Summary
Comparisons were made of the eleotrophysiological responses of the maxillary gustatory receptors of the following categories of caterpillars: (1) three closely related species (Papilio polyxenes L.,P. troilus L., andP. glaucus L.) each of which feeds on a different group of plants; (2) two unrelated oligophagous species (P. glaucus L. andMalacosoma americana Fabr.) that have one preferred food plant in common; (3) three unrelated monophagous species (Danaus plexippus L.,Euchaetias egle Drury, andPygarctia eglenensis Clemens) that share the same plant. Materials tested included sodium chloride, carbohydrates, amino acids, glycosides, and the saps ofDaucus carota L. andFoeniculum vulgare Mill. (the food plants ofP. polyxenes),Sassafras albidum (Nutt.) andLindera Benzoin (L.) (the food plants ofP. troilus),Prunus virginiana L. (a favored food ofP. glaucus andM. americana),Asclepias syriaca L. andApocynum androsaemifolium L. (eaten byD. plexippus,E. egle, andP. eglenensis), andBrassica oleraceae L. (food plant ofPieris rapae).
The following conclusions were drawn: (1) no species of caterpillar gives a single standard electrophysiological response to all of the plants it rejects; that is, rejection is not a unitary modality; (2) a plant that is unacceptable to several species of caterpillars does not elicit the same pattern of response from each; (3) a food plant that is shared by several species of caterpillars does not elicit the same pattern of response from each; (4) a species of caterpillar that has more than one food plant does not generate the same sensory pattern to each; (5) there is no universal difference between sensory patterns for acceptance and those for rejection.
A model based upon the hypothesis of across-fiber patterning is proposed to explain these results. The essence of this model is that the receptors have unique but overlapping action spectra and that each compound or mixture of compounds in leaf saps that can be discriminated generates a unique total pattern of response. Whether or not a plant is ingested depends, therefore, not on the presence or absence of a single stimulant or deterrent but upon the total sensory impression derived from integrated response to multiple plant components. Prior to the first bite a caterpillar makes its first discrimination on the basis of olfactory clues.
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References
Bernays, E. A., Chapman, R. F.: Food selection byChorthippus parallelus (Zetterstedt) (Orthoptera: Acrididae) in the field. J. Animal Ecol.39, 383–394 (1970).
Bernays, E. A., Chapman, R. F.: Experiments to determine the basis of food selection byChorthippus parallelus (Zetterstedt) (Orthoptera: Acrididae) in the field. J. Animal Ecol.39, 761–776 (1970).
Bongers, W.: Aspects of host-plant relationship of the Colorado beetle. Mededelingen Landbouwhogeschool Wageningen 70-10, 1–77 (1970).
Chin, Chun-Teh: Studies on the physiological relations between the larvae ofLeptinotarsa decemlineata Say and some solanaceous plants. Tijdschr. Pl. ziekt.56, 1–88 (1950).
Colowick, S. P., Kaplan, N. O.: Methods in enzymology, vol. I, p. 143. New York and London: Academic Press 1955.
David, W. A. L., Gardiner, B. O. C.: The effect of sinigrin on the feeding ofPieris brassicae L. larvae transferred from various diets. Ent. exp. & appl.9, 95–98 (1966a).
David, W. A. L., Gardiner, B. O. C.: Mustard oil glucosides as feeding stimulants forPieris brassicae larvae in a semi-synthetic diet. Ent. exp. & appl.9, 247–255 (1966b).
Dethier, V. G.: Gustation and olfaction in lepidopterous larvae. Biol. Bull.72, 7–23 (1937).
Dethier, V. G.: Chemical factors determining the choice of food plants by Papilio larvae. Amer. Natur.75, 61–73 (1941).
Dethier, V. G., Kuch, J. H.: Electrophysiological studies of gustation in lepidopterous larvae. I. Comparative sensitivity to sugars, amino acids, and glycosides. Z. vergl. Physiol.72, 343–363 (1971).
Eger, H.: Über den Geschmackssinn von Schmetterlingsraupen. Biol. Zbl.57, 293–308 (1937).
Erickson, R.: Sensory neural patterns and gustation. In: Olfaction and taste, Y. Zotterman (ed.), p. 205–213. London-New York: Pergamon Press 1963.
Frings, H.: Gustatory rejection thresholds for the larvae of the cecropia moth,Samia cecropia (Linn). Biol. Bull.88, 37–43 (1945).
Götz, B.: Beiträge zur Analyse des Verhaltens von Schmetterlingsraupen beim Aufsuchen des Futters und des Verpuppungsplatzes. Z. vergl. Physiol.23, 429–503 (1936).
Goodhue, D.: Feeding stimulants required by a polyphagous insect.Schistocerca gregaria. Nature (Lond.)197, 405–406 (1963).
Hamamura, Y.: On the feeding mechanism and artificial food of silkworm,Bombyx mon. Mem. Kōnan Univ. Science Series, No. 8, Article 38, 19–22 (1965).
Hamamura, Y., Hayashiya, K., Naito, K., Matsuura, K., Nishida, J.: Food selection by silkworm larvae. Nature (Lond.)194, 754–755 (1962).
Haskell, P. T., Mordue, A. J.: The role of mouthpart receptors in the feeding behaviour ofSchistocerca gregaria. Ent. exp. et appl.12, 591–610 (1969).
Haskell, P. T., Paskin, M. W. J., Moorhouse, J. E.: Laboratory observations on factors affecting the movements of hoppers of the desert locust. J. Insect Physiol.8, 53–78 (1962).
Haskell, P. T., Schoonhoven, L. M.: The function of certain mouthpart receptors in relation to feeding inSchistocerca gregaria andLocusta migratoria migratorioides. Ent. exp. et appl.12, 423–440 (1969).
Hirao, T., Ishikawa, S.: Studies on olfactory sensation in the larvae of the silkworm,Bombyx mori (I) Chemotaxis of hatched larvae by olfactometer method [in Japanese]. J. Sericult. Sci. Japan33, 277–285 (1964).
House, H. L.: Effects of varying the ratio between the amino acids and the other nutrients in conjunction with a salt mixture on the flyAgria affinis (Fall). J. Insect Physiol.12, 299–310 (1966).
Ishikawa, S.: Responses of maxillary chemoreceptors in the larva of the silkworm,Bombyx mori, to stimulation by carbohydrates. J. cell. comp. Physiol.61, 99–107 (1963).
Ishikawa, S.: Electrical response and function of a bitter substance receptor associated with the maxillary sensilla of the silkworm,Bombyx mori L. J. cell Physiol.67, 1–11 (1966).
Ishikawa, S., Hirao, T.: Electrophysiological studies of taste sensation in the larvae of the silkworm,Bombyx mori. Responsiveness of sensilla styloconia in the maxilla [in Japanese]. Bull. Sericult. Exp. Sta.18, 297–357 (1963).
Ishikawa, S., Hirao, T.: Studies on olfactory sensation in the larvae of the silkworm,Bombyx mori (II) Chemotaxis of hatched larvae to various plantleaves [in Japanese]. J. Sericult. Sci. Japan34, 15–20 (1964).
Ishikawa, S., Hirao, T.: Studies on olfactory sensation in the larvae of the silkworm,Bombyx mori (III) Attractants and repellents of hatched larvae [in Japanese]. Bull. Sericult. Exp. Sta. Japan20, 21–36 (1965).
Ishikawa, S., Hirao, T.: Studies on feeding of the silkworm,Bombyx mori L. (I) Analysis of hostplant preference, especially of feeding-inhibition mechanisms [in Japanese]. Bull. Sericult. Exp. Sta.20, 291–321 (1966).
Ishikawa, S., Hirao, T., Arai, N.: Chemosensory basis of host plant selection in the silkworm. Ent. exp. & appl.12, 544–554 (1969).
Ishikawa, S., Tazima, Y., Hirao, T.: Responses of the chemoreceptors of maxillary sensory hairs in a “non-preference” mutant of the silkworm [in Japanese]. J. Sericult. Sci. Japan32, 125–129 (1963).
Jermy, T.: On the nature of the oligophagy inLeptinotarsa decemlineata Say (Coleoptera: Chrysomelidae). Acta Zool. Acad. Sci. Hungaricae7, 119–132 (1961 a).
Jermy, T.: Néhány szervetlen só rejektiv hátasa a burgonyabogár (Leptinolarsa decemlineata Say) imágóira és lárváira. (The rejective effects of some inorganic salts on Colorado beetle adults and larvae). Ann. Inst. Prot. Plant Hung.8, 121–130 (1961 b).
Jermy, T.: The role of rejective stimuli in the host selection of phytophagous insects. Proc. XII Int. Congr. Ent. London, Sec. 9a, p. 547 (1964).
Jermy, T.: Feeding inhibitors and food preference in chewing phytophagous insects. Ent. exp. & appl.9, 1–12 (1966).
Jermy, T., Hanson, F. E., Dethier, V. G.: Induction of specific food preference in lepidopterous larvae. Ent. exp. & appl.11, 211–230 (1968).
Krishna, S. S., Sinha, A. K.: Chemosensory relationship betweenEpilachna vigintiocto-punctata and its host plant,Luffa aegyptiaca. Ann. Ent. Soc. Amer.62, 928–929 (1969).
Lin, K., Kato, M., Yamada, M.: The effect of buffer solutions on the feeding activity of the silkworm,Bombyx mori L. Mem. Fac. Sci., Kyoto Univ., Series of Biology5, 57–65 (1971).
Ma, Wei-Chun: Some properties of gustation in the larva ofPieris brassicae. Ent. exp. & appl.12, 584–590 (1969).
Ma, Wei-Chun: Dynamics of feeding responses inPieris brassicae Linn. as a function of chemosensory input: a behavioural, ultrastructural and electrophysiological study. Mededelingen Landbouwhogeschool Wageningen 72-11, 1–162 (1972).
Nakajima, S.: Physiological functions of alkaloids and glycosides on silkworm larvae. J. Sericult. Sci. Japan10, 58–63 (1939) [in Japanese].
Nayar, J. K., Thornsteinson, A. J.: Further investigations into the chemical basis of insect-host relationships in an oligophagous insect,Plutella maculipennis (Curtis). Can. J. Zool.41, 923–929 (1963).
Niimura, M., Ito, T.: Feeding on filter paper by larvae of the silkworm,Bombyx mori L. J. Insect Physiol.10, 425–430 (1964).
Rees, C. J. C.: Chemoreceptor specificity associated with choice of feeding site by the beetle,Chrysolina brunsvicensis on its foodplant,Hypericum hirsutum. Ent. exp. & appl.12, 565–583 (1969).
Ritter, F. J.: Feeding stimulants for the Colorado beetle. Mededelingen Rijksfaculteit Landbouwwetenschappen Gent32, 291–305 (1967).
Schoonhoven, L. M.: Chemoreception of mustard oil glucosides in larvae ofPieris brassicae. Koninkl. Nederl. Akademie van Wetenschappen Amsterdam Proc., Series C,70, 556–568 (1967).
Schoonhoven, L. M.: Gustation and foodplant selection in some lepidopterous larvae. Ent. expl. & appl.12, 555–564 (1969).
Schoonhoven, L. M.: Plant recognition by lepidopterous larvae. Symp. Roy. Ent. Soc. London (1972a).
Schoonhoven, L. M.: Secondary plant substances and insects. Structural and functional aspects of phytochemistry, p. 197–224. New York and London: Academic Press 1972b.
Schoonhoven, L. M., Dethier, V. G.: Sensory aspects of host-plant discrimination by lepidopterous larvae. Arch, néerl. Zool.16, 497–530 (1966).
Schreiber, K.: Über einige Inhaltsstoffe der Solanaceen und ihre Bedeutung für die Kartoffelkäferresistenz. Ent. exp. & appl.1, 28–37 (1958).
Verschaffelt, E.: The cause determining the selection of food in some herbivorous insects. Proc. Roy. Acad. Amsterdam13, 536–542 (1910).
Wardojo, S.: Some factors relating to the larval growth of the Colorado potato beetleLeptinotarsa decemlineata Say (Coleoptera: Chrysomelidae), on artificial diets. Thesis, Wageningen 1–75 (1969).
Wensler, R. J. D.: Mode of host selection by an aphid. Nature (Lond.)195, 830–831 (1962).
Wilde, J. de: Host plant selection in the Colorado beetle larva (Leptinotarsa decemlineata Say). Ent. exp. & appl.1, 14–22 (1958).
Williams, L. H.: The feeding habits and food preferences of Acrididae and the factors which determine them. Trans. Roy. Ent. Soc. London105, 423–454 (1954).
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This work was supported by National Science Foundation Grant GB 1472 and the Class of 1877 Professorship of Princeton University.
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Dethier, V.G. Electrophysiological studies of gustation in lepidopterous larvae. J. Comp. Physiol. 82, 103–134 (1973). https://doi.org/10.1007/BF00696148
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DOI: https://doi.org/10.1007/BF00696148