Marginal eyespots on butterfly wings deflect bird attacks under low light intensities with UV wavelengths

Abstract

Background: Predators preferentially attack vital body parts to avoid prey escape. Consequently, prey adaptations that make predators attack less crucial body parts are expected to evolve. Marginal eyespots on butterfly wings have long been thought to have this deflective, but hitherto undemonstrated function.

Methodology/principal findings: Here we report that a butterfly, Lopinga achine, with broad-spectrum reflective white scales in its marginal eyespot pupils deceives a generalist avian predator, the blue tit, to attack the marginal eyespots, but only under particular conditions-in our experiments, low light intensities with a prominent UV component. Under high light intensity conditions with a similar UV component, and at low light intensities without UV, blue tits directed attacks towards the butterfly head.

Conclusions/significance: In nature, birds typically forage intensively at early dawn, when the light environment shifts to shorter wavelengths, and the contrast between the eyespot pupils and the background increases. Among butterflies, deflecting attacks is likely to be particularly important at dawn when low ambient temperatures make escape by flight impossible, and when insectivorous birds typically initiate another day's search for food. Our finding that the deflective function of eyespots is highly dependent on the ambient light environment helps explain why previous attempts have provided little support for the deflective role of marginal eyespots, and we hypothesize that the mechanism that we have discovered in our experiments in a laboratory setting may function also in nature when birds forage on resting butterflies under low light intensities.

Figure 1. Photography's of the prey, the woodland brown butterfly, Lopinga achine.

a. The woodland brown butterfly, L. achine, photographed in natural light. b. The butterfly photographed with a UV filter (Schneider 49 ES Ultraviolet Black 403 which passes UV A radiation (320 to 385 nm)) revealing the strongly UV-reflecting pupils on the hindwing eyespots.

Figure 2. Light environments in the three treatments.

Irradiance measurements in the experimental room demonstrate the difference in light composition between the three treatments (A High, UV+; B Low, UV+ and C Low, UV -).

Figure 3. Bird attack on butterfly under high light intensity conditions with UV.

a. Visual inspection of the butterfly by a blue tit–just preceding the bird's attack. b. The bird with the head of the butterfly in its beak after the attack.

Figure 4. Distribution of attacks in the three treatments.

a. Distribution of blue tit attacks under high light intensity in the presence of UV wavelengths (High, UV+, n = 13). b. Distribution of blue tit attacks under low light intensity in the presence of UV wavelengths (Low, UV+, n = 14). c. Distribution of blue tit attacks under low light intensity in the absence of UV wavelengths (Low, UV-, n = 13).