Visual superpowers of butterflies and moths

How do insects see?

In her article, Marlies Craig covers the subject of insect vision via compound and simple eyes, how they differ from our eyes, and how it gives them superpowers. I’m going to expand on what that means for my area of speciality, lepidoptera (butterflies and moths). As an underpinning to what I’m going to say I advise readers to look at her article first. Compound eyes with their arrays of ommatidia are miracles of natural miniaturisation and together with insects’ small size they grant them capabilities we can only dream of.

Eyes are tools all sighted creatures use to resolve spatial details within a visual scene. Those details are in effect contrasts – light and dark, colour, polarisation etc. They are intrinsic to the ability to see and navigate our way around the world. How they do this follows some common physical principles but there are several ways that this can happen. In lepidoptera these factors affect behaviour and the different groups have evolved varying ways to use compound eyes to interact with their environment.

Butterfly and moth superpowers

Basic structure of a compound eye.

Source: Wikipedia Commons

Each ommatidium consists of a lens and a crystalline cone to focus and direct light, primary pigment cells that can isolate it from stray light, and a ‘rhabdom’ that contains the light-sensitive retinula cells and secondary pigments to control the colour sensitivity of the ommatidia. Each of these is connected to the nervous system via an axon – the connection end of a single nerve. This is a vast over-simplification, however. There are several types of compound eye, some of which are better in low light (like nocturnal moths’) and others in bright light (like dragonflies’ and diurnal lepidoptera).

Their ability to focus, degree of binocular vision, and resolution power is also variable. In general, the larger the eye the more visually powerful it is, because larger eyes have more ommatidia. Small insects like ants may only have a few ommatidia in their compound eyes and they are circular. Larger insects that need visual acuity, like dragonflies, have more than 10000 ommatidia per eye. In these they are so closely packed that they are hexagonal in shape. This works rather like digital camera sensors (whose development has followed advances in our understanding of how tiny eyes work) in that the more light-sensitive pixels on the sensor, the greater the resolution power it has. Like digital camera sensors ‘noise’ can be a problem in low light. Nocturnal lepidoptera have evolved some ingenious ways around this.

Compared to dragonflies, butterflies and moths have smaller eyes typically having 3-5000 ommatidia each, so one might expect them to have relatively poor resolution. However, as we can see from their behaviour, their compound eyes allow them to do some amazing things. You might call them ‘superpowers!’

To begin with, they provide a panoramic view of the world with a large field of vision. Lepidoptera have large compound eyes in relation to their bodies (of a similar ratio to dragonflies). The neural connections between their ‘retinas’ (more correctly, ‘rhabdoms’) are very short. Messages get from eye to muscle hundreds of times faster than in humans. These messages can bypass the brain and directly control flight muscles via reflexes.

There are two basic types of compound eye. Day flying lepidoptera have what is called ‘apposition’ compound eyes. In these, each ommatidium’s light path is separated from its neighbours by a dark, light-absorbing pigment. These work best in brightly lit scenes.

When viewed closely hexagonal pattern of ommatidia can be seen on a butterfly’s eye, like this one.

A typical butterfly, the Silver-barred Emperor, Charaxes druceanus druceanus, has up to 4000 ommatidia on its compound eyes.

Silver-barred Emperor female adult.

Moths, being mostly nocturnal, have what are called ‘superposition’ compound eyes in which the connections between the ommatidial lenses and the rhabdom are optically transparent. Hence more than one ommatidial lens can focus light on a single photoreceptor cell on the rhabdom. This reduces the resolution power but greatly increases the sensitivity to light and motion.

Nocturnal superpowers

The Natal Sphinx moth, Macropoliana natalensis, has relatively huge compound eyes.

Natal Sphinx moth, Macropoliana natalensis

Hawkmoths can perceive motion of a favoured night-blooming nectar source, orchid flowers, moving about in a strong wind in starlight, well enough to put their proboscis accurately into their narrow throats and find the hidden nectaries. The flowers are strongly scented which helps the moth to locate them, but they need motion detection to control their hovering flight well enough to ‘thread the needle’. There are trade-offs for good motion perception in poor light, like lack of colour sensitivity. For example, moth collectors have known for years that, like honeybees, moths cannot perceive red light.

Like some other insects like dung beetles, some moths can perceive the plane of polarised light and use this in night-time navigation. How they do this is to do with the way their brains process the light. It partly explains why fewer moths are attracted to artificial light on full moon nights than in earlier or later quarters (when the proportion of polarisation of moonlight is greater).

In researching this article, I fell down several ‘rabbit holes’ created by the fascinating research being done on insect vision and how intricate it is. In one of them I discovered that the modern ultra-fast motion sensors in our security systems are based on ‘biomimicry’ of an insect’s motion detection.

Nocturnal insects in general have visual ‘superpowers.’ They can see in colour (not necessarily those we are familiar with), use object detection to control flight, navigate using polarised light from the moon, see by starlight, and find their way home in what to us would be pitch blackness. There is a very good article on this by Dr EJ Warrant in Philosophical Transactions of the Royal Society (see references).

In my own experience I’ve witnessed low light visual navigation by a local butterfly.

This Common Mother of Pearl Protogoniomorpha parhassus spent the whole winter of 2020 hiding on the same leaf of one of my Forest Peach Rawsonia lucida trees in the dark, dense understorey.

On sunny days this butterfly would sally forth and perch on the forest edge and perhaps have a drink of nectar but would disappear as the sun went down the sky. Throughout the lockdowns I saw him often and every time I went into my forest patch, he was sitting in the same place, on the same leaf. This said to me that he was able to see enough detail, and remember it, to get ‘home.’ Even when the light in the understorey was many f-stops lower than what it was out in the sun. Butterflies have more mental powers than we imagine!

Diurnal superpowers

Motion sensing and detection are more insect ‘superpowers.’ The ommatidia and associated retinula cells can detect micron-scale detail on a moving object and directly control flight via single neurons connected to the flight muscles. This allows Skipper butterflies like the Black-branded Swift Pelopidas mathias to have startle reflexes as fast as 3.5 milliseconds (ms). Ours are around 70 ms!

Black-branded Swift executing a sub 3.5 millisecond vertical take-off.

He was sitting still, and I had him in focus on my Canon R7. I pressed the shutter which has a curtain transit time of 3.5 ms, during which the flash gives off a burst of light. The effective shutter speed here was 1/1000 s (1 ms) but the clever design of the shutter causes the lower curtain to follow the upper curtain upwards (or downwards – you can choose) so that only about 1/3rd of the sensor is exposed at any one time. A band of light carrying the image crosses the sensor in 3.5 ms. This means that as the flash began firing, and the butterfly’s reflex kicked in, he took off, and the band of light ‘painted’ his image onto the sensor. As you can see, he was fully airborne inside that time, casting a clear shadow. The shape distortion you can see is caused by his wings moving at the same time as the band of light did, a phenomenon called ‘rolling shutter’.

End of photography lecture!

This superpower is common in insects, including houseflies. We all know how good they are at avoiding being swatted by a hand (or even a big swatter). That reflex gets them airborne in time to take off in the opposite direction to the first image detected by one of the eyes. They are MUCH faster than a single hand moving. The way to defeat this is the so-called ‘sweet slap’ where one claps one’s hands just above the insect. There being two motion stimuli acting on both eyes simultaneously, it confuses its software, and it takes off vertically – into the gap between the clapping hands, with fatal results for the fly.

Another superpower is multichromaticity – extremely sensitive colour vision. Much research has been done over the past few years into insect colour detection. Butterflies are of particular interest because they rely on flowers, which are coloured, for food. Why are some colours more attractive than others? Is there a hidden signal that says, ‘pollinate me!’ in a field full of coloured flowers?

I could find no research results into African butterflies, but I found an excellent one by Dr Kentaro Arikawa that goes into a lot of detail and explains a lot of things. It’s cited at the end of this article if you really want to fry your brain. In some ways it poses more questions than it answers, but there are salient points that caught my eye. Quoting him,

‘Butterflies use colour vision when searching for flowers. Unlike the trichromatic retinas of humans (blue, green and red cones; plus rods) and honeybees (ultraviolet, blue and green photoreceptors), butterfly retinas typically have six or more photoreceptor classes with distinct spectral sensitivities. The eyes of the Japanese yellow swallowtail (Papilio xuthus) contain ultraviolet, violet, blue, green, red, and broad‐band receptors, with each ommatidium housing nine photoreceptor cells in one of three fixed combinations. The Papilio eye is thus a random patchwork of three types of spectrally heterogeneous ommatidia.’

It goes a lot deeper than that. Swallowtails are effectively tetrachromatic which makes them extremely good at detecting useful flowers. And they can see in the ultraviolet.

Compound eye of Mocker Swallowtail Papilio dardanus cenea through which she can see many more colours than we can, including ultraviolet.

Many flowers are red in colour. Honeybees are known to be blind in the red part of the spectrum as are nocturnal moths, but many butterflies are not only sensitive to it but are actively attracted to red flowers.

This male Mocker Swallowtail was photographed at a Kloof Open Gardens event nectaring on the Coral Senecio Kleinia fulgens.

Swallowtails and Whites aren’t the only butterflies attracted to red flowers. Table Mountain Beauty Aeropetes tulbaghia is strongly attracted to red and is the only known pollinator of the Red Disa Disa uniflora.

Photo: Prof. S Johnson

This male Large Vagrant Nepheronia argia varia was attracted to the red flower spikes of Red Poker Kniphofia linearifolia. The same butterflies were frequenting the orange flowers of a Leonotis species nearby.

This image of a Large Vagrant’s compound eye shows its ‘pseudopupil’, and the pattern of pigmentation in the eye.

The pseudopupil appears black because one is looking directly along the visual axis of the ommatidia in that region, which is closest to us. The ommatidia in a diurnal insect’s apposition eye are sheathed in dark light-absorbing pigment so the ones directly facing us appear black. The insect’s vision is best in the region of its eye closest to what it is seeing.

Females of species like the Large Vagrant are known to have extra sensitivity in the green range of the colour spectrum. This is thought to help them detect the right host plants on which to lay their eggs. We know that butterflies use scent to do this, but I’ve often seen them laying eggs on the wrong plant that was close to the (strongly scented) correct one. Being able to see more than ’40 shades of green’ must be a help in such circumstances!

Some insects, like Praying Mantids, move their heads around to watch our movements. As a result, the pseudopupil appears to follow us, which can look spooky, as if they were sizing us up as prey and not a potential predator!

Underside of Squinting Bush Brown, Bicyclus anynana.

Another use of UV perception is in mate recognition and choice. The white spots in the ‘pupils’ of the Squinting Bush Brown, Bicyclus anynana, reflect strongly in the UV spectrum and males can see this, using it to assess female reproductive suitability, as reported in recent research. The effect is stronger in wet season individuals when there is more foliage cover in the habitat, making it harder for the males to see the visual cues.

In a similar way to some flowers, UV colours exist in some butterflies that to us appear to be pure white or yellow, as in some of the Pieridae (whites and yellows).

UV reflectance image of a dandelion Taraxacum vulgare

Photo: © Birna Rørslett-NN/Nærfoto

Many flowers have ‘nectar guides’, sometimes only visible in UV light, that induce pollinators to probe their relevant parts. These can take the form of lines pointing to the nectaries or a ‘bullseye’ pattern like this dandelion. The common genus Sonchus found in Africa is similar – it looks plain yellow to us but not to a butterfly! This can be photographed using special cameras whose sensors can record in the ultraviolet part of the spectrum. We cannot perceive such colours, so the photographers use ‘false colour’, in this case red for the UV reflection and white for the visible part.

Why is this significant?

Insects make up 75% of the world’s animal species and are not the only invertebrates to possess compound eyes. Crustaceans, myriapods, and some molluscs (like clams) have them too. There have been some astounding discoveries recently about their capabilities and adaptations to a host of ecological circumstances, but we are clearly only just scratching the surface of what they can do. Two examples of practical applications of these discoveries are motion sensors that work in darkness and low noise, high sensitivity digital camera sensors. There must be many more!

References

Warrant EJ. 2017 The remarkable visual capacities of nocturnal insects: vision at the limits with small eyes and tiny brains. Phil. Trans. R. Soc. B 372: 20160063. http://dx.doi.org/10.1098/rstb.2016.0063

Arikawa K. The eyes and vision of butterflies. J Physiol. 2017 Aug 15;595(16):5457-5464. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5556174. Epub 2017 May 8. PMID: 28332207; PMCID: PMC5556174.

Manizah Huq, Shivam Bhardwaj, Antónia Monteiro, Male Bicyclus anynana Butterflies Choose Females on the Basis of Their Ventral UV-Reflective Eyespot Centers, Journal of Insect Science, Volume 19, Issue 1, January 2019, 25, https://doi.org/10.1093/jisesa/iez014

Steve Woodhall is a butterfly enthusiast and photographer who began watching and collecting butterflies at an early age. He was President of the Lepidopterists’ Society of Africa for eight years, and has contributed to and authored several books, including Field Guide to Butterflies of South Africa and Gardening for Butterflies. His app, Woodhall’s Butterflies of South Africa, is described as the definitive butterfly ID guide for South Africa.

Steve has been a valuable and informative informal guide on many butterfly outings but recently qualified as a formal FGASA Field Guide and is now available to officially guide tours via his ButterflyGear business entity. Steve can be contacted on +27 82 825 8450 or steve@butterflygear.co.za