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Ontogenic development of chemical defense by seedling resin birch: Energy cost of defense production

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Abstract

Whether production of chemical defenses by plants is or is not an energetically costly process is an important, but unresolved, question in chemical ecology. We suggest studies of the ontogenetic development of plant defense systems can help resolve the question. As an example of this approach to the cost question, we explore the problems associated with production of immobile chemical defenses that defend juvenile resin birches against browsing by mammals. From this exploration we draw two conclusions: (1) Shortly after germination, production of chemical defenses by small-seeded species, such as birch, is energetically costly. (2) Opposing selection for defense versus competitive ability in the seedling stage of birch has resulted in a trade-off in allocation of carbon to production of immobile chemical defense versus allocation of carbon to production of storage reserves. We suggest this trade-off results in a large indirect cost of defense because carbon used for production of immobile chemical defenses is unavailable for support of growth in the future, but stored carbon can be used to support future growth.

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References

  • Basey, J.M., Jenkins, S.W., andBusher, P.E. 1988. Optimal central place foraging by beavers: Tree-size selection in relation to defensive chemicals of quaking aspen.Oecologia (Berlin) 76:278–282.

    Google Scholar 

  • Bazzaz, F.A., Chiariello, N.R., Coley, P.D., andPitelka, J.F. 1987. Allocating resources to reproduction and defense.BioScience 137:58–67.

    Google Scholar 

  • Bernays, E.A. 1994. Insect-Plant Interactions, Vol. 5. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Bloom, A.J., Chapin, F.S., III, andMooney, H.A. 1985. Resource limitation in plants—an economic analogy.Annu. Rev. Ecol. Syst. 16:363–392.

    Google Scholar 

  • Borchert, R. 1976. The concept of juvenility in woody plants.Acta Horitic. 56:21–35.

    Google Scholar 

  • Bowers, M.D., andStamp, N.E. 1993. Effects of plant age, genotype, and herbivory onPlantago performance and chemistry.Ecology 74:1778–1791.

    Google Scholar 

  • Bryant, J.P. 1981. Phytochemical deterrence of snowshoe hare browsing by adventitious shoots of four Alaskan trees.Science 313:889–890.

    Google Scholar 

  • Bryant, J.P. 1987. Feltleaf willow-snowshoe hare interactions: Plant carbon/nutrient balance and floodplain succession.Ecology 68:1319–1327.

    Google Scholar 

  • Bryant, J.P., Chapin, F.S., III, andKlein, D.R. 1983a. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory.Oikos 40:357–368.

    Google Scholar 

  • Bryant, J.P., Wieland, G.D., Reichardt, P.B., Lewis, V.E., andMcCarthy, M.C. 1983b. Pinosylvin methyl ether deters snowshoe hare feeding on green alder.Science 222:1023–1025.

    Google Scholar 

  • Bryant, J.P., Wieland, G.D., Clausen, T., andKuropat, P. 1985a. Interactions of snowshoe hares and feltleaf willow (Salix alaxensis) in Alaska.Ecology 66:1564–1573.

    Google Scholar 

  • Bryant, J.P., Chapin, F.S., III,Reichardt, P., andClausen, T. 1985b. Adaptation to resource availability as a determinant of chemical defense strategies in woody plants.Recent Adv. Phytochem. 19:219–237.

    Google Scholar 

  • Bryant, J.P., Tahvanainen, J., Sulkinoja, M., Julkunen-Tiitto, R., Reichardt, P., andGreen, T. 1989. Biogeographic evidence for the evolution of chemical defense by boreal birch and willow against mammalian browsing.Am. Nat. 134:20–34.

    Google Scholar 

  • Bryant, J.P., Kuropat, P.J., Reichardt, P.B., andClausen, T.P. 1991. Controls over the allocation of resources by woody plants to chemical antiherbivore defense, pp. 83–102,in R.T. Palo and C.T. Robbins (eds.). Plant Defense Against Mammalian Herbivory. CRC Press. Boca Raton, Florida.

    Google Scholar 

  • Bryant, J.P., Reichardt, P.B., Clausen, T.P., Provenza, F.D., andKuropat, P.J. 1992. Woody plant-mammal interactions, pp. 344–371,in G.A. Rosenthal and M.R. Berenbaum (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites, Vol. II, 2nd ed., Ecological and Evolutionary Processes. Academic Press, New York.

    Google Scholar 

  • Bryant, J.P., Swihart, R.K., Reichardt, P.B., andNewton, L. 1994. Biogeography of woody plant chemical defense against snowshoe hare browsing: Comparison of Alaska and eastern North America.Oikos 70:385–395.

    Google Scholar 

  • Chapin, F.S., III,Schulze, E., andMooney, H.A.. 1990. The ecology and economics of storage in plants.Annu. Rev. Ecol. Syst. 21:423–447.

    Google Scholar 

  • Clausen, T.P., Bryant, J.P., andReichardt, P.B. 1986. Defense of winter-dormant green alder against snowshoe hares.J. Chem. Ecol. 12:2117–2131.

    Google Scholar 

  • Coley, P.D. 1983. Herbivory and defensive characteristics of tree species in a lowland tropical forest.Ecol. Monogr. 53:209–233.

    Google Scholar 

  • Coley, P.D., Bryant, J.P., andChapin, F.S., III. 1985. Resource availability and plant antiherbivore defense.Science 230:895–899.

    Google Scholar 

  • Danell, K., Elmqvist, T., Ericson, L., andSalmonson, A. 1987. Are there general patterns in bark-eating voles on different shoot types from woody plants.Oikos 50:396–402.

    Google Scholar 

  • Danell, K., Bergstrom, R., andDirke, K. 1990. Moose browsing on juvenile and adult birches (Betula pendula andBetula pubescens): Test of a hypothesis on chemical defense. Proceedings. International Union of Game Biologists, Vyoske Tatary, Strbske, Pleso, USSR.

    Google Scholar 

  • Dimock, E.J., II. 1974. Animal resistant Douglas-fir: How likely and how soon? pp. 95–101,in H.C. Black (ed.). Wildlife and Forest Management in the Pacific Northwest. Forest Research Laboratory School of Forestry, Oregon State University, Corvallis, Oregon.

    Google Scholar 

  • Dimock, E.J., II,Silen, R.R., andAllen, V.E. 1976. Genetic resistance in Douglas-fir to damage by snowshoe hare and black-tailed deer.For. Sci. 22:106–121.

    Google Scholar 

  • Ehrlich, P.R., andRaven, P.H. 1964. Butterflies and plants: A study in coevolution.Evolution 18:586–608.

    Google Scholar 

  • Feeny, P. 1976. Plant apparency and chemical defense, pp. 1–40,in W.J. Wallace and R.L. Mansell (eds.). Biochemical Interactions between Plants and Insects. Plenum, New York.

    Google Scholar 

  • Feeny, P. 1992. The evolution of chemical ecology: Contributions from the study of herbivorus insects, pp. 1–44,in G.A. Rosenthal and M.R. Berenbaum (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites, Vol. II, 2nd ed., Ecological and Evolutionary Processes. Academic Press, New York.

    Google Scholar 

  • Gershenzon, J. 1994. The cost of plant chemical defense against herbivory: A biochemical perspective, pp. 205–173,in E.A. Bernays (ed.). Insect-Plant Interactions, Vol. 5. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Gulmon, S.L., andMooney, H.A. 1986. Costs of defense on plant productivity, pp. 681–698,in T.J. Givnish and R. Robichaux (eds.). On the Economy of Plant Form and Function. Cambridge University Press, Cambridge, England.

    Google Scholar 

  • Harper, J.L. 1977. Population Biology of Plants. Academic Press, London, England.

    Google Scholar 

  • Hay, M.E., andFenical, W. 1988. Marine plant-herbivore interactions: The ecology of chemical defense.Annu. Rev. Ecol. Syst. 19:111–145.

    Google Scholar 

  • Hay, M.E., andSteinberg, P.D. 1992. The chemical ecology of plant-herbivore interactions in marine versus terrestrial ecosystems, pp. 372–414,in G.A. Rosenthal and M.R. Berenbaum (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites, Vol. II, 2nd ed., Ecological and Evolutionary Processes. Academic Press, New York.

    Google Scholar 

  • Herms, D.A., andMattson, W.J. 1992. The dilemma of plants: To grow or defend.Q. Rev. Biol. 67:283–335.

    Google Scholar 

  • Huntly, N. 1991. Herbivores and the dynamics of communities and ecosystems.Annu. Rev. Ecol. Syst. 22:477–503.

    Google Scholar 

  • Ingestad, T. 1962. Macro element nutrition of pine, spruce and birch seedlings in nutrient solutions.Medd. Statens Skogsf-Inst. 51:1–150.

    Google Scholar 

  • Ingestad, T. 1970. A definition of optimum nutrient requirements in birch seedlings.I. Physiol. Plant. 23:1127–1128.

    Google Scholar 

  • Ingestad, T. 1971. A definition of optimum nutrient requirements in birch seedlings. II.Physiol. Plant. 24:118–125.

    Google Scholar 

  • Ingestad, T. 1979. Nitrogen stress in birch seedlings II: N, K, P, Ca, and Mg nutrition.Physiol. Plant. 45:149–157.

    Google Scholar 

  • Ingestad, T., andAgren, G.T. 1991. The influence of plant nutrition on biomass allocation.Ecol. Appl. 2:168–174.

    Google Scholar 

  • Ingestad, T., andLund, A. 1979. Nitrogen stress in birch seedlings: I. Growth technique and growth.Physiol. Plant. 45:137–148.

    Google Scholar 

  • Ingestad, T., andMcDonald, A.J.S. 1989. The influence of photon flux density on nutrition and growth of birch seedlings at different relative nitrogen addition rates.Physiol. Plant. 45:137–148.

    Google Scholar 

  • Jachmann, H. 1989. Food selection by elephants in the “Miombo” biome in relation to leaf chemistry.Biochem. Syst. Ecol. 17:15–24.

    Google Scholar 

  • Karban, R. 1993. Costs and benefits of induced resistance and plant density.Ecology 74:9–19.

    Google Scholar 

  • Kearsely, M.J.C., andWhitham, T.G. 1989. Developmental changes in resistance in herbivory: implications for individuals and populations.Ecology 70:1040–1047.

    Google Scholar 

  • Knight, T.A. 1795.Phil. Trans. 85:290–295.

    Google Scholar 

  • Kozlowski, T.T. 1971. Growth and Development of Trees, Vol. 1. Academic Press, New York.

    Google Scholar 

  • Kozlowski, T.T., andKeller, T. 1966. Food relations of woody plants.Bot. Rev. 22:293–382.

    Google Scholar 

  • Langenheim, J.H., andStubblebine, W.H. 1983. Variation in leaf resin composition between parent tree and progeny inHymenaea: Implications for herbivory in humid tropics.Bicohem. Syst. Ecol. 11:97–106.

    Google Scholar 

  • Lapinjoki, S.P., Elo, H.A., andTaipale, H.T. 1991. Development and structure of resin glands on tissues ofBetula pendula Roth. during growth.New Phytol. 117:219–223.

    Google Scholar 

  • Libby, W.J., andHood, J.V. 1976. Juvenility in hedged radiata pine.Acata Hortic. 56:91–98.

    Google Scholar 

  • Lorio, P.L. 1986. Growth-differentiation balance: a basis for understanding southern pine beetletree interactions.For. Ecol. Manage. 14:259–273.

    Google Scholar 

  • Macedo, C.A., andLangenheim, J.H. 1989. Microlepidopteran herbivory in relation to leaf sesquiterpenes inCopifera langsdorfii adult trees and their seedling progeny in a Brazilian woodland.Biochem. Syst. Ecol. 17:217–224.

    Google Scholar 

  • Palo, R.T., andRobbins, C.T. 1991. Plant Defense against Mammalian Herbivory. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Reichardt, P.B. 1981. Papyriferic acid: A triterpenoid from Alaskan paper birch.J. Org. Chem. 46:1576–1578.

    Google Scholar 

  • Reichardt, P.B., Bryant, J.P., Clausen, T.P., andWieland, G. 1984. Defense of winter-dormant Alaska paper birch against Snowshoe hare.Oecologia (Berlin) 65:58–59.

    Google Scholar 

  • Reichardt, P.B., Bryant, J.P., Mattes, B.R., Clausen, T.P., Chapin, F.S., III, andMeyer, M. 1990. The winter chemical defense of balsam poplar against snowshoe hares.J. Chem. Ecol. 16:1941–1959.

    Google Scholar 

  • Rhoades, D.F. 1979. Evolution of plant chemical defense against herbivores, pp. 4–48,in G.A. Rosenthal and D.H. Janzen (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites. Academic Press, New York.

    Google Scholar 

  • Rhoades, D.F., andCates, R.G. 1976. Toward a general theory of plant antiherbivore chemistry, pp. 168–213,in J.W. Wallace and R.L. Mansell (eds.). Biochemical Interactions between Plants and Insects. Plenum, New York.

    Google Scholar 

  • Roitberg, B.D., andIsman, M.B. 1992. Insect Chemical Ecology: An Evolutionary Approach. Chapman & Hall, New York.

    Google Scholar 

  • Rousi, M. 1990. Breeding forest trees for resistance to mammalian herbivores—a study based on European white birch.Acta For. Fenn. 210:1–20.

    Google Scholar 

  • Rousi, M., Tahvanainen, J., andUotila, I. 1991. Mechanism of resistance to hare browsing in winter-dormant silver birch (Betula pendula).Am. Nat. 137:64–82.

    Google Scholar 

  • Rousi, M., Tahvanainen, J., Henttonen, H., andUotila, I. 1993. Effects of shading and fertilization on resistance of winter-dormant birch (Betula pendula) to voles and hares.Ecology 74:30–38.

    Google Scholar 

  • Sax, K. 1962. Aspects of aging in plants.Annu. Rev. Plant. Physiol. 13:489–506.

    Google Scholar 

  • Schaffalitzky de Muckadell, M. 1954. Juvenile stages in woody plants.Physiol. Plant. 7:782–796.

    Google Scholar 

  • Schaffalitzky de Muckadell, M. 1969. Environmental factors in developmental stages of trees, pp. 289–298,in T.T. Kozlowski (ed.). Tree Growth, Ronald Press, New York.

    Google Scholar 

  • Scriber, J.M., andAyers, M.P. 1988. Leaf chemistry as a defense against insects. Atlas of science:Plants and Animals. 1:117–123.

    Google Scholar 

  • Seigler, D., andPrice, P.W. 1976. Secondary compounds in plants: Primary functions.Am. Nat. 110:101–105.

    Google Scholar 

  • Simms, E.L. 1992. Costs of plant resistance to herbivory, pp. 392–425,in R.S. Fritz and E.L. Simms (eds.). Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics. University of Chicago Press, Chicago.

    Google Scholar 

  • Simms, E.L., andRausher, M.D. 1987. Costs and benefits of plant defense to herbivory.Am. Nat. 130:570–581.

    Google Scholar 

  • Simms, E.L., andRausher, M.D. 1989. The evolution of resistance to herbivory inIpomoea purpurea. II. Natural selection by insects and costs of resistance.Evolution 43:573–585.

    Google Scholar 

  • Sinclair, A.R.E., Jogia, M.K., andAnderson, R.J. 1988. Camphor from juvenile white spruce as an antifeedent for snowshoe hares.J. Chem. Ecol. 14:1505–1514.

    Google Scholar 

  • Swihart, R.K., Bryant, J.P., andNewton, L. 1994. Latitudinal patterns in consumption of woody plants by snowshoe hares in the eastern United States.Oikos 70:427–434.

    Google Scholar 

  • Tahvanainen, J., Helle, E., Julkunen-Tiitto, R., andLavola, A. 1985. Phenolic compounds of willow bark as deterrents against feeding by mountain hare.Oecologia (Berlin) 65:319–323.

    Google Scholar 

  • Taipale, H.T., andLapinjoki, S.P. 1992. Use of evaporative light scattering mass detection in high performance liquid chromatography of triterpenes in the bark resin ofBetula species. Phytochem. Anal. 2:84–86.

    Google Scholar 

  • Tilman, D. 1982. Resource Competition and Community Structure. Princeton University Press, Princeton.

    Google Scholar 

  • Vainiotalo, P., Julkunen-Tiitto, R., Juntheikki, M.R., Reichardt, P., andAuriola, S. 1991. Chemical characteristics of herbivore defenses inBetula pendula winter-dormant young stems.J. Chromatogr. 547:367–376.

    Google Scholar 

  • Wagner, M.R. 1988. Induced defenses in ponderosa pine against defoliating insects, pp. 141–156,in W.J. Mattson, J. Levieux, and C. Bernard-Dagen (eds.). Mechanisms of Woody Plant Defenses Against Insects; Search for a Pattern. Springer-Verlag, New York.

    Google Scholar 

  • Waring, P.F. 1959. Problems of juvenility and flowering in trees.J. Linn. Soc. London, Bot. 56:282–289.

    Google Scholar 

  • Watkinson, A.R. 1986. Plant population dynamics, pp. 137–184,in M.J. Crawley (ed.). Plant Ecology. Blackwell Scientific, Oxford, England.

    Google Scholar 

  • Zangeri, A.R., andBazzaz, F.A. 1992. Theory and pattern in plant defense allocation, pp. 363–392,in R.S. Fritz and E.L. Simms (ed.). Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics. University of Chicago Press, Chicago.

    Google Scholar 

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Bryant, J.P., Julkunen-Tiitto, R. Ontogenic development of chemical defense by seedling resin birch: Energy cost of defense production. J Chem Ecol 21, 883–896 (1995). https://doi.org/10.1007/BF02033796

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