Eyespots—round or oval spots, usually accompanied by one or more concentric rings, that together imitate vertebrate eyes—are found in insects of at least three orders and in some tropical fishes (Stevens 2005). They are particularly frequent in Lepidoptera, where they occur on wings of adults in many species (Monteiro et al. 2006), and in caterpillars of many others (Janzen et al. 2010). The resemblance of eyespots to vertebrate eyes often extends to details, such as fake « pupils » (round or slit-like) and « eye sparkle » (Blut et al. 2012). Larvae of one hawkmoth species even have fake eyes that appear to blink (Hossie et al. 2013). Eyespots have interested evolutionary biologists for well over a century. While they appear to play a role in mate choice in some adult Lepidoptera, their adaptive significance in adult Lepidoptera, as in caterpillars, is mainly as an anti-predator defense (Monteiro 2015). However, there are two competing hypotheses about the mechanism by which eyespots confer defense against predators. The « intimidation » hypothesis postulates that eyespots intimidate potential predators, startling them and reducing the probability of attack. The « deflection » hypothesis holds that eyespots deflect attacks to parts of the body where attack has relatively little effect on the animal’s functioning and survival. In caterpillars, there is little scope for the deflection hypothesis, because attack on any part of a caterpillar’s body is likely to be lethal. Much observational and some experimental evidence supports the intimidation hypothesis in caterpillars (Hossie & Sherratt 2012). In adult Lepidoptera, however, both mechanisms are plausible, and both have found support (Stevens 2005). The most spectacular examples of intimidation are in butterflies in which eyespots located centrally in hindwings and hidden in the natural resting position are suddenly exposed, startling the potential predator (e.g., Vallin et al. 2005). The most spectacular examples of deflection are seen in butterflies in which eyespots near the hindwing margin combined with other traits give the appearance of a false head (e.g., Chotard et al. 2022; Kodandaramaiah 2011). 

Most studies have attempted to test for only one or the other of these mechanisms—usually the one that seems a priori more likely for the butterfly species being studied. But for many species, particularly those that have neither spectacular startle displays nor spectacular false heads, evidence for or against the two hypotheses is contradictory.  

Iserhard et al. (2024) attempted to simultaneously test both hypotheses, using the neotropical nymphalid butterfly Caligo martia. This species has a large ventral hindwing eyespot, exposed in the insect’s natural resting position, while the rest of the ventral hindwing surface is cryptically coloured. In a previous study of this species, De Bona et al. (2015) presented models with intact and disfigured eyespots on a computer monitor to a European bird species, the great tit (Parus major). The results favoured the intimidation hypothesis. Iserhard et al. (2024) devised experiments presenting more natural conditions, using fairly realistic dummy butterflies, with eyespots manipulated or unmanipulated, exposed to a diverse assemblage of insectivorous birds in nature, in a tropical forest. Using color-printed paper facsimiles of wings, with eyespots present, UV-enhanced, or absent, they compared the frequency of beakmarks on modeling clay applied to wing margins (frequent attacks would support the deflection hypothesis) and (in one of two experiments) on dummies with a modeling-clay body (eyespots should lead to reduced frequency of attack, to wings and body, if birds are intimidated). Their experiments also included dummies without eyespots whose wings were either cryptically coloured (as in unmanipulated butterflies) or not. Their results, although complex, indicate support for the deflection hypothesis: dummies with eyespots were mostly attacked on these less vital parts. Dummies lacking eyespots were less frequently attacked, especially when they were camouflaged. Camouflaged dummies without eyespots were in fact the least frequently attacked of all the models. However, when dummies lacking eyespots were attacked, attacks were usually directed to vital body parts. These results show some of the complexity of estimating costs and benefits of protective conspicuous signals vs. camouflage (Stevens et al. 2008).

Two complementary experiments were conducted. The first used facsimiles with « wings » in a natural resting position (folded, ventral surfaces exposed), but without a modeling-clay « body ». In the second experiment, facsimiles had a modeling-clay « body », placed between the two unfolded wings to make it as accessible to birds as the wings. However, these dummies displayed the ventral surfaces of unfolded wings, an unnatural resting position. The study was thus not able to compare bird attacks to the body vs. wings in a natural resting position. One can understand the reason for this methodological choice, but it is a limitation of the study.

The naturalness of the conditions under which these field experiments were conducted is a strong argument for the biological significance of their results. However, the uncontrolled conditions naturally result in many questions being left open. The butterfly dummies were exposed to at least nine insectivorous bird species. Do bird species differ in their behavioral response to eyespots? Do responses depend on the distance at which a bird first detects the butterfly? Do eyespots and camouflage markings present on the same animal both function, but at different distances (Tullberg et al. 2005)? Do bird responses vary depending on the particular light environment in the places and at the times when they encounter the butterfly (Kodandaramaiah 2011)? Answering these questions under natural, uncontrolled conditions will be challenging, requiring onerous methods, (e.g., video recording in multiple locations over time). The study indicates the interest of pursuing these questions.

References

Blut, C., Wilbrandt, J., Fels, D., Girgel, E.I., & Lunau, K. (2012). The ‘sparkle’ in fake eyes–the protective effect of mimic eyespots in Lepidoptera. Entomologia Experimentalis et Applicata, 143, 231-244. https://doi.org/10.1111/j.1570-7458.2012.01260.x

Chotard, A., Ledamoisel, J., Decamps, T., Herrel, A., Chaine, A.S., Llaurens, V., & Debat, V. (2022). Evidence of attack deflection suggests adaptive evolution of wing tails in butterflies. Proceedings of the Royal Society B, 289, 20220562. https://doi.org/10.1098/rspb.2022.0562

De Bona, S., Valkonen, J.K., López-Sepulcre, A., & Mappes, J. (2015). Predator mimicry, not conspicuousness, explains the efficacy of butterfly eyespots. Proceedings of the Royal Society B, 282, 1806. https://doi.org/10.1098/RSPB.2015.0202

Hossie, T.J., & Sherratt, T.N. (2012). Eyespots interact with body colour to protect caterpillar-like prey from avian predators. Animal Behaviour, 84, 167-173. https://doi.org/10.1016/j.anbehav.2012.04.027

Hossie, T.J., Sherratt, T.N., Janzen, D.H., & Hallwachs, W. (2013). An eyespot that “blinks”: an open and shut case of eye mimicry in Eumorpha caterpillars (Lepidoptera: Sphingidae). Journal of Natural History, 47, 2915-2926. https://doi.org/10.1080/00222933.2013.791935

Iserhard, C.A., Malta, S.T., Penz, C.M., Brenda Barbon Fraga; Camila Abel da Costa; Taiane Schwantz; & Kauane Maiara Bordin (2024). The large and central Caligo martia eyespot may reduce fatal attacks by birds : a case study supports the deflection hypothesis in nature. Zenodo, ver. 1 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.5281/zenodo.10980357

Janzen, D.H., Hallwachs, W., & Burns, J.M. (2010). A tropical horde of counterfeit predator eyes. Proceedings of the National Academy of Sciences, USA, 107, 11659-11665. https://doi.org/10.1073/pnas.0912122107

Kodandaramaiah, U. (2011). The evolutionary significance of butterfly eyespots. Behavioral Ecology, 22, 1264-1271. https://doi.org/10.1093/beheco/arr123

Monteiro, A. (2015). Origin, development, and evolution of butterfly eyespots. Annual Review of Entomology, 60, 253-271. https://doi.org/10.1146/annurev-ento-010814-020942

Monteiro, A., Glaser, G., Stockslager, S., Glansdorp, N., & Ramos, D. (2006). Comparative insights into questions of lepidopteran wing pattern homology. BMC Developmental Biology, 6, 1-13. https://doi.org/10.1186/1471-213X-6-52

Stevens, M. (2005). The role of eyespots as anti-predator mechanisms, principally demonstrated in the Lepidoptera. Biological Reviews, 80, 573–588. https://doi.org/10.1017/S1464793105006810

Stevens, M., Stubbins, C.L., & Hardman C.J. (2008). The anti-predator function of ‘eyespots’ on camouflaged and conspicuous prey. Behavioral Ecology and Sociobiology, 62, 1787-1793. https://doi.org/10.1007/s00265-008-0607-3

Tullberg, B.S., Merilaita, S., & Wiklund, C. (2005). Aposematism and crypsis combined as a result of distance dependence: functional versatility of the colour pattern in the swallowtail butterfly larva. Proceedings of the Royal Society B, 272, 1315-1321. https://doi.org/10.1098/rspb.2005.3079

Vallin, A., Jakobsson, S., Lind, J., & Wiklund, C. (2005). Prey survival by predator intimidation: an experimental study of peacock butterfly defence against blue tits. Proceedings of the Royal Society B, 272, 1203-1207. https://doi.org/10.1098/rspb.2004.3034