Skip to main content
Log in

CHEMOTYPIC Variation in Volatiles and Herbivory for Sagebrush

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Plants that are damaged by herbivores emit complex blends of volatile compounds that often cause neighboring branches to induce resistance. Experimentally clipped sagebrush foliage emits volatiles that neighboring individuals recognize and respond to. These volatiles vary among individuals within a population. Two distinct types are most common with either thujone or camphor as the predominate compound, along with other less common types. Individuals respond more effectively to cues from the same type, suggesting that some of the informative message is contained in the compounds that differentiate the types. In this study, we characterized the chemical profiles of the two common types, and we examined differences in their microhabitats, morphologies, and incidence of attack by herbivores and pathogens. Analysis by gas chromatography coupled with mass spectrometry revealed that the camphor type had higher emissions of camphor, camphene, and tricyclene, while the thujone type emitted more α-thujone, β-thujone, (Z)-salvene, (E)-salvene, carvacrol, and various derivatives of sabinene. We were unable to detect any consistent morphological or microhabitat differences associated with the common types. However, plants of the thujone type had consistently higher rates of damage by chewing herbivores. One galling midge species was more common on thujone plants, while a second midge species was more likely to gall plants of the camphor type. The diversity of preferences of attackers may help to maintain the variation in volatile profiles. These chemical compounds that differentiate the types are likely to be informative cues and deserve further attention.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agrawal AA, Colfer RG (2000) Consequences of thrips-infested plants for attraction of conspecifics and parasitoids. Ecol Ent 25:493–496

    Article  Google Scholar 

  • Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949

    Article  CAS  Google Scholar 

  • Amiot J, Salmon Y, Collin C, Thompson JD (2005) Differential resistance to freezing and spatial distribution in a chemically polymorphic plant Thymus vulgaris. Ecol Lett 8:370–377

    Article  Google Scholar 

  • Amo L, Jansen JJ, van Dam NM, Dicke M, Visser ME (2013) Birds exploit herbivore-induced plant volatiles to locate herbivorous prey. Ecol Lett 16:1348–1355

    Article  PubMed  Google Scholar 

  • Bidart-Bouzat MG, Kliebenstein DJ (2008) Differential levels of insect herbivory in the field associated with genotypic variation in glucosinolates in Arabidopsis thaliana. J Chem Ecol 34:1026–1037

    Article  CAS  PubMed  Google Scholar 

  • Davies NW (1990) Gas chromatographic retention indices of monoterpenes and sesquiterpenes on methyl silicone and carbowax 20 M phases. J Chromatogr A 503:1–24

    Article  CAS  Google Scholar 

  • De Moraes CM, Lewis WJ, Pare PW, Tumlinson JH (1998) Herbivore infested plants selectively attract parasitoids. Nature 393:570–574

    Article  CAS  Google Scholar 

  • Deiml T, Haseneder R, Zieglgansberger W, Rammes G, Eisensamer B, Rupprecht R, Hapfelmeier G (2004) Alpha-thujone reduces 5-HT3 receptor activity by an effect on the agonist-induced desensitization. Neuropharmacology 46:192–201

    Article  CAS  PubMed  Google Scholar 

  • Delphia CM, Rohr JR, Stephenson AG, De Moraes CM, Mescher MC (2009) Effects of genetic variation and inbreeding on volatile production in a field population of horsenettle. Intl. J Plant Sci 170:12–20

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dethier VG (1947) The response of hymenopterous parasites to chemical stimulation of the ovipositor. J Exp Zool 105:199–207

    Article  CAS  PubMed  Google Scholar 

  • Dicke M (1986) Volatile spider-mite pheromone and host-plant kairomone, involved in spaced-out gregariousness in the spider mite, Tetranychus urticae. Physiol Ent 11:251–262

    Article  Google Scholar 

  • Dicke M, van Loon JA (2000) Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Ent Exp Appl 97:237–249

    Article  CAS  Google Scholar 

  • Drukker B, Scutareanu P, Sabelis MW (1995) Do Anthocorid predators respond to synomones from Psylla-infested pear trees under field conditions? Ent Exp Appl 77:193–203

    Article  Google Scholar 

  • Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiol 135:1893–1902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: recent advances and future prospects. Crit Rev Plant Sci 25:417–440

    Article  CAS  Google Scholar 

  • Egerton-Warburton LM, Ghisalberti EL, Considine JA (1998) Intraspecific variability in the volatile leaf oils of Chamelaucium uncinatum (Myrtaceae). Biochem Syst Ecol 26:873–888

    Article  CAS  Google Scholar 

  • Foster AJ, Hall DE, Mortimer L, Abercromby S, Gries R, Gries G, Bohlmann J, Russell J, Mattsson J (2013) Identification of genes in Thuja plicata foliar terpenoid defenses. Plant Physiol 161:1993–2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fournier DA, Skaug HJ, Ancheta J, Ianelli J, Magnusson A, Maunder M, Nielsen A, Sibert J (2012) AD model builder: Using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optimization Models and Software 27:233–249

    Article  Google Scholar 

  • Frost CJ, Mescher MC, Dervinis C, Davis JM, Carlson JE, De Moraes CM (2008) Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytol 180:722–734

    Article  CAS  PubMed  Google Scholar 

  • Gotelli NJ, Ellison GN (2004) A primer of ecological statistics. Sinauer, Sunderland MA

    Google Scholar 

  • Gouinguene S, Degen T, Turlings TCJ (2011) Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte. Chemoecology 11:9–16

    Article  Google Scholar 

  • Gouyon PH, Vernet P, Guillerm JL, Valdeyron G (1986) Polymorphisms and environment – the adaptive value of the oil polymorphisms in Thymus vulgaris L. Heredity 57:59–66

    Article  Google Scholar 

  • Grausgruber-Groger S, Schmiderer C, Steinborn R, Novak J (2012) Seasonal influence on gene expression of monoterpene synthases in Salvia officinalis (Lamiaceae). J Plant Physiol 169:353–359

    Article  PubMed  Google Scholar 

  • Grayer RJ, Kite GC, Goldstone FJ, Bryan SE, Paton A, Putievsky E (1996) Intraspecific taxonomy and essential oil chemotypes in sweet basil, Ocimum basilicum. Phytochemistry 43:1033–1039

    Article  CAS  PubMed  Google Scholar 

  • Hare JD (2007) Variation in herbivore and methyl jasmonate-induced volatiles among genetic lines of Datura wrightii. J Chem Ecol 33:2028–2043

    Article  CAS  PubMed  Google Scholar 

  • Hare JD (2011) Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annu Rev Entomol 56:161–180

    Article  CAS  PubMed  Google Scholar 

  • Heil M, Silva-Bueno C (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci U S A 104:5467–5472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holopainen M, Hiltunen R, Lokki J, Forsen K, Schantz MV (1987) Model for the genetic control of thujone, sabinene and umbellulone in tansy (Tanacetum vulgare L). Hereditas 106:205–208

    Article  CAS  Google Scholar 

  • Horiuchi J, Arimura G, Ozawa R, Shimoda T, Takabayashi J, Tishioka T (2003) A comparison of the responses of Tetranychus urticae (Acari: Tetranychidae) and Phytoseiulus persimilis (Acari: Phytosdiidae) to volatiles emitted from lima bean leaves with different levels of damage made by T. urticae or Spodoptera exigua (Lepidoptera: Noctuidae). Appl Entomol Zool 38:109–116

    Article  Google Scholar 

  • Jirovetz L, Buchbauer G, Stoyanova AS, Georgiev EV, Damianova ST (2003) Composition, quality control, and antimicrobial activity of the essential oil of long-time stored dill (Anethum graveolens L.) seeds from Bulgaria. J Agric Food Chem 51:3854–3857

    Article  CAS  PubMed  Google Scholar 

  • Karban R (2007a) Damage to sagebrush attracts predators but this does not reduce herbivory. Entomol Exp Appl 125:71–80

    Article  Google Scholar 

  • Karban R (2007b) Experimental clipping of sagebrush inhibits seed germination of neighbors. Ecol Lett 10:791–797

    Article  PubMed  Google Scholar 

  • Karban R (2015) Plant sensing and communication. Univ Chicago Press, Chicago

    Book  Google Scholar 

  • Karban R, Baldwin IT, Baxter KJ, Laue G, Felton GW (2000) Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia 125:66–71

    Article  Google Scholar 

  • Karban R, Shiojiri K, Huntzinger M, McCall AC (2006) Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication. Ecology 87:922–930

    Article  PubMed  Google Scholar 

  • Karban R, Shiojiri K, Ishizaki S (2010) An air transfer experiment confirms the role of volatile cues in communication between plants. Am Nat 176:381–384

    Article  PubMed  Google Scholar 

  • Karban R, Wetzel WC, Shiojiri K, Ishizaki S, Ramirez SR, Blande JD (2014) Deciphering the language of plant communication: volatile chemotypes of sagebrush. New Phytol 204:380–385

    Article  PubMed  Google Scholar 

  • Keefover-Ring K, Thompson JD, Linhart YB (2008) Beyond six scents: Defining a seventh Thymus vulgaris chemotype new to southern France by ethanol extraction. Flav Frag J 24:117–122

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Khan ZR, James DG, Midega CAO, Pickett J (2008) Chemical ecology and conservation biological control. Biol Cont 45:210–214

    Article  CAS  Google Scholar 

  • Kikuta Y, Ueda H, Nakayama K, Katsuda Y, Ozawa R, Takabayashi J, Hatanaka A, Matsuda K (2011) Specific regulation of pyrethrin biosynthesis in Chrysanthemum cinerariaefolium by a blend of volatiles emitted from artificially damaged conspecific plants. Plant Cell Physiol 52:588–596

    Article  CAS  PubMed  Google Scholar 

  • Linhart YB, Thompson JD (1995) Terpene-based selective herbivory by Helix aspersa (Mollusca) on Thymus vulgaris (Labiatae). Oecologia 102:126–132

    Article  Google Scholar 

  • Linhart YB, Thompson JD (1999) Thyme is of the essence: biochemical polymorphism and multi-species deterrence. Evol Ecol Res 1:151–171

    Google Scholar 

  • Linhart YB, Gauthier P, Keefover-Ring K, Thompson JD (2015) Variable phytotoxic effects of Thymus vulgaris (Lamiaceae) terpenes on associated species. Intl J Plant Sci 176:20–30

    Article  Google Scholar 

  • Lloyd SR, Schoonbeek H, Trick M, Zipfel C, Ridout CJ (2014) Methods to study PAMP-triggered immunity in Brassica species. MPMI 27:286–295

    Article  CAS  PubMed  Google Scholar 

  • Mäntylä E, Alessio GA, Blande JD, Heijari J, Holopainen JK, Laaksonen T, Piirtola P, Klemola T (2008) From plants to birds: higher avian predation rates in trees responding to insect herbivory. PLoS One 3:–e2832

  • Mattiacci L, Dicke M, Posthumus MA (1995) Beta-glucosidase – an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proc Natl Acad Sci U S A 92:2036–2040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michaeli S, Fromm H (2015) Closing the loop on the GABA shunt in plants: are GABA metabolism and signaling entwined? Front Plant Sci 6:–419

  • Mirabella R, Rauwerda H, Struys EA, Jakobs C, Triantaphylides C, Haring MA, Schuurink RC (2008) The Arabidopsis her1 mutant implicates GABA in E-2-hexenal responsiveness. Plant J 53:–19213

  • Moqrich A, Hwang SW, Earley TJ, Petrus MJ, Murray AN, Spencer KSR, Andahazy M, Story GM, Patapoutian A (2005) Impaired thermosensation in mice lacking TRPV3, a heat and camphor sensor in the skin. Science 307:1468–1472

    Article  CAS  PubMed  Google Scholar 

  • Mumm R, Dicke M (2010) Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Can J Zool 88:628–667

    Article  CAS  Google Scholar 

  • Pallini A, Janssen A, Sabelis MW (1997) Odour-mediated responses of phytophagous mites to conspecifics and heterospecific competitors. Oecologia 110:179–185

    Article  Google Scholar 

  • Pare PW, Tumlinson JH (1997) De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol 114:1161–1167

    CAS  PubMed  PubMed Central  Google Scholar 

  • Perez-Alonso MJ, Velasco-Negueruela A, Pala-Paul J, Sanz J (2003) Variations in the essential oil composition of Artemisia pedemontana gathered in Spain: chemotype camphor-1,8-cineole and chemotype davanone. Biochem Syst Ecol 31:77–84

    Article  CAS  Google Scholar 

  • Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237–243

    Article  CAS  PubMed  Google Scholar 

  • Quintana-Rodriguez E, Morales-Vargas AT, Molina-Torres J, Adame-Alvarez RM, Acosta-Gallegos JA, Heil M (2015) Plant volatiles cause direct, induced and associational resistance in common bean to the fungal pathogen Colletotrichum lindemuthianum. J Ecol 103:250–260

    Article  CAS  Google Scholar 

  • R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation, Vienna, Austria

  • Ravid U, Putievsky E, Katzir I, Carmeli D, Eshel A, Schenk HP (1992) The essential oils of Artemisia judaica L. Flav Frag J 7:69–72

    Article  CAS  Google Scholar 

  • Rodriguez-Saona CR, Rodriguez-Saona LE, Frost CJ (2009) Herbivore-induced volatiles in the perennial shrub, Vaccinium corymbosum, and their role in inter-branch signaling. J Chem Ecol 35:621–649

    Article  Google Scholar 

  • Romagni JG, Allen SN, Dayan FE (2000) Allelopathic effects of volatile cineoles on two weedy plant species. J Chem Ecol 26:303–313

    Article  CAS  Google Scholar 

  • Scheiner SM (2001) MANOVA: Multiple response variables and multispecies interactions. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments, 2nd edn Oxford Univ Press, New York, pp 99–115.

  • Schuman MC, Heinzel N, Gaquerel E, Svaros A, Baldwin IT (2009) Polymorphism in jasmonate signaling partially accounts for the variety of volatiles produced by Nicotiana attenuata plants in a native population. New Phytol 183:1134–1148

    Article  CAS  PubMed  Google Scholar 

  • Shulaev V, Silverman P, Raskin I (1997) Airborne signaling by methyl salicylate in plant pathogen resistance. Nature 385:718–721

    Article  CAS  Google Scholar 

  • Skaug H, Fournier D, Nielsen A, Magnusson A, Bolker B (2012) Generalized linear mixed models using AD model builder. R package version 0.7.2.12.

  • Takabayashi J, Sabelis MW, Janssen A, Shiojiri K, van Wijk M (2006) Can plants betray the presensce of multiple herbivore species to predators and parasitoids? The role of learning in phytochemical information networks. Ecol Res 21:3–8

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Thompson JD, Gauthier P, Amiot J, Ehlers BK, Collin C, Fossat J, Barrios V, Arnaud-Miramont F, Keefover-Ring D, Linhart YB (2007) Ongoing adaptation to Mediterranean climate extremes in a chemically polymorphic plant. Ecol Monogr 77:421–439

    Article  Google Scholar 

  • Veličković DT, Ristić MS, Milosavljević NP, Karabegović IT, Stojičević SS, Lazić ML (2012) Chemical composition of the essential oils of Salvia austriaca Jacq. and Salvia amplexicaulis Lam. from Serbia. Agro Food Industry Hi-tech 23:7–9

    Google Scholar 

  • Vernet P, Gouyon PH, Valdeyron G (1986) Genetic control of the oil content in Thymus vulgaris L: a case of polymorphism in a biosynthetic chain. Genetica 69:227–231

    Article  CAS  Google Scholar 

  • Wallaart TE, Pras N, Beckman AC, Quax WJ (2000) Seasonal variation of artemisinin and its biosynthetic precursors in plant of Artemisia annua of different geographical origin: proof for the existence of chemotypes. Planta Med 66:57–62

    Article  CAS  PubMed  Google Scholar 

  • Wason EL, Agrawal AA, Hunter MD (2013) A genetically-based latitudinal cline in the emission of herbivory-induced plant volatile organic compounds. J Ecol 39:1101–1111

    CAS  Google Scholar 

  • Wu W, Yuan M, Zhang Q, Zhu Y, Yong L, Wang W, Qi Y, Guo D (2011) Chemotype-dependent metabolic response to methyl jasmonate elicitation in Artemisia annua. Planta Med 77:1048–1053

    Article  CAS  PubMed  Google Scholar 

  • Xu HX, Blair NT, Clapham DE (2005) Camphor activates and strongly desensitizes the transient receptor potential vanilloid subtype 1 channel in a vanilloid-independent mechanism. J Neurosci 25:8924–8937

    Article  CAS  PubMed  Google Scholar 

  • Yin Q-H, Yan F-X, X-Y Z, WuY-H WX-P, Liao M-C, Deng S-W, Yin L-L, Zhang Y-Z (2012) Anti-proliferative and pro-apoptotic effect of carvacrol on human hepatocellular carcinoma cell line HepG-2. Cytotechnology 64:43–51

    Article  CAS  PubMed  Google Scholar 

  • Zust T, Heichinger C, Grossniklaus U, Harrington R, Kliebenstein DJ, Turnbull LA (2012) Natural enemies drive geographic variation in plant defenses. Science 338:116–119

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Mikaela Huntzinger, Hongjun Li, Enrico Pezzola, and Kaori Shiojiri for help in the field. Shree Prasad identified pathogens of sagebrush and Will Wetzel identified some of the herbivores. Tao Li provided advice on the PCA analysis. Wittko Francke and Martin Heil improved the manuscript. The work was conducted in UC Sagehen Experimental Forest and other sites in the Tahoe National Forest, and we thank Jeff Brown and Faerthan Felix for facilitating our research at these sites.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard Karban.

Electronic supplementary material

ESM 1

(DOCX 12 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Karban, R., Grof-Tisza, P. & Blande, J.D. CHEMOTYPIC Variation in Volatiles and Herbivory for Sagebrush. J Chem Ecol 42, 829–840 (2016). https://doi.org/10.1007/s10886-016-0741-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-016-0741-8

Keywords

Navigation