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Disruption of web structure and predatory behavior of a spider by plant-derived chemical defenses of an aposematic aphid

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Abstract

Two toxic and bitter-tasting cardenolides (cardiac-active steroids) were sequestered by the brightly colored oleander aphid,Aphis nerii B. de F., from the neotropical milkweed host plantAsclepias curassavica L. After feeding on milkweed-reared aphids, the orb-web spiderZygiella x-notata (Clerck) built severely disrupted webs and attacked fewer nontoxic, control aphids, whereas the webs of spiders fed only nontoxic aphids remained intact. The regularity and size of the prey-trapping area of webs were reduced significantly in proportion to the amount of toxic aphids eaten. The effects of toxic aphids on spider web structure were mimicked by feeding spiders the bitter-tasting cardenolide digitoxin, a cardenolide with similar steroidal structure and pharmacological activity to the two aphid cardenolides. These results show that the well-known effects of psychoactive drugs on spider web structure are more than interesting behavioral assays of drag activity. Similar effects, produced by plant-derived chemicals in the spider's aphid prey, are relevant to the ecology and evolution of interactions between prey defense and predator foraging.

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References

  • Barth, F.G. 1982. Spiders and vibratory signals: sensory reception and behavioral significance, pp. 67–122,in P.N. Witt and J.S. Rovner (eds.). Spider Communication: Mechanisms and Ecological Significance. Princeton University Press, Princeton, New Jersey.

    Google Scholar 

  • Blum, M.S. 1981. Chemical Defenses of Arthropods. Academic Press, New York.

    Google Scholar 

  • Brower, L.P. 1969. Ecological chemistry.Sci. Am. 220:22–29.

    Google Scholar 

  • Brower, L.P., Ryerson, W.N., Coppinger, L.L., andGlazier, S.C. 1968. Ecological chemistry and the palatability spectrum.Science 161:1349–1351.

    Google Scholar 

  • Brower, L.P., Edmunds, M., andMoffitt, C.M. 1975. Cardenolide content and palatability of a population ofDanaus chrysippus butterflies from West Africa.J. Entomol. (A) 49:183–196.

    Google Scholar 

  • Brown, K.S., Jr. 1984. Adult-obtained pyrrolizidine alkaloids defend ithomiine butterflies against a spider predator.Nature 309:707–709.

    Google Scholar 

  • Brown, K.S., Jr., Cameron, D.W., andWeiss, U. 1969. Chemical constituents of the bright orange aphidAphis nerii Fonscolombe. I. Neriaphin and 6-hydroxymusizin 8-0-β-d-glucoside.Tetrahedron Lett. 6:471–476.

    Google Scholar 

  • Carrel, J.E., andEisner, T. 1984. Spider sedation induced by defensive chemicals of millipede prey.Proc. Natl. Acad. Sci. USA 81:806–810.

    Google Scholar 

  • Craig, C.L. 1986. Orb-web visibility: The influence of insect flight behaviour and visual physiology on the evolution of web designs within the Araneoidea.Anim. Behav. 34:54–68.

    Google Scholar 

  • Duffey, S.S. 1977. Arthropod allomones: chemical effronteries and antagonists. Proceedings of XV International Congress of Entomology, 1976. Washington, D.C. pp. 323–394.

  • Eberhard, W. 1986. Effects of orb-web geometry on prey interception and retention, pp. 70–100,in W.A. Shear (ed.). Spiders. Webs, Behavior, and Evolution. Stanford University Press, Stanford, California.

    Google Scholar 

  • Foelix, R.F. 1982. Biology of Spiders. Harvard University Press, Cambridge, Massachusetts.

    Google Scholar 

  • Ford, M.J. 1977. Energy costs of the predation strategy of the web-spinning spiderLepthyphantes zimmermanni Berktau (Linyphiidae).Oecologia 28:341–349.

    Google Scholar 

  • Gertsch, W.J. 1964. The spider genusZygiella in North America (Araneae, Argiopidae).Am. Mus. Novit. 2188:1–21.

    Google Scholar 

  • Gillespie, R.G. 1981. The quest for prey by the web-building spiderAmaurobius similis (Blackwell).Anim. Behav. 29:953–954.

    Google Scholar 

  • Hurlbert, S.H. 1984. Pseudoreplication and the design of ecological field experiments.Ecol. Monogr. 54:187–211.

    Google Scholar 

  • Jackson, R.R. 1974. Effects ofd-amphetamine sulfate and diazepam on thread connection fine structure in a spider's web.J. Arachnol. 2:37–41.

    Google Scholar 

  • Janetos, A.C. 1982. Foraging tactics of two guilds of web-spinning spiders.Behav. Ecol. Sociobiol. 10:19–27.

    Google Scholar 

  • Janetos, A.C. 1986. Web-site selection: are we asking the right questions? pp. 9–22,in W.A. Shear (ed.). Spiders. Webs, Behavior, and Evolution. Stanford University Press, Stanford, California.

    Google Scholar 

  • Klärner, D., andBarth, R. 1982. Vibratory signals and prey capture in orb-weaving spiders (Zygiella x-notata, Nephila clavipes; Araneidae).J. Comp. Physiol. 148:445–455.

    Google Scholar 

  • Lehninger, A.L. 1975. Biochemistry. 2nd ed. Worth Publishers, New York.

    Google Scholar 

  • Levi, H.W. 1974. The orb-weaver genusZygiella (Araneae: Araneidae).Bull. Mus. Comp. Zool. 146:267–290.

    Google Scholar 

  • Malcolm, S.B. 1981. Defensive use of plant-derived cardenolides byAphis nerii Boyer de Fonscolombe against predation. D. Phil, thesis. University of Oxford, U.K.

    Google Scholar 

  • Malcolm, S.B. 1986. Aposematism in a soft-bodied insect: A case for kin seiection.Behav. Ecol. Sociobiol. 18:387–393.

    Google Scholar 

  • Masters, W.M. 1984a. Vibrations in the orbwebs ofNuctenea sclopetaria (Araneidae) I. Transmission through the web.Behav. Ecol. Sociobiol. 15:207–215.

    Google Scholar 

  • Masters, W.M. 1984b. Vibrations in the orbwebs ofNuctenea sclopetaria (Araneidae) II. Prey and wind signals and the spider's response threshold.Behav. Ecol. Sociobiol. 15:217–223.

    Google Scholar 

  • Meyer, W. 1979. Phosphatases in the central nervous system of spiders (Arachnida, Araneae).Histochemistry 59:177–187.

    Google Scholar 

  • Murakami, Y. 1983. Factors determining the prey size of the orb-web spider,Argiope amoena (L. Koch)(Argiopidae).Oecologia 57:72–77.

    Google Scholar 

  • Murdoch, W.W. 1971. The developmental response of predators to changes in prey density.Ecology 52:132–137.

    Google Scholar 

  • Nentwig, W. 1983. The non-filter function of orb webs in spiders.Oecologia 58:418–420.

    Google Scholar 

  • Nentwig, W., andWissel, C. 1986. A comparison of prey lengths among spiders.Oecologia 68:595–600.

    Google Scholar 

  • Nie, N.H., Hull, C.H., Jenkins, J.G., Steinbrenner, K., andBrent, D.H. 1975. Statistical Package for the Social Sciences. 2nd ed. McGraw-Hill, New York.

    Google Scholar 

  • Nyffeler, M., andBenz, G. 1981. Freilanduntersuchungen zur Nahrangsökologie der Spinnen: Beobachtungen aus der Region Zürich.Anz. Schaedlingskd. Pflanz. Umweltschutz 54:33–39.

    Google Scholar 

  • Olive, C.W. 1982. Behavioral response of a sit-and-wait predator to spatial variation in foraging gain.Ecology 63:912–920.

    Google Scholar 

  • Parsons, J.A. 1965. A digitalis-like toxin in the monarch butterflyDanaus plexippus.J. Physiol. London. 178:290–304.

    Google Scholar 

  • Reichstein, T. 1967. Cardenolide (herzwirksame Glykoside) als Abwehrstoffe bei Insekten.Naturwiss. Rundsch. 20:499–511.

    Google Scholar 

  • Reichstein, T., Von Euw, J., Parsons, J.A., andRothschild, M. 1968. Heart poisons in the monarch butterfly.Science 161:861–866.

    Google Scholar 

  • Riechert, S.E., andGillespie, R.G. 1986. Habitat choice and utilization in web-building spiders, pp. 23–48,in W.A. Shear (ed.). Spiders. Webs, Behavior, and Evolution. Stanford University Press, Stanford, California.

    Google Scholar 

  • Riechert, S.E., andLuczak, J. 1982. Spider foraging: Behavioral responses to prey, pp. 353–385,in P.N. Wittand, J.S. Rovner (eds.). Spider Communication: Mechanisms and Ecological Significance. Princeton University Press, Princeton, New Jersey.

    Google Scholar 

  • Roeske, C.N., Seiber, J.N., Brower, L.P., andMoffitt, C.M. 1976. Milkweed cardenolides and their comparative processing by monarch butterflies (Danaus plexippus L.).Recent Adv. Phytochem. 10:93–167.

    Google Scholar 

  • Rothschild, M., von Euw, J., andReichstein, T. 1970. Cardiac glycosides in the oleander aphidAphis nerii.J. Insect Physiol. 16:1191–1195.

    Google Scholar 

  • Rothschild, M., von Euw, J., Reichstein, T., Smith, D.A.S., andPierre, J. 1975. Cardenolide storage inDanaus chrysippus (L.) with additional notes onD. plexippus (L.).Proc. R. Soc. (B) 190:1–31.

    Google Scholar 

  • Rypstra, A.L. 1982. Building a better insect trap; an experimental investigation of prey capture in a variety of spider webs.Oecologia 52:31–36.

    Google Scholar 

  • Suter, R.B. 1978.Cyclosa turbinata (Araneae, Araneidae): Prey discrimination via web-borne vibrations.Behav. Ecol. Sociobiol. 3:283–296.

    Google Scholar 

  • Stephens, D.W., andKrebs, J.R. 1986. Foraging Theory. Princeton University Press, Princeton, New Jersey.

    Google Scholar 

  • Turnbull, A.L. 1964. The search for prey by a web-building spiderAchaearanea tepidarionum (C.L. Koch) (Araneae, Theridiidae).Can. Entomol. 96:568–579.

    Google Scholar 

  • Uetz, G.W., Johnson, A.D., andSchemske, D.W. 1978. Web placement, web structure, and prey capture in orb-weaving spiders.Bull. Br. Arachnol. Soc. 4:141–148.

    Google Scholar 

  • Vasconcellos-Neto, J., andLewinsohn, T.M. 1984. Discrimination and release of unpalatable butterflies byNephila davipes, a neotropical orb-weaving spider.Ecol. Entomol. 9:337–344.

    Google Scholar 

  • Witt, P.N., andReed, C.F. 1965. Spider-web building.Science 149:1190–1197.

    Google Scholar 

  • Witt, P.N., Reed, C.F., andPeakall, D.B. 1968. A Spider's Web. Problems in Regulatory Biology. Springer-Verlag, Berlin.

    Google Scholar 

  • Woodson, R.E., Jr. 1954. The North American species ofAsclepias L.Ann. Mo. Bot. Gard. 41:1–211.

    Google Scholar 

  • Wright, S.E. 1960. The Metabolism of Cardiac Glycosides. A Review of the Absorption, Metabolism and Excretion of Clinically Important Cardiac Glycosides. Blackwell Scientific Publications, Oxford, U.K.

    Google Scholar 

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Malcolm, S.B. Disruption of web structure and predatory behavior of a spider by plant-derived chemical defenses of an aposematic aphid. J Chem Ecol 15, 1699–1716 (1989). https://doi.org/10.1007/BF01012259

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