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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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References

  1. Akino T (2005) Chemical and behavioral study on the phytomimetic giant geometer Biston robustum Butler (Lepidoptera: Geometridae). Appl Entomol Zool 40:497–505

  2. Arimura G, Huber DPW, Bohlmann J (2004) Forest tent caterpillars (Malacosoma disstria) induce local and systemic diurnal emissions of terpenoid volatiles in hybrid poplar (Populus trichocarpa x deltoides): cDNA cloning, functional characterization, and patterns of gene expression of (−)-germacrene D synthase, PtdTPS1. Plant J 37:603–616

  3. Attygalle AB, Smedley SR, Meinwald J, Eisner T (1993) Defensive secretion of two notodontid caterpillars (Schizura unicornis, S. badia). J Chem Ecol 19:2089–2104

  4. Becker VO (2014) Checklist of New World Notodontidae (Lepidoptera: Noctuoidea). Lepid Novae 7:1–40

  5. Copolovici L, Kännaste A, Remmel T, Vislap V, Niinemets Ü (2011) Volatile emissions from Alnus glutionosa induced by herbivory are quantitatively related to the extent of damage. J Chem Ecol 37:18–28

  6. Coppedge BR (2011) Twig morphology and host effects on reproductive success of the twig girdler Oncideres cingulata (Say) (Coleoptera: Cerambycidae). Coleopt Bull 65:405–410

  7. Corella-Madueño MA, Harris MK, Fu-Castillo AA, Martínez-Téllez MA, Valenzuela-Soto EM, Gálvez-Ruiz JC, Vargas-Arispuro I (2011) Volatiles emitted by Carya illinoinensis (Wang.) K. Koch as a prelude for semiochemical investigations to focus on Acrobasis nuxvorella Nuenzig (Lepidoptera: Pyralidae). Pest Manag Sci 67:1522–1527

  8. Degenhardt J (2008) Ecological roles of vegetative terpene volatiles. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, New York, pp 433–442

  9. Delaney KJ (2008) Injured and uninjured leaf photosynthetic responses after mechanical injury on Nerium oleander leaves, and Danaus plexippus herbivory on Asclepias curassavica leaves. Plant Ecol 199:187–200

  10. Delaney KJ, Higley LG (2006) An insect countermeasure impacts plant physiology: midrib vein cutting, defoliation and leaf photosynthesis. Plant, Cell Environ 29:1245–1258

  11. Delphia CM, Mescher MC, Felton GW, De Moraes CM (2006) The role of insect-derived cues in eliciting indirect plant defenses in tobacco, Nicotiana tabacum. Plant Signal Behav 1:243–250

  12. Detwiler JD (1922) The ventral prothoracic gland of the red-humped apple caterpillar (Schizura concinna Smith & Abbot). Can Entomol 54:176–191

  13. Dussourd DE (1993) Foraging with finesse: caterpillar adaptations for circumventing plant defenses. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constraints on foraging. Chapman and Hall, New York, pp 92–131

  14. Dussourd DE (2009) Do canal-cutting behaviours facilitate host-range expansion by insect herbivores? Biol J Linn Soc 96:715–731

  15. Dussourd DE (2015) Theroa zethus caterpillars use acid secretion of anti-predator gland to deactivate plant defense. PLoS ONE 10(10):e0141924. doi:10.1371/journal.pone.0141924

  16. Dussourd DE, Denno RF (1991) Deactivation of plant defense: correspondence between insect behavior and secretary canal architecture. Ecology 72:1383–1396

  17. Edwards PB, Wanjura WJ (1989) Eucalypt-feeding insects bite off more than they can chew: sabotage of induced defenses? Oikos 54:246–248

  18. Eichenseer H, Mathews MC, Powell JS, Felton GW (2010) Survey of a salivary effector in caterpillars: glucose oxidase variation and correlation with host range. J Chem Ecol 36:885–897

  19. Eisner T, Kluge AF, Carrel JC, Meinwald J (1972) Defense mechanisms of arthropods. XXXIV. Formic acid and acyclic ketones in the spray of a caterpillar. Ann Entomol Soc Am 65:765–766

  20. Fahn A (1979) Secretory tissues in plants. Academic Press, New York

  21. Farag MA (2008) Headspace analysis of volatile compounds in leaves from the Juglandaceae (walnut) family. J Essent Oil Res 20:323–327

  22. Felton GW (2008) Caterpillar secretions and induced plant responses. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, Berlin, pp 369–387

  23. Felton GW, Chung SH, Hernandez MGE, Louis J, Peiffer M, Tian D (2014) Herbivore oral secretions are the first line of protection against plant-induced defences. In: Voelckel C, Jander G (eds) Annual plant reviews, vol 47. Insect-plant interactions. Wiley, Oxford, pp 37–76

  24. Ganong CN, Dussourd DE, Swanson JD (2012) Girdling by notodontid caterpillars: distribution and occurrence. Arthropod-Plant Interact 6:621–633

  25. Girón-Calva PS, Li T, Koski T-M, Klemola T, Laaksonen T, Huttunen L, Blande JD (2014) A role for volatiles in intra- and inter-plant interactions in birch. J Chem Ecol 40:1203–1211

  26. Gueldner RC, Yates IE, Reilly CC, Wood BW, Smith MT (1994) Levels of hydrojuglone glucoside in developing pecan leaves in relation to scab susceptibility. J Am Soc Hortic Sci 119:498–504

  27. Harmel N, Létocart E, Cherqui A, Giordanengo P, Mazzuccelli G, Guillonneau F, De Pauw E, Haubruge E, Francis F (2008) Identification of aphid salivary proteins: a proteomic investigation of Myzus persicae. Insect Mol Biol 17:165–172

  28. Heckel DG (2014) Insect detoxification and sequestration strategies. In: Voelckel C, Jander G (eds) Annual plant reviews, vol 47. Insect-plant interactions. Wiley, Oxford, pp 77–114

  29. Heinrich B, Collins SL (1983) Caterpillar leaf damage, and the game of hide-and-seek with birds. Ecology 64:592–602

  30. Kant MR, Jonckheere W, Knegt B, Lemos F, Liu J, Schimmel BCJ, Villarroel CA, Ataide LMS, Dermauw W, Glas JJ, Egas M, Janssen A, Van Leeuwen T, Schuurink RC, Sabelis MW, Alba JM (2015) Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities. Ann Bot 115:1015–1051

  31. Karban R, Agrawal AA (2002) Herbivore offense. Ann Rev Ecol Syst 33:641–664

  32. Lindroth RL, Anson BD, Weisbrod AV (1990) Effects of protein and juglone on gypsy moths: growth performance and detoxification enzyme activity. J Chem Ecol 16:2533–2547

  33. McCormick AC, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 17:303–310

  34. Metcalfe CR, Chalk L (1983) Anatomy of the Dicotyledons, vol II. Clarendon Press, Oxford

  35. Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy JB, Felton GW (2002) Caterpillar saliva beats plant defenses. Nature 416:599–600

  36. Paro CM, Arab A, Vasconcellos-Neto J (2014) Specialization of Atlantic rain forest twig-girdler beetles (Cerambycidae: Lamiinae: Onciderini): variation in host-plant use by microhabitat specialists. Arthropod-Plant Interact 8:557–569

  37. Peiffer M, Felton GW (2005) The host plant as a factor in the synthesis and secretion of salivary glucose oxidase in larval Helicoverpa zea. Arch Insect Biochem Physiol 58:106–113

  38. R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org. Accessed on 10 July 2014

  39. Risley LS, Crossley DA Jr (1988) Herbivore-caused greenfall in the southern Appalachians. Ecology 69:1118–1127

  40. Roth LM, Eisner T (1962) Chemical defenses of arthropods. Ann Rev Entomol 7:107–137

  41. Schintlmeister A (2013) Notodontidae and Oenosandridae (Lepidoptera). Brill, Boston

  42. Scriber JM (1996) Tiger tales: natural history of native North American swallowtails. Am Entomol 42:19–22

  43. Thiboldeaux RL, Lindroth RL, Tracy JW (1994) Differential toxicity of juglone (5-hydroxy-1,4-naphthoquinone) and related naphthoquinones to saturniid moths. J Chem Ecol 20:1631–1641

  44. Turlings TCJ, Wäckers F (2004) Recruitment of predators and parasitoids by herbivore-injured plants. In: Cardé R, Millar JG (eds) Advances in insect chemical ecology. Cambridge University Press, Cambridge, pp 21–75

  45. Vargas-Arispuro I, Corella-Madueño MAG, Harris MK, Martínez-Téllez MA, Gardea AA, Fu-Castillo A, Orozco-Avitia A (2013) Semiochemicals released by pecan alleviate physiological suppression in overwintering larvae of Acrobasis nuxvorella (Lepidoptera: Pyralidae). Environ Entomol 42:942–948

  46. Voelckel C, Jander G (2014) Annual plant reviews, vol 47. Insect-plant interactions. Wiley, Oxford

  47. Weech M, Chapleau M, Pan L, Ide C, Bede JC (2008) Caterpillar saliva interferes with induced Arabidopsis thaliana defence responses via the systemic acquired resistance pathway. J Exp Bot 59:2437–2448

  48. Weinstein P (1990) Leaf petiole chewing and sabotage of induced defenses. Oikos 58:231–233

  49. Wu S, Peiffer M, Luthe DS, Felton GW (2012) ATP hydrolyzing salivary enzymes of caterpillars suppress plant defenses. PLoS ONE 7:e41947

  50. Zebelo SA, Maffei ME (2012) The ventral eversible gland (VEG) of Spodoptera littoralis triggers early responses to herbivory in Arabidopsis thaliana. Arthropod-Plant Interact 6:543–551

  51. Zebelo S, Piorkowski J, Disi J, Fadamiro H (2014) Secretions from the ventral eversible gland of Spodoptera exigua caterpillars activate defense-related genes and induce emission of volatile organic compounds in tomato, Solanum lycopersicum. BMC Plant Biol 14:140

  52. Zhu H, Liu G, Cao F, Sheng J, Zhou B (2013) Volatile components of pecan leaves from different cultivars of Carya illinoensis Koch. J Essent Oil Bear Plants 16:144–150

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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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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)

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)

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