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

Journal of Chemical Ecology

Volumn 37, Issue 7, 2011, Pages 705-713

  Markó, Gábor ^a,b   Novák, Ildikó ^b   Bernáth, Jeno ^b   Altbäcker, Vilmos ^a  

^a EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^b Institute of Entrepreneurship and Innovation   (Hungary)

Author keywords

pinene; 3 carene; Chemical polymorphism; Chemotype; Electronic nose; Essential oil; Gas chromatography flame ionization detection (GC FID); Juniperus communis; Odor; Ovis aries; Sheep

Indexed keywords

ALPHA-PINENE; BICYCLO COMPOUND; DELTA(3) CARENE; DELTA(3)-CARENE; ESSENTIAL OIL; PINENE; SABINENE; TERPENE;

ANTIHERBIVORE DEFENSE; BIOCHEMICAL COMPOSITION; BROWSING; CHEMICAL DEFENSE; CHEMICAL ECOLOGY; ESSENTIAL OIL; GAS CHROMATOGRAPHY; MONOTERPENE; ODOR; PLANT-HERBIVORE INTERACTION; POLYMORPHISM; SECONDARY METABOLITE; SHEEP; SHRUB; SURVIVAL; TOXIN;

ANIMAL; ARTICLE; CHEMISTRY; FEEDING BEHAVIOR; GAS CHROMATOGRAPHY; INSTRUMENTATION; JUNIPERUS; METABOLISM; PHYSIOLOGY; SHEEP;

ANIMALS; BICYCLO COMPOUNDS; CHROMATOGRAPHY, GAS; FEEDING BEHAVIOR; JUNIPERUS; MONOTERPENES; OILS, VOLATILE; SHEEP, DOMESTIC;

JUNIPERUS; JUNIPERUS COMMUNIS; MAMMALIA; OVIS ARIES;

EID: 79959699572     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-011-9974-8     Document Type: Article

References (81)

1. Adams, R. P. 1998. The leaf essential oils and chemotaxonomy of Juniperus sect. Juniperus. Biochem. Syst. Ecol. 26: 637-645.
2. 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.
3. 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.
4. 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.
5. 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.
6. 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.
7. Augner, M., Provenza, F. D., and Villalba, J. J. 1998. A rule of thumb in mammalian herbivores? Anim. Behav. 56: 337-345.
8. 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.
9. Bakkali, F., Averbeck, S., Averbeck, D., and Waomar, M. 2008. Biological effects of essential oils-a review. Food Chem. Toxicol. 46: 446-475.
10. Berec, L. 2000. Mixed encounters, limited perception and optimal foraging. Bull. Math. Biol. 62: 849-868.
11. Bryant, J. P., Reichardt, P., and Clausen, T. 1985. Plant carbon/nutrient balance-implications for chemical defense. Abstr. Pap. Am. Chem. Soc. 190: 91.
12. Buck, L., and Axel, R. 1991. A novel multigene family may encode odorant receptors-a molecular-basis for odor recognition. Cell 65: 175-187.
13. 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.
14. 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.
15. 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.
16. Cleland, T. A., Morse, A., Yue, E. L., and Linster, C. 2002. Behavioral models of odor similarity. Behav. Neurosci. 116: 222-231.
17. Dearing, M. D., Mangione, A. M., and Karasov, W. H. 2000. Diet breadth of mammalian herbivores: nutrient versus detoxification constraints. Oecologia 123: 397-405.
18. 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.
19. Eisner, T., and Grant, R. P. 1981. Toxicity, odor aversion, and olfactory aposematism. Science 213: 476-476.
20. 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.
21. 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.
22. 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.
23. 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.
24. 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.
25. 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.
26. 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.
27. Freeland, W. J., and Janzen, D. H. 1974. Strategies in herbivory in mammals: the role of plant secondary compounds. Am. Nat. 110: 269-289.
28. Friedman, L., and Miller, J. G. 1971. Odor incongruity and chirality. Science 172: 1044-1046.
29. 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.
30. Hiltunen, R. 1975. Variation and inheritance of some monoterpenes in Pinus sylvestris. Planta Med. 28: 315-323.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. Kinloch, B. B., Westfall, R. D., and Forrest, G. I. 1986. Caledonian Scots pine: origins and genetic structure. New Phytol. 104: 703-729.
38. 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.
39. 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.
40. 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.
41. 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.
42. Lledo, P. M., Gheusi, G., and Vincent, J. D. 2005. Information processing in the mammalian olfactory system. Physiol. Rev. 85: 281-317.
43. 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.
44. 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.
45. 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.
46. 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.
47. 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.
48. 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.
49. 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.
50. 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.
51. 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.
52. 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.
53. 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.
54. Orav, A., Kailas, T., and Koel, M. 1997. Chemometric analysis of conifer needle oils. Proc. Est. Acad. Sci. Chem. 46: 3-10.
55. Pearce, T. C. 1997a. Computational parallels between the biological olfactory pathway and its analogue 'The Electronic Nose'.1. Biological olfaction. Biosystems 41: 43-67.
56. 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.
57. Provenza, F. D. 1995. Postingestive feedback as an elementary determinant of food preference and intake in ruminants. J. Range Manage. 48: 2-17.
58. Provenza, F. D. 1996. Acquired aversions as the basis for varied diets of ruminants foraging on rangelands. J. Anim. Sci. 74: 2010-2020.
59. 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.
60. 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.
61. 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.
62. 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.
63. 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.
64. 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.
65. 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.
66. 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.
67. 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.
68. 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.
69. 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.
70. 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.
71. 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.
72. Trapp, S., and Croteau, R. 2001. Defensive resin biosynthesis in conifers. Annu. Rev. Plant Physiol. 52: 689-724.
73. 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.
74. Végh, A. (ed.). 1986. Pharmacopoea Hungarica. VII. ed., pp. 395-398. Medicina, Budapest.
75. 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.
76. 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.
77. Vosshall, L. B., Wong, A. M., and Axel, R. 2000. An olfactory sensory map in the fly brain. Cell 102: 147-159.
78. 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.
79. Westoby, M. 1978. What are biological bases of varied diets. Am. Nat. 112: 627-631.
80. 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.
81. 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.