How do we know eyespots mimic eyes?

Canadian tiger swallowtail (Papilio canadensis) caterpillar in its defensive posture.

Many animals possess large, conspicuous eye-like markings, and the longstanding claim by naturalists is that these spots mimic eyes. The implication that follows is that large eyespots intimidate insect-eating birds from their attack because these birds think they are confronted with one of their own predators. In caterpillars, this inference is often taken a step further, and it is suggested that caterpillars with eyespots are actually mimicking bird-eating or venomous snakes.

A "bird's eye" view of a Canadian tiger swallowtail caterpillar in it's defensive posture.

There are many good reasons to expect that these claims may in fact be true (see here and here), but there has been growing interest in testing the validity of this claim. This work has been spearheaded by a research group in the UK led by Dr. Martin Stevens, who suggests that eyespots may intimidate insect-eating birds simply because many animals avoid attacking prey with large, conspicuous markings. Their research group has conducted some compelling research that illustrates that this may in fact be a plausible alternative (Stevens and Ruxton 2014), despite the claims regarding eye-mimicry made by various researchers. Last year some colleagues and I developed an experiment to test the claim that the eyespots make caterpillars intimidating to birds because of the resemblance to eyes (i.e., eye mimicry), and not simply because they are conspicuous markings.

First, we had to come up with a way to design different kinds of prey items that possessed equally conspicuous markings, but where these markings differed in in how eye-like they were. Instead of doing this by changing the shape or colour of the eyespots themselves, as others before us had done (Stevens et al 2008, Stevens et al 2009), we changed the body position where they eyespots were located. Specifically we created three different kinds of artificial caterpillars:

1. No eyespots (Control)
2. Eyespots towards on end of the body (Eye-like)
3. Eyespots in the center of their body (Less eye-like)

Eyespots are not the only feature which has been implicated in the apparent mimicry of snakes by these caterpillars. Many of these caterpillars also swell their anterior body segments when confronted with a predator. This makes their anterior section look more head-like (at least to human observers). The same logic applies here, if these enlarged segments intimidate birds because it makes the caterpillar appear to be something dangerous like a snake, then it should only be effective when the end of the caterpillar is swollen. In a parallel experiment, our three caterpillar-types here were:

1. No enlarged segments (Control)
2. Enlarged segments at one end (Head-like)
3. Enlarged segments in the center of the body (Not head-like)

We presented these caterpillars to naive domestic chicks who had never seen a caterpillar or a snake in their life. Nine individual chicks were each presented with a single artificial caterpillar from of the 6 types outlined above. We measured two things: 

i) Inspection time: the time until the chick closely approached the prey to examine it.

ii) Latency to attack: the time until the chick pecked the prey item.

Results:

The results couldn't have been clearer. Eyespots and swollen body segments are only intimidating to the chicks when placed in an eye-like or head-like context. When compared to the control prey, chicks delayed their attack longer, and inspected the prey longer, when confronted with artificial caterpillars that has eyespots or a swollen "head". Note however that this was not the case if the swollen segments and the eyespots were not placed in a head-like context.

Have a look at the figure below:

Figure originally published in Skelhorn et al 2014, Behavioral Ecology.

So at least in caterpillars it appears that we have some solid empirical evidence to suggest that these two traits are likely mimetic. Also, both of these traits appear to work in isolation from each other, as we had observed previously in a field experiment. Our results here reinforces another key result from our previous work - that the birds' aversion to these traits appears to be innate, or genetically pre-programmed as Dan Janzen has long suggested.

The full version of our paper can be found here:

Skelhorn, J., Dorrington, G., Hossie, T. J., & Sherratt, T. N. 2014. The position of eyespots and thickened segments influence their protective value to caterpillars. Behavioral Ecology 25:1417–1422

Other recent work:

More recently, there has been research illustrating that eyespots on the wings of butterflies do in fact mimic eyes (De Bona et al 2015). In this paper the researchers presented birds with images of an owl's face with or without eyespots, but also presented birds with three different types of butterfly images:

1. Butterfly with real eyespots (Positive control)
2. Butterfly with modified eyespots (Less eye-like)
3. Butterfly with eyespots digitally removed (Negative control)

They found that real eyespots worked as well as real owl eyes in deterring the birds from their attack. Real eyespots were also more effective than the inverted eyespots, which were equally conspicuous but less eye-like, and images with real eyespots worked better than the no-eyespot control.

De Bona, S., Valkonen, J. K., Lo´pez-Sepulcre, A. & Mappes, J. 2015. Predator mimicry, not conspicuousness, explains the efficacy of butterfly eyespots. Proceedings B: Biological Sciences 282: 20150202