Insect antennae have been the focus of interest and speculation for as long as people have been observing our six-legged friends. We have seen in previous blogs in this series on Insect Antennae (I, II and III), how they are used for a wide variety of different purposes, from feeding ants, to detecting pheromones and finding mates. In this blog, I will take a brief look at how antennae are used in flight. There is of course much we don’t know about antennae. Take for example, the special ‘hooked’ feature at the end of the antennae of most skippers (Hesperiidae). I have no idea why they have this terminal ‘hook’, called the apiculus; perhaps someone out there does?

The antennae of butterflies are frequently stripped, but why is this? Presumably to make them more ‘apparent’? To stand out more against the background?

In some species, males and females can tell each other apart by their antennae. For example, male and female Wood whites (Leptidea sinapis) can distinguish each other via their antennae: the males have a large white patch on the underside of theirs (below).

The club-shaped antennae of the small tortoiseshell, Aglais urticae L. are made up of 34–37 segments (below), including the scape (base), the pedicel (second segment) and the flagellar segments (or flagellomeres). The antennae are moved by muscles connected to the scape and the pedicel, a bit like a ball-and-socket joint (Niehaus and Gewecke, 1978).

Insect antennae are covered in minute sensillae of different shapes and structures, which have evolved to receive and pass on (to the brain) a host of different signals from the environment. For example, each the antenna (also called a flagellum) of the moth, Manduca sexta, bears about 100,000 sensilla, which are connected to about 250,000 sensory neurons (Sanes and Hildebrand, 1976). That’s an impressive number, even if there are lots of segments on hawkmoth antennae (see below, related species), and mechanosensillae – which are the receptor organs specialized to detect mechanical displacement – were of the greatest diversity.

Although insects like hawkmoths use their eyes as well to help them during flight, it is the mechanosensory feedback from their antennae that tells them about their body position, and in particular helps them carry out really fast flight manoeuvres (Dahake et al., 2018). So when we see a fast-moving moth, like a Hummingbird hawk-moth (below), we need to think of it using its antennae as well as its eyes to help it manoeuvre so fast and efficiently.

Scientists have given these microscopic sensillae a variety of different names, based on their shapes, like: trichoid, leaflike, campaniform, coeloconic, basiconic, placoid and so on. They come in all shapes and sizes and are there are different receptors for evaluating different things; olfactory sensilla (smells), gustatory sensilla (tastes), mechanosensilla (movements), hygro- (water) and thermosensilla (temperature). The electron micrograph of olfactory receptors (scales and holes) on the antenna of the peacock butterfly, is particularly beautiful I think (below).

Here’s a rather larger image of this butterfly (below). I wonder why the antennae have yellow tips, like they have been tipped in paint? I suppose it makes them stand out when the butterfly waves its antennae around?

As we have seen, it is the mechanosensors that sense antennal vibrations and are involved in flight control, which is something skippers (below) do very well. They are among the fastest flying lepidopterans.

If you cut off the antennae of a Small Tortoiseshell butterfly – not very nice, I know – the poor thing can still fly. In fact, it beats its wings even faster, even though the capacity for lift decreases (Gewecke and Niehaus, 1981). In another experiment, when the antennae were ‘ablated’ – that’s a nice way of saying cut off! – from hawk moths, it causes them to make frequent collisions with their flapping wings. It turns out that people have been doing ‘experiments’ like this since the Victorian era (and maybe earlier for all I know!). One American (not so gentle) gentleman (Porter, 1883) describes cutting off the antennae of a humble (=bumble)bee.

I noticed that it immediately let the stump drop, but otherwise it did not seem to care at first. But I soon found that it began to feel dizzy and to fly very unsteadily, and when taken into the middle of the room and let fly toward the window would not always strike it, but would hit the wall often several feet to one side or the other. (Porter, 1883)

The poor bumblebee staggered on:

On reaching the window for the last time, it buzzed up and down the pane a few times but soon ceased and began to walk back and forth on the sill in a very restless manner, stopping every few inches to rub the stumps of its antenna with its fore feet and seeming to be in great pain. (Porter, 1883)

It goes on like this for pages, before the hapless bee eventually succumbs. Don’t ask what was concluded from this ‘experiment’: very little. Here’s one with its antennae intact, from Germany.

Another Victorian era ‘experimenter’ describes cutting off the antennae of ‘about a dozen’ living Viceroy butterflies and throwing them into the air to see if they could fly! He observed ‘a certain hesitation in the flight which gave less boldness and accuracy to their movements‘ (Trouvelot, 1877). Not surprising really, or is it?! He went on, merrily cutting off the antennae, legs or wings of various moths and butterflies, blinding some, and eventually coming to the conclusion that ‘when deprived of sight, insects fly with less boldness and accuracy‘. Really?! He got through 50 or 60 viceroy butterflies (below) in this manner. Fortunately, it was not, and still is not, threatened.

Most insects fly with their antennae held out in front, at least to some degree. In fact, sticking the antennae out into a forward position is said to be a good indication that the insect is about to take flight (Krishnan et al., 2012). This behaviour probably helps the insect gather information – mechanosensory and olfactory inputs – via its antennae during flight. I don’t have very many photos of flying insects, but the few I have found (see below) show that the forward positioning of the antennae seems to occur, to some degree, at least in butterflies.

Antennae are full of secrets; they even help butterflies – like the iconic Monarch butterfly (below) – to navigate and migrate. The antennae contain molecular clocks which enable the butterflies to migrate using a time-compensated sun compass. The circadian clock in the antennae (it only needs one!) ‘provides the timing mechanism that allows for the adjustment of flight orientation’ (Guerra et al., 2012).

Finally, I should mention that there is a really excellent article on butterfly antennae on the Butterflies of Singapore website: here.

References

Dahake, A., Stöckl, A. L., Foster, J. J., Sane, S. P., & Kelber, A. (2018). The roles of vision and antennal mechanoreception in hawkmoth flight control. Elife, 7, e37606.

Gewecke, M., & Niehaus, M. (1981). Flight and flight control by the antennae in the Small Tortoiseshell (Aglais urticae L., Lepidoptera). Journal of comparative physiology, 145(2), 249-256.

Guerra, P. A., Merlin, C., Gegear, R. J., & Reppert, S. M. (2012). Discordant timing between antennae disrupts sun compass orientation in migratory monarch butterflies. Nature communications, 3(1), 1-7.

Krishnan, A., Prabhakar, S., Sudarsan, S., & Sane, S. P. (2012). The neural mechanisms of antennal positioning in flying moths. Journal of Experimental Biology, 215(17), 3096-3105.

Niehaus, M. (1981). Flight and flight control by the antennae in the Small Tortoiseshell (Aglais urticae L., Lepidoptera). Journal of comparative physiology, 145(2), 257-264.

Niehaus, M., & Gewecke, M. (1978). The antennal movement apparatus in the small tortoiseshell (Aglais urticae L., Insecta, Lepidoptera). Zoomorphologie, 91(1), 19-36. Porter, C. J. A. (1883). Experiments with the Antennae of Insects. The American Naturalist, 17(12), 1238-1245.

Porter, C. J. A. (1883). Experiments with the Antennae of Insects. The American Naturalist, 17(12), 1238-1245.

Sanes, J. R., & Hildebrand, J. G. (1976). Structure and development of antennae in a moth, Manduca sexta. Developmental biology, 51(2), 282-299.

Trouvelot, L. (1877). The use of the antennae in insects. The American Naturalist, 11(4), 193-196.