Hostname: page-component-76fb5796d-vvkck Total loading time: 0 Render date: 2024-04-26T09:17:05.290Z Has data issue: false hasContentIssue false
  • English
  • Français

Effectiveness of the defence mechanism of the turnip sawfly, Athalia rosae (Hymenoptera: Tenthredinidae), against predation by lizards

Published online by Cambridge University Press:  09 March 2007

L. Vlieger ,
P.M. Brakefield  and
C. Müller
L. Vlieger
Affiliation:
Institute of Biology, Leiden University, PO Box 9516, NL-2300 RA Leiden, The Netherlands
P.M. Brakefield
Affiliation:
Institute of Biology, Leiden University, PO Box 9516, NL-2300 RA Leiden, The Netherlands
C. Müller*
Affiliation:
Institute of Biology, Leiden University, PO Box 9516, NL-2300 RA Leiden, The Netherlands Institut für Biowissenschaften, Universität Würzburg, Julius-von-Sachs-Platz 3, D-97082 Würzburg, Germany
*
*Fax: + 49 / 931 888 62 35 E-mail: cmueller@botanik.uni-wuerzburg.de
Get access Rights & Permissions [Opens in a new window]

Abstract

The turnip sawfly, Athalia rosae Linnaeus, is a pest on cruciferous crops. Larvae sequester secondary plant compounds, namely glucosinolates, in their haemolymph. When attacked, their integument is easily disrupted and a droplet of haemolymph is exuded (‘easy bleeding’). This has been shown to be an effective, chemical-based, defence against invertebrate predators. The efficiency of this proposed defence was tested against a vertebrate predator, using groups of the iguanid lizard Anolis carolinensis Voigt as a model predator. Caterpillars of Pieris rapae Linnaeus and Pieris brassicae Linnaeus served as control prey species that do not sequester glucosinolates. Lizards attacked far fewer sawfly larvae than pierid caterpillars. Several of the sawfly larvae were rejected after an initial attack, demonstrating unpalatability to the lizards, while the Pieris larvae were not rejected. However, P. rapae larvae topically treated with extracts of haemolymph of A. rosae had no deterrent effect on the lizards and no avoidance learning occurred over a period of two weeks. Adult sawflies do not easy bleed but have glucosinolates carried over from the larval stage. Lizards attacked them at a higher rate than larvae and they were never rejected. The results suggest that for the defensive effectiveness of the pest sawfly species against vertebrates the chemical cue is not necessarily sufficient. Movement and colour may be important additional factors triggering the behaviour of vertebrate predators.

Type
Review Article
Information
Bulletin of Entomological Research , Volume 94 , Issue 3 , June 2004 , pp. 283 - 289
Copyright
Copyright © Cambridge University Press 2004

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aliabadi, A., Renwick, J.A.A. & Whitman, D.W. (2002) Sequestration of glucosinolates by Harlequin bug Murcantia histrionica. Journal of Chemical Ecology 28, 1749–1762.CrossRefGoogle ScholarPubMed
Aplin, R.T., D'Arcy, Ward R. & Rothschild, M. (1975) Examination of the large white and small white butterflies (Pieris spp.) for the presence of mustard oils and mustard oil glycosides. Journal of Entomology, Part A: Physiology and Behaviour 50, 73–78.Google Scholar
Benson, R.B. (1950) An introduction to the natural history of British sawflies (Hymenoptera Symphyta). Transactions of the Society for British Entomology 10, 45–142.Google Scholar
Boevé, J.-L. & Schaffner, U. (2003) Why does the larval integument of some sawfly species disrupt so easily? The harmful hemolymph hypothesis. Oecologia 134, 104–111.Google ScholarPubMed
Bowers, M.D. (1992) The evolution of unpalatability and the cost of chemical defense in insects. pp. 216–244in Roitberg, B.D. & Isman, M.B. (Eds) Insect chemical ecology. An evolutionary approach. New York, Chapman and Hall.Google Scholar
Boyden, T.C. (1976) Butterfly palatability and mimicry. Experiments with Ameiva lizards. Evolution 30, 73–81.CrossRefGoogle ScholarPubMed
Burghardt, G. (1964) Effects of prey size and movement on the feeding behaviour of the lizards Anolis carolinensis and Eucemes faciatus. Copeia 1, 576–578.CrossRefGoogle Scholar
Chew, F.S. (1988) Biological effects of glucosinolates. pp. 155–181in Cutler, H.G.(Ed.) Biologically active natural products - potential use in agriculture. Washington DC, American Chemical Society Symposium.CrossRefGoogle Scholar
Chew, F.S. (1995) Host plant choice in Pieris butterflies. pp. 214–238in Carde, R.T. & Bell, W.J. (Eds) Chemical ecology of insects. New York, Chapman and Hall.CrossRefGoogle Scholar
Curio, E. (1970) Die Selektion dreier Raupenformen eines Schwarmers (Lepidopt., Shingidae) durch einen Anolis (Rept., Iguanidae). Zeitschrift für Tierpsychologie 27, 899–914.CrossRefGoogle Scholar
Fahey, J.W., Zalcmann, A.T. & Talalay, P. (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56, 5–51.CrossRefGoogle ScholarPubMed
Fleishman, L.J. (1986) Motion detection in the presence and absence of background motion in an Anolis lizard. Journal of Comparative Physiology A, Sensory, Neural and Behavioural Physiology 159, 711–720.CrossRefGoogle Scholar
Fleishman, L.J. (1992) The influence of the sensory system and the environment on motion patterns in the visual display of anoline lizards and other vertebrates. American Naturalist 139, 36–61.CrossRefGoogle Scholar
Giamoustaris, A. & Mithen, R. (1995) The effect of modifying the glucosinolate content of leaves of oilseed rape (Brassica napus ssp. oleifera) on its interaction with specialist and generalist pests. Annals of Applied Biology 126, 347–363.CrossRefGoogle Scholar
Goodman, D. (1971) Differential selection of immobile prey among terrestrial and riparian lizards. American Midland Naturalist 86, 217–219.CrossRefGoogle Scholar
Guilford, D. (1990) The secrets of aposematism – unlearned responses to specific colors and patterns. Trends in Ecology and Evolution. 5, 323.CrossRefGoogle Scholar
Heads, P.A. (1986) Bracken, ants and extrafloral nectaries. IV. Do wood ants (Formica lugubris) protect the plant against insect herbivores?. Journal of Animal Ecology 55, 795–809.CrossRefGoogle Scholar
Heads, P.A. & Lawton, J.H. (1985) Bracken, ants and extrafloral nectaries. III. How insect herbivores avoid ant predation. Ecological Entomology 10, 29–42.CrossRefGoogle Scholar
Hilker, M.Köpf, A. (1994) Evaluation of the palatability of chrysomelid larvae containing anthraquinones to birds. Oecologia 100, 421–429.CrossRefGoogle ScholarPubMed
Louda, S. & Mole, S. (1991) Glucosinolates: chemistry and ecology. pp. 123–164in Rosenthal, G.A. & Berenbaum, M.R. (Eds) Herbivores and their interactions with secondary plant metabolites. Chemical participants. New York, Academic Press.CrossRefGoogle Scholar
Lyytinen, A., Brakefield, P.M. & Mappes, J. (2003) Significance of butterfly eyespots as an anti-predator device in ground-based and aerial attacks. Oikos 100, 373–379.CrossRefGoogle Scholar
Müller, C. & Brakefield, P.M. (2003) Analysis of a chemical defence in sawfly larvae: easy bleeding targets predatory wasps in late summer. Journal of Chemical Ecology 29, 2683–2694.CrossRefGoogle ScholarPubMed
Müller, C., Agerbirk, N., Olsen, C.E., Boevé, J.L., Schaffner, U. & Brakefield, P.M. (2001) Sequestration of host plant glucosinolates in the defensive haemolymph of the sawfly Athalia rosae. Journal of Chemical Ecology 27, 2505–2516.CrossRefGoogle ScholarPubMed
Müller, C.Boevé, J.L. & Brakefield, P.M. (2002) Host plant derived feeding deterrence towards ants in the turnip sawfly Athalia rosae. Entomologia Experimentalis et Applicata 104, 153–157.CrossRefGoogle Scholar
Müller, C., Agerbirk, N. & Olsen, C.E. (2003) Lack of sequestration of host plant glucosinolates in Pieris rapae and P. brassicae. Chemoecology, 47–54.CrossRefGoogle Scholar
Newman, R.M., Hanscom, Z. & Kerfoot, W.C. (1992) The watercress glucosinolates-myrosinase system: a feeding deterrent to caddisflies, snails and amphipods. Oecologia 92, 1–7.CrossRefGoogle Scholar
Nielsen, J.K. (1988) Crucifer-feeding Chrysomelidae: mechanisms of host plant ?nding and acceptance. pp. 25–40in Jolivet, P., Petitpierre, E. & Hsiao, T.H. (Eds) Biology of Chrysomelidae. Dordrecht, Kluwer Academic Publishers.CrossRefGoogle Scholar
Nishida, R. & Fukami, H. (1990) Sequestration of distasteful compounds by some pharmacophagous insects. Journal of Chemical Ecology 16, 151–164.CrossRefGoogle ScholarPubMed
Odendaal, F.J., Rausher, M.D., Benrey, B. & Nunez-Farfan, J. (1987) Predation by Anolis lizards on Battus philenor raises questions about butterfly mimicry systems. Journal of the Lepidopterists’ Society 41, 141–144.Google Scholar
Ohara, Y., Nagasaka, K. & Ohsaki, N. (1993) Warning coloration on sawfly Athalia rosae larva and concealing coloration in butterfly Pieris rapae larva feeding on similar plants evolved through individual selection. Research on Population Ecology 35, 223–230.CrossRefGoogle Scholar
Renwick, J.A.A. (2002) The chemical world of crucifers: lures, treats and traps. Entomologia Experimentalis et Applicata 104, 35–42.CrossRefGoogle Scholar
Roughgarden, J. (1995) Anolis lizards of the Caribbean; ecology, evolution and plate tectonics. New York, Oxford University Press.CrossRefGoogle Scholar
Schaffner, U., Boevé, J.L., Gfeller, H. & Schlunegger, U.P. (1994) Sequestration of Veratrum alkaloids by specialist Rhadinoceraea nodicornis Konow (Hymenoptera, Tenthredinidae) and its ecoethological implications. Journal of Chemical Ecology 20, 3233–3250.CrossRefGoogle Scholar
Schoonhoven, L.M., Jermy, L., van & Loon, J.J.A. (1998) Insect-plant biology. From physiology to evolution. London, Chapman and Hall.CrossRefGoogle Scholar
Schwenk, K. (1995) Occurrence, distribution and functional significance of taste buds in lizards. Copeia 1, 91–101.Google Scholar
Sexton, O.J. (1960) Experimental studies of artificial Batesian mimics. Behaviour 15, 244–252.CrossRefGoogle Scholar
Sexton, O.J. (1964) Differential predation by the lizard Anolis carolinensis upon unicoloured and polycoloured insects after an interval of no contact. Animal Behaviour 12, 101–110.CrossRefGoogle Scholar
Sexton, O.J., Hoger, C. & Ortleb, E. (1966) Anolis carolinensis: effects of feeding on reaction to aposematic prey. Science 153, 1140.CrossRefGoogle ScholarPubMed
Shafir, S. & Roughgarden, J. (1994) Instrumental discrimination conditioning of Anolis cristatellus in the field with food as a reward. Caribbean Journal of Science 30, 228–233.Google Scholar
Stanger-Hall, K.F., Zelmer, D.A., Bergren, C. & Burns, S.A. (2001) Taste discrimination in a lizard (Anolis carolinensis, Polychrotidae). Copeia 2, 490–498.CrossRefGoogle Scholar
Sword, G.A. (1999) Density-dependent warning coloration. Nature 397, 217.CrossRefGoogle Scholar
Sword, G.A. (2001) Tasty on the outside, but toxic in the middle: grasshopper regurgitation and host-plant mediated toxicity to a vertebrate predator. Oecologia 128, 416–421.CrossRefGoogle ScholarPubMed
Sword, G.A., Simpson, S.J., El Hadi, O.T.M. & Wilps, H. (2000) Density-dependent aposematism in the desert locust. Proceedings of the Royal Society, Series B 267, 63–68.CrossRefGoogle ScholarPubMed
Trigo, J.R. (2000) The chemistry of antipredator defense by secondary compounds in neotropical Lepidoptera: facts, perspectives and caveats. Journal of the Brazilian Chemical Society 11, 551–561.CrossRefGoogle Scholar
Weber, G., Oswald, S.Zöllner, U. (1986) Die Wirtseignung von Rapssorten unterschiedlichen Glucosinolatgehaltes für Brevicoryne brassicae (L.) und Myzus persicae (Sulzer) (Hemiptera, Aphididae). Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz 93, 113–124.Google Scholar
Whelan, C.J., Holmes, R.T. & Smith, H.R. (1989) Bird predation on gypsy moth (Lepidoptera: Lymantriidae) larvae: an aviary study. Environmental Entomology 18, 43–45.CrossRefGoogle Scholar