The most erroneous stories are those we think we know best—and therefore never scrutinize or question.
— Stephen Jay Gould
Full House: The Spread of Excellence from Plato to Darwin (1997), 57.
Ask any naturalist and they’ll tell you, eyespots protect prey animals because they resemble the eyes of a predator or other dangerous animal and thereby startle or intimidate would-be attackers; but how do we know this? How can we know that these markings, which look like eyes to us, similarly resemble eyes to birds or other animals? More fundamentally, what evidence do we have to even suggest that these markings deter predators from their attack?
In February of 2007 I took part in a tropical field course set in the Peruvian Amazon. This gave me the chance to observe and study tropical ecology first hand. Knowing that I may never get a chance to return I took every chance I could to see more. Halfway through our trip while hiking as a group one of my classmates was startled by what appeared to be an arboreal viper reaching from the branches. In reality, it was a caterpillar. Specifically, this was Hemeroplanes ornatus (or possibly H. triptolemus as they are difficult to distinguish as caterpillars), a spectacular sight - these caterpillars are among the best of the snake mimics. At rest they are well concealed, the dorsal side of their body resembling tree bark, but when discovered they reach out from the foliage inflating their anterior body segments into a viperine-shaped head. In a manner unlike any other species I have encountered, these caterpillars display ventral side up. Only upon inflation of the anterior segments do the eyespots become visible. The caterpillar throws itself backward and sways this false head towards the perceived threat, not in a jerky thrash one might expect from a large bodied caterpillar, but in a smooth, sinuous, fluid motion.
|A page out of my field notebook from a trip to Peru in 2007 depicting a final instar Hemeroplanes sp. caterpillar.|
Even with my limited knowledge of mimicry at the time I knew of Bates and Müller’s theories, and knew that Bates formulated his ideas while travelling in the Amazon (though primarily based on his observations of adult butterflies). It wouldn't be until much later (early 2010) that I would realize the Bates likely encountered this same species of caterpillar during his own travels from 1848-1859. In fact, in the very paper where Bates first put forward his theory of adaptive resemblance, now known as Batesian mimicry, he included a description of his encounter:
“The most extraordinary instance of imitation I ever met with was that of a very large Caterpillar, which stretched itself from amidst the foliage of a tree which I was one day examining, and startled me by its resemblance to a small Snake. The first three segments behind the head were dilatable at the will of the insect, and had on each side a large black pupillated spot, which resembled the eye of the reptile: it was a poisonous or viperine species mimicked, and not an innocuous or colubrine Snake; this was proved by the imitation of keeled scales on the crown, which was produced by the recumbent feet, as the Caterpillar threw itself backwards. The Rev. Joseph Greene, to whom I gave a description, supposes the insect to have belonged to the family Notodontida?, many of which have the habit of thus bending themselves. I carried off the Caterpillar, and alarmed every one in the village where I was then living, to whom I showed it. It unfortunately died before reaching the adult state.”-Henry Walter Bates, 1862, p509
Clearly Bates saw this as an important example of adaptive resemblance. There are a number of Notodonta caterpillars that have eyespots, yet his description points to a Hemeroplanes caterpillar. Specifically, he highlights that the caterpillar threw itself backwards such that the recumbent feet (i.e., the true legs) were visible and, to my knowledge, Hemeroplanes are among the only species that display this way (i.e., ventral side up). Furthermore, no New World caterpillar of which I'm aware is as convincingly viper-like when threatened.
Like Bates, I did not need convincing that this caterpillar was mimicking a snake. In fact, I have not encountered a single skeptic of the view that this caterpillar is a snake-mimic once they have seen photos or video footage. Clearly this caterpillar is a snake mimic, and clearly those large black pupillated spots are mimicking eyes. Was this judgement subjective? Perhaps. But what else could possibly explain the appearance and behaviour of this caterpillar? For decades this line of reasoning was the principal evidence put forth to support the widely-held contention that those caterpillars possessing eyespots, including but not limited to Hemeroplanes, mimicked snakes and were thereby protected from insect-eating birds. As a scientist however, subjective assessments aren't good enough. Objective empirical evidence is required to justify our faith in our ideas, irrespective of how obvious they seem or how widely held the belief. Only through this pursuit can we ever hope to fully appreciate the complexity of the world in which we live.