • Havill NP, Raffa KF (2000) Compound effects of induced plant responses on insect herbivores and parasitoids: implications for tritrophic interactions. Ecol Entomol 25:171–179

    Article  Google Scholar 

  • Heil M (2004) Induction of two indirect defences benefits Lima bean (Phaseoulus lunatus, Fabaceae) in nature. J Ecol 92:527–536

    Article  Google Scholar 

  • Inbar M, Doostdar H, Leibee GL, Mayer RT (1999) The role of plant rapidly induced responses in asymmetric interspecific interactions among insect herbivores. J Chem Ecol 25:1961–1979

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144

    Article  PubMed  CAS  Google Scholar 

  • Kuussaari M, Singer M, Hanski I (2000) Local specialization and landscape-level influence on host use in an herbivorous insect. Ecology 81:2177–2187

    Article  Google Scholar 

  • Landolt PJ (1993) Effects of host plant leaf damage on cabbage looper moth attraction and oviposition. Entomol Exp Appl 67:79–85

    Article  Google Scholar 

  • Lill JT, Marquis RJ, Ricklefs RE (2002) Host plants influence parasitism of forest caterpillars. Nature 417:170–173

    Article  PubMed  CAS  Google Scholar 

  • Niki T, Mitsuhara I, Seo S, Ohtsubo N, Ohashi Y (1998) Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol 39:500–507

    CAS  Google Scholar 

  • Ohsaki N, Sato Y (1994) Food plant choice of Pieris butterflies as a trade-off between parasitoid avoidance and quality of plants. Ecology 75:59–68

    Article  Google Scholar 

  • Orians CM, Pomerleau J, Ricco R (2000) Vascular architecture generates fine scale variation in systemic induction of proteinase inhibitors in tomato. J Chem Ecol 26:471–485

    Article  CAS  Google Scholar 

  • Paul ND, Hatcher PE, Taylor JE (2000) Coping with multiple enemies: an integration of molecular and ecological perspectives. Trends Plant Sci 5:220–225

    Article  PubMed  CAS  Google Scholar 

  • Peña-Cortés H, Albrecht T, Prat S, Weiler EW, Willmitzer L (1993) Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191:123–128

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65

    Article  Google Scholar 

  • Rodriguez-Saona C, Crafts-Brandner SJ, Paré PW, Henneberry TJ (2001) Exogenous methyl jasmonate induces volatile emissions in cotton plants. J Chem Ecol 27:679–695

    Article  PubMed  CAS  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 29:2521–2532

    Article  Google Scholar 

  • Sato Y, Yano S, Takabayashi J, Ohsaki N (1999) Pieris rapae (Lepidoptera: Pieridae) females avoid oviposition on Rorippa indica plants infested by conspecific larvae. Appl Entomol Zool 34:333–337

    Google Scholar 

  • Shiojiri K, Takabayashi J, Yano S, Takafuji A (2001) Infochemically mediated tritrophic interaction webs on cabbage plants. Popul Ecol 43:23–29

    Article  Google Scholar 

  • Shiojiri K, Takabayashi J, Yano S, Takafuji A (2002) Oviposition preferences of herbivores are affected by tritrophic interaction webs. Ecol Lett 5:186–192

    Article  Google Scholar 

  • Stout MJ, Duffey SS (1996) Characteristics of induced resistance in tomato plants. Entamol Exp Appl 79:273–283

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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). Entamol Exp Appl 86:267–279

    Article  CAS  Google Scholar 

  • Strauss SY (1991) Direct, indirect, and cumulative effects of three native herbivores on a shared host plant. Ecology 72:543–558

    Article  Google Scholar 

  • Thaler JS (1999) Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399:686–688

    Article  CAS  Google Scholar 

  • Thaler JS (2002) Effect of jasmonate-induced plant responses on the natural enemies of herbivores. J Anim Ecol 71:141–150

    Article  Google Scholar 

  • Thaler JS, Fidantsef AL, Duffey SS, Bostock 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

    Article  CAS  Google Scholar 

  • Thaler JS, Karban R, Ullman DE, Boege K, Bostock RM (2002a) Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites. Oecologia 131:227–235

    Article  Google Scholar 

  • Thaler JS, Farag MA, Paré PW, Dicke M (2002b) Jasmonate-deficient plants have reduced direct and indirect defences against herbivores. Ecol Lett 5:764–774

    Article  Google Scholar 

  • Thompson JN (1998) Coping with multiple enemies: 10 years of attack on Lomatium dissectum plants. Ecology 79:2550–2554

    Google Scholar 

  • Thompson JN, Pellmyr O (1991) Evolution of oviposition behavior and host preference in Lepidoptera. Annu Rev Entomol 36:65–89

    Article  Google Scholar 

  • Turlings TCJ, Tumlinson JH, Eller FJ, Lewis WJ (1991) Larval-damaged plants: source of volatile synomones that guide the parasitoid Cotesia marginiventris to the micro-habitat of its hosts. Entomol Exp Appl 58:75–82

    Article  Google Scholar 

  • Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172

    Article  Google Scholar 

  • Vos M, Moreno Berrocal S, Karamaouna F, Hemerik L, Vet LEM (2001) Plant-mediated indirect effects and the persistence of parasitoid-herbivore communities. Ecol Lett 4:38–45

    Article  Google Scholar 

  • Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216

    PubMed  CAS  Google Scholar 

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Acknowledgements

Thanks to John Ruberson (University of Georgia) and Gay McCain (USDA-ARS Biological Control and Mass Rearing Unit, MS, USA) for providing us with C. marginiventris, Lisa Plane for assistance in maintaining the colonies and conducting experiments, and Chris Darling for his assistance in measuring tibial lengths of C. marginiventris. The manuscript was improved by comments by A. Agrawal, M. Vos, P. Barbosa, C. Muis, D. Viswanathan, N. Kurashige, M. Lajeunesse, and M. Johnson. This research was funded by a Premier’s Research Excellence Award and a NSERC Discovery Grant to J. Thaler.

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Correspondence to Cesar Rodriguez-Saona.

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Communicated by Richard Lindroth

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Rodriguez-Saona, C., Chalmers, J.A., Raj, S. et al. Induced plant responses to multiple damagers: differential effects on an herbivore and its parasitoid. Oecologia 143, 566–577 (2005). https://doi.org/10.1007/s00442-005-0006-7

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