Chew and spit: tree-feeding notodontid caterpillars anoint girdles with saliva

Abstract

Caterpillars of the notodontid Oedemasia leptinoides (formerly Schizura) use their mandibles to cut shallow girdles that encircle the petioles and stems of tree hosts. When girdles are complete, the larvae bathe the girdle surface with fluid. We test whether the fluid originates from the labial salivary glands or ventral eversible gland by blocking the openings to the glands and observing whether fluid is still released onto the girdles. Only larvae with functional labial salivary glands anointed girdles with fluid. Analysis of girdle rinses for a prominent salivary enzyme, glucose oxidase, confirmed that larvae apply saliva and documented that application occurs primarily at the end of girdling. We propose that girdling by notodontids, together with related furrowing and leaf-clipping behaviors exhibited by diverse caterpillar groups, serve at least in part to introduce salivary components to exposed vascular tissues; these compounds presumably function to suppress plant defensive responses normally elicited by caterpillar feeding.

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Acknowledgments

Many thanks to Madalyn Van Valkenburg for assistance in the laboratory and field, to Daniel Champion for assistance editing movies, to two anonymous reviewers for helpful suggestions, and to Jim Miller and David Wagner for providing useful information on notodontids. Financial support was provided by US Department of Agriculture–National Institute of Food and Agriculture Grant 2011-67013-30352 and National Science Foundation Grant IOS-1256326 (G.W.F), the University of Central Arkansas Research Council (D.E.D.), and the Arkansas Center for Plant-Powered Production (P3). The P3 Center is funded through the RII: Arkansas ASSET Initiatives (AR EPSCoR) I (EPS-0701890) and II (EPS-1003970) by the National Science Foundation and the Arkansas Science and Technology Authority.

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Correspondence to David E. Dussourd.

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Handling Editor: John F. Tooker.

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11829_2016_9416_MOESM1_ESM.m2v

Movie 1 Final instar Oedemasia leptinoides larva cutting a girdle in a pecan rachis. After 24 s, the film speed is gradually increased to ten times normal speed (m2v 152834 kb)

Movie 2 Closeup of a final instar Oedemasia leptinoides larva completing a girdle in a pecan rachis. The white fibrous girdle appears dry during the cutting procedure. At the end, the larva moves its head side to side as it rubs its spinneret back and forth over the surface, painting the girdle with saliva (mpg 121514 kb)

11829_2016_9416_MOESM3_ESM.m2v

Movie 3 Final instar Oedemasia leptinoides on filter paper impregnated with alkaline phenolphthalein. Contact with forceps caused the larva to discharge its VEG repeatedly, each time expelling formic acid directly at the forceps causing the pH sensitive paper to change from pink to white (m2v 21020 kb)

11829_2016_9416_MOESM4_ESM.m2v

Movie 4 Final instar Schizura ipomoeae completing a girdle in river birch, Betula nigra. During and especially after girdling, the larva wiped its labium over the girdle surface, thereby drenching the girdle in fluid, presumably saliva, as documented with O. leptinoides (m2v 238532 kb)

Movie 1 Final instar Oedemasia leptinoides larva cutting a girdle in a pecan rachis. After 24 s, the film speed is gradually increased to ten times normal speed (m2v 152834 kb)

Movie 3 Final instar Oedemasia leptinoides on filter paper impregnated with alkaline phenolphthalein. Contact with forceps caused the larva to discharge its VEG repeatedly, each time expelling formic acid directly at the forceps causing the pH sensitive paper to change from pink to white (m2v 21020 kb)

Movie 4 Final instar Schizura ipomoeae completing a girdle in river birch, Betula nigra. During and especially after girdling, the larva wiped its labium over the girdle surface, thereby drenching the girdle in fluid, presumably saliva, as documented with O. leptinoides (m2v 238532 kb)

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Dussourd, D.E., Peiffer, M. & Felton, G.W. Chew and spit: tree-feeding notodontid caterpillars anoint girdles with saliva. Arthropod-Plant Interactions 10, 143–150 (2016). https://doi.org/10.1007/s11829-016-9416-1

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Keywords

  • Girdling behavior
  • Saliva
  • Glucose oxidase
  • Labial salivary gland
  • Oedemasia leptinoides
  • Notodontidae