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Caterpillar Labial Saliva Alters Tomato Plant Gene Expression

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Abstract

We examined the effects of Helicoverpa zea caterpillar labial saliva on tomato plant gene expression. Caterpillars with labial salivary glands (mock-ablated) and without (ablated) were fed on tomato plants for 24 hr; then, the leaf mRNA was analyzed with tomato microarrays. Analysis of the transcript profiles revealed 384 expressed sequence tags (ESTs) that were significantly altered due to herbivory compared to the non-wounded plants. The majority of the ESTs were quantitatively altered more so by mock-ablated caterpillars with labial salivary glands than ablated caterpillars. Particularly notable, ESTs encoding acid phosphatase, arginase, acidic endochitinase, dehydrin, polyphenol oxidase, protease inhibitors, and threonine deaminase were more highly stimulated by mock-ablated caterpillars than ablated caterpillars. In addition, tomato leaves were mechanically wounded with scissors and painted with labial salivary gland extract, autoclaved salivary gland extract, or water, and compared to non-wounded tomato plants. After 4 hr, these leaves were collected and a tomato microarray analysis of the mRNA revealed correlation of the gene expression of these leaves altered by mechanical wounding and painted with salivary gland extract to the gene expression of leaves fed on by mock-ablated caterpillars. We show that caterpillar labial saliva is an important component of herbivory that can alter plant gene expression.

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References

  • Adams, D. O. and Yang, S. F. 1979. Ethylene biosynthesis: Identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. Proc. Natl. Acad. Sci. USA 76:170–174.

    Article  PubMed  CAS  Google Scholar 

  • Alba, R., Fei, Z., Payton, P., Liu, Y., Moore, S. L., Debbie, P., Cohn, J., D’Ascenzo, M., Gordon, J. S., Rose, J. K., Martin, G., Tanksley, S. D., Bouzayen, M., Jahn, M. M., and Giovannoni, J. 2004. ESTs, cDNA microarrays, and gene expression profiling: tools for dissecting plant physiology and development. Plant J. 39:697–714.

    Article  PubMed  CAS  Google Scholar 

  • Alborn, H. T., Turlings, T. C. J., Jones, T. H., Stenhagen, G., Loughrin, J. H., and Tumlinson, J. H. 1997. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949.

    Article  CAS  Google Scholar 

  • Alborn, H. T., Jones, T. H., Stenhagen, G. S., and Tumlinson, J. H. 2000. Identification and synthesis of volicitin and related components from beet armyworm oral secretions. J. Chem. Ecol. 26:203–220.

    Article  CAS  Google Scholar 

  • Babic, B., Poisson, A., Darwish, S., Lacasse, J., Merkx-Jacques, M., Despland, E., and Bede, J. C. 2008. Influence of dietary nutritional composition on caterpillar salivary enzyme activity. J. Insect Physiol. 54:286–296.

    Article  PubMed  CAS  Google Scholar 

  • Bae, E.-K., Lee, H., Lee, J.-S., and Noh, E.-W. 2009. Differential expression of a poplar SK2-type dehydrin gene in response to various stresses. Biochem. Mol. Biol. Rep. 42:439–443.

    CAS  Google Scholar 

  • Bede, J. C., Musser, R. O., Felton, G. W., and Korth, K. L. 2006. Caterpillar herbivory and salivary enzymes decrease transcript levels of Medicago truncatula genes encoding early enzyme in terpenoid biosynthesis. Plant Mol. Biol. 60:519–531.

    Article  PubMed  CAS  Google Scholar 

  • Benjamini, Y. and Hochberg, Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. 57:289–300.

    Google Scholar 

  • Borovskii, G. B., Stupnikova, I. V., Antipina, A. I., Vladimirova, S. V., and Voinikov, V. K. 2002. Accumulation of dehydrin-like proteins in the mitochondria of cereals in response to cold, freezing, drought and ABA treatment. BMC Plant Biol. 2:5.

    Article  PubMed  Google Scholar 

  • Bradford, M. M. 1976. A dye binding assay for protein. Anal. Biochem. 72:248–254.

    Article  PubMed  CAS  Google Scholar 

  • Broadway, R. M. and Duffey, S. S. 1986. The effect of dietary protein on the growth and digestive physiology of larval Heliothis zea and Spodoptera exigua. J. Insect Physiol. 32:673–680.

    Article  CAS  Google Scholar 

  • Celorio-Mancera, M. D. L. P., Courtiade, J., Muck, A., Heckel, D. G., Musser, R. O., and Vogel, H. 2011. Sialome of a generalist lepidopteran herbivore: identification of transcripts and proteins from helicoverpa armigera labial salivary glands. PLoS One 6:e26676.

    Article  Google Scholar 

  • Chen, H., Wilkerson, C. G., Kuchar, J. A., Phinney, B. S., and Howe, G. A. 2005. Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Plant Biol. 102:19237–19242.

    CAS  Google Scholar 

  • Chippendale, G. M. 1970. Metamorphic changes in fat body proteins of the southwestern corn borer Diatraea grandiosella. J. Insect Physiol. 16:1057–1068.

    Article  PubMed  CAS  Google Scholar 

  • Constabel, P., Bergey, D., and Ryan, C. 1995. Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc. Natl. Acad. Sci. USA 92:407–411.

    Article  PubMed  CAS  Google Scholar 

  • Darwish, S. A., Pan, L., Ide, C., and Bede, J. C. 2008. Caterpillar-specific gene expression in the legume, Medicago truncatula. Plant Mol. Biol. Rep. 26:12–31.

    Article  CAS  Google Scholar 

  • Delphia, C. M., Mescher, M. C., Felton, G. W., and de Moraes, C. M. 2006. The role of insect-derived cues in eliciting indirect plant defenses in tobacco, Nicotiana tabacum. Plant Signal. Behav. 1:243–250.

    Article  PubMed  Google Scholar 

  • de Vos, M., van Osten, V. R., van Poecke, R. M., van Pelt, J. A., Pozo, M. J., Mueller, M. J., Buchala, A. J., Métraux, J. P., van Loon, L. C., Dicke, M., and Pieterse, C. M. 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant Microbe Interact. 18:923–937.

    Article  PubMed  Google Scholar 

  • de Vos, M., van Zaanen, W., Koornneef, A., Korzelius, J. P., Dicke, M., van Loon, L. C., and Pieterse, C. M. J. 2006. Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiol. 142:352–363.

    Article  PubMed  Google Scholar 

  • Diezel, C., von Dahl, C., Gaquerel, E., and Baldwin, I. T. 2009. Different Lepidopteran elicitors account for crosstalk in herbivory-induced phytohormone sgnaling. Plant Physiol. 150:1576–1586.

    Article  PubMed  CAS  Google Scholar 

  • Eichenseer, H., Mathews, M. C., Jian, L. B., Murphy, J. B., and Felton, G. W. 1999. Salivary glucose oxidase: multifunctional roles for Helicoverpa zea? Arch. Insect Biochem. Physiol. 42:99–109.

    Article  PubMed  CAS  Google Scholar 

  • Eichenseer, H., Mathews, M. C., Powell, J. S., and Felton, G. W. 2010. Survey of a salivary effector in caterpillars: glucose oxidase variation and correlation with host range. J. Chem. Ecol. 36:885–897.

    Article  PubMed  CAS  Google Scholar 

  • Felton, G. W. 2005. Indigestion is a plant’s best defense. Proc. Natl. Acad. Sci. USA 102:18771–18772.

    Article  PubMed  CAS  Google Scholar 

  • Felton, G. W. and Eichenseer, H. 1999. Herbivore saliva and its effect on plant defense against herbivores and pathogens, pp. 390, in A. A. Agrawal, S. Tuzun, and E. Bent (eds.), Induced plant defenses against pathogens and herbivores. APS Press, St. Paul.

    Google Scholar 

  • Gao, W. R., Wang, X. S., Liu, Q. Y., Peng, H., Chen, C., Li, J. G., Zhang, J. S., Hub, S. N., and Maa, H. 2008. Comparative analysis of ESTs in response to drought stress in chickpea (C. arietinum L.). Biochem. Biophys. Res. Commun. 376:578–583.

    Article  PubMed  CAS  Google Scholar 

  • Glazebrook, J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205–227.

    Article  PubMed  CAS  Google Scholar 

  • Gomez, S. K., Cox, M. M., Bede, J. C., Inoue, K., Alborn, H. T., Tumlinson, J. H., and Korth, K. L. 2005. Lepidopteran herbivory and oral factors induce transcripts encoding novel terpene synthases in Medicago truncatula. Arch. Insect Biochem. Physiol. 58:114–127.

    Article  PubMed  CAS  Google Scholar 

  • Graham, J., Pearce, G., Merryweather, J., Koiti, T., Ericsson, L., and Ryan, C. 1985. Wound-induced proteinase inhibitors from tomato leaves. J. Biol. Chem. 260:6555–6560.

    PubMed  CAS  Google Scholar 

  • Green, T. R. and Ryan, C. A. 1972. Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776–777.

    Article  PubMed  CAS  Google Scholar 

  • Heiden, A. C., Hoffmann, T., Kahl, J., Klockow, D., Langebartels, C., Mehlhorn, H., Sandermann Jr., H., Schraudner, M., Schuh, G., and Wildt, J. 1999. Emission of volatile organic compounds from ozone-exposed plants. Ecol. Appl. 9:1160–1167.

    Article  Google Scholar 

  • Hermsmeier, D., Schittko, U., and Baldwin, I. T. 2001. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth- and defense-related plant mRNAs. Plant Physiol. 125:683–700.

    Article  PubMed  CAS  Google Scholar 

  • Howe, G. A. and Jander, G. 2008. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59:41–66.

    Article  PubMed  CAS  Google Scholar 

  • Koornneef, A. and Pieterse, C. M. J. 2008. Cross talk in defense signaling. Plant Physiol. 146:839–844.

    Article  PubMed  CAS  Google Scholar 

  • Korth, K. L. 2003. Profiling plant responses to herbivorous insects. Genome Biol. 4(7):221.1–221.4.

    Article  Google Scholar 

  • Korth, K. L. and Thompson, G. A. 2006. Chemical signals in plants: jasmonates and the role of insect-derived elicitors in responses to herbivores, pp. 259–278, in S. Tuzun and E. Bent (eds.), Multigenic and induced systemic resistance in plants. Springer Publishing, New York.

    Chapter  Google Scholar 

  • Lawrence, S. D., Novak, N. G., Ju, C. J.-T., and Cooke, J. E. K. 2008. Potato, Solanum tuberosum, defense against Colorado Potato Beetle, Leptinotarsa decemlineata (Say): microarray gene expression profiling of potato by Colorado Potato Beetle regurgitant treatment of wounded leaves. J. Chem. Ecol. 34:1013–1025.

    Article  PubMed  CAS  Google Scholar 

  • Lawrence, S. D. and Novak, N. G. 2004. Maize genes induced by herbivory and volicitin. J. Chem. Ecol. 30:2543–2557.

    Article  PubMed  CAS  Google Scholar 

  • Leon, J., Lawton, M. A., and Raskin, I. 1995. Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol. 108:1673–1678.

    PubMed  CAS  Google Scholar 

  • Leon-Reyes, A., Spoel, S. H., de Lange, E. S., Abe, H., Kobayashi, M., Tsuda, S., Millenaar, F. F., Welschen, R. A. M., Ritsema, T., and Pieterse, C. M. J. 2009. Ethylene modulates the role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 in cross talk between salicylate and jasmonate signaling. Plant Physiol. 149:1797–1809.

    Article  PubMed  CAS  Google Scholar 

  • Lou, Y. and Baldwin, I. T. 2003. Manduca sexta recognition and resistance among allopolyploid Nicotiana host plants. Proc. Natl. Acad. Sci. 100:14581–14586.

    Article  PubMed  CAS  Google Scholar 

  • Liu, Y., Hoffman, N. E., and Yang, S. F. 1985. Promotion by ethylene of the capability to convert 1-aminocyclopropane-1-carboxylic acid to ethylene in preclimacteric tomato and cantelope fruits. Plant Physiol. 77:407–411.

    Article  PubMed  CAS  Google Scholar 

  • Maffei, M. E., Mithöfer, A., and Boland, W. 2007a. Insects feeding on plants: Rapid signals and responses precede the induction of phytochemical release. Phytochemistry 68:2946–2959.

    Article  PubMed  CAS  Google Scholar 

  • Maffei, M. E., Mithöfe, R. A., and Boland, W. 2007b. Before gene expression: early events in plant herbivore interactions. Trends Plant Sci. 12:310–316.

    Article  PubMed  CAS  Google Scholar 

  • Mattiacci, L., Dicke, M., and Posthumus, M. A. 1995. β-glucosidase: an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proc. Natl. Acad. Sci. USA 92:2036–2040.

    Article  PubMed  CAS  Google Scholar 

  • Mithöfer, A. and Boland, W. 2008. Recognition of herbivory-associated molecular patterns. Plant Physiol. 146:825–831.

    Article  PubMed  Google Scholar 

  • Mithöfer, A., Wanner, G., and Boland, W. 2005. Effects of feeding Spodoptera littoralis on Lima Bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol. 137:1160–1168.

    Article  PubMed  Google Scholar 

  • Musser, R. O., Hum-Musser, S. M., Eichenseer, H., Peiffer, M., Ervin, G., Murphy, J. B., and Felton, G. W. 2002a. Caterpillar saliva beats plant defences: a new weapon emerges in the evolutionary arms race between plants and herbivores. Nature 416:599–600.

    Article  PubMed  CAS  Google Scholar 

  • Musser, R. O., Hum-Musser, S. M., Slaten-Bickford, S. E., Felton, G. W., and Gergerich, R. C. 2002b. Evidence that ribonuclease activity present in beetle regurgitant is found to stimulate virus resistance in plants. J. Chem. Ecol. 28:1691–1696.

    Article  PubMed  CAS  Google Scholar 

  • Musser, R. O., Cipollini, D. F., Hum-Musser, S. M., Williams, S. A., Brown, J. K., and Felton, G. W. 2005a. Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in Solanaceous plants. Arch. Insect Biochem. Physiol. 58:128–137.

    Article  PubMed  CAS  Google Scholar 

  • Musser, R. O., Kwon, H. S., Willams, S. A., White, C. J., Romano, M., Bradbury, S., Brown, J. K., and Felton, G. W. 2005b. Evidence that caterpillar labial saliva suppresses pathogencity of potential bacterial pathogens. Arch. Insect Biochem. Physiol. 58:138–144.

    Article  PubMed  CAS  Google Scholar 

  • Musser, R. O., Farmer, E. E., Peiffer, M., Williams, S. A., and Felton, G. W. 2006. Ablation of caterpillar labial salivary glands: technique for determining the role of saliva in insect–plant interactions. J. Chem. Ecol. 32:981–992.

    Article  PubMed  CAS  Google Scholar 

  • O’Donnell, P., Calvert, C., Atzorn, R., Wasternack, C., Leyser, H. M. O., and Bowles, D. J. 1996. Ethylene as a signal mediating the wound response of tomato plants. Science 274(5294):1914–1917.

    Article  PubMed  Google Scholar 

  • Orozco-Cárdenas, M. L., Narváez-Vásquez, J., and Ryan, C. A. 2001. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, methyl jasmonate. Plant Cell 13:179–191.

    PubMed  Google Scholar 

  • Peiffer, M. and Felton, G. W. 2005. The host plant as a factor in the synthesis and secretion of salivary glucose oxidase in the larval Helicoverpa zea. Arch. Insect Biochem. Physiol. 58:106–113.

    Article  PubMed  CAS  Google Scholar 

  • Ralph, S., Oddy, C., Cooper, D., Yueh, H., Jancsik, S., Kolosova, N., Philippe, R. N., Aeschliman, D., White, R., Huber, D., Ritland, C. E., Benoit, F., Rigby, T., Nantel, A., Butterfield, Y. S. N., Kirkpatrick, R., Chun, E., Liu, J., Palmquist, D., Wynhoven, B., Stott, J., Yang, G., Barber, S., Holt, R. A., Siddiqui, A., Jones, S. J. M., Marra, M. A., Ellis, B. E., Douglas, C. J., Ritland, K., and Bohlmann, J. 2006a. Genomics of hybrid poplar (Populus trichocarpa x deltoides) interacting with forest tent caterpillars (Malacosoma disstria): normalized and full-length cDNA libraries, expressed sequence tags, and a cDNA microarray for the study of insect-induced defences in poplar. Mol. Ecol. 15:1275–1297.

    Article  PubMed  Google Scholar 

  • Ralph, S., Yueh, H., Friedmann, M., Aeschliman, D., Zeznik, J. A., Nelson, C. C., Butterfield, Y. S. N., Kirkpatrick, R., Liu, J., Jones, S. J. M., Marra, M. A., Douglas, C. J., Ritland, K., and Bohlmann, J. 2006b. Conifer defence against insects: microarray gene expression profiling of Sitka spruce (Picea sitchensis) induced by mechanical wounding or feeding by spruce budworms (Choristoneura occidentalis) or white pine weevils (Pissodes strobi) reveals large-scale changes of the host transcriptome. Plant Cell Environ. 29:1545–1570.

    Article  PubMed  Google Scholar 

  • Reymond, P., Bodenhausen, N., van Poecke, R., Krishnamurthy, V., Dicke, M., and Farmer, E. E. 2004. A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16:3132–3147.

    Article  PubMed  CAS  Google Scholar 

  • Reymond, P., Weber, H., Damond, M., and Farmer, E. E. 2000. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707–719.

    PubMed  CAS  Google Scholar 

  • Richard, S., Morency, M.-J., Drevet, C., Jouanin, L., and Seguin, A. 2000. Isolation and characterization of a dehydrin gene from white spruce induced upon wounding, drought and cold stresses. Plant Mol. Biol. 43:1–10.

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Saona, C. R., Musser, R. O., Vogel, H., Hum-Musser, S. M., and Thaler, J. S. 2010. Molecular, biochemical, and organismal analyses of tomato plants simultaneously attacked by herbivores from two feeding guilds. J. Chem. Ecol. 36:1043–1057.

    Article  PubMed  CAS  Google Scholar 

  • Skibbe, M., Qu, N., Galis, I., and Baldwin, I. T. 2008. Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 20:1984–2000.

    Article  PubMed  CAS  Google Scholar 

  • Schittko, U., Hermsmeier, D., and Baldwin, I. T. 2001. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. II. Accumulation of plant mRNA in response to insect-derived cues. Plant Physiol. 125:701–710.

    Article  PubMed  CAS  Google Scholar 

  • Schmelz, E. A., Engelberth, J., Alborn, H. T., Tumlinson III, J. A., and Teal, P. E. A. 2009. Phytohormone-based activity mapping of insect herbivore-produced elicitors. Proc. Natl. Acad. Sci. USA 106(2):653–657.

    Article  PubMed  CAS  Google Scholar 

  • Schmelz, E. A., Carroll, M. J., Leclere, S., Phipps, S. M., Meredith, J., Chourey, P. S., Alborn, H. T., and Teal, P. E. A. 2006. Fragments of ATP synthase mediate plant perception of insect attack. Proc. Natl. Acad. Sci. USA 103:8894–8899.

    Article  PubMed  CAS  Google Scholar 

  • Storey, J. D. and Tibshirani, R. 2003. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. USA 100:9440–9445.

    Article  PubMed  CAS  Google Scholar 

  • Tian, D., Peiffer, M., Shoemaker, E., Tooker, J., Haubruge, E., Francis, F., Luthe, D. S., and Felton, G. W. 2012. Salivary glucose oxidase from caterpillars mediates the induction of rapid and delayed-induced defenses in the tomato plant. PLoS One 7:e36168.

    Article  PubMed  CAS  Google Scholar 

  • Thipyapong, P. and Steffens, J. 1997. Tomato polyphenol oxidase (differential response of the polyphenol oxidase F promoter to injuries and wound signals). Plant Physiol. 115:409–418.

    PubMed  CAS  Google Scholar 

  • Townsend, J. P. 2003. Multifactorial experimental design and the transitivity of ratios withspotted DNA microarrays. BMC Genomics 4:41.

    Article  PubMed  Google Scholar 

  • Weech, M. H., Chapleau, M., Pan, L., Ide, C., and Bede, J. C. 2008. Caterpillar saliva interferes with induced Arabidopsis thaliana defense responses via the systemic acquired resistance pathway. J. Exp. Bot. 59:2437–2448.

    Article  PubMed  CAS  Google Scholar 

  • Yang, S. F. and Hoffman, N. E. 1984. Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. 35:155–189.

    Article  CAS  Google Scholar 

  • Yeboah, N. A., Arahira, M., Nong, V. H., Zhang, D., Kadokura, K., Watanabe, A., and Fukawaza, C. 1998. A class III acidic endochitinase is specifically expressed in the developing seeds of Soybean (Glycine max (L.) Merr.). Plant Mol. Biol. 36:407–415.

    Article  PubMed  CAS  Google Scholar 

  • Zong, N. and Wang, C. 2004. Induction of nicotine in tobacco by herbivory and its relation to glucose oxidase activity in the labial gland of three noctuid caterpillars. Chin. Sci. Bull. 49:1596–1601.

    CAS  Google Scholar 

  • Zong, N. and Wang, C. 2007. Larval feeding induced defensive responses in tobacco: comparison of two sibling species of Helicoverpa with different diet breadths. Planta 226:215–224.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

Funding was provided by the National Science Foundation Plant Genome Research Initiative (No. 0820367 to ROM and SMH), the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service (No. 2004–01540 to ROM and SMH) and the Western Illinois University research council. We thank Drs. Amy Patrick Mossman (WIU), Patrick Dowd (USDA-ARS, Peoria), and Eric T. Johnson (USDA-ARS, Peoria) for their review of this manuscript. We also thank the Genome Consortium for Active Teaching for assistance in obtaining microarray chips used by undergraduate students in this project.

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Musser, R.O., Hum-Musser, S.M., Lee, H.K. et al. Caterpillar Labial Saliva Alters Tomato Plant Gene Expression. J Chem Ecol 38, 1387–1401 (2012). https://doi.org/10.1007/s10886-012-0198-3

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