Skip to main content
SpringerLink
Log in

Both Gas Chromatography and an Electronic Nose Reflect Chemical Polymorphism of Juniper Shrubs Browsed or Avoided by Sheep

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

Abstract

Chemical polymorphism may contribute to variation in browsing damage by mammalian herbivores. Earlier, we demonstrated that essential oil concentration in juniper, Juniperus communis, was negatively associated with herbivore browsing. The aim of the present study was to characterize the volatile chemical composition of browsed and non-browsed J. communis. By using either gas chromatography with flame ionization detection (GC-FID) or an electronic nose device, we could separate sheep-browsed or non-browsed juniper shrubs by their essential oil pattern and complex odor matrix. The main components of the essential oil from J. communis were monoterpenes. We distinguished three chemotypes, dominated either by α-pinene, sabinene, or δ-3-carene. Shrubs belonging to the α-pinene- or sabinene-dominated groups were browsed, whereas all individuals with the δ-3-carene chemotype were unused by the local herbivores. The electronic nose also separated the browsed and non-browsed shrubs indicating that their odor matrix could guide sheep browsing. Responses of sheep could integrate the post-ingestive effects of plant secondary metabolites with sensory experience that stems from odor–phytotoxin interactions. Chemotype diversity could increase the survival rate in the present population of J. communis as certain shrubs could benefit from relatively better chemical protection against the herbivores.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Adams, R. P. 1998. The leaf essential oils and chemotaxonomy of Juniperus sect. Juniperus. Biochem. Syst. Ecol. 26:637–645.

    Article  CAS  Google Scholar 

  • Adams, R. P., and Pandey, R. N. 2003. Analysis of Juniperus communis and its varieties based on DNA fingerprinting. Biochem. Syst. Ecol. 31:1271–1278.

    Article  CAS  Google Scholar 

  • Adams, R. P., Pandey, R. N., Leverenz, J. W., Dignard, N., Hoegh, K., and Thorfinnsson, T. 2003. Pan-Arctic variation in Juniperus communis: historical biogeography based on DNA fingerprinting. Biochem. Syst. Ecol. 31:181–192.

    Article  CAS  Google Scholar 

  • Almquist, A. C., Fäldt, J., Yart, A., Chevet, Y., Sauvard, D., Lieutier, F., and Borg-Karlson, A. K. 2006. Host selection in Tomicus piniperda L.: composition of monoterpene hydrocarbons in relation to attack frequency in the shoot feeding phase. Z. Naturforsch. C 61:439–444.

    CAS  PubMed  Google Scholar 

  • Angioni, A., Barra, A., Russo, M. T., Coroneo, V., Dessi, S., and Cabras, P. 2003. Chemical composition of the essential oils of Juniperus from ripe and unripe berries and leaves and their antimicrobial activity. J. Agric. Food Chem. 51:3073–3078.

    Article  PubMed  Google Scholar 

  • Aparicio, R., Morales, M. T., and Alonso, M. V. 1996. Relationship between volatile compounds and sensory attributes of olive oils by the sensory wheel. J. Am. Oil Chem. Soc. 73:1253–1264.

    Article  CAS  Google Scholar 

  • Augner, M., Provenza, F. D., and Villalba, J. J. 1998. A rule of thumb in mammalian herbivores? Anim. Behav. 56:337–345.

    Article  PubMed  Google Scholar 

  • Baby, R., Cabezas, I., Castro, E., Filip, R., and de Reca, N. E. W. 2005. Quality control of medicinal plants with an electronic nose. Sens. Actuators B Chem. 106:24–28.

    Article  Google Scholar 

  • Bakkali, F., Averbeck, S., Averbeck, D., and Waomar, M. 2008. Biological effects of essential oils—a review. Food Chem. Toxicol. 46:446–475.

    Article  CAS  PubMed  Google Scholar 

  • Berec, L. 2000. Mixed encounters, limited perception and optimal foraging. Bull. Math. Biol. 62:849–868.

    Article  CAS  PubMed  Google Scholar 

  • Bryant, J. P., Reichardt, P., and Clausen, T. 1985. Plant carbon/nutrient balance—implications for chemical defense. Abstr. Pap. Am. Chem. Soc. 190:91.

    Google Scholar 

  • Buck, L., and Axel, R. 1991. A novel multigene family may encode odorant receptors—a molecular-basis for odor recognition. Cell 65:175–187.

    Article  CAS  PubMed  Google Scholar 

  • Butkiene, R., Nivinskiene, O., and Mockute, D. 2004. Chemical composition of unripe and ripe berry essential oils of Juniperus communis L. growing wild in Vilnius district. Chemija 19:57–63.

    Google Scholar 

  • Butkiene, R., Nivinskiene, O., Mockute, D., and Miliute, A. 2007. Variety of the essential oils composition of wood, needles (leaves), unripe and ripe berries of Juniperus communis var. communis growing wild in Druskininkai district. Chemija 18:35–40.

    CAS  Google Scholar 

  • Butkiene, R., Nivinskiene, O., and Mockute, D. 2009. Two chemotypes of essential oils produced by the same Juniperus communis L. growing wild in Lithuania. Chemija 20:195–201.

    CAS  Google Scholar 

  • Cleland, T. A., Morse, A., Yue, E. L., and Linster, C. 2002. Behavioral models of odor similarity. Behav. Neurosci. 116:222–231.

    Article  PubMed  Google Scholar 

  • Dearing, M. D., Mangione, A. M., and Karasov, W. H. 2000. Diet breadth of mammalian herbivores: nutrient versus detoxification constraints. Oecologia 123:397–405.

    Article  Google Scholar 

  • Duncan, A. J., Ginane, C., Elston, D. A., Kunaver, A., and Gordon, I. J. 2006. How do herbivores trade-off the positive and negative consequences of diet selection decisions? Anim. Behav. 71:93–99.

    Article  Google Scholar 

  • Eisner, T., and Grant, R. P. 1981. Toxicity, odor aversion, and olfactory aposematism. Science 213:476–476.

    Article  CAS  PubMed  Google Scholar 

  • El Barbri, N., Llobet, E., El Bari, N., Correig, X., and Bouchikhi, B. 2008. Electronic nose based on metal oxide semiconductor sensors as an alternative technique for the spoilage classification of red meat. Sensors-Basel 8:142–156.

    CAS  Google Scholar 

  • Elliott, S., and Loudon, A. 1987. Effects of monoterpene odors on food selection by red deer calves (Cervus elaphus). J. Chem. Ecol. 13:1343–1349.

    Article  CAS  Google Scholar 

  • Estell, R. E., Fredrickson, E. L., Tellez, M. R., Havstad, K. M., Shupe, W. L., Anderson, D. M., and Remmenga, M. D. 1998. Effects of volatile compounds on consumption of alfalfa pellets by sheep. J. Anim. Sci. 76:228–233.

    CAS  PubMed  Google Scholar 

  • Fäldt, J., Martin, D., Miller, B., Rawat, S., and Bohlmann, J. 2003. Traumatic resin defense in Norway spruce (Picea abies): Methyl jasmonate-induced terpene synthase gene expression, and cDNA cloning and functional characterization of (+)-3-carene synthase. Plant Mol. Biol. 51:119–133.

    Article  PubMed  Google Scholar 

  • Filipowicz, N., Kaminski, M., Kurlenda, J., Asztemborska, M., and Ochocka, J. R. 2003. Antibacterial and antifungal activity of juniper berry oil and its selected components. Phytother. Res. 17:227–231.

    Article  CAS  PubMed  Google Scholar 

  • Filipowicz, N., Piotrowski, A., Ochocka, J. R., and Asztemborska, M. 2006. The phytochemical and genetic survey of common and dwarf juniper (Juniperus communis and Juniperus nana) identifies chemical races and close taxonomic identity of the species. Planta Med. 72:850–853.

    Article  CAS  PubMed  Google Scholar 

  • Filipowicz, N., Madanecki, P., Golebiowski, M., Stepnowski, P., and Ochocka, J. R. 2009. HS-SPME/GC analysis reveals the population variability of terpene contents in Juniperus communis needles. Chem. Biodiv. 6:2290–2301.

    Article  CAS  Google Scholar 

  • Freeland, W. J., and Janzen, D. H. 1974. Strategies in herbivory in mammals: the role of plant secondary compounds. Am. Nat. 110:269–289.

    Article  Google Scholar 

  • Friedman, L., and Miller, J. G. 1971. Odor incongruity and chirality. Science 172:1044–1046.

    Article  CAS  PubMed  Google Scholar 

  • Gomez, D., Azorin, J., Bastida, J., Viladomat, F., and Codina, C. 2003. Seasonal and spatial variations of alkaloids in Merendera montana in relation to chemical defense and phenology. J. Chem. Ecol. 29:1117–1126.

    Article  CAS  PubMed  Google Scholar 

  • Hiltunen, R. 1975. Variation and inheritance of some monoterpenes in Pinus sylvestris. Planta Med. 28:315–323.

    Article  CAS  PubMed  Google Scholar 

  • Hiltunen, R., and Laakso, I. 1995. Gas chromatographic analysis and biogenetic relationships of monoterpene enantiomers in Scots pine and juniper needle oils. Flavour Fragr. J. 10:203–210.

    Article  CAS  Google Scholar 

  • Hobbs, P. J., Misselbrook, T. H., and Pain, B. F. 1995. Assessment of odors from livestock wastes by a photoionization detector, an electronic nose, olfactometry and gas-chromatography mass-spectrometry. J. Agric. Eng. Res. 60:137–144.

    Article  Google Scholar 

  • Hogben, P., Drage, B., and Stuetz, R. M. 2004. Electronic sensory systems for taste and odour monitoring in water—developments and limitations. Environ. Sci. Bio/Technol. 3:15–22.

    Article  CAS  Google Scholar 

  • Huber, D. P. W., Ralph, S., and Bohlmann, J. 2004. Genomic hardwiring and phenotypic plasticity of terpenoid-based defenses in conifers. J. Chem. Ecol. 30:2399–2418.

    Article  CAS  PubMed  Google Scholar 

  • Iason, G. R., and Villalba, J. J. 2006. Behavioral strategies of mammal herbivores against plant secondary metabolites: the avoidance-tolerance continuum. J. Chem. Ecol. 32:1115–1132.

    Article  CAS  PubMed  Google Scholar 

  • Illius, A. W., Gordon, I. J., Elston, D. A., and Milne, J. D. 1999. Diet selection in goats: a test of intake-rate maximization. Ecology 80:1008–1018.

    Article  Google Scholar 

  • Kinloch, B. B., Westfall, R. D., and Forrest, G. I. 1986. Caledonian Scots pine: origins and genetic structure. New Phytol. 104:703–729.

    Article  Google Scholar 

  • Laska, M., Liesen, A., and Teubner, P. 1999. Enantioselectivity of odor perception in squirrel monkeys and humans. Am. J. Physiol-Reg. I. 277:R1098–R1103.

    CAS  Google Scholar 

  • Legin, A., Rudnitskaya, A., Lvova, L., Vlasov, Y., Di Natale, C., and D’Amico, A. 2003. Evaluation of Italian wine by the electronic tongue: recognition, quantitative analysis and correlation with human sensory perception. Anal. Chim. Acta. 484:33–44.

    Article  CAS  Google Scholar 

  • Leitereg, T. J., Guadagni, D. G., Harris, J., Mon, T. R., and Teranishi, R. 1971. Evidence for the difference between the odours of the optical isomers (+)- and (−)-carvone. Nature 230:455–456.

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Lledo, P. M., Gheusi, G., and Vincent, J. D. 2005. Information processing in the mammalian olfactory system. Physiol. Rev. 85:281–317.

    Article  PubMed  Google Scholar 

  • Maricou, H., Pereira, D., Verschuere, L., Philips, S., and Verstraete, W. 1998. Measurements of some volatile compounds by means of the electronic nose. Water Air Soil Pollut. 107:423–442.

    Article  CAS  Google Scholar 

  • Markó, G., Gyuricza, V., Bernáth, J., and Altbäcker, V. 2008. Essential oil yield and composition reflect browsing damage of Junipers. J. Chem. Ecol. 34:1545–1552.

    Article  PubMed  Google Scholar 

  • Martin, D. M., Fäldt, J., and Bohlmann, J. 2004. Functional characterization of nine Norway spruce TPS genes and evolution of gymnosperm terpene synthases of the TPS-d subfamily. Plant Physiol. 135:1908–1927.

    Article  CAS  PubMed  Google Scholar 

  • Miller, B., Madilao, L. L., Ralph, S., and Bohlmann, J. 2005. Insect-induced conifer defense. White pine weevil and methyl jasmonate induce traumatic resinosis, de novo formed volatile emissions, and accumulation of terpenoid synthase and putative octadecanoid pathway transcripts in Sitka spruce. Plant Physiol. 137:369–382.

    Article  CAS  PubMed  Google Scholar 

  • Nagy, J. G., and Tengerdy, R. P. 1968. Antibacterial action of essential oils of Artemisia as an ecological factor II. Antibacterial action of the volatile oils of Artemisia tridentata (big sagebrush) on bacteria from the rumen of mule deer. Appl. Microbiol. 16:441–444.

    CAS  PubMed  Google Scholar 

  • Narjisse, H., Malechek, J. C., and Olsen, J. D. 1996. Influence of odor and taste of monoterpenoids on food selection by anosmic and intact sheep and goats. Small Rumin. Res. 23:109–115.

    Article  Google Scholar 

  • Norin, T. 1996. Chiral chemodiversity and its role for biological activity. Some observations from studies on insect/insect and insect/plant relationships. Pure Appl. Chem. 68:2043–2049.

    Article  CAS  Google Scholar 

  • Novák, I., Zámbori-Németh, E., Horváth, H., Seregély, Z., and Kaffka, K. 2001. Evaluation of essential oils by gas-chromatography and a new method: “electronic nose”. J. Hortic. Sci. 7:85–89.

    Google Scholar 

  • Novák, I., Zámbori-Németh, E., Horváth, H., Seregély, Z., and Kaffka, K. 2003. Study of essential oil components in different Origanum species by GC and sensory analysis. Acta Aliment. Hung. 32:141–150.

    Article  Google Scholar 

  • Ochocka, J. R., Asztemborska, M., Zook, D. R., Sybilska, D., Perez, G., and Ossicini, L. 1997. Enantiomers of monoterpenic hydrocarbons in essential oils from Juniperus communis. Phytochemistry 44:869–873.

    Article  CAS  Google Scholar 

  • Oh, H. K., Sakai, T., Jones, M. B., and Longhurst, W. M. 1967. Effect of various essential oils isolated from Douglas fir needles upon sheep and deer rumen microbial activity. Appl. Microbiol. 15:777–784.

    CAS  PubMed  Google Scholar 

  • Orav, A., Kailas, T., and Koel, M. 1997. Chemometric analysis of conifer needle oils. Proc. Est. Acad. Sci. Chem. 46:3–10.

    CAS  Google Scholar 

  • Pearce, T. C. 1997a. Computational parallels between the biological olfactory pathway and its analogue ‘The Electronic Nose’ .1. Biological olfaction. Biosystems 41:43–67.

    Article  CAS  PubMed  Google Scholar 

  • Pearce, T. C. 1997b. Computational parallels between the biological olfactory pathway and its analogue ‘The Electronic Nose’ .2. Sensor-based machine olfaction. Biosystems 41:69–90.

    Article  CAS  PubMed  Google Scholar 

  • Provenza, F. D. 1995. Postingestive feedback as an elementary determinant of food preference and intake in ruminants. J. Range Manage. 48:2–17.

    Article  Google Scholar 

  • Provenza, F. D. 1996. Acquired aversions as the basis for varied diets of ruminants foraging on rangelands. J. Anim. Sci. 74:2010–2020.

    CAS  PubMed  Google Scholar 

  • Provenza, F. D., Pfister, J. A., and Cheney, C. D. 1992. Mechanisms of learning in diet selection with reference to phytotoxicosis in herbivores. J. Range Manage. 45:36–45.

    Article  Google Scholar 

  • Provenza, F. D., Villalba, J. J., Cheney, C. D., and Werner, S. J. 1998. Self-organization of foraging behaviour: from simplicity to complexity without goals. Nutr. Res. Rev. 11:199–222.

    Article  CAS  PubMed  Google Scholar 

  • Provenza, F. D., Villalba, J. J., Dziba, L. E., Atwood, S. B., and Banner, R. E. 2003. Linking herbivore experience, varied diets, and plant biochemical diversity. Small Rumin. Res. 49:257–274.

    Article  Google Scholar 

  • Riddle, R. R., Taylor, C. A., Kothmann, M. M., and Huston, J. E. 1996. Volatile oil contents of ashe and redberry juniper and its relationship to preference by Angora and Spanish goats. J. Range Manage. 49:35–41.

    Article  Google Scholar 

  • Rocchini, L. A., Lindgren, B. S., and Bennett, R. G. 2000. Effects of resin flow and monoterpene composition on susceptibility of lodgepole pine to attack by the Douglas-fir pitch moth, Synanthedon novaroensis (Lep., Sesiidae). J. Appl. Entomol. 124:87–92.

    Article  CAS  Google Scholar 

  • Rogosic, J., Estell, R. E., Skobic, D., and Stanic, S. 2007. Influence of secondary compound complementarity and species diversity on consumption of Mediterranean shrubs by sheep. Appl. Anim. Behav. Sci. 107:58–65.

    Article  Google Scholar 

  • Schmidt, A., Bischof-Deichnik, C., and Stahl-Biskup, E. 2004. Essential oil polymorphism of Thymus praecox subsp arcticus on the British Isles. Biochem. Syst. Ecol. 32:409–421.

    Article  CAS  Google Scholar 

  • Schwartz, C. C., Nagy, J. G., and Regelin, W. L. 1980a. Juniper oil yield, terpenoid concentration, and anti-microbial effects on deer. J. Wildl. Manage. 44:107–113.

    Article  CAS  Google Scholar 

  • Schwartz, C. C., Regelin, W. L., and Nagy, J. G. 1980b. Deer preference for juniper forage and volatile oil treated foods. J. Wildl. Manage. 44:114–120.

    Article  Google Scholar 

  • Seregély, Z., and Novák, I. 2005. Evaluation of the signal response of the electronic nose measured on oregano and lovage samples using different methods of multivariate analysis. Acta Aliment. Hung. 34:131–139.

    Article  Google Scholar 

  • Sjödin, K., Persson, M., Borgkarlson, A. K., and Norin, T. 1996. Enantiomeric compositions of monoterpene hydrocarbons in different tissues of four individuals of Pinus sylvestris. Phytochemistry 41:439–445.

    Article  Google Scholar 

  • Squillace, A. E., Wells, O. O., and Rockwood, D. L. 1980. Inheritance of monoterpene composition in cortical oleoresin of loblolly pine. Silvae Genet. 29:141–151.

    Google Scholar 

  • Thoss, V., O’Reilly-Wapstra, J., and Iason, G. R. 2007. Assessment and implications of intraspecific and phenological variability in monoterpenes of Scots pine (Pinus sylvestris) foliage. J. Chem. Ecol. 33:477–491.

    Article  CAS  PubMed  Google Scholar 

  • Trapp, S., and Croteau, R. 2001. Defensive resin biosynthesis in conifers. Annu. Rev. Plant Physiol. 52:689–724.

    Article  CAS  Google Scholar 

  • Van Tien, D., Lynch, J. J., Hinch, G. N., and Nolan, J. V. 1999. Grass odor and flavor overcome feed neophobia in sheep. Small Rumin. Res. 32:223–229.

    Article  Google Scholar 

  • Végh, A. (ed.).1986. Pharmacopoea Hungarica. VII. ed., pp. 395–398. Medicina, Budapest.

  • Villalba, J. J., and Provenza, F. D. 2005. Foraging in chemically diverse environments: energy, protein, and alternative foods influence ingestion of plant secondary metabolites by lambs. J. Chem. Ecol. 31:123–138.

    Article  CAS  PubMed  Google Scholar 

  • Vokou, D., Douvli, P., Blionis, G. J., and Halley, J. M. 2003. Effects of monoterpenoids, acting alone or in pairs, on seed germination and subsequent seedling growth. J. Chem. Ecol. 29:2281–2301.

    Article  CAS  PubMed  Google Scholar 

  • Vosshall, L. B., Wong, A. M., and Axel, R. 2000. An olfactory sensory map in the fly brain. Cell 102:147–159.

    Article  CAS  PubMed  Google Scholar 

  • Vourc’h, G., Martin, J. L., Duncan, P., Escarre, J., and Clausen, T. P. 2001. Defensive adaptations of Thuja plicata to ungulate browsing: a comparative study between mainland and island populations. Oecologia 126:84–93.

    Article  Google Scholar 

  • Westoby, M. 1978. What are biological bases of varied diets. Am. Nat. 112:627–631.

    Article  Google Scholar 

  • Wibe, A., Borg-Karlson, A. K., Persson, M., Norin, T., and Mustaparta, H. 1998. Enantiomeric composition of monoterpene hydrocarbons in some conifers and receptor neuron discrimination of alpha-pinene and limonene enantiomers in the pine weevil, Hylobius abietis. J. Chem. Ecol. 24:273–287.

    Article  CAS  Google Scholar 

  • Yazdani, R., Rudin, D., Alden, T., Lindgren, D., Harbom, B., and Ljung, K. 1982. Inheritance pattern of five monoterpenes in Scots pine (Pinus sylvestris L.). Hereditas 97:261–272.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Zsolt Seregély for his contribution to the electronic nose measuring. We are also grateful to our referees for their useful comments. We thank Robyn Elisabeth Hudson for her linguistic revision on previous versions of the manuscript. We also thank the Kiskunság National Park for the support of our field surveys. During the manuscript preparation GM was supported by TÁMOP-4.2.1./B-09/1-KMR-2010-0005.

Author information

Authors and Affiliations

  1. Department of Ethology, Eötvös Loránd University, Pázmány Péter sétány 1/C, 1117, Budapest, Hungary

    Gábor Markó & Vilmos Altbäcker

  2. Department of Plant Pathology, Corvinus University of Budapest, Ménesi út 44, 1118, Budapest, Hungary

    Gábor Markó

  3. Department of Medicinal and Aromatic Plants, Corvinus University of Budapest, Villányi út 29-43, Budapest, 1118, Hungary

    Ildikó Novák & Jenő Bernáth

Authors
  1. Gábor Markó
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ildikó Novák
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jenő Bernáth
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vilmos Altbäcker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gábor Markó.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Markó, G., Novák, I., Bernáth, J. et al. Both Gas Chromatography and an Electronic Nose Reflect Chemical Polymorphism of Juniper Shrubs Browsed or Avoided by Sheep. J Chem Ecol 37, 705–713 (2011). https://doi.org/10.1007/s10886-011-9974-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-011-9974-8

Key Words

Search

Navigation