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Variação de terpenos em Hyptis suaveolens e seu papel na defesa contra herbívoros

The role of terpene variation in Hyptis suaveolens in the defense against herbivores

Resumos

Acompanhou-se o desenvolvimento de populações de Hyptis suaveolens (L.) Poit. (Labiatae) em três localidades paulistas: Horto Florestal de Sumaré, Câmpus da UNICAMP (Campinas) e Fazenda Santa Genebra (Distrito de Barão Geraldo, Campinas), em 1981-83. Em cada local, escolheu-se uma população exposta à luz e outra, à sombra, com o objetivo de verificar em que fase do ciclo de vida as populações se tornavam mais suscetíveis ao ataque de herbívoros; de estimar a abundância dos herbívoros naturais e seus efeitos nas populações e a conseqüência da variação química dos monoterpenos que nelas ocorrem sobre os herbívoros. As populações tornavam-se mais suscetíveis aos herbívoros no período que antecedia a floração. Não se observou forte ataque de herbívoros nessa fase, embora se apresentassem em maior densidade. Os resultados sugerem que a variação na composição química possa afetar o desenvolvimento de herbívoros generalistas. No entanto, o Pyrausta insignatalis Guenée (Lep.-Pyralidae-Pyraustinae), provavelmente bem adaptado à planta, parece não ter sido afetado por esses terpenos. Não se detectaram diferenças entre populações expostas ao sol ou à sombra. Tais resultados apóiam a idéia de que a variabilidade química dentro de populações vegetais é importante estratégia de defesa contra herbívoros, dificultando-lhes a especialização.

Hyptis suaveolens; herbivoria; variabilidade genética


Populations of Hyptis suaveolens (L.) Poit. (Labiatae) were accompanied during their development in three sites: Horto Florestal de Sumaré, Campus of UNICAMP (Campinas), and Fazenda Santa Genebra (Distrito de Barão Geraldo, Campinas), all in the State of São Paulo, Brazil, from 1981 through 1983. At each site, a population exposed to full sunlight and another in the shade were studied. The objective was to evaluate, during plant development, the period when they were more susceptible to attack by herbivores; to consider the abundance of herbivores, and the role of variation in the chemistry of monoterpenes in the development of herbivores. Populations were more susceptible to attack by herbivores in the period preceding flowering. Heavy herbivore damage was not detected during this period, in spite of higher herbivore densities. The results suggest that the variation in chemical composition probably has an effect on the development of generalist herbivores. On the other hand, Pyrausta insignatalis Guenée (Lep.-Pyralidae-Pyraustinae) is probably well adapted to the plant and appears to be resistent to the terpenes. Differences in chemistry and differences in protection against herbivores were not observed between populations in sunny and shady sites. The results support an important role for genetic variability in populations in protection against herbivory and inhibition of specialization.

Hyptis suaveolens; herbivory; genetic variability


I. FITOQUÍMICA E FISIOLOGIA VEGETAL

Variação de terpenos em Hyptis suaveolens e seu papel na defesa contra herbívoros1 1 Parte da Tese de Mestrado do primeiro autor.

The role of terpene variation in Hyptis suaveolens in the defense against herbivores

Rachel Benetti Queiroz-VoltanI; William Henry StubblebineII; George ShepherdIII

ISeção de Botânica Econômica, Instituto Agronômico, Caixa Postal 28, 13001-970 Campinas (SP)

II6001 Shelter Bay Avenue, New Valley, California CA 94941, USA

IIIDepartamento de Botânica, Instituto de Biologia, Universidade Estadual de Campinas, Caixa Postal 6109, 13081 Campinas (SP)

RESUMO

Acompanhou-se o desenvolvimento de populações de Hyptis suaveolens (L.) Poit. (Labiatae) em três localidades paulistas: Horto Florestal de Sumaré, Câmpus da UNICAMP (Campinas) e Fazenda Santa Genebra (Distrito de Barão Geraldo, Campinas), em 1981-83. Em cada local, escolheu-se uma população exposta à luz e outra, à sombra, com o objetivo de verificar em que fase do ciclo de vida as populações se tornavam mais suscetíveis ao ataque de herbívoros; de estimar a abundância dos herbívoros naturais e seus efeitos nas populações e a conseqüência da variação química dos monoterpenos que nelas ocorrem sobre os herbívoros. As populações tornavam-se mais suscetíveis aos herbívoros no período que antecedia a floração. Não se observou forte ataque de herbívoros nessa fase, embora se apresentassem em maior densidade. Os resultados sugerem que a variação na composição química possa afetar o desenvolvimento de herbívoros generalistas. No entanto, o Pyrausta insignatalis Guenée (Lep.-Pyralidae-Pyraustinae), provavelmente bem adaptado à planta, parece não ter sido afetado por esses terpenos. Não se detectaram diferenças entre populações expostas ao sol ou à sombra. Tais resultados apóiam a idéia de que a variabilidade química dentro de populações vegetais é importante estratégia de defesa contra herbívoros, dificultando-lhes a especialização.

Termos de indexação:Hyptis suaveolens, herbivoria, variabilidade genética.

ABSTRACT

Populations of Hyptis suaveolens (L.) Poit. (Labiatae) were accompanied during their development in three sites: Horto Florestal de Sumaré, Campus of UNICAMP (Campinas), and Fazenda Santa Genebra (Distrito de Barão Geraldo, Campinas), all in the State of São Paulo, Brazil, from 1981 through 1983. At each site, a population exposed to full sunlight and another in the shade were studied. The objective was to evaluate, during plant development, the period when they were more susceptible to attack by herbivores; to consider the abundance of herbivores, and the role of variation in the chemistry of monoterpenes in the development of herbivores. Populations were more susceptible to attack by herbivores in the period preceding flowering. Heavy herbivore damage was not detected during this period, in spite of higher herbivore densities. The results suggest that the variation in chemical composition probably has an effect on the development of generalist herbivores. On the other hand, Pyrausta insignatalis Guenée (Lep.-Pyralidae-Pyraustinae) is probably well adapted to the plant and appears to be resistent to the terpenes. Differences in chemistry and differences in protection against herbivores were not observed between populations in sunny and shady sites. The results support an important role for genetic variability in populations in protection against herbivory and inhibition of specialization.

Index terms:Hyptis suaveolens, herbivory, genetic variability.

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Full text available only in PDF format.

REFERÊNCIAS BIBLIOGRÁFICAS

AIDE, T.M. Dry season leaf production: an escape from herbivory. Biotropica, College Park, 24(4):532-537, 1992.

AIDE, T.M. Patterns of leaf development and herbivory in a tropical understory community. Ecology, Durham 74(2):455-466, 1993.

ARRHENIUS, S.P. & LANGENHEIM, J.H. Inhibitory effects of Hymenaea and Copaifera leaf resins on the leaf fungus, Pestalotia subcuticulares. Biochemical Systematics and Ecology, Oxford, 11(4):361-366, 1983.

ATSATT, P.R. & O'DOWD, D.J. Plant defense guilds. Science, Washington, 193:24-29, 1976.

BEGOSSI, A. & BENSON, W.W. Host plants and defense mechanisms in Oedionychina (Alticinae). In: JOLIVET, P.; PETITPIERRE, E. & HSIAO, T.H. Biology of Chrysomelidae. Dordrecht, Kluwer Academic Publishers, 1988. p.57-71.

BRATTSTEN, L.B.; WILKINSON, C.F. & EISNER, T. Herbivore-plant interactions: mixed-function oxidases and secondary plant substances. Science, Washington, 196:1349-1352, 1977.

BROWN JR., K.S. Adult-obtained pyrrolizidine alkaloids defend Ithomiine butterflies against a spider predator. Nature, London, 309:707-709, 1984.

BROWN JR., K.S. Chemical ecology of the hydropyrrolizidine alkaloids in adult Ithomiinae (Lepidoptera: Nymphalidae). Revista Brasileira de Biologia, 44: 435-460, 1985.

BROWN JR., K.S. Chemistry at the Solanaceae/Ithomiinae interface. Annals of the Missouri Botanical Garden, Saint Louis, 74:359-397, 1987.

BULL, D.L & WHITTEN, C.J. Factors influencing organophosphorus insecticide resistence in tobacco budworms. Journal of the agricultural and food chemistry, Washington, 20(3):561-564, 1972. CAMMERLOHER, H. Blütenbiologie I - Wechselbezie-hungen zwischen blumen und insekten. Berlin, Gebrüder, 1931. 199p.

CATES, R.G. The interface between slugs and wild ginger: some evolutionary aspects. Ecology, Durham, 56:391-400, 1975.

CATES, R.G. & ORIANS, G.H. Successional status and the palatability of plants to generalized herbivores. Ecology, Durham, 56:410-418, 1975.

CHAN, B.G.; MAHONEY, N. & WAISS, JR., A.C. A quantitative method for gossypol and its analogs. In: BELTWIDE COTTON PRODUCTION RESEARCH CONFERENCES, San Antonio, 1983. Proceedings. Memphis National Cotton Council of America, 1983. p.64-65.

CHAN, B.G.; WAISS JR., A. C. & LUKHPAHR, M. Condensed tannin an antibiotic chemical from Gossypium hirsutum. Journal of Insect Physiology, Oxford, 24:113-118, 1978.

COLEY, P. D, Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecological Monographs, Durham, 53:209-233, 1983.

COLEY, P.D. Patrones en las defensas de las plantas: porqué los herbívoros prefieren ciertas especies? Revista de Biologia Tropical, San José, 35(1):151-164, 1987.

COLEY, P.D. Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia, Heidelberg, 74:531-536, 1988.

COLEY, P. D. & AIDE, T. M. Comparison of herbivory and plant defenses in temperate and tropical broad-leafed forests. In: PRICE, P. W.; LEWINSOHN, T. M.; FERNANDES, G.W. & BENSON, W.W. Plant-animal interactions: evolutionary ecology in tropical and temperate regions. New York, John Wiley & Sons, 1991. p.25-49.

CRAVEIRO, A.A.; FERNANDES, A.G.; ANDRADE, C.H.S.; MATOS, F.J. de A.; ENCAR, J.W. de & MACHADO, M.I.L. Óleos essenciais de plantas do Nordeste. Fortaleza, Universidade Federal do Ceará, 1981. 210p. FEENY, P. Plant apparency and chemical defense. Recent Advances in Phytochemistry, New York, 10:1-40, 1976.

FEENY, P. Defensive ecology of the Cruciferac. Annals of the Missouri Botanical Garden, Saint Louis, 64:221-234, 1977.

FLORES, S.E. & MEDINA, J.D. Estudio preliminar de los componentes del aceite esencial de Hyptis suaveolens (L.) Poit. Acta Cientifica Venezolana, Caracas, 21:161-162, 1970.

GILBERT, L.E. The role of insect-plant coevolution in the organization of ecosystems. In: LABYRIE,V., ed. Comportment des insects et milieu trophique. Paris, C.N.R.S., 1977. p.399-413. (Colloques internationaux du C.N.R.S., 265)

GILBERT, L.E. Food web organization and the conservation of Neotropical diversity. In: SOULE, M. & WILCOX, B. Conservation biology: an evolutionary ecological perspective. Sunderland, M.A., Sia-nuer, 1980. p.5-36.

GILDEMEISTER, E. & HOFFMAN, Fr. Ol von Hyptis suaveolens. In: GILDEMEISTER, E. & HOFFMAN, Fr., eds. Die aetherischen oele, Berlin, Akademie Verlag, 1961. v.7, p.472-473.

GOTTLIEB, O.R.; KOKETSU, M.; MAGALHÃES, M.T.; MAIA, J.G.S.; MENDES, P.H.; ROCHA, A.I. da; SILVA, M.L. da & WILBERG, V.C. Óleos essenciais da Amazônia VII (1). Acta Amazonica, Manaus, 11(1):143-148, 1981.

GROSS, D. Growth regulating substance of plant origin. Phytochemistry, Oxford, 14:2105-2112, 1975.

HALLIGAN, J.R Toxic terpenes from Artemisia Californica. Ecology, Durham, 56:999-1003, 1975.

HESS, D. Terpenoids. In: HESS, D. Plant physiology; molecular, biochemical and physiological fundamentals of metabolism and development. New York, Springer-Verlag, 1975. p.99-116.

JANZEN, D.H. Tropical agroecosystems. Science, Washington, 182:1212-1219, 1973.

LANGENHEIM, J.H.; FOSTER, C.E. & McGINLEY, R.B. Inhibitory effects of different quantitative compositions of Hymenaea leaf resins on a generalist herbivore Spodoptera exigua. Biochemical Systematics and Ecology, Oxford, 8:385-396, 1980.

LANGENHEIM, I.H.; STUBBLEBINE, W.; FOSTER, C. & NASCIMENTO, J.C. Estudos comparativos da variabilidade na composição da resina da folha entre árvores parental e progênie de espécies selecionadas de Hymenaea. I. Comparação de populações amazônicas e venezuelanas. Acta Amazônica, Manaus, 7(3): 335-354, 1977.

LEVIN, D.A. The chemical defenses of plants to pathogens and herbivores. Annual Review of Ecologie and Systematics, Palo Alto, 7:121-159, 1976.

LUZ, A.I.R.; ZOGHBI, M.G.B.; RAMOS, L.S.; MAIA, J.G.S. & SILVA, M. L. da. Essential oils of some amazonian Labiatae I - Genus Hyptis. Journal of Natural Products, Pittsburg, 47(4):745-747, 1984.

MANCHAND, P.S.; WHITE, J.D.; FAYOS, J. & CLAR-DY, J. Structures of suaveolic acid and suaveolol. Journal of Organic Chemistry, Washington, 39:2306-2307, 1974.

MISRA, T.N.; SINGH, R.S.; OJHA, T.N. & UPADHYAY, J. Chemical constituents of Hyptis suaveolens - Part. I - Spectral and biological studies on a triterpene acid. Lloidia, Cincinnatti, 44(6):735-738, 1981.

MOONEY, H.A. & GULMON, S.L. Constraints on leaf structure and function in reference to herbivory. Bios-cience, Washington, 32(3):198-206, 1982.

NAYAK, U.G. & GUHA, P.C. Essential oil from Hyptis suaveolens Poit. Journal of the Indian Chemical Society, Calcutta, 29:183-186, 1952.

ORIANS, G.H. & JANZEN, D.H. Why are embryos so tasty? American Naturalist, Chicago, 108(963):581-592, 1974.

QUEIROZ, R.B.; STUBBLEBINE, W.H. & SHEPHERD, G. Variação na composição de terpenos dentro e entre populações de Hyptis suaveolens (L.) Poit. (Labiatae) na região de Campinas-SP. Revista brasileira de Botânica, São Paulo, 13:75-81, 1990.

REHR, S.S.; JANZEN, D.H. & FEENY, P.P. L-Dopa in legumes seeds: a chemical barrier to insect attack. . Science, Washington, 181:81-82, 1973.

RHOADES, D.F. & CATES, R.G. Toward a general theory of plant antiherbivore chemistry. Recent Advances in Phytochemistry, New York, 10:168-213, 1976.

RICE, E.L. Some roles of allelophathic coumpounds in plant communities. Biochemical Systematics and Ecology, Oxford, 5(3):201-206, 1977.

RISCH, S.J.; ANDOW, D. & ALTIERI, M.A. Agro-ecosystem diversity and pest control: data, tentative conclusions, and new research directions. Environmental Entomology, College Park, 12:625-629, 1983.

ROCKWOOD, L.L. The effect of defoliation on seed production of six Costa Rican tree species. Ecology, Durham, 54(6):1363-1369, 1973.

SEIGLER, D.S. Primary roles for secondary compounds. Biochemical Systematics and Ecology, Oxford, 5(3):195-199, 1977.

SMITH, R.H. Effect of monoterpene vapors on the western pine beetle. Journal Economic Entomology, Washington, 58(3):509-510, 1965.

SMITH, R.H. Resin quality as a factor in the resistance of pines to bark beetles. In: GERHOLD, H.D.; McDERMOTT, R.E.; SCHEINER, E.J. & WINIESHEI, J.A., eds. Breeding pest-resistant trees. Oxford, Pergamon, 1966. p. 189-196.

SOKAL, R.R. & ROHLF, F.J. Biometry. 2.ed. San Francisco, Freeman, 1981. 859p.

UPADHYAY, J.; SINGH, R.S. & MISRA, T.N. Chemical constituents of Hyptis suaveolens Poit. Indian Journal Pharmaceutical Science, Bombay, 44(2): 19-20, 1982.

WHITTAKER, R.H. & FEENY, P.P. Allelochemics: chemical interactions between species. Science, Washington, 171:757-770, 1971.

WILLIAMS, N. H. Floral fragrances as cues in animal behavior. In: JONES, C.E. & LITTLE, R.J., eds. Handbook of experimental pollination biology. New York, Scientific and Academic, 1983. p.50-72.

ZUCKER, W.V. Tannins: does structure determine function? An ecological perspective. American Naturalist, Chicago, 121:335-365, 1983.

Recebido para publicação em 15 de abril de 1994 e aceito em 7 de abril de 1995

  • AIDE, T.M. Dry season leaf production: an escape from herbivory. Biotropica, College Park, 24(4):532-537, 1992.
  • AIDE, T.M. Patterns of leaf development and herbivory in a tropical understory community. Ecology, Durham 74(2):455-466, 1993.
  • ARRHENIUS, S.P. & LANGENHEIM, J.H. Inhibitory effects of Hymenaea and Copaifera leaf resins on the leaf fungus, Pestalotia subcuticulares. Biochemical Systematics and Ecology, Oxford, 11(4):361-366, 1983.
  • ATSATT, P.R. & O'DOWD, D.J. Plant defense guilds. Science, Washington, 193:24-29, 1976.
  • BEGOSSI, A. & BENSON, W.W. Host plants and defense mechanisms in Oedionychina (Alticinae). In: JOLIVET, P.; PETITPIERRE, E. & HSIAO, T.H. Biology of Chrysomelidae. Dordrecht, Kluwer Academic Publishers, 1988. p.57-71.
  • BRATTSTEN, L.B.; WILKINSON, C.F. & EISNER, T. Herbivore-plant interactions: mixed-function oxidases and secondary plant substances. Science, Washington, 196:1349-1352, 1977.
  • BROWN JR., K.S. Adult-obtained pyrrolizidine alkaloids defend Ithomiine butterflies against a spider predator. Nature, London, 309:707-709, 1984.
  • BROWN JR., K.S. Chemical ecology of the hydropyrrolizidine alkaloids in adult Ithomiinae (Lepidoptera: Nymphalidae). Revista Brasileira de Biologia, 44: 435-460, 1985.
  • BROWN JR., K.S. Chemistry at the Solanaceae/Ithomiinae interface. Annals of the Missouri Botanical Garden, Saint Louis, 74:359-397, 1987.
  • BULL, D.L & WHITTEN, C.J. Factors influencing organophosphorus insecticide resistence in tobacco budworms. Journal of the agricultural and food chemistry, Washington, 20(3):561-564, 1972.
  • CAMMERLOHER, H. Blütenbiologie I - Wechselbezie-hungen zwischen blumen und insekten. Berlin, Gebrüder, 1931. 199p.
  • CATES, R.G. The interface between slugs and wild ginger: some evolutionary aspects. Ecology, Durham, 56:391-400, 1975.
  • CATES, R.G. & ORIANS, G.H. Successional status and the palatability of plants to generalized herbivores. Ecology, Durham, 56:410-418, 1975.
  • CHAN, B.G.; MAHONEY, N. & WAISS, JR., A.C. A quantitative method for gossypol and its analogs. In: BELTWIDE COTTON PRODUCTION RESEARCH CONFERENCES, San Antonio, 1983. Proceedings. Memphis National Cotton Council of America, 1983. p.64-65.
  • CHAN, B.G.; WAISS JR., A. C. & LUKHPAHR, M. Condensed tannin an antibiotic chemical from Gossypium hirsutum. Journal of Insect Physiology, Oxford, 24:113-118, 1978.
  • COLEY, P. D, Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecological Monographs, Durham, 53:209-233, 1983.
  • COLEY, P.D. Patrones en las defensas de las plantas: porqué los herbívoros prefieren ciertas especies? Revista de Biologia Tropical, San José, 35(1):151-164, 1987.
  • COLEY, P.D. Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia, Heidelberg, 74:531-536, 1988.
  • COLEY, P. D. & AIDE, T. M. Comparison of herbivory and plant defenses in temperate and tropical broad-leafed forests. In: PRICE, P. W.; LEWINSOHN, T. M.; FERNANDES, G.W. & BENSON, W.W. Plant-animal interactions: evolutionary ecology in tropical and temperate regions. New York, John Wiley & Sons, 1991. p.25-49.
  • CRAVEIRO, A.A.; FERNANDES, A.G.; ANDRADE, C.H.S.; MATOS, F.J. de A.; ENCAR, J.W. de & MACHADO, M.I.L. Óleos essenciais de plantas do Nordeste. Fortaleza, Universidade Federal do Ceará, 1981. 210p.
  • FEENY, P. Plant apparency and chemical defense. Recent Advances in Phytochemistry, New York, 10:1-40, 1976.
  • FEENY, P. Defensive ecology of the Cruciferac. Annals of the Missouri Botanical Garden, Saint Louis, 64:221-234, 1977.
  • FLORES, S.E. & MEDINA, J.D. Estudio preliminar de los componentes del aceite esencial de Hyptis suaveolens (L.) Poit. Acta Cientifica Venezolana, Caracas, 21:161-162, 1970.
  • GILBERT, L.E. The role of insect-plant coevolution in the organization of ecosystems. In: LABYRIE,V., ed. Comportment des insects et milieu trophique. Paris, C.N.R.S., 1977. p.399-413. (Colloques internationaux du C.N.R.S., 265)
  • GILBERT, L.E. Food web organization and the conservation of Neotropical diversity. In: SOULE, M. & WILCOX, B. Conservation biology: an evolutionary ecological perspective. Sunderland, M.A., Sia-nuer, 1980. p.5-36.
  • GILDEMEISTER, E. & HOFFMAN, Fr. Ol von Hyptis suaveolens. In: GILDEMEISTER, E. & HOFFMAN, Fr., eds. Die aetherischen oele, Berlin, Akademie Verlag, 1961. v.7, p.472-473.
  • GOTTLIEB, O.R.; KOKETSU, M.; MAGALHÃES, M.T.; MAIA, J.G.S.; MENDES, P.H.; ROCHA, A.I. da; SILVA, M.L. da & WILBERG, V.C. Óleos essenciais da Amazônia VII (1). Acta Amazonica, Manaus, 11(1):143-148, 1981.
  • GROSS, D. Growth regulating substance of plant origin. Phytochemistry, Oxford, 14:2105-2112, 1975.
  • HALLIGAN, J.R Toxic terpenes from Artemisia Californica. Ecology, Durham, 56:999-1003, 1975.
  • HESS, D. Terpenoids. In: HESS, D. Plant physiology; molecular, biochemical and physiological fundamentals of metabolism and development. New York, Springer-Verlag, 1975. p.99-116.
  • JANZEN, D.H. Tropical agroecosystems. Science, Washington, 182:1212-1219, 1973.
  • LANGENHEIM, J.H.; FOSTER, C.E. & McGINLEY, R.B. Inhibitory effects of different quantitative compositions of Hymenaea leaf resins on a generalist herbivore Spodoptera exigua. Biochemical Systematics and Ecology, Oxford, 8:385-396, 1980.
  • LANGENHEIM, I.H.; STUBBLEBINE, W.; FOSTER, C. & NASCIMENTO, J.C. Estudos comparativos da variabilidade na composição da resina da folha entre árvores parental e progênie de espécies selecionadas de Hymenaea. I. Comparação de populações amazônicas e venezuelanas. Acta Amazônica, Manaus, 7(3): 335-354, 1977.
  • LEVIN, D.A. The chemical defenses of plants to pathogens and herbivores. Annual Review of Ecologie and Systematics, Palo Alto, 7:121-159, 1976.
  • LUZ, A.I.R.; ZOGHBI, M.G.B.; RAMOS, L.S.; MAIA, J.G.S. & SILVA, M. L. da. Essential oils of some amazonian Labiatae I - Genus Hyptis. Journal of Natural Products, Pittsburg, 47(4):745-747, 1984.
  • MANCHAND, P.S.; WHITE, J.D.; FAYOS, J. & CLAR-DY, J. Structures of suaveolic acid and suaveolol. Journal of Organic Chemistry, Washington, 39:2306-2307, 1974.
  • MISRA, T.N.; SINGH, R.S.; OJHA, T.N. & UPADHYAY, J. Chemical constituents of Hyptis suaveolens - Part. I - Spectral and biological studies on a triterpene acid. Lloidia, Cincinnatti, 44(6):735-738, 1981.
  • MOONEY, H.A. & GULMON, S.L. Constraints on leaf structure and function in reference to herbivory. Bios-cience, Washington, 32(3):198-206, 1982.
  • NAYAK, U.G. & GUHA, P.C. Essential oil from Hyptis suaveolens Poit. Journal of the Indian Chemical Society, Calcutta, 29:183-186, 1952.
  • ORIANS, G.H. & JANZEN, D.H. Why are embryos so tasty? American Naturalist, Chicago, 108(963):581-592, 1974.
  • QUEIROZ, R.B.; STUBBLEBINE, W.H. & SHEPHERD, G. Variação na composição de terpenos dentro e entre populações de Hyptis suaveolens (L.) Poit. (Labiatae) na região de Campinas-SP. Revista brasileira de Botânica, São Paulo, 13:75-81, 1990.
  • REHR, S.S.; JANZEN, D.H. & FEENY, P.P. L-Dopa in legumes seeds: a chemical barrier to insect attack. . Science, Washington, 181:81-82, 1973.
  • RHOADES, D.F. & CATES, R.G. Toward a general theory of plant antiherbivore chemistry. Recent Advances in Phytochemistry, New York, 10:168-213, 1976.
  • RICE, E.L. Some roles of allelophathic coumpounds in plant communities. Biochemical Systematics and Ecology, Oxford, 5(3):201-206, 1977.
  • RISCH, S.J.; ANDOW, D. & ALTIERI, M.A. Agro-ecosystem diversity and pest control: data, tentative conclusions, and new research directions. Environmental Entomology, College Park, 12:625-629, 1983.
  • ROCKWOOD, L.L. The effect of defoliation on seed production of six Costa Rican tree species. Ecology, Durham, 54(6):1363-1369, 1973.
  • SEIGLER, D.S. Primary roles for secondary compounds. Biochemical Systematics and Ecology, Oxford, 5(3):195-199, 1977.
  • SMITH, R.H. Effect of monoterpene vapors on the western pine beetle. Journal Economic Entomology, Washington, 58(3):509-510, 1965.
  • SMITH, R.H. Resin quality as a factor in the resistance of pines to bark beetles. In: GERHOLD, H.D.; McDERMOTT, R.E.; SCHEINER, E.J. & WINIESHEI, J.A., eds. Breeding pest-resistant trees. Oxford, Pergamon, 1966. p. 189-196.
  • SOKAL, R.R. & ROHLF, F.J. Biometry. 2.ed. San Francisco, Freeman, 1981. 859p.
  • UPADHYAY, J.; SINGH, R.S. & MISRA, T.N. Chemical constituents of Hyptis suaveolens Poit. Indian Journal Pharmaceutical Science, Bombay, 44(2): 19-20, 1982.
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  • 1
    Parte da Tese de Mestrado do primeiro autor.
  • Datas de Publicação

    • Publicação nesta coleção
      16 Out 2007
    • Data do Fascículo
      1995

    Histórico

    • Aceito
      07 Abr 1995
    • Recebido
      15 Abr 1994
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