Journal of Chemical Ecology

, Volume 29, Issue 11, pp 2499–2514

Synergistic Effects of Three Piper Amides on Generalist and Specialist Herbivores

  • L. A. Dyer
  • C. D. Dodson
  • J. O. StiremanIII
  • M. A. Tobler
  • A. M. Smilanich
  • R. M. Fincher
  • D. K. Letourneau
Article

Abstract

The tropical rainforest shrub Piper cenocladum, which is normally defended against herbivores by a mutualistic ant, contains three amides that have various defensive functions. While the ants are effective primarily against specialist herbivores, we hypothesized that these secondary compounds would be effective against a wider range of insects, thus providing a broad array of defenses against herbivores. We also tested whether a mixture of amides would be more effective against herbivores than individual amides. Diets spiked with amides were offered to five herbivores: a naïve generalist caterpillar (Spodoptera frugiperda), two caterpillar species that are monophagous on P. cenocladum (Eois spp.), leaf-cutting ants (Atta cephalotes), and an omnivorous ant (Paraponera clavata). Amides had negative effects on all insects, whether they were naïve, experienced, generalized, or specialized feeders. For Spodoptera, amide mixtures caused decreased pupal weights and survivorship and increased development times. Eois pupal weights, larval mass gain, and development times were affected by additions of individual amides, but increased parasitism and lower survivorship were caused only by the amide mixture. Amide mixtures also deterred feeding by the two ant species, and crude plant extracts were strongly deterrent to P. clavata. The mixture of all three amides had the most dramatic deterrent and toxic effects across experiments, with the effects usually surpassing expected additive responses, indicating that these compounds can act synergistically against a wide array of herbivores.

Synergy amides Piper herbivory chemical defense specialists generalists caterpillars 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ayres, M. P., Clausen, T. P., Maclean, J., Redman, A. M., and Reichardt, P. B. 1997. Diversity of structure and antiherbivore activity in condensed tannins. Ecology 78:1696–1712.Google Scholar
  2. Belofsky, G. N., Gloer, J. B., Wicklow, D. T., and Dowd, P. F. 1995. Antiinsectan alkaloids—Shearinines-A-C and a new paxilline derivative from the ascostromata of Eupenicillium shearii. Tetrahedron 51:3959–3968.Google Scholar
  3. Berenbaum, M. and Neal, J. J. 1985. Synergism between myristicin and xanthotoxin, a naturally cooccurring plant toxicant. J. Chem. Ecol. 11:1349–1358.Google Scholar
  4. Berenbaum, M. R., Nitao, J. K., and Zangerl, A. R. 1991. Adaptive significance of furanocoumarin diversity in Pastinaca sativa (Apicaceae). J. Chem. Ecol. 17:207–215.Google Scholar
  5. Berenbaum, M. R. and Zangerl, A. R. 1993. Furanocoumarin metabolism in Papilio polyxenes—Biochemistry, genetic variability, and ecological significance. Oecologia 95:370–375.Google Scholar
  6. Burger, W. 1971. Flora Costaricensis. Fieldiana Bot. 35:1–227.Google Scholar
  7. Calcagno, M. P., Coll, J., Lloria, J., Faini, F., and Alonso-Amelot, M. E. 2002. Evaluation of synergism in the feeding deterrence of some furanocoumarins on Spodoptera littoralis. J. Chem. Ecol. 28:175–191.Google Scholar
  8. Capron, M. A. and Wiemer, D. F. 1996. Piplaroxide an ant-repellent piperidine epoxide from Piper tuburculatum. J. Nat. Prod. 59:794–795.Google Scholar
  9. Cespedes, C. L., Alarcon, J., Aranda, E., Becerra, J., and Silva, M. 2001. Insect growth regulator and insecticidal activity of beta-dihydroagarofurans from Maytenus spp. (Celastraceae). Zeitschrift fur Naturforschung C-A 56:603–613.Google Scholar
  10. Dodson, C. D., Dyer, L. A., Searcy, J., Wright, Z., and Letourneau, D. K. 2000. Cenocladamide, a dihydropyridone alkaloid from Piper cenocladum. Phytochemistry 53:51–54.Google Scholar
  11. Duh, C. Y., Wu, Y. C., and Wang, S. K. 1990. Cytotoxic pyridine alkaloids from Piper aborescens. Phytochemistry 29:2689–2691.Google Scholar
  12. Dyer, L. A. 1995. Tasty generalists and nasty specialists? A comparative study of antipredator mechanisms in tropical lepidopteran larvae. Ecology 76:1483–1496.Google Scholar
  13. Dyer, L. A., Dodson, C., and Gentry, G. in press. A broad bioassay for insect deterrent compounds in plant and animal tissues. Phytochem. Anal.Google Scholar
  14. Dyer, L. A., Dodson, C. D., Beihoffer, J., and Letourneau, D. K. 2001. Trade-offs in antiherbivore defenses in Piper cenocladum: Ant mutualists versus plant secondary metabolites. J. Chem. Ecol. 27:581–592.Google Scholar
  15. Dyer, L. A. and Letourneau, D. 2003. Top–down and bottom–up diversity cascades in detrital vs. living food webs. Ecol. Lett. 6:60–68.Google Scholar
  16. Dyer, L. A. and Letourneau, D. K. 1999a. Trophic cascades in a complex terrestrial community. Proc. Nat. Acad. Sci. USA 96:5072–5076.Google Scholar
  17. Dyer, L. A. and Letourneau, D. K. 1999b. Relative strengths of top–down and bottom–up forces in a tropical forest community. Oecologia 119:265–274.Google Scholar
  18. Folgarait, P. J., Dyer, L. A., Marquis, R. J., and Braker, H. E. 1996. Leaf-cutting ant (Atta cephalotes) preferences for five native tropical plantation tree species growing under different light conditions. Ent. Exp. Et Appl. 80:521–531.Google Scholar
  19. Gbewonyo, W. S. K., Candy, D. J., and Anderson, M. 1993. Structure-activity relationships of insecticidal amides from Piper quieneese. Root Pest. Sci. 37:57–66.Google Scholar
  20. Harborne, J. B. 1988. Introduction to Ecological Biochemistry. Academic Press, San Diego, California.Google Scholar
  21. Hay, M. E., Kappel, Q. E., and Fenical, W. 1994. Synergisms in plant defenses against herbivores—interactions of chemistry, calcification, and plant-quality. Ecology 75:1714–1726.Google Scholar
  22. Jones, C. G. and Firn, R. D. 1991. On the evolution of plant secondary chemical diversity. Philos. Trans. Royal Soc. Lond. Ser. B-Biol. Sci. 333:273–280.Google Scholar
  23. Jones, D. G. (ed.). 1998. Piperonyl Butoxide: The Insect Synergist. Academic Press, London.Google Scholar
  24. Kubo, I. and Muroi, H. 1993. Combination effects of antibacterial compounds in green tea flavor against Streptococcus mutans. J. Agric. Food Chem. 41:1102–1105.Google Scholar
  25. Kumar, J. and Parmar, V. S. 1996. Physiochemical and chemical variation in neem oils and some bioactivity leads against Spodoptera litura F.J. J. Agric. Food Chem. 44:2137–2143.Google Scholar
  26. Letourneau, D. K. 1998. Ants, stem-borers, and fungal pathogens: Experimental tests of a fitness advantage in Piper ant-plants. Ecology 79:593–603.Google Scholar
  27. Lindroth, R. L. and Hwang, S. Y. 1996. Diversity, redundancy, and multiplicity in chemical defense systems of aspen, pp. 25–56, in J. T. Romeo, J. A. Saunders, and P. Barbosa (Eds.). Phytochemical Diversity and Redundancy in Ecological Interactions. Plenum, New York.Google Scholar
  28. Lockwood, J. R. 1998. On the statistical analysis of multiple-choice feeding preference experiments. Oecologia 116:475–481.Google Scholar
  29. McDonald, R. A., Seifert, C. F., Lorenzet, S. J., Givens, S., and Jaccard, J. 2002. The effectiveness of methods for analyzing multivariate factorial data. Org. Res. Methods 5:255–274.Google Scholar
  30. Miyakado, M., Nakayama, I., and Ohno, N. 1989. Insecticidal unsaturated isobutylamides, pp. 173–187, in J. T. Arnason, B. J. R. Philogene, and P. Morand (Eds.). Insecticides of Plant Origin. American Chemical Society, New York.Google Scholar
  31. Nelson, A. C. and Kursar, T. A. 1999. Interactions among plant defense compounds: A method for analysis. Chemoecology 9:81–92.Google Scholar
  32. Parmar, V. S., Jain, S. C., Bisct, K. S., Jain, R., Taneja, P., Jha, A., Tyagi, O. D., Prasad, A. K., Wengel, J., Olsen, C. E., and Boll, P. M. 1997. Phytochemistry of the genus Piper. Phytochemistry 46:597–673.Google Scholar
  33. Richards, J. L., Myhre, S. M., and Jay, J. I. 2001. Total synthesis of piplartine, 13–desmethylpiplartine, and cenocladamide: Three compounds isolated from Piper cenocladum. Abstr. Pap. Am. Chem. Soc. 221:522.Google Scholar
  34. Romeo, J. T., Saunders, J. A., and Barbosa, P. 1996. Phytochemical Diversity and Redundancy in Ecological Interactions. Plenum, New York.Google Scholar
  35. Scott, I. M., Puniani, E., Durst, T., Phelps, D., Merali, S., Assabgui, R. A., Sanchez-Vindas, P., Poveda, L., Philogene, B. J. R., and Arnason, J. T. 2002. Insecticial activity of Piper tuberculatum Jacq. extracts: Synergistic interaction of Piperamides. Agric. Forest Entomol. 4:137–144.Google Scholar
  36. Stermitz, F. R., Lorenz, P., Tawara, J. N., Zenewicz, L. A., and Lewis, K. 2000. Synergy in a medicinal plant: Antimicrobial action of berberine potentiated by 5′-methoxyhydnocarpin, a multidrug pump inhibitor. Proc. Nat. Acad. Sci. USA 97:1433–1437.Google Scholar
  37. Stewart, D. 1998. The evaluation of synergistic action in the laboratory and field, pp. 173–198 in: Jones, D. G. (ed.). Piperonyl Butoxide: The Insect Synergist. Academic Press, London.Google Scholar
  38. Su, H. C. F. and Horvat, R. 1981. Isolation, identification, and insecticidal properties of Piper nigrum amides. J. Agric. Food Chem. 29:115–118.Google Scholar
  39. Wheeler, G. S., Slansky, F., and Yu, S. J. 2001. Food consumption, utilization and detoxification enzyme activity of larvae of three polyphagous noctuid moth species when fed the botanical insecticide rotenone. Ent. Exp. et Appl. 98: 225–239.Google Scholar

Copyright information

© Plenum Publishing Corporation 2003

Authors and Affiliations

  • L. A. Dyer
    • 1
  • C. D. Dodson
    • 2
  • J. O. StiremanIII
    • 1
  • M. A. Tobler
    • 1
  • A. M. Smilanich
    • 1
  • R. M. Fincher
    • 1
  • D. K. Letourneau
    • 3
  1. 1.Department of Ecology and Evolutionary BiologyTulane UniversityNew OrleansUSA
  2. 2.Department of Physical and Environmental SciencesMesa State CollegeGrand JunctionUSA
  3. 3.Department of Environmental StudiesUniversity of CaliforniaSanta CruzUSA

Personalised recommendations