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Journal of Chemical Ecology

, Volume 25, Issue 6, pp 1455–1479 | Cite as

Effects of Cyanogenesis Polymorphism in Turnera ulmifolia on Euptoieta hegesia and Potential Anolis Predators

  • Phillip J. Schappert
  • Joel S. Shore
Article

Abstract

We examine the effects of the cyanogenesis polymorphism in Turnera ulmifolia on larvae, pupae, and adults of Euptoieta hegesia, the most damaging herbivore of T. ulmifolia in terms of tissue loss per unit time. We provide evidence that female E. hegesia do not show preference for host plants on the basis of their cyanogenesis level but do prefer T. ulmifolia over equally cyanogenic, closely related secondary host-plant species (Passiflora sp.). Similarly, cyanogenesis in T. ulmifolia has little effect on the food preference, growth, or development of the larvae. The potential host range of E. hegesia is limited, even within the genus Turnera, but this does not appear to be due to host-plant cyanogenesis. Pupae suffer very high mortality levels in the wild that are not associated with host-plant cyanogenesis, although our studies indicate that larvae are capable of sequestering cyanogenic glycosides from their host plants and possibly of synthesizing these or similar compounds. We provide evidence that the presence of sequestered cyanogenic compounds in the larvae protects them from terrestrial-based predators such as Anolis lizards

Turnera ulmifolia Euptoieta hegesia cyanogenesis Anolis sagrei tritrophic interactions host range sequestration growth development oviposition 

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REFERENCES

  1. Ackery, P. R. 1988. Hostplants and classification: A review of the nymphalid butterflies. Biol. J. Linn. Soc. 33:95-203.Google Scholar
  2. Baker, A. M., and Shore, J. S. 1995. Pollen competition in Turnera ulmifolia (Turneraceae). Am. J. Bot. 82:717-725.Google Scholar
  3. Barrett, S. C. H. 1978. Heterostyly in a tropical weed: The reproductive biology of the Turnera ulmifolia complex (Turneraceae). Can. J. Bot. 56:1713-1725.Google Scholar
  4. Barrett, S. C. H., and Shore, J. S. 1987. Variation and evolution of breeding systems in the Turnera ulmifolia L. complex (Turneraceae). Evolution 41:340-354.Google Scholar
  5. Belaoussoff, S., and Shore, J. S. 1995. Floral correlates and fitness consequences of mating system variation in Turnera ulmifolia. Evolution 49:545-556.Google Scholar
  6. Berenbaum, M. R., and Seigler, D. S. 1992. Biochemicals: engineering problems for natural selection, pp. 89-121, in B. D. Roitberg and M. B. Isman (eds.). Insect Chemical Ecology: An Evolutionary Approach. Chapman and Hall, New York.Google Scholar
  7. Bernays, E. A., and Chapman, R. F. 1987. The evolution of deterrent responses in plant-feeding insects, pp. 159-173, in R. F. Chapman, E. A. Bernays, and J. G. Stoffolano, Jr. (eds.). Perspectives in Chemoreception and Behavior. Springer-Verlag, New York.Google Scholar
  8. Bernays, E. A., Chapman, R. F., Leather, E. M., McCaffery, A. R., and Modder, W. W. D. 1977. The relationship of Zonocerus variegatus (L.) (Acridoidea: Pyrgomorphidae) with cassava (Manihot esculenta). Bull. Entomol. Res. 67:391-404.Google Scholar
  9. Bowers, M. D. 1993. Aposematic caterpillars: Life-styles of the warningly-coloured and unpalatable, pp. 331-371, in N. E. Stamp and T. M. Casey (eds.). Caterpillars: Ecological and Evolutionary Constraints on Foraging. Chapman and Hall, New York.Google Scholar
  10. Bowers, M. D., and Puttick, G. M. 1988. Response of generalist and specialist insects to qualitative allelochemical variation. J. Chem. Ecol. 14:319-334.Google Scholar
  11. Boyden, T. C. 1976. Butterfly palatability and mimicry: experiments with Ameiva lizards. Evolution 30:73-81.Google Scholar
  12. Brattsten, L. B., Samuelian, J. H., Long, K. Y., Kincaid, S. A., and Evans, C. K. 1983. Cyanide as feeding stimulant for the southern armyworm, Spodoptera eridania. Ecol. Entomol. 8:125-132.Google Scholar
  13. Brinker, A. M., and Seigler, D. S. 1989. Methods for the detection and quantitative determination of cyanide in plant materials. Phytochem. Bull. 21:24-31.Google Scholar
  14. Brown, F. M., and Heineman, B. 1972. Jamaica and Its Butterflies. Classey, London, 478 pp.Google Scholar
  15. Brown, K. S., Jr., and Francini, R. B. 1990. Evolutionary strategies of chemical defense in aposematic bufferflies: Cyanogenesis in Asteraceae-feeding American Acraeinae. Chemoecology 1:52-56.Google Scholar
  16. Brown, K. S., Jr., Trigo, J. R., Francini, R. B., Barros de Morais, A. B., and Motta, P. C. 1991. Aposematic insects on toxic host plants: coevolution, colonization and chemical emancipation, pp. 375-402 in P. W. Price, T. M. Lewinsohn, G. W. Fernandes and W. W. Benson (eds.). Plant-Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions. Wiley & Sons, New York.Google Scholar
  17. Burgess, R. S. L., and Ennos, R. A. 1987. Selective grazing of acyanogenic white clover: Variation in behaviour among populations of the slug Deroceras reticulatum. Oecologia 73:432-435.Google Scholar
  18. Chai, P. 1988. Wing coloration of free-flying Neotropical butterflies as a signal learned by a specialized avian predator. Biotropica 20:20-30.Google Scholar
  19. Chase, M. W., and Swenson, S. M. 1995. Relationships of Violales sensu Cronquist from the perspective of cladistic analyses of rbcL sequence data. Am. J. Bot. 82:119.Google Scholar
  20. Clark, A. H. 1947. The interrelationships of the several groups within the butterfly superfamily Nymphaloidea. Proc. Entomol. Soc. Wash. 49:131-140.Google Scholar
  21. Compton, S. G., and Jones, D. A. 1985. An investigation of the responses of herbivores to cyanogenesis in Lotus corniculatus L. Biol. J. Linn. Soc. 26:21-38.Google Scholar
  22. Cronquist, A. 1981. An Integrated System of Classification of Flowering Plants. Columbia University Press, New York, 1262 pp.Google Scholar
  23. Davis, R. H., and Nahrstedt, A. 1987. Biosynthesis of cyanogenic glycosides in butterflies and moths. Insect Biochem. 17:689-693.Google Scholar
  24. DeVries, P. J. 1987. The Butterflies of Costa Rica and Their Natural History. Princeton University Press, Princeton, New Jersey, 327 pp.Google Scholar
  25. Dos Passos, C. F., and Grey, L. P. 1945. A genitalic survey of Argynninae (Lepidoptera: Nymphalidae). Am. Mus. Novit. 1296:1-29.Google Scholar
  26. Dritschilo, W., Krummel, J., Nafus, D., and Pimentel, D. 1979. Herbivorous insects colonizing cyanogenic and acyanogenic Trifolium repens. Heredity 42:49-56.Google Scholar
  27. DuQuesnay, M. C. 1971. Variation in Turnera ulmifolia L. in Jamaica. Unpublished MSc thesis. University of the West Indies, Mona, Kingston, Jamaica. 263 pp.Google Scholar
  28. Ehrlich, P. R. 1958. The comparative morphology, phylogeny and higher classification of the butterflies (Lepidoptera: Papilionoidea). Univ. Kans. Sci. Bull. 39:305-370.Google Scholar
  29. Ehrlich, P. R., and Ehrlich, A. H. 1982. Lizard predation on tropical butterflies. J. Lepid. Soc. 36:148-152.Google Scholar
  30. Ehrlich, P. R., and Raven, P. H. 1964. Butterflies and plants: a study in coevolution. Evolution 18:586-608.Google Scholar
  31. Ellis, W. M., Keymer, R. J., and Jones, D. A. 1977. The defensive function of cyanogenesis in natural populations. Experientia 33:309-311.Google Scholar
  32. Faeth, S. H., Conner, E. F., and Simberloff, D. 1981. Early leaf abscission: A neglected source of mortality for folivores. Am. Nat. 117:409-415.Google Scholar
  33. Feeny, P., Rosenberry, L., and Carter, M. 1983. Chemical aspects of oviposition behavior in butterflies, pp. 27-76, in S. Ahmad (ed.). Herbivorous Insects: Host-Seeking Behavior and Mechanisms. Academic Press, New York.Google Scholar
  34. Feeny, P., StÄdler, E., Ahman, I., and Carter, M. 1989. Effects of plant odor on oviposition by the black swallowtail butterfly, Papilio polyxenes (Lepidoptera: Papilionidae). J. Insect Behav. 2:803-827.Google Scholar
  35. Floyd, H. B., and Jenssen, T. A. 1983. Food habits of the Jamaican lizard Anolis opalinus: Resource partitioning and seasonal effects examined. Copeia 1983:319-331.Google Scholar
  36. Hallman, G. 1979. Importancia de algunas relaciones naturales plantas—artopodos en la agricultura de la zona Calida del Tolima central. Rev. Colomb. Entomol. 5:19-26.Google Scholar
  37. Harvey, D. J. 1991. Higher classification of the Nymphalidae, pp. 255-273, in H. F. Nijhout (ed.). The Development and Evolution of Butterfly Wing Patterns. Smithsonian Institution Press, Washington, D.C.Google Scholar
  38. Johki, Y., and Hidaka, T. 1979. Function of the “warning coloration” in larvae of a diurnal moth, Pryeria sinica Moore (Lepidoptera: Zygaenidae). Appl. Entomol. Zool. 14:164-172.Google Scholar
  39. Jones, D. A. 1971. Chemical defense mechanisms and genetic polymorphism. Science 173:945.Google Scholar
  40. Jones, D. A. 1988. Cyanogenesis in animal-plant interactions, pp. 151-176, in D. Evered and S. Harnett (eds.). Cyanide Compounds in Biology. Wiley & Sons, Chichester, U.K.Google Scholar
  41. Kirk, R. E. 1982. Experimental Design, 2nd ed. Brooks/Cole Publishing, Pacific Grove, California.Google Scholar
  42. Larsen, T. B. 1992. A chameleon as predator of butterflies and its avoidance of known aposematic species. Trop. Lepid. 3:101-104.Google Scholar
  43. Martin, J. A., and Pashley, D. P. 1992. Molecular systematic analysis of butterfly family and some subfamily relationships (Lepidoptera: Papilionoidea). Ann. Entomol. Soc. Am. 85:127-139.Google Scholar
  44. Moermond, T. C. 1981. Prey-attack behavior of Anolis lizards. Z. Tierpsychol. 56:128-136.Google Scholar
  45. Nahrstedt, A. 1988. Cyanogenesis and the role of cyanogenic compounds in insects, pp. 131-150, in D. Evered and S. Harnett (eds.). Cyanide Compounds in Biology. Wiley & Sons, Chichester, U.K.Google Scholar
  46. Nahrstedt, A., and Davis, R. H. 1981. The occurrence of the cyanoglucosides linamarin and lotaustralin in Acraea and Heliconius butterflies. Comp. Biochem. Physiol. 68B:575-577.Google Scholar
  47. Nahrstedt, A., and Davis, R. H. 1983. Occurrence, variation and biosynthesis of the cyanogenic glucosides linamarin and lotaustralin in species of the Heliconiini (Insecta: Lepidoptera). Comp. Biochem. Physiol. 75B:65-73.Google Scholar
  48. Odendaal, F. J., Rausher, M. D., Benrey, B., and Nunez-Farfan, J. 1987. Predation by Anolis lizards on Battus philenor raises questions about butterfly mimicry systems. J. Lepid. Soc. 41:141-144.Google Scholar
  49. Owen, D. F., and Smith, D. A. S. 1990. Interpopulation variation and selective predation in the meadow brown butterfly, Maniola jurtina (L.) (Lepidoptera: Satyridae) in the Canary Islands. Biol. J. Linn. Soc. 39:251-267.Google Scholar
  50. Peterson, S. C. 1986. Breakdown products of cyanogenesis: Repellency and toxicity to predatory ants. Naturwissenschaften 73:627-628.Google Scholar
  51. Raubenheimer, D. 1989. Cyanoglycoside gynocardin from Acraea horta (L.) (Lepidoptera: Acraeinae): possible implications for the evolution of Acraeine host choice. J. Chem. Ecol. 15:2177-2189.Google Scholar
  52. Rausher, M. D. 1979. Larval habitat suitability and oviposition preference in three related butterflies. Ecology 60:503-511.Google Scholar
  53. Renwick, J. A. A. 1989. Chemical ecology of oviposition in phytophagous insects. Experientia 45:223-228.Google Scholar
  54. Rohlf, F. J. 1984. BIOM, A Package of Statistical Programs. Published by the author, Ecology and Evolution, SUNY, Stony Brook, New York.Google Scholar
  55. Roughgarden, J. 1995. Anolis Lizards of the Caribbean: Ecology, Evolution and Plate Tectonics. Oxford University Press, New York, 200 pp.Google Scholar
  56. SAS. 1996. SAS/STAT User's Guide, Release 6.11. SAS Institute, Cary, North Carolina.Google Scholar
  57. Schappert, P. J. 1997. Studies of the cyanogenesis polymorphism in Turnera ulmifolia L. (Turneraceae) and its interaction with the butterfly Euptoieta hegesia Cramer (Nymphalidae) on Jamaica. PhD dissertation. York University, North York, Ontario, Canada.Google Scholar
  58. Schappert, P. J., and Shore, J. S. 1995. Cyanogenesis in Turnera ulmifolia L. (Turneraceae). I. Phenotypic distribution and genetic variation for cyanogenesis on Jamaica. Heredity 74:392-404.Google Scholar
  59. Schappert, P. J., and Shore, J. S. 1998. Ecology, population biology and mortality of Euptoieta hegesia Cramer (Nymphalidae) on Jamaica. J. Lepid. Soc. 52:9-39.Google Scholar
  60. Schappert, P. J., and Shore, J. S. (in press) Cyanogenesis, herbivory and plant defense in Turnera ulmifolia on Jamaica. Ecoscience.Google Scholar
  61. Scriber, J. M. 1978. Cyanogenic glycosides in Lotus corniculatus: Their effect upon growth, energy budget, and nitrogen utilization of the southern armyworm, Spodoptera eridania. Oecologia 34:143-155.Google Scholar
  62. Seigler, D. S. 1991. Cyanide and cyanogenic glycosides, pp. 35-77, in G. A. Rosenthal and M. R. Berenbaum (eds.). Herbivore: Their Interaction with Secondary Plant Metabolites, 2nd ed., Vol. 1: The Chemical Participants. Academic Press, San Diego, California.Google Scholar
  63. Sexton, O. J., Bauman, J., and Ortleb, E. 1972. Seasonal food habits of Anolis limifrons. Ecology 53:182-186.Google Scholar
  64. Shore, J. S., and Obrist, C. M. 1992. Variation in cyanogenesis within and among populations and species of Turnera series Canaligerae (Turneraceae). Biochem. Syst. Ecol. 20:9-15.Google Scholar
  65. Singer, M. C. 1986. The definition and measurement of oviposition preference in plant-feeding insects, pp. 65-94, in J. R. Miller and T. A. Miller (eds.). Insect-Plant Interactions. Springer-Verlag, New York.Google Scholar
  66. Singer, M. C., Thomas, C. D., Billington, H. L., and Parmesan, C. 1994. Correlates of speed of evolution of host preference in a set of twelve populations of the butterfly Euphydryas editha. Ecoscience 1:107-114.Google Scholar
  67. Smiley, J. T. 1983. Passiflora foetida (Bombillo, Calzoncillo, Norbo, Granadilla del Monte, Passion Flower), pp. 298-299, in D. H. Janzen (ed.). Costa Rican Natural History. University of Chicago Press, Chicago, Illinois.Google Scholar
  68. Smiley, J. T., and Wisdom, C. S. 1985. Determinants of growth rate on chemically heterogeneous host plants by specialist insects. Biochem. Syst. Ecol. 13:305-312.Google Scholar
  69. Smith, D. S., Miller, L. D., and Miller, J. Y. 1994. The butterflies of the West Indies and South Florida. Oxford University Press, Oxford, 264 pp.Google Scholar
  70. Spencer, K. C. 1988. Chemical mediation of coevolution in the Passiflora-Heliconius interaction, pp. 167-240, in K. C. Spencer (ed.), Chemical Mediation of Coevolution. Academic Press, San Diego, California.Google Scholar
  71. Spencer, K. C., Seigler, D. S., and Fraley, S. W. 1985. Cyanogenic glycosides of the Turneraceae. Biochem. Syst. Ecol. 13:433-435.Google Scholar
  72. Stamp, N. E., and Bowers, M. D. 1990. Phenology of nutritional differences between new and mature leaves and its effect on caterpillar growth. Ecol. Entomol. 15:447-454.Google Scholar
  73. Thomas, C. D. 1987. Behavioural determination of diet breadth in insect herbivores: The effect of leaf age on choice of host species by beetles feeding on Passiflora vines. Oikos 48:211-216.Google Scholar
  74. Thompson, J. N. 1983. Selection pressures on phytophagous insects feeding on small host plants. Oikos 40:438-444.Google Scholar
  75. Thompson, J. N., and Pellmyr, O. 1991. Evolution of oviposition behavior and host preference in Lepidoptera. Ann. Rev. Ecol. Syst. 36:65-89.Google Scholar
  76. Tober, I., and Conn, E. E. 1985. Cyclopentenylglycine, a precursor of deidaclin in Turnera ulmifolia. Phytochemistry 24:1215-1218.Google Scholar
  77. Vijayaraghavan, M. R., and Kaur, D. 1966. Morphology and embryology of Turnera ulmifolia L. and affinities of the family Turneraceae. Phytomorphology 16:539-553.Google Scholar
  78. Weller, S. J., Pashley, D. P., and Martin, J. A. 1996. Reassessment of butterfly family relationships using independent genes and morphology. Ann. Entomol. Soc. Am. 89:184-192.Google Scholar
  79. White, R. R. 1987. The trouble with butterflies. J. Res. Lepid. 25:207-212.Google Scholar
  80. Woodhead, S., and Bernays, E. A. 1978. The chemical basis of resistance of Sorghum bicolor to attack by Locusta migratoria. Entomol. Exp. Appl. 24:123-144.Google Scholar
  81. Zangerl, A. R., and Berenbaum, M. R. 1993. Plant chemistry, insect adaptations to plant chemistry, and host plant utilization patterns. Ecology 74:47-54.Google Scholar

Copyright information

© Plenum Publishing Corporation 1999

Authors and Affiliations

  • Phillip J. Schappert
    • 1
  • Joel S. Shore
    • 1
  1. 1.Department of BiologyYork UniversityNorth YorkCanada. Department of Zoology, University of Texas, Austin, Texas 78712-1064

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