Evolutionary Ecology

, Volume 6, Issue 6, pp 527–536 | Cite as

Predator exaptations and defensive adaptations in evolutionary balance: No defence is perfect

  • Reuven Yosef
  • Douglas W. Whitman


The lubber grasshopper,Romalea guttata, is large, aposematic, and extremely toxic. In feeding trials with 21 bird and lizard species, none were able to consume this chemically defended prey. Predators that attempted to eat lubbers, often gagged, regurgitated, and sometimes died. Loggerhead shrikes,Lanius ludovicianus, regularly impale this toxic prey in peninsular Florida. They, like other bird species, are unable to consume fresh lubbers. However, our tests show that they are able to consume lubbers if the prey are allowed to ‘age’ for 1–2 days. This suggests that lubber toxins degrade following death and that shrike impaling behaviour serves as a preadaptation for overcoming the toxic defences of this large and abundant prey. These results also imply that counter adaptations against chemical defences need not involve major morphological or metabolic specializations, but that simple behavioural traits can enable a predator to utilize toxic prey.


Romalea guttata Lanius ludovicianus chemical defences predation impaling defensive behaviour 


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  1. Balick, M. J., Furth, D. G. and Cooper-Driver, G. (1978) Biochemical and evolutionary aspects of arthropod predation on ferns.Oecol. 35, 55–89.Google Scholar
  2. Blum, M. S., Severson, R. F., Arrendale, R. F., Whitman, D. W., Escoubas, P., Adeyeye, O. and Jones C. G. (1990) A generalist herbivore in a specialist mode: metabolic, sequestrative, and defensive consequences.J. Chem. Ecol. 16, 223–44.Google Scholar
  3. Brower, L. P. and Calvert, W. H. (1985) Foraging dynamics of bird predators on overwintering monarch butterflies in Mexico.Evolution 39, 852–68.Google Scholar
  4. Brower, L. P., Horner, B. E., Marty, M. A., Moffitt, C. M. and Villa, R. B. (1985) Mice (Peromyscus maniculatus, P. spicilegus, andMicrotus mexicanus) as predators of overwintering monarch butterflies (Danaus plexippus) in Mexico.Biotropica 17, 89–99.Google Scholar
  5. Brower, L. P., Seiber, J. N., Nelson, C. J., Lynch, S. P. and Holland, M. M. (1984) Plant-determined variation in the cardenolide content, thin-layer chromatography profiles, and emetic potency of monarch butterflies,Danaus plexippus L. reared on milkweed plants in California: 2.Asclepias speciosa.J. Chem. Ecol. 10, 601–39.Google Scholar
  6. Brower, L. P. Seiber, J. N., Nelson, C. J., Lynch, S. P. and Tuskes, P. M. (1982) Plant-determined variation in the cardenolide content, thin-layer chromatography profiles, and emetic potency of monarch butterflies,Danaus plexippus, reared on the milkweed,Asclepias eriocarpa in California.J. Chem. Ecol. 8, 579–633.Google Scholar
  7. Burr, T. C. (1968) Cave ecology and the evolution of troglodytes. InEvolutionary biology. (T. Dobzhansky, M. K. Hecht, and W. C. Steere, eds). Plenum Press, USA.Google Scholar
  8. Calvert, W. H. Hedrick, L. E. and Brower, L. P. (1979) Mortality of the monarch butterfly (Danaus plexippus L.): avian predation at five overwintering sites in Mexico.Science 204, 847–51.Google Scholar
  9. Culver, D. C. (1982)Cave life. Harvard University Press, Cambridge, MA, USA.Google Scholar
  10. Eisner, T. (1970) Chemical defense against predation in arthropods. InChemical ecology. (E. Sondheimer and J. B. Simeone, eds) pp. 157–217. Academic Press, USA.Google Scholar
  11. Eisner, T. A., Hendry, L. B., Peakall, D. B. and Meinwald, J. (1971) 2-5-Dichlorophenol (from ingested herbicide?) in defensive secretion of grasshopper.Science 172, 277–8.Google Scholar
  12. Fink, L. S. and Brower, L. P. (1981) Birds can overcome the cardenolide defence of monarch butterflies in Mexico.Nature 291, 67–70.Google Scholar
  13. Glendinning, J. I., Alonso Mieja, A. and Brower, L. P. (1988) Behavioral and ecological interactions of foraging mice (Peromyscus melanotis) with overwintering monarch butterflies (Danaus plexippus) in Mexico.Oecol. 75, 222–7.Google Scholar
  14. Hendrix, S. D. (1980) An evolutionary and ecological perspective of the insect fauna of ferns.Am. Nat. 115, 171–96.Google Scholar
  15. Jones, C. G., Hess, T. A., Whitman, D. W. Silk, P. J. and Blum, M. S. (1986) Idiosyncratic variation in chemical defenses among individual generalist grasshoppers.J. Chem. Ecol. 12, 749–61.Google Scholar
  16. Jones, C. G., Whitman, D. W., Compton, S. J., Silk, P. J. and Blum, M. S. (1989) Reduction in diet breadth results in sequestration of plant chemicals and increases efficacy of chemical defense in a generalist grasshopper.J. Chem. Ecol. 15, 1811–22.Google Scholar
  17. Jones, C. G., Whitman, D. W., Silk, P. J. and Blum, M. S. (1988) Diet breadth and insect chemical defenses: a generalist grasshopper and general hypothesis. InChemical mediation of coevolution (K. Spencer, ed.) pp. 477–512. Academic Press, San Diego, USA.Google Scholar
  18. Jones, D. A. (1974) Co-evolution and cyanogenesis. InTaxonomy and ecology. (V. Heywood, ed.) pp. 213–42. Academic Press, London, UK.Google Scholar
  19. Jones, D. A., Keymer, R. J. and Ellis, W. M. (1978)Biochemical aspects of plant and animal coevolution. (J. Harborne, ed.) pp. 21–34. Academic Press, London, UK.Google Scholar
  20. Kelley, R. B., Seiber, H. N., Jones, A. D., Segall, H. J. and Brower, L. P. (1987) Pyrrolizidine alkaloids in overwintering monarch butterflies (Danaus plexippus) from Mexico.Experienta 43, 943–6.Google Scholar
  21. Lawton, J. H. (1976) The structure of the arthropod community on bracken (Pteridium aquilinum L. Kuhn).Botan. J. Linn. Soc. 31, 187–216.Google Scholar
  22. Macarthur, R. H. and Wilson, E. O. (1967)The theory of island biogeography. Princeton University Press, Princeton, NJ.Google Scholar
  23. Miller, A. H. (1931) A comparison of behavior of certain North American and European shrikes.Condor 39, 119–22.Google Scholar
  24. Pasteels, J. M., Gregoire, J. C., and Rowell-Rahier, M. (1983) The chemical ecology of defense in arthoropods.Annu. Rev. Entomol. 28, 263–89.Google Scholar
  25. Poulson, T. C. and White, W. B. (1969) The cave environment.Science 165, 971–81.Google Scholar
  26. Rehn, J. A. G. and Grant, H. J. (1959) A review of the Romaleinae (Orthoptera: Acrididae) found in America north of Mexico.Proc. Acad. Nat. Sci. Phil. 111, 109–271.Google Scholar
  27. Schaller, G. B. (1972)The Serengeti lion. The University of Chicago Press, Chicago, USA.Google Scholar
  28. Tuskes, P. M. and Brower, L. P. (1978) Overwintering ecology of the monarch butterfly.Ecol. Entomol. 3, 141–53.Google Scholar
  29. Urquhart, F. A. and Urquhart, N. R. (1976) The overwintering site of the eastern population of the monarch butterfly (Danus p. plexippus: Danaidae) in southern Mexico.J. Lepid. Soc. 30, 153–8.Google Scholar
  30. Watson, J. R. (1941) Migrations and food preferences of the lubery locust.Fla. Entomol. 24, 40–2.Google Scholar
  31. Whitman, D. W. (1988) Allelochemical interactions among plants, herbivores, and their predators. InNovel aspects of insect-plant interactions. (P. Barbosa and D. Letourneau, eds) pp. 11–64. John Wiley, NY, USA.Google Scholar
  32. Whitman, D. W. (1990) Grasshopper chemical communication. InBiology of grasshoppers. (R. F. Chapman and A. Joern, eds) pp. 357–91. John Wiley, NY, USA.Google Scholar
  33. Whitman, D. W., Billen, J. P., Alsop, D. and Blum, M. S. (1991) Anatomy, ultrastructure, and functional morphology of the metathoracic tracheal defensive glands of the grasshopperRomalea guttata.Can. J. Zool. 69, 2100–8.Google Scholar
  34. Whitman, D. W., Blum, M. S. and Alsop, D. W. (1990) Allomones: chemicals for defense. InInsect defenses. (D. L. Evans and J. O. Schmidt, eds) pp. 289–351. SUNY, Albany, NY, USA.Google Scholar
  35. Whitman, D. W., Blum, M. S. and Jones, C. G. (1985) Chemical defense inTaeniopoda eques (Orthoptera: Acrididae): role of the metathoracic secretion.Ann. Entomol. Soc. Am. 78, 451–5.Google Scholar
  36. Yosef, R. (1989) The breeding biology of the Great-grey Shrike and the ecological implications of its impaling prey. M.Sc. thesis, Ben-Gurion University of the Negev, Beer Sheva, Israel.Google Scholar
  37. Yosef, R. and Lohrer, F. E. (1992) A composite treadle-bal chatri trap for Loggerhead Shrikes.Wildl. Soc. Bull. 20, 116–18.Google Scholar
  38. Yosef, R. and Pinshow, B. (1989) Cache size influences female mate choice and reproductive success in the Northern Shrike,Lanius excubitor.Auk 106, 418–21.Google Scholar

Copyright information

© Chapman & Hall 1992

Authors and Affiliations

  • Reuven Yosef
    • 1
    • 2
  • Douglas W. Whitman
    • 3
  1. 1.Department of ZoologyThe Ohio State UniversityColumbusUSA
  2. 2.Archbold Biological StationLake PlacidUSA
  3. 3.Department of Biological SciencesIllinois State UniversityNormalUSA

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