Eyespots

Eyespots, also called false eyes or ocelli, are color patterns which consist of roughly concentric rings of contrasting colors and are found in a diversity of organisms including reptiles, fish, birds, mollusks, flatworms, lepidopterans (butterflies, moths, and skippers), and even some cat species. They are so named because they more or less resemble the vertebrate eye. Independent studies on various taxa have identified multiple different functions of eyespots, including courtship, intraspecific communication and competition between juveniles and adults, and anti-predation benefits. The pattern-forming process, or morphogenesis, of eyespots is controlled by a small number of genes during embryonic development. During morphogenesis, the expression of specific genes that direct cells to produce pigment at particular points radiate from a central point, resulting in a circular design. Their conspicuous nature and widespread occurrence have made eyespots historically appealing to study, and they’ve received continual research attention since the 19th century.

Peacocks have ornate eyespots in their plumage, which they use to signal their quality as potential mates to hens. There is a correlation between the number of eyespots in a peacock’s train and his popularity with the ladies. Bobcats have white circular markings on the backs of their ears. Ear positioning in cats has a social function in signaling kittens and in communicating a cat’s mood to other bobs. Eye images in shopping malls have been shown to increase charitable donations to human services and decrease bike theft. And while there are other examples of eyespot uses unrelated to predation, it’s generally accepted that eyespots in many, or even most, species have anti-predation functions, even if they simultaneously have other biological functions.

Many silk worm moths flip their forewings forward when threatened, exposing large eyespots on their back wings. Often, the eyespots have white highlights resembling reflections from the eyes of vertebrates. Such markings have been shown to startle birds. Lycaenid butterflies have filamentous fringes on the edges of the hind-wings; combined with nearby wing markings, they not only have false eyes, but a whole false head. Predators like birds and jumping spiders are effectively misdirected in their attacks by this deception. Studies of rear-wing damage supports the hypothesis of the false head as an effective strategy in deflecting attacks away from the butterfly’s body. These are forms of mimicry. The silk worm moth mimics the eyes of a different animal to appear larger and more threatening than it really is – the Intimidation Hypothesis. The Lycaenid employs self-mimicry, drawing the predator’s attention away from its most vulnerable parts – the Deflection Hypothesis. Another possibility, which has been suggested for some raptors, is that eyespots may deceive predators into thinking they have been noticed – the Detection Hypothesis. Similarly, in the Sundarbans in eastern India and western Bangladesh, woodcutters and other forest workers have worn ornamental human face masks on the back of their heads to deter tiger attacks. In Africa, eyespots painted on the rumps of cows have been shown to reduce cattle predation. These ‘pursuit-deterrent’ signals cause predators to think twice based on the potential costs associated with going forward with the hunt. In this case, eyespots mimic prey vigilance. Conceivably, eyespots may have multiple anti-predator functions, which are not necessarily mutually exclusive. One predator may be startled into not attacking, while another is misdirected to less vital bits. Both are beneficial to the prey.

Sir Edward Bagnall Poulton (a researcher in the 1800s) was among the first to suggest that eyespots were likely to have an anti-predator function. Poulton introduced a small heath butterfly (Coenonympha pamphilus) into a lizard's cage and observed that “It was at once obvious that the lizard was greatly interested in the large eye-like mark on the underside of the fore wing; it examined this mark intently, and several times attempted to seize the butterfly at this spot” – the conception of the Deflection Hypothesis. The main idea of this hypothesis is that eyespots draw predator attacks towards the less vital parts of the prey's body, thus increasing the prey’s chance of survival.

In addition to redirecting attacks towards less vital body parts, eyespots could also be used to direct attacks in a direction that, in combination with the escape trajectory of the prey, would increase the chance of a successful escape. For example, many fishes have spots located in the areas on, or close to, their caudal fins, and because fish primarily swim head first, an attack directed towards the posterior region could facilitate the escape of a fish. Interestingly, in many species of fish that have an eyespot in the posterior region, the real eye is obscured by an eye stripe (a stripe running across the eye) or the eyespot is larger than the real eye, which might also indicate that competition for the predator's visual attention between the eyespot and the real eye may influence the evolution of color patterns.

Eyespots in aquatic environments are widespread. You might recognize them from our very popular redfish, or red drum, Sciaenops ocellatus. Their iconic spotted tail is easily recognizable and used in branding and advertising of many coastal products. Like most other species with eyespots, their coloration is purely genetic, and an individual’s spots don’t change over time. Nor are they an indicator of hatchery origin, a common myth. TPWD hatchery broodstock are wild caught and rotated regularly to ensure genetic diversity and a healthy wild stock. So why are some redfish covered in spots, instead of just one or two eyespots? Genetic mutations are how species evolve. If a particular mutation increases the rate of survival and reproduction, those genes are passed down through the generations and become more prevalent. Multiple spots also lead us to the next anti-predation hypothesis – the Conspicuousness Hypothesis. Predators are often wary of prey with striking patterns which may warn of poison or venom. High contrast spot patterns may cause predators to hesitate, not because they mimic eyes, but because they are conspicuous.

It is widely recognized that predators have profound effects on species diversity by influencing abundance, composition, and traits of prey communities. Because a close encounter with a predator can rapidly become a dead end for its prey, any form of deceptive appearance that prevents detection or recognition in the first place, or deflects attacks to less vital parts of the body, is highly beneficial. Across the animal kingdom, there are a variety of cryptic color patterns and deflective markings, which have long been assumed to provide protection from predators and increase prey survivorship. Though other markings might also misdirect attacks, it is assumed that the misdirecting function of eyespots have played an important role in their evolution in aquatic environments.

The foureye butterflyfish gets its name from a large eyespot on each side of the body near the tail. A black vertical bar on the head runs through the actual eye, making it hard to see. This deceives predators in two ways: into attacking the tail rather than the head, and about the fish's likely direction of travel. It is thus an example of self-mimicry and the Deflection Hypothesis. For the same reason, many juvenile fish display eyespots that disappear during their adult phase. Butterflyfishes can actually lose up to 10% of their posterior body region in an attack by a predator and still survive, recover, and reproduce.

A study in 2013 published by the Royal Society using three-spined stickleback as the predator (chosen in part because it is considered to be a primarily visual predator) found supporting evidence for the Deflection Hypothesis, but interestingly, not for the Intimidation Hypothesis – even though this hypothesis has received strong support in numerous terrestrial studies. One possible explanation is that, when viewed from the front, the projection of eyes in predatory fish is quite different owing to their lateral placement compared with many terrestrial predators, such as raptors. Therefore, an eyespot may not mimic the threat of a predator as closely in aquatic environments as it does in many terrestrial systems. Additionally, the artificial prey items used in the study had only one eyespot, so it’s possible that two spots could be more likely to cause an intimidating effect in fish, because it might better mimic the frontal view of an approaching predator. Another study in 2021 used a heat-mapping technique to show that the location of eyespots is different between active fishes that swim above the benthos versus cryptobenthic fishes that rest on the benthos. (Cryptobenthics: the ‘hidden half’ of the reef fish community, typically less than 5 cm long, camouflaged, and often hanging out in nooks or crevices.)

The results of all the various studies over the century suggest that, while eyespots are generally accepted to have anti-predation functions, they may, in fact, have multiple roles, with their functional significance changing during the lifetime of an animal – from juvenile advertisements to deceptive and/or seductive adult signals, and perhaps functions we haven’t even discovered yet.

Where I learned about eyespots, and you can too!

The Colours of Animals: Their Meaning and Use, Especially Considered in the Case of Insects
By Sir Edward Bagnall Poulton
books.google.com/books?hl=en&lr=&id=Uf4vAAAAYAAJ&oi=fnd&pg=PA18&ots=eyiXvqPcmA&sig=g-wDDUvt4aOKsA2Y6ozWFUrfMOw#v=onepage&q&f=false

The Royal Society of Publishing
royalsocietypublishing.org/doi/10.1098/rspb.2013.1458#d8404263e1

National Library of Medicine
www.ncbi.nlm.nih.gov/pmc/articles/PMC7414152/
www.ncbi.nlm.nih.gov/pmc/articles/PMC3572176/

Wiley Online Library
onlinelibrary.wiley.com/doi/full/10.1002/ece3.6509
onlinelibrary.wiley.com/doi/abs/10.1111/evo.14197

Oxford Academic
academic.oup.com/beheco/article/19/4/733/202072?login=false

University of Bristol
www.bristol.ac.uk/news/2017/september/fish-eyespots.html

Abaco Scientist
appliedecology.cals.ncsu.edu/absci/2013/08/false-eyed-fishes-fool-predators/

Nature
www.nature.com/articles/srep02259

Sibley Nature Center
sibleynaturecenter.org/photo-essays/eyespots

Wikipedia
en.wikipedia.org/wiki/Eyespot_(mimicry)#In_fish