Advertisement

Behavioral Ecology and Sociobiology

, Volume 3, Issue 3, pp 203–243 | Cite as

Ultraviolet reflection and its behavioral role in the courtship of the sulfur butterflies Colias eurytheme and C. philodice (Lepidoptera, Pieridae)

  • Robert E. Silberglied
  • Orley R. TaylorJr.
Article

Summary

  1. 1.

    The courtship behavior of the sulfur butterflies, Colias eurytheme and C. philodice (Lepidoptera, Pieridae), was studied in the field and in large outdoor flight cages. Experiments were performed to investigate the nature of releasers of male courtship behavior and to determine the basis of conspecific mate recognition by females.

     
  2. 2.

    The courtship of these species is extremely brief and does not involve the elaborate displays characteristic of many other butterflies. Mature females employ a mate-refusal posture (Fig. 10) to effect mate selection against, and insure reproductive isolation from, non-conspecific males. The same behavior is also employed by unreceptive females in response to conspecific males.

     
  3. 3.

    Males rely on visual cues to locate and identify females. They respond to paper dummies of the appropriate color (Figs. 15 and 16) and attempt to mate with them (Fig. 7B). No chemical stimuli are necessary to elicit this behavior. The most attractive dummies closely match the yellowish green, ultraviolet-absorbing color of the female ventral hind wing (Fig. 17). Ultraviolet reflection added to an otherwise attractive dummy (Fig. 18A) strongly inhibits male approaches (Fig. 18B). One function of the ultraviolet reflection of male C. eurytheme (Fig. 1) is its use as an inhibitory signal directed to other males. This signal is displayed by individual males to communicate their sex to others, as well as by males in copulo to inhibit courtship attempts of intruders (Fig. 11).

     
  4. 4.

    Visible color differences between C. eurytheme (orange) and C. philodice (yellow) males play no role in mate selection by females of either species (Table 8). The ultraviolet reflection difference between male C. eurytheme (reflecting) and male C. philodice (absorbing) (Figs. 1 and 8) is used as a mate-recognition signal by females of C. eurytheme and in this way functions as a component of the system of isolating mechanisms in this species. C. philodice females do not respond to ultraviolet reflection patterns in any way and appear not to use any visual stimuli in mate selection (Table 8).

     
  5. 5.

    Females of both species rely on chemical cues for conspecific mate recognition. The chemical signals are not associated with so-called ‘androconial’ scales (Fig. 19) located in the black borders of the male wings. These scales are not necessary for successful courtship (Table 7) and no sexual function can presently be ascribed to them. For these and other reasons, we suggest that the term ‘androconia’ not be used for the black border scales of male Colias. No species-recognition pheromones are associated with the dorsal discal region of the male's wings (Table 6), but olfactory signals may be associated with their ventral surfaces, the anterior or posterior margins of their dorsal surfaces, the legs, or the body.

     
  6. 6.

    All male F1 hybrids are ultraviolet-absorbing. F1 hybrid females, derived from crosses between female C. eurytheme and male C. philodice, display the same mate-selection behavior as is characteristic for butterflies of their paternal parents' species (Table 4).

     

Keywords

Courtship Behavior Mate Selection Hind Wing Male Wing Flight Cage 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allyn, A.C., Jr., Downey, J.C.: Observations on male U-V reflectance and scale ultrastructure in Phoebis (Pieridae). Bull. Allyn Mus. 42, 1–20 (1977)Google Scholar
  2. Brower, L.P., Brower, J.V.Z., Cranston, F.P.: Courtship behavior of the Queen butterfly, Danaus gilippus berenice (Cramer). Zoologica (NY) 50, 1–39 (1965)Google Scholar
  3. Brues, C.T.: Photographic evidence on the visibility of color patterns in butterflies to the human and insect eye. Proc. Amer. Acad. Arts Sci. 74, 281–285 (1941)Google Scholar
  4. Crane, J.: Spectral reflectance characteristics of butterflies (Lepidoptera) from Trinidad, B.W.I. Zoologica (NY) 39, 85–115 (1954)Google Scholar
  5. Crane, J.: Imaginal behavior of a Trinidad butterfly, Heliconius erato hydara Hewitson, with special reference to the social use of color. Zoologica (NY) 40, 167–196 (1955)Google Scholar
  6. Daumer, K.: Blumenfarben, wie sie die Bienen sehen. Z. vergl. Physiol. 38, 413–478 (1958)Google Scholar
  7. Edmunds, M.: Defense in animals. Essex: Longman Group 1974Google Scholar
  8. Ehrlich, P.R.: The comparative morphology, phylogeny and higher classification of the butterflies (Lepidoptera: Papilionoidea). Univ. Kans. Sci. Bull. 39, 305–370 (1958)Google Scholar
  9. Eisner, T., Silberglied, R.E., Aneshansley, D., Carrel, J.E., Howland, H.C.: Ultraviolet videoviewing: The television camera as an insect eye. Science (NY) 166, 1172–1174 (1969)Google Scholar
  10. Emmel, T.C.: Mate selection and balanced polymorphism in the tropical nymphalid butterfly, Anartia fatima. Evolution (Lancaster, PA) 26, 96–107 (1972)Google Scholar
  11. Emmel, T.C.: On the nature of the polymorphism and mate selection phenomena in Anartia fatima (Lepidoptera: Nymphalidae). Evolution (Lancaster, PA) 27, 164–165 (1973)Google Scholar
  12. Gerould, J.H.: Inheritance of white wing colour, a sex-limited (sex-controlled) variation in yellow Pierid butterflies. Genetics (Princeton) 8, 495–551 (1923)Google Scholar
  13. Gerould, J.H.: Genetic and seasonal variations of orange wing-color in Colias butterflies. Proc. Amer. Phil. Soc. 86, 405–438 (1943)Google Scholar
  14. Ghiradella, H., Aneshansley, D., Eisner, T., Silberglied, R.E., Hinton, H.E.: Ultraviolet reflection of a male butterfly: Interference color caused by thin-layer elaboration of wing scales. Science (NY) 178, 1214–1217 (1972)Google Scholar
  15. Goldsmith, T.H., Bernard, G.D.: The visual system of insects. In: The physiology of insecta, Vol. 2, 2nd ed. (ed. M. Rockstein), pp. 165–272. New York: Academic 1974Google Scholar
  16. Gray, P.H.H.: Correlations between characters in species of Colias (Lepidoptera: Pieridae). Entomologist 1967, 62–63 (1967a)Google Scholar
  17. Gray, P.H.H.: Some biometrics in Pieris and Colias (Lepidoptera: Pieridae) in Quebec and Nova Scotia. J. NY Entomol. Soc. 75, 12–17 (1967b)Google Scholar
  18. Grula, J., Taylor, O.R., Jr.: Artificial diets for Colias eurytheme and C. philodice. (In preparation) (1978)Google Scholar
  19. Hovanitz, W.: The nomenclature of the Colias chrysotheme complex in North America (Lepidoptera, Pieridae). Amer. Mus. Novit. 1240, 1–4 (1943)Google Scholar
  20. Hovanitz, W.: The ecological significance of the color phases of Colias chrysotheme in North America. Ecology 25, 45–60 (1944)Google Scholar
  21. Hovanitz, W.: Ecological segregation of inter-fertile species of Colias. Ecology 29, 461–469 (1948)Google Scholar
  22. Hovanitz, W.: Interspecific matings between Colias eurytheme and Colias philodice in wild populations. Evolution (Lancaster, PA) 3, 170–173 (1949)Google Scholar
  23. Hovanitz, W.: The biology of Colias butterflies. I. The distribution of the North American species. Wasmann J. Biol. 8, 49–75 (1950a)Google Scholar
  24. Hovanitz, W.: The biology of Colias butterflies. II. Parallel geographical variation of dimorphic color phases in North American species. Wasmann J. Biol. 8, 197–219 (1950b)Google Scholar
  25. Klots, A.B.: A generic revision of the Pieridae (Lepidoptera), together with a study of the male genitalia. Entomologica Am (n.s.) 12, 139–254 (1931)Google Scholar
  26. Klots, A.B.: Genus Colias Fabricius. In: The butterflies of North America (ed. W.H. Howe), pp. 354–367. Garden City, New York: Doubleday 1975Google Scholar
  27. Lutz, F.E.: ‘Invisible’ colors of flowers and butterflies; attempting to get a better idea of how things in this world look to its principal inhabitants, the insects. Nat. Hist. (NY) 33, 565–576 (1933)Google Scholar
  28. Magnus, D.B.E.: Beobachtungen zur Balz und Eiablage des Kaisermantels Argynnis paphia L. (Lep. Nymphalidae). Z. Tierpsychol. 7, 435–449 (1950)Google Scholar
  29. Magnus, D.B.E.: Experimental analysis of some ‘overoptimal’ sign-stimuli in the mating behaviour of the fritillary butterfly Argynnis paphia L. (Lepidoptera: Nymphalidae). Proc. Tenth Int. Congr. Ent. 2, 405–418 (1958)Google Scholar
  30. Mayr, E.: Animal species and evolution. Cambridge: Harvard University 1963Google Scholar
  31. Makino, K., Satoh, K., Koike, M., Ueno, N.: Sex in Pieris rapae L. and the pteridin content of their wings. Nature 170, 933–934 (1952)Google Scholar
  32. Mazokhin-Porshnyakov, G.A.: Ultraviolet radiation of the sun as a factor in insect habitats. Zh. Obshchei. Biol. 15, 362–367 (1954) (In Russian)Google Scholar
  33. Mazokhin-Porshnyakov, G.A.: Reflecting properties of butterfly wings and role of ultra-violet rays in the vision of insects. Biofizika 2, 358–368 (1957) (In Russian); Biophysics 2, 352–362 (English translation)Google Scholar
  34. Mazokhin-Porshnyakov, G.A.: Insect vision. New York: Plenum 1969Google Scholar
  35. Menzel, R.: Colour receptors in insects. In: The compound eye and vision of insects (ed. G.A. Horridge), pp. 121–153. Oxford: Clarendon 1975Google Scholar
  36. Nekrutenko, Y.P.: The hidden wing-pattern of some Palaearctic species of Gonepteryx and its taxonomic value. J. Res. Lepidoptera 3, 65–68 (1964)Google Scholar
  37. Nekrutenko, Y.P.: ‘Gynadromorphic effect’ and the optical nature of hidden wing-pattern in Gonepteryx rhamni L. (Lepidoptera, Pieridae). Nature 205, 417–418 (1965a)Google Scholar
  38. Nekrutenko, Y.P.: Three cases of gynadromorphism in Gonepteryx: An observation with ultraviolet rays. J. Res. Lepidoptera 4, 103–108 (1965b)Google Scholar
  39. Nekrutenko, Y.P.: Phylogeny and geographical distribution of the genus Gonepteryx (Lepidoptera, Pieridae): An attempt of study in historical zoogeography. Kiev: Naukova Dumka 1968Google Scholar
  40. Obara, Y.: Mating behavior of the cabbage white, Pieris rapae crucivora. II. The ‘mate-refusal posture’ of the female. Zool. Mag. (Tokyo) (Dobutsugaku Zasshi) 73, 175–178 (1964) (In Japanese)Google Scholar
  41. Obara, Y.: Studies on the mating behavior of the white cabbage butterfly, Pieris rapae crucivora Boisduval. III. Near ultraviolet reflection as the signal of intraspecific communication. Z. vergl. Physiol. 69, 99–116 (1970)Google Scholar
  42. Obara, Y., Hidaka, T.: Mating behavior of the cabbage white Pieris rapae crucivora. I. The ‘flutter response’ of resting male to flying males. Zool. Mag. (Tokyo) (Dobutsugaku Zasshi) 73, 131–135 (1964) (In Japanese)Google Scholar
  43. Obara, Y., Hidaka, T.: Recognition of the female by the male, on the basis of ultra-violet reflection, in the white cabbage butterfly, Pieris rapae crucivora Boisduval. Proc. Jpn. Acad. 44, 829–832 (1968)Google Scholar
  44. Petersen, B., Tenow, O.: Studien am Rapsweissling und Bergweissling (Pieris napi L. und Pieris bryoniae O.). Isolation und Paarungsbiologie. Zool. Bidr. Upps. 30, 169–198 (1954)Google Scholar
  45. Petersen, B., Törnblom, O., Bodin, N.-O.: Verhaltensstudien am Rapsweissling und Bergweissling (Pieris napi L. und Pieris bryoniae Ochs.) Behaviour 4, 67–84 (1952)Google Scholar
  46. Pliske, T.E., Eisner, T.: Sex pheromone of the Queen butterfly. Biology. Science (NY) 164, 1170–1172 (1969)Google Scholar
  47. Post, C.T., Jr., Goldsmith, T.H.: Physiological evidence for color receptors in the eye of a butterfly. Ann. Entomol. Soc. Amer. 62, 1497–1498 (1969)Google Scholar
  48. Remington, C.L.: The genetics of Colias (Lepidoptera). Advanc. Genet. 6, 403–450 (1954)Google Scholar
  49. Remington, C.L.: Suture-zones of hybrid interaction between recently joined biotas. In: Evolutionary biology, Vol. 2 (eds. T. Dobzhansky, J.K. Hecht, W.C. Steere) pp. 321–428. New York: Appleton-Century-Crofts 1968Google Scholar
  50. Remington, C.L.: Ultraviolet reflectance in mimicry and sexual signals in the Lepidoptera. J. NY entomol. Soc. 81, 124 (1973)Google Scholar
  51. Robinson, R.: Lepidoptera genetics. International series of monographs in pure and applied biology, Vol. 46. New York: Pergamon 1971Google Scholar
  52. Rutowski, R.L.: The use of visual cues in sexual and species discrimination by males of the smail sulphur butterfly Eurema lisa (Lepidoptera, Pieridae). J. comp. Physiol. 115, 61–74 (1977a)Google Scholar
  53. Rutowski, R.L.: Chemical communication in the courtship of the small sulphur butterfly Eurema lisa (Lepidoptera, Pieridae). J. comp. Physiol. 115, 75–85 (1977b)Google Scholar
  54. Scott, J.A.: Mating of butterflies. J. Res. Lepidoptera 11, 99–127 (1973a)Google Scholar
  55. Scott, J.A.: Survey of ultraviolet reflectance of nearctic butterflies. J. Res. Lepidoptera 12, 150–160 (1973b)Google Scholar
  56. Scott, J.A.: Mate-locating behavior of butterflies. Amer. Midl. Nat. 91, 103–117 (1974)Google Scholar
  57. Silberglied, R.E.: Ultraviolet reflection of pierid butterflies: Phylogenetic implications and biological significance. M.S. thesis, Cornell University (1969) (Unpublished)Google Scholar
  58. Silberglied, R.E.: Ultraviolet reflection of butterflies and its behavioral role in the genus Colias (Lepidoptera-Pieridae). Ph. D. thesis, Harvard University (1973)Google Scholar
  59. Silberglied, R.E.: Visualization and recording of longwave ultraviolet reflection from natural objects. Functional Photography 11 (2), 20–29; (3) 30–33 (1976)Google Scholar
  60. Silberglied, R.E.: Communication in the Lepidoptera. In: How animals communicate (ed. T.A. Sebeok), pp. 362–402. Bloomington: Indiana University 1977Google Scholar
  61. Silberglied, R.E., Taylor, O.R.: Ultraviolet differences between the sulphur butterflies, Colias eurytheme and C. philodice, and a possible isolating mechanism. Nature 241, 406–408 (1973)Google Scholar
  62. Stride, G.O.: On the courtship behaviour of Hypolimnas misippus L., (Lepidoptera, Nymphalidae), with notes on the mimetic association with Danaus chrysippus L. (Lepidoptera, Danaidae). Brit. J. Anim. Behav. 4, 52–68 (1956)Google Scholar
  63. Stride, G.O.: Investigations into the courtship behaviour of the male of Hypolimnas misippus L. (Lepidoptera, Nymphalidae), with special reference to the role of visual stimuli. Brit. J. Anim. Behav. 5, 153–167 (1957)Google Scholar
  64. Stride, G.O.: Further studies on the courtship of African mimetic butterflies. Anim. Behav. 6, 224–230 (1958a)Google Scholar
  65. Stride, G.O.: On the courtship behaviour of a tropical mimetic butterfly, Hypolimnas misippus L. (Nymphalidae). Proc. Tenth Int. Congr. Entomol. 2, 419–424 (1958b)Google Scholar
  66. Swihart, S.L.: Hearing in butterflies (Nymphalidae: Heliconius, Ageronia). J. Insect Physiol. 13, 469–476 (1967)Google Scholar
  67. Taylor, O.R.: Reproductive isolation in Colias eurytheme and Colias philodice (Lepidoptera; Pieridae). Ph. D. thesis, University of Connecticut (1970)Google Scholar
  68. Taylor, O.R.: Reproductive isolation in Colias eurytheme and Colias philodice (Lepidoptera: Pieridae). Abstr. Diss. Abstr. Int. 31 (No. 12) (1971)Google Scholar
  69. Taylor, O.R.: Random vs. non-random mating in the sulfur butterflies, Colias eurytheme and Colias philodice (Lepidoptera: Pieridae). Evolution (Lancaster, PA) 26, 344–356 (1972)Google Scholar
  70. Taylor, O.R.: Reproductive isolation in Colias eurytheme and C. philodice (Lepidoptera: Pieridae): Use of olfaction in mate selection. Ann. Entomol. Soc. Am. 66, 621–626 (1973a)Google Scholar
  71. Taylor, O.R.: A non-genetic ‘polymorphism’ in Anartia fatima (Lepidoptera: Nymphalidae). Evolution (Lancaster, PA) 27, 161–164 (1973b)Google Scholar
  72. Tinbergen, N.: Curious naturalists. p. 164–178. London: Country Life 1958Google Scholar
  73. Tinbergen, N., Meeuse, B.J.D., Boerema, L.K., Varossieau, W.W.: Die Balz des Samtfalters, Eumenis (=Satyrus) semele (L.). Z. Tierpsychol. 5, 182–226 (1942); English translation: Tinbergen, N. In: The animal in its world, Field studies. Vol. 1, pp. 197–249. Cambridge: Harvard University 1972Google Scholar
  74. Wickler, W.: Mimicry in plants and animals. World University Library. London: Weidenfeld and Nicolson 1968Google Scholar
  75. Yagi, N., Omoto, K.: Two strains in Colias based on the cytophylogeny of androgenic scales in marginal band of the wings. Kontyu 27, 10–17 (1959)Google Scholar

Copyright information

© Springer-Verlag 1978

Authors and Affiliations

  • Robert E. Silberglied
    • 1
  • Orley R. TaylorJr.
    • 2
  1. 1.Museum of Comparative ZoologyHarvard UniversityCambridgeUSA
  2. 2.Department of Systematics and EcologyThe University of KansasLawrenceUSA

Personalised recommendations