“Did you hear that?” Said the butterfly.

Blue morpho (Morpho peleides) and Owl butterfly (Caligo atreus)
Blue morpho (Morpho peleides) and Owl butterfly (Caligo atreus)

It used to be thought that butterflies could not hear; that they were deaf. Well I suppose it is understandable, as they do not have ears sticking out from their tiny heads! But it turns out that they can hear – at least some of them can – and they do have ears, but not where you might think. As we shall see, they are on the base of the fore-wings.

It’s long been known that moths (and some butterflies)  have ears which are sensitive to ultrasound – high frequencies above our audible range – and that this trait probably evolved separately numerous times in the family Lepidoptera. Night-flying moths use their high-frequency hearing to detect bats and there is an evolutionary sound war – driven by natural selection – going on between these two nocturnal contestants: predator and prey. The so-called tympanal ears of noctuoid moths, such as the one shown below which I snapped in Thailand, are located on the side of moth (the metathorax) and are said to be tuned to respond to the ultrasonic calls of insectivorous bats.

Asota plana plana (Erebidae). Moths like this have tympanal ears at the junction between the thorax and abdomen.
Asota plana plana (Erebidae). Moths like this have tympanal ears at the junction between the thorax and abdomen.

Butterflies in contrast, evolved into day-flying species, with no need to be able to echo-locate bats like their ancestors did. They have grown bat-deaf! What would be useful for them though, is a way of detecting their daytime predators: birds. It seems that the old bat-detecting ears ears have been adapted to this new purpose in some species like the Blue Morpho butterfly (Morpho peleides).

blue-morpho-morpho-peleides-feeding-on-oranges in a butterfly house
Blue Morpho (Morpho peleides) feeding on oranges in a butterfly house

Ear-like structures have long been noticed at the base of the wings in some nymphalid butterflies. This tiny structure is called Vogel’s Organ. In the Blue Morpho butterfly (shown below) it is an oval-shaped structure composed of inner and outer membranes, which it has been suggested, might allow it to hear two different types of sound frequencies (high and low). It is possible that these butterflies might be ‘listening to the flight sounds of avian predators’ (Lane et al., 2008) and M. peleides may use its two membrane ‘ear’ to ‘detect both singing and flying birds’ (Lucas et al., 2009). It’s not proven yet, but the fact that these butterflies can hear in the range which covers the lower frequency sounds associated with the flapping of bird wings, provides good circumstantial evidence for a putative bird detection system, which can be tested in future experiments (Link 1).

Blue morpho (Morpho peleides) with Vogel's organ at the base of the forewing
Blue morpho (Morpho peleides) with Vogel’s organ at the base of the forewing

The owl butterfly, Caligo eurilochus, also has an ear on the base of its forewings, but according to researchers it is a simpler structure than in the Blue Morpho butterfly. The C. eurilochus ear was most sensitive to sound at frequencies between 1 and 4 kHz, similarly the M. peleides Vogel’s organ is most sensitive to sounds between 2-4 kHz. These could be used to detect the low-frequency components of approaching birds. In other words, they are bird detectors.

Owl butterfly (Caligo atreus) feeding on oranges in a butterfly house
Owl butterfly (Caligo atreus) feeding on oranges in a butterfly house

The owl butterfly is crepuscular, which means that it is most active around dawn and dusk, i.e. during low-light conditions. The ear – or Vogel’s Organ – in C. eurilochus is said to be rather anatomically simple, in comparison to the Blue Morpho.

Owl butterfly (Caligo atreus) - approximate location of Vogel's organ
Owl butterfly (Caligo atreus) – approximate location of Vogel’s organ

We usually know if an animal like a dog or cat can hear us, because it responds in some way to what we say. But it is not easy working out whether something like a butterfly can hear, even if you can find what appears to be its ears.  And when you do work out that they can hear some sounds, it’s not easy to know exactly what they are listening too, and why.

Some butterflies known the ‘crackers’ – Hamadryas spp. – emit surprisingly loud clicks, or ‘clacks’! The clicking or clacking sounds – take your pick – is mostly, but not exclusively, made by males.

Epinome cracker (Hamadryas epinone) from Argentina
Epinome cracker (Hamadryas epinone) from Argentina

A study of the beautiful blue cracker, Hamadryas feronia, in Venezuela, by Jayne Yack (Link 2) and others (2000 paper) at Carleton University (Ottawa, Canada), showed that the males made the ‘sharp clicking sounds’ during chases involving both other males, and females. Typically, a male resting or perching, on the trunk of a tree will take off and fly after another butterfly of the same species as it flies past. If it is another male, they pursue each other, making clicks when they are close to one another. If the male ends up chasing a female, then he ends up conducting what the researchers described as an ‘on-the-wing pendulous display involving continuous clicking’ for the benefit of the female! If she is receptive, then he lands and copulates with her.

Epinome cracker (Hamadryas epinone) puddling
Epinome cracker (Hamadryas epinone) puddling

So it seems that there is a lot more to learn about the sound worlds of butterflies. It is very exciting to think that there may be more complex acoustic interactions going on between butterflies and their avian predators than we ever imagined. So much research has been carried out on the visual markings of butterflies, but it may be that they also rely on sound as well as startling images on their wings to help them avoid the depredations of birds.

All photographs taken by myself either in Argentina or Amsterdam Zoo butterfly house.

Links

  1. http://io9.gizmodo.com/now-we-know-why-butterflies-evolved-to-have-ears-1152166029
  2. https://carleton.ca/biology/people/jayne-yack/

Relevant references

Lucas, K. M., Windmill, J. F., Robert, D., & Yack, J. E. (2009). Auditory mechanics and sensitivity in the tropical butterfly Morpho peleides (Papilionoidea, Nymphalidae). Journal of Experimental Biology, 212(21), 3533-3541.

Lucas, K. M., Mongrain, J. K., Windmill, J. F., Robert, D., & Yack, J. E. (2014). Hearing in the crepuscular owl butterfly (Caligo eurilochus, Nymphalidae). Journal of Comparative Physiology A, 200(10), 891-898.

Conner, W. E., and A. J. Corcoran (2012). Sound Strategies: the 65-million-year-old battle between bats and insects Annual Review of Entomology 57: 21-39.

Ribarič, D., & Gogala, M. (1996). Acoustic behaviour of some butterfly species of the genus Erebia (Lepidoptera: Satyridae). Acta entomologica slovenica, 4(1), 5-12.

Vogel R. 1912. Uber die Chordotonalorgane in der Wurzel der Schmetterlingsflugel. Z Wiss Zool 100:210–244.

Yack, J. E., Otero, L. D., Dawson, J. W., Surlykke, A. & Fullard, J. H. (2000). Sound production and hearing in the blue cracker butterfly Hamadryas feronia (Lepidoptera, Nymphalidae) from Venezuela.Journal of Experimental Biology203(24), 3689-3702.

Yack, J. E. (2004). The structure and function of auditory chordotonal organs in insects. Microscopy research and technique, 63(6), 315-337.

 

 

 

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