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Journal of Chemical Ecology

, Volume 36, Issue 5, pp 461–466 | Cite as

Dynamics of the Volatile Defense of Winter “Dormant” Balsam Poplar (Populus balsamifera)

  • Thomas P. ClausenEmail author
  • Janice Chen
  • John P. Bryant
  • Frederick D. Provenza
  • Juan Villalba
Article

Abstract

6-Hydroxycylohex-2-en-1-one (6-HCH) has been reported as a major chemical defense of the winter-dormant internodes of balsam poplar (Populus balsamifera) against feeding by herbivores such as the snowshoe hare (Lepus americanus). We report that the concentration of 6-HCH in the fall internodes is triggered by a single hard frost, and then undergoes an exponential decline through volatilization over the winter that results in barely detectable quantities by early spring. We conclude that the role of 6-HCH in the defense of mature balsam poplar is more complex than simply acting as a toxin. Rather, 6-HCH’s role as a defensive agent must evolve over the course of the winter from being a co-toxin to a cue for a conditioned flavor aversion (CFA) to finally having no role by late spring.

Keywords

Balsam poplar Populus balsamifera Snowshoe hare 6-HCH Conditioned flavor aversion Salicortin Plant defense 

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References

  1. Ayres, M. P., Clausen, T. P., MacLean, S. F., Redman, A. M., and Reichardt, P. B. 1997. Diversity of structure and antiherbivore activity in condensed tannins. Ecology 78:1696–1712.CrossRefGoogle Scholar
  2. Bookhout, T. A. 1965. The snowshoe hare in Upper Michigan and its biology and feeding coactions with white-tailed deer. Mich. Dept. Conserv. Res. Develop. Rep. No. 38, 198pp.Google Scholar
  3. Bryant, J. P. 1981a. Phytochemical deterrence of snowshoe hare browsing by Adventitious shoots of 4 Alaskan trees. Science 213:889–890.CrossRefPubMedGoogle Scholar
  4. Bryant, J.P. 1981b. The regulation of snowshoe hare feeding behavior during winter by plant antiherbivore chemistry, pp. 720–731, in K. Meyers and C. D. MacInnes (eds). Proceedings 1st International Lagomorph Conference, Guelph Univ., Canada.Google Scholar
  5. Clausen, T. P., Reichardt, P. B., Bryant, J. P., Werner, R. A., Post, K., and Frisby, K. 1989. A chemical model for short-term induction in quaking aspen (Populus tremuloides) foliage against herbivores. J. Chem. Ecol. 15:2335–2346.CrossRefGoogle Scholar
  6. Clausen, T. P., Keller, J. W., and Reichardt, P. B. 1990. Aglycon fragmentation accompanies β-glucosidase catalyzed hydrolysis of salicortin, a naturally occurring phenol glycoside. Tetrahedron Lett. 31:4537–4538.CrossRefGoogle Scholar
  7. Clausen, T. P., Reichardt, P. B., Bryant, J. P., and Sinclair, T. 1992. The chemical defense of winter-dormant balsam poplar: a clarification. J. Chem. Ecol. 18:1505–1510.CrossRefGoogle Scholar
  8. du Toit, J. T., Provenza, F. D., and Nastis, A. S. 1991. Conditioned taste aversions: how sick must a ruminant get before it detects toxicity in foods? Appl. Anim. Behav. Sci. 30:35–46.CrossRefGoogle Scholar
  9. Haruta, M., Pedersen, J.A., Jens, A., and Constabel, C.P. 2001. Polyphenol oxidase and herbivore defense in trembling aspen (Populus tremuloides): cDNA cloning, expression, and potential substrates. Physiol. Plant. 112:552–558.CrossRefPubMedGoogle Scholar
  10. Hemming, J. D. C., and Lindroth, R. L. 2000. Effects of phenolic glycosides and protein on gypsy moth (Lepidoptera: lymantriidae) and forest tent caterpillar (Lepidoptera: lasiocampidae) performance and detoxification activities. Environ. Entomol. 29:1108–1115.CrossRefGoogle Scholar
  11. Jianjun, Z., Withers, S. G., Reichardt, P. B., Treadwell, E., and Clausen, T. P. 1998. Salicortin: a repeat-attack new-mechanism-based Agrobacterium faecalis β-glucosidase inhibitor. Biochem. J. 332:367–371.Google Scholar
  12. Jogia, M. K., Sinclair, A. R. E., and Andersen, R. J. 1989. An antifeedant in balsam poplar inhibits browsing by snowshoe hares. Oecologia 79:189–192.CrossRefGoogle Scholar
  13. Julkunen-Tiitto, R., and Sorsa, S. 2001. Testing the effects of drying methods on willow flavonoids, tannins, and salicylates. J. Chem. Ecol. 27:779–789.CrossRefPubMedGoogle Scholar
  14. Julkunen-Tiitto, R., and Tahvanainen, J. 1989. The effect of the sample preparation method of extractable phenolics of Salicaceae species. Planta Med. 55:55–58.CrossRefPubMedGoogle Scholar
  15. Julkunen-Tiitto, R., Hakulinen, J., and Meier, B. 1994. The response of growth and secondary metabolism to Melampsora rusts in field cultivated willow (Salix) clones. Acta Hortic. 381:679–682.Google Scholar
  16. Kelly, M. T., and Curry, J. P. 1991. The influence of phenolic compounds on the suitability of three Salix species as host for the willow beetle. Ent. Exper. Appl. 61:25–32.CrossRefGoogle Scholar
  17. Kleiner, K. W., Ellis, D. D., McCown, B. H., and Raffa, K. F. 2003. Leaf ontogeny influences leaf phenolics and the efficacy of genetically expressed bacillus thruinglensis crylA(α) d-endotoxin in hybrid poplar against gypsy moth. J. Chem. Ecol. 29:2585–2602.CrossRefPubMedGoogle Scholar
  18. Launchbaugh, K. L., and Provenza, F. D. 1993. Can plants practice mimicry to avoid grazing by mammalian herbivores? Oikos 66:501–504.CrossRefGoogle Scholar
  19. Lawler, I. R., Foley, W. J., Eschler, B. M., Pass, D. M., and Handasyde, K. 1998. Intraspecific variation in Eucalyptus secondary metabolites determines food intake by folivorous marsupials. Oecologia 116:160–169.CrossRefGoogle Scholar
  20. Lawler, I. R., Stapley, J., Foley, W. J., and Eschler, B. M. 1999. Ecological example of conditioned flavor aversion in plant–herbivore interactions: effect of terpenes of Eucalyptus leaves on feeding by common ringtail and brushtail possums. J. Chem. Ecol. 25:401–415.CrossRefGoogle Scholar
  21. Lindroth, R. L., and Koss, P. A. 1996. Preservation of Salicaceae leaves for phytochemical analyses: further assessment. J. Chem. Ecol. 22:765–771.CrossRefGoogle Scholar
  22. Lindroth, R. L., Scriber, J. J., and Hsia, S. M. T. 1988. Chemical ecology of the tiger swallowtail: mediation of host use by phenolic glycosides. Ecology 69:814–822.CrossRefGoogle Scholar
  23. Mattes, B. R., Clausen, T. P., and Reichardt, P. B. 1987. Volatile constituents of balsam poplar: the phenol glycoside connection. Phytochemistry 26:1361–1366.CrossRefGoogle Scholar
  24. Mitchelson, F. 1992. Pharmacological agents affecting emesis: a review (part I). Drugs 43:295–315.CrossRefPubMedGoogle Scholar
  25. Miyoshi, H., Pedersen, J. A., and Constabel, P. C. 2001. Polyphenol oxidase and herbivore defense in trembling aspen (Populus tremuloides): cDNA cloning, expression, and potential substrates. Physiol. Plant. 112:552–558.CrossRefGoogle Scholar
  26. Moore, B. D., Wallis, I. R., Palá-Paứl, Brophy, J. J., Willis, R. H., and Foley, W. J. 2004. Antiherbivore chemistry of Eucalyptus—cues and deterrents for marsupial folivores. J. Chem. Ecol. 9:1743–1769.Google Scholar
  27. Moore, B. D., Foley, W. J., Wallis, I. R. Cowling, A., and Handasyde, K. A. 2005. Eucalyptus foliar chemistry explains selective feeding by koalas. Biol. Lett. 1:64–67.CrossRefPubMedGoogle Scholar
  28. Orians, C. M. 1995. Preserving leaves for tannin and phenolic glycoside analyses: a comparison of methods using three willow taxa. J. Chem. Ecol. 21:1235–1243.CrossRefGoogle Scholar
  29. Pease, J. L, Vowles, R. H., and Keith, L. B. 1979. Interaction of snowshoe hares and woody vegetation. J. Wildl. Manage. 43:43–60.CrossRefGoogle Scholar
  30. Provenza, F. D. 1995. Postingestive feedback as an elementary determinant of food preference and intake in ruminants. J. Range Manag. 48:2–17.CrossRefGoogle Scholar
  31. Provenza, F. D. 1996. Acquired aversions as the basis for varied diets of ruminants foraging on rangelands. J. Anim. Sci. 74:2010–2020.PubMedGoogle Scholar
  32. Provenza, F. D., Burritt, E. A., Clausen, T. P., Bryant, J. P., Reichardt, P. B., and Distel, R. A. 1990. Conditioned flavor aversion: a mechanism for goats to avoid condensed tannins in blackbrush. Am. Nat. 136:810–828.CrossRefGoogle Scholar
  33. Provenza, F. D., Ortega-Reyes, L., Scott, C. B., Lynch, J. J., and Burrit, E. A. 1994. Antiemetic drugs attenuate food aversions in sheep. J. Anim. Sci. 72:1989–1994.PubMedGoogle Scholar
  34. Provenza, F. D., Kimball, B. R., and Villalba, J. J. 2000. Roles of odor, taste, and toxicity in the food preferences of lambs. Oikos 88:424–432.CrossRefGoogle Scholar
  35. Reichardt, P. B., Clausen, T. P., and Bryant, J. P. 1988. Phenol glycosides in plant defense against herbivores, pp. 130–142, in H. G. Cutler (ed.). Biologically Active Natural Products. Potential in Agriculture. ACS Symposium Series, vol. 380. Washington, D.C.Google Scholar
  36. Reichardt, P. B., Bryant, J. B., Mattes, B. R., Clausen, T. P., Chappin, F. S. III, and Meyer, M. 1990. The winter chemical defense of Alaskan balsam poplar against snowshoe hares. J. Chem. Ecol. 16:1941–1960.CrossRefGoogle Scholar
  37. Ruuhola, T., Tikkanen, O., and Tahvanainen, J. 2001. Differences in host use efficiency of larvae of a generalist moth, Operophtera brumata on three chemically divergent Salix species. J. Chem. Ecol. 27:1595–1615.CrossRefPubMedGoogle Scholar
  38. Ruuhola, T., Julkunen-Tiitto, R., and Vainiotalo, P. 2003. In vitro degradation of willow salicylates. J. Chem. Ecol. 29:1083–1097.CrossRefPubMedGoogle Scholar
  39. Schmitz, O. J., Hik, D. S., and Sinclair, A. R. E. 1992. Plant chemical defense and twig selection by snowshoe hare: an optimal foraging perspective. Oikos 65:295–300.CrossRefGoogle Scholar
  40. Sinclair, A. R. E., and Smith, J. N. M. 1984. Do plant secondary compounds determine feeding preferences of snowshoe hares? Oecologia (Berl.) 61:403–410.CrossRefGoogle Scholar
  41. Stolter, C., Ball, J. P., Julkunen-Tiitto, R., Lieberei, R., and Ganzhorn, J. U. 2009. Winter browsing of moose on two different willow species: food selection in relation to plant chemistry and plant response. Can. J. Zool. 83:807–819.CrossRefGoogle Scholar
  42. Tahvanainen, J., Helle, E., Julkunen-Tiitto, and Lavola, A. 1985. Phenolic compounds of willow bark as deterrents against feeding by mountain hare. Oecologia 65:319–323.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Thomas P. Clausen
    • 1
    Email author
  • Janice Chen
    • 2
  • John P. Bryant
    • 3
  • Frederick D. Provenza
    • 4
  • Juan Villalba
    • 4
  1. 1.Department of Chemistry & BiochemistryUniversity of Alaska FairbanksFairbanksUSA
  2. 2.Department of PsychologyStanford UniversityStanfordUSA
  3. 3.Institute of Arctic BiologyUniversity of Alaska FairbanksFairbanksUSA
  4. 4.Department of Wildland ResourcesUtah State UniversityLoganUSA

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