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Chemical Stimulants of Leaf-Trenching by Cabbage Loopers: Natural Products, Neurotransmitters, Insecticides, and Drugs

Abstract

Larvae of the cabbage looper, Trichoplusia ni (Lepidoptera: Noctuidae), often transect leaves with a narrow trench before eating the distal section. The trench reduces larval exposure to exudates, such as latex, during feeding. Plant species that do not emit exudate, such as Plantago lanceolata, are not trenched. However, if exudate is applied to a looper's mouth during feeding on P. lanceolata, the larva will often stop and cut a trench. Dissolved chemicals can be similarly applied and tested for effectiveness at triggering trenching. With this assay, I have documented that lactucin from lettuce latex (Lactuca sativa), myristicin from parsley oil (Petroselinum crispum), and lobeline from cardinal flower (Lobelia cardinalis) elicit trenching. These compounds are the first trenching stimulants reported. Several other constituents of lettuce and parsley, including some phenylpropanoids, monoterpenes, and furanocoumarins had little or no activity. Cucurbitacin E glycoside found in cucurbits, another plant family trenched by cabbage loopers, also was inactive. Lactucin, myristicin, and lobeline all affect the nervous system of mammals, with lobeline acting specifically as an antagonist of nicotinic acetylcholine receptors. To determine if cabbage loopers respond selectively to compounds active at acetylcholine synapses, I tested several neurotransmitters, insecticides, and drugs with known neurological activity, many of which triggered trenching. Active compounds included dopamine, serotonin, the insecticide imidacloprid, and various drugs such as ipratropium, apomorphine, buspirone, and metoclopramide. These results document that noxious plant chemicals trigger trenching, that loopers respond to different trenching stimulants in different plants, that diverse neuroactive chemicals elicit the behavior, and that feeding deterrents are not all trenching stimulants. The trenching assay offers a novel approach for identifying defensive plant compounds with potential uses in agriculture or medicine. Cabbage loopers in the lab and field routinely trench and feed on plants in the Asteraceae and Apiaceae. However, first and third instar larvae enclosed on Lobelia cardinalis (Campanulaceae) failed to develop, even though the third instar larvae attempted to trench. Trenching ability does not guarantee effective feeding on plants with canal-borne exudates. Cabbage loopers must not only recognize and respond to trenching stimulants, they must also tolerate exudates during the trenching procedure to disable canalicular defenses.

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References

  1. Angiosperm Phylogeny Group 1998. An ordinal classification for the families of flowering plants. Ann. MO. Bot. Gard. 85:531–553.

    Google Scholar 

  2. Anonymous 1989. Crop Protection Chemicals Reference. Chemical and Pharmaceutical Press, Paris.

  3. Arena, J. M. 1970. Poisoning: Toxicology, Symptoms, Treatments. Charles C. Thomas, Springfield, Illinois.

    Google Scholar 

  4. Aydar, E. and Beadle, D. J. 1999. The pharmacological profile of GABA receptors on cultured insect neurones. J. Insect Physiol. 45:213–219.

    PubMed  Google Scholar 

  5. Basset, Y. and Novotny, V. 1999. Species richness of insect herbivore communities on Ficus in Papua New Guinea. Biol. J. Linn. Soc. 67:477–499.

    Google Scholar 

  6. Becerra, J. X. 1994. Squirt-gun defense in Bursera and the chrysomelid counterploy. Ecology 75:1991–1996.

    Google Scholar 

  7. Becerra, J. X., Venable, D. L., Evans, P. H., and Bowers, W. S. 2001. Interactions between chemical and mechanical defenses in the plant genus Bursera and their implications for herbivores. Am. Zool. 41:865–876.

    Google Scholar 

  8. Benson, J. A. 1993. The electrophysiological pharmacology of neurotransmitter receptors on locust neuronal somata, pp. 390–413, in Y. Pichon (ed.). Comparative Molecular Neurobiology. Birkhäuser, Basel, Switzerland.

    Google Scholar 

  9. Berenbaum, M. R. 1990. Evolution of specialization in insect-umbellifer associations. Annu. Rev. Entomol. 35:319–343.

    Google Scholar 

  10. Berenbaum, M. and Neal, J. J. 1985. Synergism between myristicin and xanthotoxin, a naturally cooccurring plant toxicant. J. Chem. Ecol. 11:1349–1358.

    Google Scholar 

  11. Bernath, J. (Ed.)1998. Poppy: The Genus Papaver. Harwood Academic, Amsterdam.

    Google Scholar 

  12. Burrows, M. 1996. The Neurobiology of an Insect Brain. Oxford University Press, Oxford.

    Google Scholar 

  13. Camm, E. L., Wat, C., and Towers, G. H. N. 1976. An assessment of the roles of furanocoumarins in Heracleum lanatum. Can. J. Bot. 54:2562–2566.

    Google Scholar 

  14. Carroll, C. R. and Hoffman, C. A. 1980. Chemical feeding deterrent mobilized in response to insect herbivory and counteradaptation in Epilachna tredecimnotata. Science. 209:414–416.

    Google Scholar 

  15. Casida, J. E. and Quistad, G. B. 1998. Golden age of insecticide research: Past, present, or future? Annu. Rev. Entomol. 43:1–16.

    PubMed  Google Scholar 

  16. Chapman, R. F. 1995. Chemosensory regulation of feeding, pp. 101–136 in R. F. Chapman and G. de Boer (Eds.). Regulatory Mechanisms in Insect Feeding. Chapman and Hall, New York.

    Google Scholar 

  17. Clarke, A. R. and Zalucki, M. P. 2000. Foraging and vein-cutting behaviour of Euploea core corinna (W. S. Macleay) (Lepidoptera: Nymphalidae) caterpillars feeding on latex-bearing leaves. Aust. J. Entomol. 39:283–290.

    Google Scholar 

  18. Cohen, R. W., Mahoney, D. A., and Can, H. D. 2002. Possible regulation of feeding behavior in cockroach nymphs by the neurotransmitter octopamine. J. Insect Behav. 15:37–50.

    Google Scholar 

  19. Crellin, J. K. and Philpott, J. 1990. Herbal Medicine Past and Present. II: A Reference Guide to Medicinal Plants. Duke University Press, Durham, North Carolina.

    Google Scholar 

  20. Cremlyn, R. J. 1991. Agrochemicals: Preparation and Mode of Action. Wiley, New York.

    Google Scholar 

  21. Detzel, A. and Wink, M. 1993. Attraction, deterrence or intoxication of bees (Apis mellifera) by plant allelochemicals. Chemoecology 4:8–18.

    Google Scholar 

  22. Dollahite, J. W. and Allen, T. J. 1962. Poisoning of cattle, sheep, and goats with Lobezla and Centaurium species. Southwest. Vet. 15:126–130.

    Google Scholar 

  23. Duke, J. A. 1985. CRC Handbook of Medicinal Herbs. CRC Press, Boca Raton, Florida.

    Google Scholar 

  24. Dussourd, D. E. 1993. Foraging with finesse: Caterpillar adaptations for circumventing plant defenses, pp. 92–131, in N. E. Stamp and T. M. Casey (Eds.). Caterpillars: Ecological and Evolutionary Constraints on Foraging. Chapman and Hall, New York.

    Google Scholar 

  25. Dussourd, D. E. 1997. Plant exudates trigger leaf-trenching by cabbage loopers, Trichoplusia ni. Oecologia 112:362–369.

    Google Scholar 

  26. Dussourd, D. E. 1999. Behavioral sabotage of plant defense: Do vein cuts and trenches reduce insect exposure to exudate? J. Insect Behav. 12:501–515.

    Google Scholar 

  27. Dussourd, D. E. and Denno, R. F. 1991. Deactivation of plant defense: Correspondence between insect behavior and secretory canal architecture. Ecology 72:1383–1396.

    Google Scholar 

  28. Dussourd, D. E. and Denno, R. F. 1994. Host range of generalist caterpillars: Trenching permits feeding on plants with secretory canals. Ecology 75:69–78.

    Google Scholar 

  29. Dussourd, D. E. and Hoyle, A. M. 2000. Poisoned plusiines: Toxicity of milkweed latex and cardenolides to some generalist caterpillars. Chemoecology 10:11–16.

    Google Scholar 

  30. Dwoskin, L. P. and Crooks, P. A. 2001. Competitive neuronal nicotinic receptor antagonists: A new direction for drug discovery. J. Pharmacol. Exp. Ther. 298:395–402.

    PubMed  Google Scholar 

  31. Dwoskin, L. P. and Crooks, P. A. 2002. A novel mechanism of action and potential use for lobeline as a treatment for psychostimulant abuse. Biochem. Pharmacol. 63:89–98.

    PubMed  Google Scholar 

  32. Eichlin, T. D. and Cunningham, H. B. 1978. The Plusiinae (Lepidoptera: Noctuidae) of America north of Mexico, emphasizing genitalic and larval morphology. US Dept. Agric. Tech. Bull. 1567:1–122.

    Google Scholar 

  33. Fahn, A. 1979. Secretory Tissues in Plants. Academic Press, New York.

    Google Scholar 

  34. Farrell, B. D., Dussourd, D. E., and Mitter, C. 1991. Escalation of plant defense: Do latex and resin canals spur plant diversification? Am. Nat.. 138:881–900.

    Google Scholar 

  35. Flint, M. L. 1987. Integrated Pest Management for Cole Crops and Lettuce. University of California, Publication No. 3307.

  36. Florio, V., Fuentes, J. A., Ziegler, H., and Longo, V. G. 1972. EEG and behavioral effects in animals of some amphetamine derivatives with hallucinogenic properties. Behav. Biol. 7:401–414.

    PubMed  Google Scholar 

  37. Fodor, G. B. and Colasanti, B. 1985. The pyridine and piperidine alkaloids: Chemistry and pharmacology, pp. 1–90, in S. W. Pelletier (ed.). Alkaloids: Chemical and Biological Perspectives, Vol. 3. Wiley, New York.

    Google Scholar 

  38. Foster, S. and Tyler, V. E. 1999. Tyler's Honest Herbal: A Sensible Guide to the Use of Herbs and Related Remedies. Haworth Herbal Press, New York.

    Google Scholar 

  39. Gershenzon, J. and Croteau, R. 1991. Terpenoids, pp. 165–219, in G. A. Rosenthal and M. R. Berenbaum (Eds.). Herbivores: Their Interactions with Secondary Plant Metabolites. Academic Press, New York.

    Google Scholar 

  40. Grimes, L. R. and Neunzig, H. H. 1986. Morphological survey of the maxillae in last-stage larvae of the suborder Ditrysia (Lepidoptera): Mesal lobes (Laciniogaleae). Ann. Entomol. Soc. Am. 79:510–526.

    Google Scholar 

  41. Gromek, D., Kisiel, W., Klodzinska, A., and Chojnacka-Wojcik, E. 1992. Biologically active preparations from Lactuca virosa L. Phytother. R. 6:285–287.

    Google Scholar 

  42. Guha, J. and Sen, S. P. 1975. The cucurbitacins—A review. Plant Biochem. J. 2:12–28.

    Google Scholar 

  43. Gupta, R. N. and Spenser, I. D. 1971. Biosynthesis of lobinaline. Can. J. Chem. 49:384–397.

    Google Scholar 

  44. Hallstrom, H. and Thuvander, A. 1997. Toxicological evaluation of myristicin. Nat. Toxins 5:186–192.

    PubMed  Google Scholar 

  45. Harborne, J. B. and Baxter, H. 1993. Phytochemical Dictionary: A Handbook of Bioactive Compounds from Plants. Taylor and Francis, Washington, DC.

    Google Scholar 

  46. Hardman, J. G. and Limbird, L. E. (Eds.) 1996. Goodman and Gilman's The Pharmacological Basis of Therapeutics. McGraw-Hill, New York.

    Google Scholar 

  47. Harrod, S. B., Dwoskin, L. P., Crooks, P. A., Klebaur, J. E., and Bardo, M. T. 2001. Lobeline attenuates d-methamphetamine self-administration in rats. J. Pharmacol. Exp. Ther. 298:172–179.

    PubMed  Google Scholar 

  48. Hartmann, T. 1991. Alkaloids, pp. 79–121, in G. A. Rosenthal and M. R. Berenbaum (Eds.). Herbivores: Their Interactions with Secondary Plant Metabolites. Vol. I: The Chemical Participants. Academic Press, New York.

    Google Scholar 

  49. Hegnauer, R. 1971. Chemical patterns and relationships of Umbelliferae, pp. 267–277, in V. H. Heywood (ed.). The Biology and Chemistry of the Umbelliferae. Academic Press, New York.

    Google Scholar 

  50. Huang, Z. J., Kinghorn, A. D., and Farnsworth, N. R. 1982. Studies on herbal remedies. I: Analysis of herbal smoking preparations alleged to contain lettuce (Lactuca sativa L.) and other natural products. J. Pharm. Sci. 71:270–271.

    PubMed  Google Scholar 

  51. Jolivet, P. 1998. Interrelationship Between Insects and Plants. CRC Press, New York.

    Google Scholar 

  52. Kindscher, K. 1992. Medicinal Wild Plants of the Prairie: An Ethnobotanical Guide. University Press of Kansas, Lawrence, Kansasy.

    Google Scholar 

  53. Kingsbury, J. M. 1964. Poisonous Plants of the United States and Canada. Prentice-Hall, Englewood Cliffs, New Jersey.

    Google Scholar 

  54. Knogge, W., Kombrink, E., Schmelzer, E., and Hahlbrock, K. 1987. Occurrence of phytoalexins and other putative defense-related substances in uninfected parsley plants. Planta 171:279–287.

    Google Scholar 

  55. Krochmal, A., Wilken, L., and Chien, M. 1972. Lobeline content of four Appalachian Lobelias. Lloydia 35:303–304.

    PubMed  Google Scholar 

  56. Kubeczka, K. H. and Stahl, E. 1977. On the essential oils from the Apiaceae (Umbelliferae). II: The essential oils from the above ground parts of Pastinaca sativa. Planta Med. 31:173–184.

    PubMed  Google Scholar 

  57. Lafontaine, J. D. and Poole, R. W. 1991. Noctuoidea, noctuidae (part), in R. B. Dominick et al. (Eds.). The Moths of America North of Mexico, Fasc. 25.1. Wedge Entomological Research Foundation, Washington, DC.

    Google Scholar 

  58. Lavy, G. 1987. Nutmeg intoxication in pregnancy: A case report. J. Reprod. Med. 32:63–64.

    PubMed  Google Scholar 

  59. Lewinsohn, T. M. 1991. The geographical distribution of plant latex. Chemoecology 2:64–68.

    Google Scholar 

  60. Lewis, A. C. 1984. Plant quality and grasshopper feeding: Effects of sunflower condition on preference and performance in Melanoplus differentialis. Ecology 65:836–843.

    Google Scholar 

  61. Lichtenstein, E. P. and Casida, J. E. 1963. Myristicin, an insecticide and synergist occurring naturally in the edible parts of parsnips. J. Agric. Food Chem. 11:410–415.

    Google Scholar 

  62. Lichtenstein, E. P., Liang, T. T., Schulz, K. R., Schnoes, H. K., and Carter, G. T. 1974. Insecticidal and synergistic components isolated from dill plants. J. Agric. Food Chem. 22:658–664.

    PubMed  Google Scholar 

  63. Long, T. F. and Murdock, L. L. 1983. Stimulation of blowfly feeding behavior by octopaminergic drugs. Proc. Natl. Acad. Sci. USA 80:4159–4163.

    Google Scholar 

  64. Macleod, A. J., Snyder, C. H., and Subramanian, G. 1985. Volatile aroma constituents of parsley leaves. Phytochemistry 24:2623–2627.

    Google Scholar 

  65. Marston, A., Hostettmann, K., and Msonthi, J. D. 1995. Isolation of antifungal and larvicidal constituents of Diplolophium buchanani by centrifugal partition chromatography. J. Nat. Prod. 58:128–130.

    PubMed  Google Scholar 

  66. Matsuda, K., Buckingham, S. D., Kleier, D., Rauh, J. J., Grauso, M., and Sattelle, D. B. 2001. Neonicotinoids: Insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol. Sci. 22:573–580.

    PubMed  Google Scholar 

  67. Mccloud, E. S., Tallamy, D. W., and Halaweish, F. T. 1995. Squash beetle trenching behaviour: Avoidance of cucurbitacin induction or mucilaginous plant sap? Ecol. Entomol. 20:51–59.

    Google Scholar 

  68. Metcalf, R. L., Metcalf, R. A., and Rhodes, A. M. 1980. Cucurbitacins as kairomones for diabroticite beetles. Proc. Natl. Acad. Sci. USA 77:3769–3772.

    Google Scholar 

  69. Metcalfe, C. R. and Chalk, L. 1983. Anatomy of the Dicotyledons, Vol. II. Clarendon Press, Oxford.

    Google Scholar 

  70. Mullin, C. A., Alfatafta, A. A., Harman, J. L., Everett, S. L., and Serino, A. A. 1991. Feeding and toxic effects of floral sesquiterpene lactones, diterpenes, and phenolics from sunflower (Helianthus annuus L.) on western corn rootworm. J. Agric. Food Chem. 39:2293–2299.

    Google Scholar 

  71. Mullin, C. A., Chyb, S., Eichenseer, H., Hollister, B., and Frazier, J. L. 1994. Neuroreceptor mechanisms in insect gustation: A pharmacological approach. J. Insect Physiol. 40:913–931.

    Google Scholar 

  72. Murdock, L. L., Brookhart, G., Edgecomb, R. S., Long, T. F., and Sudlow, L. 1985. Do plants “psychomanipulate” insects? pp. 337–351, in P. A. Hedin (ed.). Bioregulators for Pest Control. ACS Symposium Series 276. American Chemical Society, Washington, DC.

    Google Scholar 

  73. Nauen, R., Ebbinghaus-kintscher, U., Elbert, A., Jeschke, P., and Tietjen, K. 2001. Acetylcholine receptors as sites for developing neonicotinoid insecticides, pp. 77–105, in I. Ishaaya (ed.). Biochemical Sites of Insecticide Action and Resistance. Springer-Verlag, Berlin.

    Google Scholar 

  74. Neal, J. J. 1989. Myristicin, safrole, and fagaramide as phytosynergists of xanthotoxin. J. Chem. Ecol. 15:309–315.

    Google Scholar 

  75. Oliver, F., Amon, E. U., Breathnach, A., Francis, D. M., Sarathchandra, P., Kobza black, A., and Greaves, M. W. 1991. Contact urticaria due to the common stinging nettle (Urtica dioica)—Histological, ultrastructural and pharmacological studies. Clin. Exp. Derm. 16:1–7.

    PubMed  Google Scholar 

  76. Osborne, R. H. 1996. Insect neurotransmission: Neurotransmitters and their receptors. Pharmacol. Ther. 69:117–142.

    PubMed  Google Scholar 

  77. Palumbo, J., Mullis, C., Jr., Reyes, F., and Amaya, A. 1997. Evaluation of foliar insecticide approaches for aphid management in head lettuce, pp. 171–177, in N. F. Oebker (ed.). 1997 Vegetable Report. University of Arizona Press, Tucson, Arizona.

    Google Scholar 

  78. Picman, A. K. 1986. Biological activities of sesquiterpene lactones. Biochem. Syst. Ecol. 14:255–281.

    Google Scholar 

  79. Porter, N. G. 1989. Composition and yield of commercial essential oils from parsley. 1: Herb oil and crop development. Flav. Frag. J. 4:207–219.

    Google Scholar 

  80. Price, K. R., Dupont, M. S., Shepherd, R., Chan, H. W., and Fenwick, G. R. 1990. Relationship between the chemical and sensory properties of exotic salad crops—Coloured lettuce (Lactuca sativa) and chicory (Cichorium intybus). J. Sci. Food Agric. 53:185–192.

    Google Scholar 

  81. Pytte, M. and Rygnestad, T. 1998. Nutmeg intoxication—A case report. Tidsskr Nor Laegeforen 118:4346–4347.

    PubMed  Google Scholar 

  82. Rees, S. B. and Harborne, J. B. 1985. The role of sesquiterpene lactones and phenolics in the chemical defense of the chicory plant. Phytochemistry 24:2225–2231.

    Google Scholar 

  83. Rehm, S., Enslin, P. R., Meeuse, A. D. J., and Wessels, J. H. 1957. Bitter principles of the Cucurbitaceae. VII: The distribution of bitter principles in this plant family. J. Sci. Food Agric. 8:679–691.

    Google Scholar 

  84. Reinold, S. and Hahlbrock, K. 1997. In situ localization of phenylpropanoid biosynthetic mRNAs and proteins in parsley (Petroselinum crispum). Bot. Acta 110:431–443.

    Google Scholar 

  85. Reitz, S. R. and Trumble, J. T. 1996. Tritrophic interactions among linear furanocoumarins, the herbivore Trichoplusia ni (Lepidoptera: Noctuidae), and the polyembryonic parasitoid Copidosoma floridanum (Hymenoptera: Encyrtidae). Environ. Entomol. 25:1391–1397.

    Google Scholar 

  86. Roberts, M. F., Mccarthy, D., Kutchan, T. M., and Coscia, C. J. 1983. Localization of enzymes and alkaloidal metabolites in Papaver latex. Arch. Biochem. Biophys. 222:599–609.

    PubMed  Google Scholar 

  87. Roeder, T. 1994. Biogenic amines and their receptors in insects. Comp. Biochem. Physiol. 107C:1–12.

    Google Scholar 

  88. Roshchina, V. V. 2001. Neurotransmitters in Plant Life. Science Publishers, Enfield, New Hampshire.

    Google Scholar 

  89. Sattelle, D. B. 1985. Acetylcholine receptors, pp. 395–434, in G. A. Kerkut and L. I. Gilbert (Eds.). Comprehensive Insect Physiology, Biochemistry and Pharmacology. Vol. 11: Pharmacology. Pergamon Press, New York.

    Google Scholar 

  90. Schenck, G. 1966. Pharmacology of nitrogen-free bitter principles of Lactuca virosa: Destruction of these substances during extraction and drying, pp. 112–117, in G. S. Sidhu, I. K. Kacker, P. B. Sattur, G. Thyagarajan, and V. R. K. Paramahamsa (Eds.). CNS Drugs: A Symposium Held at the Regional Research Laboratory Hyderabad, India, January 24–30, 1966. Sree Saraswaty Press, Calcutta, India.

    Google Scholar 

  91. Sessa, R. A., Bennett, M. H., Lewis, M. J., Mansfield, J. W., and Beale, M. H. 2000. Metabolite profiling of sesquiterpene lactones from Lactuca species. J. Biol. Chem. 275:26877–26884.

    PubMed  Google Scholar 

  92. Simon, J. E. and Quinn, J. 1988. Characterization of essential oil of parsley. J. Agric. Food Chem. 36:467–472.

    Google Scholar 

  93. Srivastava, S., Gupta, M. M., Prajapati, V., Tripathi, A. K., and Kumar, S. 2001. Insecticidal activity of myristicin from Piper mullesua. Pharm. Biol. 39:226–229.

    Google Scholar 

  94. Stahl-biskup, E. and Wichtmann, E. M. 1991. Composition of the essential oils from roots of some Apiaceae in relation to the development of their oil duct systems. Flav. Frag. J. 6:249–255.

    Google Scholar 

  95. Steelink, C., Yeung, M., and Caldwell, R. L. 1967. Phenolic constituents of healthy and wound tissues in the giant cactus (Carnegiea gigantea). Phytochemistry 6:1435–1440.

    Google Scholar 

  96. Stephens, H. A. 1980. Poisonous Plants of the Central United States. Regents Press of Kansas, Lawrence, Kansas.

    Google Scholar 

  97. Stevens, W. C. 1948. Kansas Wild Flowers. University of Kansas Press, Lawrence.

    Google Scholar 

  98. Sutherland, D. W. S. and Greene, G. L. 1984. Cultivated and wild host plants. US Dept. Agric. Tech. Bull. 1684:1–13.

    Google Scholar 

  99. Tallamy, D. W. 1985. Squash beetle feeding behavior: An adaptation against induced cucurbit defenses. Ecology 66:1574–1579.

    Google Scholar 

  100. Tallamy, D. W., Stull, J., Ehresman, N. P., Gorski, P. M., and Mason, C. E. 1997. Cucurbitacins as feeding and oviposition deterrents to insects. Environ. Entomol. 26:678–683.

    Google Scholar 

  101. Tamaki, H., Robinson, R. W., Anderson, J. L., and Stoewsand, G. S. 1995. Sesquiterpene lactones in virus-resistant lettuce. J. Agric. Food Chem. 43:6–8.

    Google Scholar 

  102. Thomson, W. T. 1998. Agricultural Chemicals Book. I: Insecticides, Acaricides and Ovicides. Thomson, Fresno, California.

    Google Scholar 

  103. Tibbitts, T. W. and Read, M. 1976. Rate of metabolite accumulation into latex of lettuce and proposed association with tipburn injury. J. Am. Soc. Hort. Sci. 101:406–409.

    Google Scholar 

  104. Trimmer, B. A. 1995. Current excitement from insect muscarinic receptors. TINS 18:104–111.

    PubMed  Google Scholar 

  105. Truitt, E. B., Jr. 1979. The pharmacology of myristicin and nutmeg, pp. 215–222, in D. H. Efron, B. Holmstedt, and N. S. Kline (Eds.). Ethnopharmacologic Search for Psychoactive Drugs. Raven Press, New York.

    Google Scholar 

  106. Truitt, E. B., Jr., Callaway, E., Braude, M. C., and Krantz, J. C., Jr. 1961. The pharmacology of myristicin: A contribution to the psychopharmacology of nutmeg. J. Neuropsychiatry 2:205–210.

    Google Scholar 

  107. Tune, R. and Dussourd, D. E. 2000. Specialized generalists: Constraints on host range in some plusiine caterpillars. Oecologia 123:543–549.

    Google Scholar 

  108. Watling, K. J. 1998. The RBI Handbook of Receptor Classification and Signal Transduction. RBI, Natick, Massachusetts.

    Google Scholar 

  109. Wink, M. 1998. Modes of action of alkaloids, pp. 301–326, in M. F. Roberts and M. Wink (Eds.). Alkaloids: Biochemistry, Ecology, and Medicinal Applications. Plenum, New York.

    Google Scholar 

  110. Wink, M. and Schneider, D. 1990. Fate of plant-derived secondary metabolites in three moth species (Syntomis mogadorensis, Syntomeida epilais, and Creatonotos transiens). J. Comp. Physiol. B 160:389–400.

    Google Scholar 

  111. Wu, S. and Hahlbrock, K. 1992. In situ localization of phenylpropanoid-related gene expression in different tissues of light-and dark-grown parsley seedlings. Z. Naturforsch.. 47c:591–600.

    Google Scholar 

  112. Zalucki, M. P., Clarke, A. R., and Malcolm, S. B. 2002. Ecology and behavior of first instar larval Lepidoptera. Annu. Rev. Entomol. 47:361–393.

    PubMed  Google Scholar 

  113. Zangerl, A. R. 1990. Furanocoumarin induction in wild parsnip: Evidence for an induced defense against herbivores. Ecology 71:1926–1932.

    Google Scholar 

  114. Zangerl, A. R. and Bazzaz, F. A. 1992. Theory and pattern in plant defense allocation, pp. 363–391, in R. S. Fritz and E. L. Simms (Eds.). Plant Resistance to Herbivores and Pathogens: Ecology, Evolution and Genetics. University of Chicago Press, Chicago, Illinois.

    Google Scholar 

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Dussourd, D.E. Chemical Stimulants of Leaf-Trenching by Cabbage Loopers: Natural Products, Neurotransmitters, Insecticides, and Drugs. J Chem Ecol 29, 2023–2047 (2003). https://doi.org/10.1023/A:1025630301162

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  • Trichoplusia ni
  • lactucin
  • myristicin
  • lobeline
  • Lactuca sativa
  • Petroselinum crispum
  • Lobelia cardinalis
  • plant–insect interactions
  • plant defense
  • laticifer
  • insect behavior