Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

Structural ultraviolet ornamentation in the butterfly Hypolimnas bolina L. (Nymphalidae): visual, morphological and ecological properties

Darrell J. Kemp A B C and Joseph M. Macedonia B
+ Author Affiliations
- Author Affiliations

A School of Tropical Biology, James Cook University, PO Box 6811, Cairns, Qld 4870, Australia.

B School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501, USA.

C Corresponding author. Email: darrell.kemp@jcu.edu.au

Australian Journal of Zoology 54(4) 235-244 https://doi.org/10.1071/ZO06005
Submitted: 11 January 2006  Accepted: 29 May 2006   Published: 11 August 2006

Abstract

Many butterflies exhibit structurally coloured wing patches that are stunningly bright and iridescent in their appearance, yet functionally obscure. These colours are often exaggerated in males, which suggests a sexually selected origin. We studied the visual properties, morphological basis, and interindividual variation of structural wing colouration in the common eggfly, Hypolimnas bolina L. (Nymphalidae). Males of this territorial species possess highly directional UV/violet colouration that fully overlaps smaller white patches on their dorsal wing surfaces. We sampled 56 males, including territorial residents and non-resident ‘floaters’ and assessed the properties of their structural colour using reflectance spectrometry and scanning electron microscopy. The patches reflect strongly in the UV range (300–400 nm), with a peak of ~360 nm, and the wing scales in these regions exhibit a ridge-lamellar surface architecture that has known function in other species as a multiple thin-film interference mirror. Peak UV brightness was variable, and both brightness and peak hue varied systematically across age classes. UV brightness was also related to hue independently of the age-related variation. Territorial residents possessed duller UV markings than their non-resident contemporaries, which is not consistent with exaggeration due to male–male competition. The high phenotypic variance is, however, consistent with a putative role for this male-limited trait as a sexual ornament.


Acknowledgments

We thank D. G. Stavenga for helpful comments on the manuscript. This work was supported by an Australian Research Council grant no. DP0557190 to DJK, and resources provided under the National Science Foundation grant no. 0316120 to R. L. Rutowski, whose support is greatly appreciated.


References

Braby M. F. (2000). ‘Butterflies of Australia: their Identification, Biology and Distribution.’ (CSIRO: Canberra.)

Brunton, C. F. A. (1998). The evolution of ultraviolet patterns in European Colias butterflies (Lepidoptera: Pieridae): a phylogeny using mitochondrial DNA. Heredity 80, 611–616.
CrossRef |

Brunton, C. F. A. , and Majerus, M. E. N. (1995). Ultraviolet colours in butterflies: intra- or inter-specific communication? Proceedings of the Royal Society of London. Series B. Biological Sciences 260, 199–204.


Burnham K. P., and Anderson D. R. (2002). ‘Model Selection and Multimodel Inference: a Practical Information–Theoretic Approach.’ (Springer: New York.)

Common I. F. B., and Waterhouse D. F. (1981). ‘Butterflies of Australia.’ (CSIRO: Melbourne.)

Eaton, M. D. , and Lanyon, S. M. (2003). The ubiquity of avian ultraviolet plumage reflectance. Proceedings of the Royal Society of London. Series B. Biological Sciences 270, 1721–1726.
CrossRef |

Endler, J. A. (1990). On the measurement and classification of colour in studies of animal colour patterns. Biological Journal of the Linnean Society 41, 315–352.


Fitzpatrick, S. (1998). Colour schemes for birds: structural coloration and signals of quality in feathers. Annales Zoologici Fennici 35, 67–77.


Fitzstephens, D. M. , and Getty, T. (2000). Colour, fat and social status in male damselflies, Calopteryx maculata. Animal Behaviour 60, 851–855.
CrossRef | PubMed |

Ghiradella, H. (1974). Development of ultraviolet-reflecting butterfly scales: how to make an interference filter. Journal of Morphology 142, 395–410.
CrossRef |

Ghiradella H. (1998). Hairs, bristles and scales. In ‘Microscopic Anatomy of Invertebrates’. (Ed. M. Locke.) pp. 257–287. (Wiley-Liss: New York.)

Ghiradella, H. , Aneshansley, D. , Eisner, T. , Silberglied, R. E. , and Hinton, H. E. (1972). Ultraviolet reflection of a male butterfly: interference color caused by thin-layer elaboration of wing scales. Science 178, 1214–1217.


Grether, G. F. , Cummings, M. E. , and Hudon, J. (2005). Countergradient variation in the sexual coloration of guppies (Poecilia reticulata): drosopterin synthesis balances carotenoid availability. Evolution 59, 175–188.
CrossRef | PubMed |

Hausmann, F. , Arnold, K. E. , Marshall, N. J. , and Owens, I. P. F. (2003). Ultraviolet signals in birds are special. Proceedings of the Royal Society of London. Series B. Biological Sciences 270, 61–67.
CrossRef |

Hill, G. E. (1996). Redness as a measure of the production cost of ornamental coloration. Ethology, Ecology and Evolution 8, 157–175.


Johnsen, A. , Andersson, S. , Örnborg, J. , and Lifjeld, J. T. (1998). Ultraviolet plumage ornamentation affects social mate choice and sperm competition in bluethroats (Aves: Luscinia s. svecica): a field experiment. Proceedings of the Royal Society of London. Series B. Biological Sciences 265, 1313–1318.
CrossRef |

Karlsson, B. (1994). Feeding habits and change of body composition with age in three nymphalid butterfly species. Oikos 69, 224–230.


Kemp, D. J. (2000). Contest behavior in male butterflies: does size matter? Behavioral Ecology 11, 591–596.
CrossRef |

Kemp, D. J. (2001a). Reproductive seasonality in the tropical butterfly Hypolimnas bolina (Lepidoptera: Nymphalidae) in northern Australia. Journal of Tropical Biology 17, 1–12.
CrossRef |

Kemp, D. J. (2001b). Age-related site fidelity in the territorial butterfly Hypolimnas bolina (L.) (Lepidoptera: Nymphalidae). Australian Journal of Entomology 40, 65–68.
CrossRef |

Kemp, D. J. (2001c). The ecology of female receptivity in the territorial butterfly Hypolimnas bolina (L.) (Nymphalidae): implications for mate location by males. Australian Journal of Zoology 49, 203–211.
CrossRef |

Kemp, D. J. (2005). Contrasting lifetime patterns of territorial success in the nymphalid butterflies Hypolimnas bolina and Melanitis leda: a question of flight physiology? Australian Journal of Zoology 53, 361–367.
CrossRef |

Kemp, D. J. (2006). Heightened phenotypic variation and age-based fading of a nano-structural ultraviolet wing ornament. Evolutionary Ecology Research 8, 515–527.


Kemp, D. J. , and Krockenberger, A. K. (2002). A novel method of behavioural thermoregulation in butterflies. Journal of Evolutionary Biology 15, 922–929.
CrossRef |

Kemp, D. J. , and Rutowski, R. L. (2001). Spatial and temporal patterns of territorial mate locating behaviour in Hypolimnas bolina (L.) (Lepidoptera: Nymphalidae). Journal of Natural History 35, 1399–1411.
CrossRef |

Kemp, D. J. , Vukusic, P. , and Rutowski, R. L. (2006). Stress mediated covariance between nanostructural architecture and ultraviolet butterfly colouration. Functional Ecology 20, 282–289.
CrossRef |

Lawrence, C. , Vukusic, P. , and Sambles, R. (2002). Grazing-incidence iridescence from a butterfly wing. Applied Optics 41, 437–441.
PubMed |

Lederhouse, R. C. , and Scriber, J. M. (1996). Intrasexual selection constrains the evolution of the dorsal color pattern of male black swallowtail butterflies, Papilio polyxenes. Evolution 50, 717–722.
CrossRef |

Lyytinen, A. , Lindström, L. , and Mappes, J. (2005). Ultraviolet reflection and predation risk in diurnal and nocturnal Lepidoptera. Behavioral Ecology 15, 982–987.
CrossRef |

McCubbin C. (1971). ‘Australian Butterflies.’ (Nelson: Melbourne.)

McGraw, K. J. , MacKillop, E. A. , Dale, J. , and Hauber, M. E. (2002). Different colors reveal different information: how nutritional stress affects the expression of melanin- and structurally based ornamental plumage. Journal of Experimental Biology 205, 2343–2347.


Osorio, D. , and Ham, A. D. (2002). Spectral reflectance and directional properties of structural coloration in bird plumage. Journal of Experimental Biology 205, 2017–2027.
PubMed |

Plaistow, S. J. , and Siva-Jothy, M. T. (1996). Energetic constraints and male mate-securing tactics in the damselfly Calopteryx splendens xanthostoma (Charpentier). Proceedings of the Royal Society of London. Series B. Biological Sciences 263, 1233–1238.


Plaistow, S. J. , and Tsubaki, Y. (2000). A selective trade-off for territoriality and non-territoriality in the polymorphic damselfly Mnais costalis. Proceedings of the Royal Society of London. Series B. Biological Sciences 267, 969–975.
CrossRef |

Ramsay, G. W. , and Ordish, R. G. (1966). Australian blue moon butterfly Hypolimnas bolina nerina in New Zealand. New Zealand Journal of Science 9, 719.


Rutowski, R. L. (1985). Evidence for mate choice in a sulphur butterfly (Colias eurytheme). Zeitschrift für Tierpsychologie 70, 103–114.


Rutowski, R. L. (1992). Male mate-locating behavior in the common eggfly, Hypolimnas bolina (Nymphalidae). Journal of the Lepidopterists’ Society 46, 24–38.


Rutowski, R. L. , Gilchrist, G. W. , and Terkanian, B. (1987). Female butterflies mated with recently mated males show reduced reproductive output. Behavioral Ecology and Sociobiology 20, 319–322.
CrossRef |

Rutowski, R. L. , Macedonia, J. M. , Morehouse, N. , and Taylor-Taft, L. (2005). Pterin pigments amplify iridescent ultraviolet signal in males of the orange sulphur butterfly, Colias eurytheme. Proceedings of the Royal Society of London. Series B. Biological Sciences 272, 2329–2335.
CrossRef |

Shawkey, M. D. , and Hill, G. E. (2005). Carotenoids need structural colours to shine. Biology Letters 1, 121–124.
CrossRef |

Silberglied, R. E. (1979). Communication in the ultraviolet. Annual Review of Ecology and Systematics 10, 373–398.
CrossRef |

Silberglied R. E. (1984). Visual communication and sexual selection among butterflies. In ‘The Biology of Butterflies’. (Eds R. I. Vane-Wright and P. R. Ackery.) pp. 207–223. (Academic Press: London.)

Silberglied, R. E. , and Taylor, O. R. (1978). Ultraviolet reflection and its behavioral role in the courtship of the sulphur butterflies Colias eurytheme and C. philodice (Lepidoptera, Pieridae). Behavioral Ecology and Sociobiology 3, 203–243.
CrossRef |

Siva-Jothy, M. T. (2000). The young sperm gambit. Ecology Letters 3, 172–174.
CrossRef |

Stride, G. O. (1956). On the courtship behaviour of Hypolimnas misippus L. (Lepidoptera, Nymphalidae), with notes on the mimetic association with Danaus chrysippus L. (Lepidoptera, Danaidae). British Journal of Animal Behaviour 4, 52–68.
CrossRef |

Stride, G. O. (1957). Investigations into the courtship behaviour of the male of Hypolimnas misippus L., (Lepidoptera, Nymphalidae), with special reference to the role of visual stimuli. Animal Behaviour 5, 153–167.
CrossRef |

Stride, G. O. (1958). Further studies on the courtship behaviour of African mimetic butterflies. Animal Behaviour 6, 224–230.
CrossRef |

Sweeney, A. , Jiggins, C. , and Johnsen, S. (2003). Polarized light as a butterfly mating signal. Nature 423, 31–32.
CrossRef | PubMed |

Vukusic, P. , and Sambles, J. R. (2003). Photonic structures in biology. Nature 424, 852–855.
CrossRef | PubMed |

Vukusic, P. , Sambles, J. R. , Lawrence, C. R. , and Wootton, R. J. (1999). Quantified interference and diffraction in single Morpho butterfly scales. Proceedings of the Royal Society of London. Series B. Biological Sciences 266, 1403–1411.
CrossRef |

Vukusic, P. , Sambles, J. R. , and Lawrence, C. R. (2000). Structural colour: colour mixing in wing scales of a butterfly. Nature 404, 457.
CrossRef | PubMed |

Vukusic, P. , Sambles, J. R. , Lawrence, C. R. , and Wootton, R. J. (2001). Structural colour: now you see it – now you don’t. Nature 410, 36.
CrossRef | PubMed |

Wallace A. R. (1889). ‘Darwinism: an Exposition of the Theory of Natural Selection, with some of its Applications.’ (Macmillan & Co.: London.)



Rent Article (via Deepdyve) Export Citation Cited By (20)