Skip to main content

Effects of Terpene Chemotypes of Melaleuca alternifolia on Two Specialist Leaf Beetles and Susceptibility to Myrtle Rust

Abstract

Plant chemical polymorphisms, or plant chemotypes, are characterized by intraspecific discrete differences of plant secondary metabolites in the same plant tissue. Chemotypes that differ in foliar terpene composition are found commonly in Myrtaceae. In this study, we focused on terpene chemotypes of medicinal tea tree, Melalecua alternifolia, to explore whether this variation affects two specialist herbivores Paropsisterna tigrina and Faex sp. (Coleoptera: Chrysomelidae), and if this could explain the maintenance of this variation. We tested whether insect performance, oviposition preference, and plant damage were associated with different chemotypes. We found that larval growth rate of Faex sp. was higher in chemotypes with high concentrations of 1,8-cineole, and that oviposition preference depended on the chemotype of the larval diet. Although performance traits and preference for oviposition of P. tigrina did not vary among chemotypes, adults inflicted less damage on plants with a high concentration of terpinolene. Additionally, we tested whether different chemotypes showed different levels of susceptibility by myrtle rust (Puccinia psidii). We found that plants with a high concentration of 1,8-cineole were more likely to be infected under controlled conditions. Although there is evidence that terpene chemotypes are a mediator of the interaction with natural enemies, the most detrimental pest of this plant, P. tigrina, does not seem to be affected by variation in plant terpenes.

This is a preview of subscription content, access via your institution.

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

References

  • Agrawal AA (2011) Current trends in the evolutionary ecology of plant defence. Funct Ecol 25:420–432

    Article  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

    CAS  Article  PubMed  Google Scholar 

  • Brophy JJ, Davies NW, Southwell IA, Stiff IA, Williams LR (1989) Gas chromatographic quality control for oil of Melaleuca terpinen-4-ol type (Australian tea tree). J Agric Food Chem 37:1330–1335

    CAS  Article  Google Scholar 

  • Butcher PA, Matheson A, Slee U (1996) Potential for genetic improvement of oil production in Melaleuca alternifolia and M. linariifolia. New forests 11:31–51

  • Carnegie AJ, Lidbetter JR (2012) Rapidly expanding host range for Puccinia psidii sensu lato in Australia. Australas Plant Pathol 41:13–29

    Article  Google Scholar 

  • Carroll AJ, Badger MR, Harvey Millar A (2010) The MetabolomeExpress Project: enabling web-based processing, analysis and transparent dissemination of GC/MS metabolomics datasets. BMC Bioinforma 11:376

    Article  Google Scholar 

  • Carson CF, Hammer KA, Riley TV (2006) Melaleuca alternifolia (Tea Tree) Oil : a review of antimicrobial and other medicinal properties. Clin Microbiol Rev 19:50–62

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Chan EKF, Rowe HC, Corwin JA, Joseph B, Kliebenstein DJ (2011) Combining genome-wide association mapping and transcriptional networks to identify novel genes controlling glucosinolates in Arabidopsis thaliana. PLoS Biol 9, e1001125

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Fritz RS, Simms EL (1992) In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. University of Chicago Press, Chicago

    Chapter  Google Scholar 

  • Hammer KA, Carson CF, Riley TV (2003) Antifungal activity of the components of Melaleuca alternifolia (tea tree) oil. J Appl Microbiol 95:853–860

    CAS  Article  PubMed  Google Scholar 

  • Hartmann T (1996) Diversity and variability of plant secondary metabolism: a mechanistic view. Entomol Exp Appl 80:177–188

    CAS  Article  Google Scholar 

  • Homer L, Leach D, Lea D, Slade Lee L, Henry R, Baverstock P (2000) Natural variation in the essential oil content of Melaleuca alternifolia Cheel (Myrtaceae). Biochem Syst Ecol 28:367–382

    CAS  Article  PubMed  Google Scholar 

  • Ireland BF, Hibbert DB, Goldsack RJ, Doran JC, Brophy JJ (2002) Chemical variation in the leaf essential oil of Melaleuca quinquenervia (Cav.) S.T. Blake. Biochem Syst Ecol 30:457–470

    CAS  Article  Google Scholar 

  • Keefover-Ring K, Thompson JD, Linhart YB (2009) Beyond six scents: defining a seventh Thymus vulgaris chemotype new to southern France by ethanol extraction. Flavour Fragr J 24:117–122

    CAS  Article  Google Scholar 

  • Keszei A, Brubaker CL, Foley WJ (2008) A molecular perspective on terpene variation in Australian Myrtaceae. Aust J Bot 56:197

    CAS  Article  Google Scholar 

  • Keszei A, Hassan Y, Foley WJ (2010) A biochemical interpretation of terpene chemotypes in Melaleuca alternifolia. J Chem Ecol 36:652–661

    CAS  Article  PubMed  Google Scholar 

  • Kleine S, Müller C (2011) Intraspecific plant chemical diversity and its relation to herbivory. Oecologia 166:175–186

    Article  PubMed  Google Scholar 

  • Kursar TA, Dexter KG, Lokvam J, Pennington RT, Richardson JE, Weber MG, Murakami ET, Drake C, McGregor R, Coley PD (2009) The evolution of antiherbivore defenses and their contribution to species coexistence in the tropical tree genus Inga. Proc Natl Acad Sci U S A 106:18073–18078

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Lee L, Brooks L, Homer L, Rossetto M, Henry R, Baverstock P (2002) Geographic variation in the essential oils and morphology of natural populations of Melaleuca alternifolia (Myrtaceae). Biochem Syst Ecol 30:343–360

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  • Linhart Y, Keefover-Ring K, Mooney KA, Breland B, Thompson JD (2005) A chemical polymorphism in a multitrophic setting: thyme monoterpene composition and food web structure. Am Nat 166:517–529

    Article  PubMed  Google Scholar 

  • May J, Chan CH, King A, Williams L, French GL (2000) Time-kill studies of tea tree oils on clinical isolates. J Antimicrob Chemother 45:639–643

    CAS  Article  PubMed  Google Scholar 

  • Mayhew PJ (2001) Herbivore host choice and optimal bad motherhood. Trends Ecol Evol 16:165–167

    Article  PubMed  Google Scholar 

  • Mithen R, Clarket J, Listert C, Deanf C (1995a) Genetics of aliphatic glucosinolates. III. Side chain structure of aliphatic glucosinolates in Arabidopsis thaliana. Heredity 74:210–215

    CAS  Article  Google Scholar 

  • Mithen R, Raybould AF, Giamoustaris A (1995b) Divergent selection for secondary metabolites between wild populations of Brassica oleracea and its implications for plant—herbivore interactions. Heredity 75:472–484

    CAS  Article  Google Scholar 

  • Moore BD, Andrew RL, Külheim C, Foley WJ (2014) Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytol 201:733–750

    Article  PubMed  Google Scholar 

  • Morin L, Aveyard R, Lidbetter JR, Wilson PG (2012) Investigating the host-range of the rust fungus Puccinia psidii sensu lato across tribes of the family Myrtaceae present in Australia. PLoS One 7, e35434

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Newton EL, Bullock JM, Hodgson DJ (2009) Glucosinolate polymorphism in wild cabbage (Brassica oleracea) influences the structure of herbivore communities. Oecologia 160:63–76

    Article  PubMed  Google Scholar 

  • Padovan A, Keszei A, Köllner TG, Degenhardt J, Foley WJ (2010) The molecular basis of host plant selection in Melaleuca quinquenervia by a successful biological control agent. Phytochemistry 71:1237–1244

    CAS  Article  PubMed  Google Scholar 

  • Poelman EH, Galiart RJFH, Raaijmakers CE, van Loon JJA, van Dam NM (2008a) Performance of specialist and generalist herbivores feeding on cabbage cultivars is not explained by glucosinolate profiles. Entomol Exp Appl 127:218–228

    Article  Google Scholar 

  • Poelman EH, van Loon JJA, Dicke M (2008b) Consequences of variation in plant defense for biodiversity at higher trophic levels. Trends Plant Sci 13:534–541

    CAS  Article  PubMed  Google Scholar 

  • Poelman EH, van Dam NM, van Loon JJA, Vet LEM, Dicke M (2009) Chemical diversity in Brassica oleracea affects biodiversity of insect herbivores. Ecology 90:1863–1877

    Article  PubMed  Google Scholar 

  • Reid C, Ohmart C (1989) Determination of the sex of pupae of Paropsis atomaria Olivier, and related Paropsina (Coleoptera: Chrysomelidae). Aust J Entomol 28:29–30

    Article  Google Scholar 

  • Rosenthal GA, Berenbaum MR (1992) In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites: ecological and evolutionary processes. Academic, San Diego

    Google Scholar 

  • Scheirs J, De Bruyn L, Verhagen R (2000) Optimization of adult performance determines host choice in a grass miner. Proc R Soc Lond B 267:2065–2069

    CAS  Article  Google Scholar 

  • Southwell IA, Stiff I (1990) Differentiation between Melaleuca alternifolia and M. linariifolia by monoterpenoid comparison. Phytochemistry 29:3529–3533

    CAS  Article  Google Scholar 

  • Southwell IA, Lowe RF (1999) Tea tree. The genus Melaleuca. Harwood Academic Publishers, Amsterdam

    Book  Google Scholar 

  • Southwell IA, Russell MF (2002) Volatile oil comparison of cotyledon leaves of chemotypes of Melaleuca alternifolia. Phytochemistry 59:391–393

    CAS  Article  PubMed  Google Scholar 

  • Southwell IA, Maddox CDA, Zalucki MP (1995) Metabolism of 1, 8-cineole in tea tree (Melaleuca alternifolia and M. linariifolia) by pyrgo beetle (Paropsisterna tigrina). J Chem Ecol 21:439–453

  • Southwell IA, Russell MF, Maddox CDA, Wheeler GS (2003) Differential metabolism of 1,8-cineole in insects. J Chem Ecol 29:83–94

  • Steppuhn A, Gase K, Krock B, Halitschke R, Baldwin IT (2004) Nicotine’s defensive function in nature. PLoS Biol 2:1074–1080

    CAS  Article  Google Scholar 

  • Vernet P, Gouyon R, Valdeyron G (1986) Genetic control of the oil content in Thymus vulgaris L: a case of polymorphism in a biosynthetic chain. Genetica 4:227–231

    Article  Google Scholar 

  • Wheeler GS (2006) Chemotype variation of the weed Melaleuca quinquenervia influences the biomass and fecundity of the biological control agent Oxyops vitiosa. Biol Control 36:121–128

    CAS  Article  Google Scholar 

  • Wheeler GS, Ordung KM (2005) Secondary metabolite variation affects the oviposition preference but has little effect on the performance of Boreioglycaspis melaleucae: a biological control agent of Melaleuca quinquenervia. Biol Control 35:115–123

    CAS  Article  Google Scholar 

  • Wise MJ, Partelow JM, Everson KJ, Anselmo MK, Abrahamson WG (2008) Good mothers, bad mothers, and the nature of resistance to herbivory in Solidago altissima. Oecologia 155:257–266

    Article  PubMed  Google Scholar 

  • Wolf VC, Gassmann A, Müller C (2012) Choice behaviour and performance of Cassida stigmatica on various chemotypes of Tanacetum vulgare and implications for biocontrol. Entomol Exp Appl 144:78–85

    Article  Google Scholar 

  • Züst 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 Penny Gullan and Chris Reid for their invaluable help regarding insect collection methods and beetle taxonomic identification. Peter Entwistle and Jared Streich helped with beetle collection in the Northern Rivers. Thanks to Andras Keszei for helpful suggestions regarding experimental design, chemical analysis of terpenes, and chemotyping. We are grateful to Karanjeet Sandhu at the University of Sydney for performing the Myrtle rust infection tests. Thanks to Damien Esquerré for the beetles pictures and to Marta Vidal and Iliana Medina for helpful suggestions throughout the manuscript. Robert Dyason kindly provided access to his tea tree plantation. Thanks to two anonymous reviewers for improving the manuscript. CBS was funded by PhD scholarships from CONACYT and ANU. The work was supported by a grant from the Australian Research Council to WJF.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Carlos Bustos-Segura.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 72 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bustos-Segura, C., Külheim, C. & Foley, W. Effects of Terpene Chemotypes of Melaleuca alternifolia on Two Specialist Leaf Beetles and Susceptibility to Myrtle Rust. J Chem Ecol 41, 937–947 (2015). https://doi.org/10.1007/s10886-015-0628-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-015-0628-0

Keywords

  • Terpenoids
  • Chemotype
  • Chemical variation
  • Melaleuca
  • Herbivory
  • Chrysomelidae
  • Myrtle rust