Red Admirals love apples! Or more precisely, they like rotten apples and other wind-fallen or over-ripe fruit which has sat on the ground for a while and started to rot and ferment. What they seek of course, are the sugars and fermenting juices provided by these windfalls to help them to get through the winter, or migrate south again to warmer climes. A small proportion try to overwinter here – they would not survive this winter (Feb 2018) – but most fly south again in the autumn. See previous blog: Red Admirals – European migrants.

I came across a group of Red Admirals – the collective name for a group of butterflies is a Kaleidoscope! – enjoying some rotting apples in Galicia (NW Spain) at the end of September last year (26-09-17). Whether they hibernate in this area, or make their way south towards the Mediterranean, I am not sure. Most European red admirals however, prefer to spend their winter around the Mediterranean Sea (Brattström et al., 2010). Hard not to blame them, I’d fly south in the autumn if I could!

Rotting fruits have relatively low, but variable amounts of sugars as well as fermentation products like ethanol (up to 1% proof!) and acetic acid. Butterflies use contact-chemoreceptor (gustatory) sensillae on their legs and proboscis (feeding tube) to assess the composition of the fluids in the fruit and to decide on whether it wants to eat it!  (Romeis et al., 2005) Butterflies are not seeking out alcohol, but they will end up consuming it as they imbibe the sugars. High levels of ethanol probably inhibit feeding but it seems that some butterflies have a certain tolerance to fermentation products and they might even enhance the feeding responses of the butterflies (Omura et al 2008).

How these butterflies detect the presence of the sugars they desire, is I think, rather interesting. They use contact-chemoreceptors called  gustatory sensillae (sensory organs) on their ‘feet’ and proboscis – or feeding tube – to taste for them.

Members of the family Nymphalidae like Red Admirals have reduced fore-limbs and therefore, use only two pairs of legs for walking (Wolfe et al., 2011). They are called ‘brush-footed’ butterflies because of the brush-like appearance of these vestigial appendages. The reduced, non-functional legs are easy to see on this South American butterfly (below) because – like the proboscis – they are bright green!!

There are three main sections to the butterfly leg: femur, tibia and tarsus. In nymphalids, the female foreleg retains all 5 tarsal sub-segments (as well as the tiny sub-tarsus), which means that the last segment of the vestigial foreleg has 4 tarsal joints, compared with the male which has none. In the male foreleg they are all fused into what looks like one segment. These features are very difficult to see in a photograph taken in the field, but I have tried to indicate the foreleg in the following, heavily cropped picture, and the main segments can be seen (below).

The last, or lowest segment, in the above photograph is the tarsus so it is very difficult to tell how many segments it has, but there is a hint of segmentation on the left foreleg (the one on the right!). So perhaps this was a female. In fact, there were a number of Red Admirals enjoying this windfall so there may have been both males and females.

The reason why forelimbs have become reduced in these butterflies, is thought to be because their function has been co-opted for sensory purposes. They evolved a new chemo-sensory function, but lost their role as limbs for walking (Wolfe et al., 2011). The situation is complex though, because the mid- and hind-tarsi also have a chemo-sensory role. For example, tiny sensory organs (trichoid sensillae) on the ventral surface of  tarsi  are able to respond to sugars (Fox 1966). The fore-tarsi are used by the female for finding host plants.

Much of the work that led to these discoveries about chemo-reception was carried using Red Admiral butterflies – presumably because they are large and common – in the 1920’s and 30’s. In 1922, an American researcher called Dwight Elmer Minnich observed that flies and butterflies extended their proboscises when their legs – walking legs in this case – were touched with sugar. Minnich (1922) describes his findings as follows: ‘the tarsi of the butterfly, Pyrameis atalanta Linn., are sensitive to contact with certain substances in solution, and hence must possess contact chemoreceptors’. The butterfly had a different (genus) name back then! According to Eltringham (1933), Minnich was also able to prove that Red Admirals could distinguish between apple juice and water using its ‘feet’! A very useful attribute in a butterfly which is so fond of rotting apples!

Further work by Ilse Weis (1930) in Germany, took things further and ranked the response of tarsal chemo-receptors in the Red Admiral to one molar solutions of various sugars. She found that they had the following preferences: first sucrose, then fucose, fructose, glucose and so on. All well and good! It is now assumed that most, if not all, butterflies have contact tarsal receptors on their legs – and on their proboscis (below) – which are sensitive to certain sugars and salts (Ahmad, 2012). The tarsi on the fore-limbs of nymphalid butterflies are however, not sensitive to sucrose.

Since these early studies, it has become clear that sensilla on the female fore-tarsi of nymphalid legs are used by female butterflies for detecting the right plant on which to lay her eggs (host plant selection). For example, females of Heliconius butterflies – such as Heliconius erato Linnaeus (Lepidoptera, Nymphalidae) – in effect taste the plant surface with their atrophied foretarsi by drumming on it; “quick alternating movements of the first pair of legs and results in forceful contact between foretarsi and plant tissues” (Bell, & Cardé, 2013). This behaviour liberates plant saps, and in this way butterfly is able to determine the chemical properties of the plant.

Recent research has demonstrated that sensilla on the fore-tarsi of female (but not male) Heliconius butterflies – and perhaps other nymphalids? – are used to select host plants on which to lay eggs (Silva et al., 2017). Whereas, sensilla on the mid- and hind tarsi are involved in sugar detection by both sexes. So there it is; nearly a century of research. We now know that the specialised sensillae on the vestigial fore-legs are used by females to find the right plants to lay on, whereas both males and females have the, rather essential ability, to detect sugars using their four other feet.

The proboscis is also used to taste for sugars. Sensillae on the tip of the proboscis provide the butterfly with a range of useful information, including tactile cues on the position of the proboscis; the extent of its insertion into a floral tube;  and chemical stimuli on the availability of sugars (Krenn, 1998).

More about the proboscis in another blog!

References

Ahmad, S. (Ed.). (2012). Herbivorous insects: host-seeking behavior and mechanisms. Elsevier.

Anderson, A. L. (1932). The sensitivity of the legs of common butterflies to sugars. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 63(1), 235-259.

Bell, W. J., & Cardé, R. T. (2013). Chemical ecology of insects. Springer.

Brattström, O., Bensch, S., Wassenaar, L. I., Hobson, K. A., & Åkesson, S. (2010). Understanding the migration ecology of European red admirals Vanessa atalanta using stable hydrogen isotopes. Ecography, 33(4), 720-729.

Eltringham, H. (1933). On the tarsal sense organs of Lepidoptera. Ecological Entomology, 81(1), 33-36.

Fox, R. M. (1966). Forlegs of butterflies I. Introduction: Chemoreception. J. Res. Lepidoptera, 5, 1-12.

Krenn, H. W. (1998). Proboscis sensilla in Vanessa cardui (Nymphalidae, Lepidoptera): functional morphology and significance in flower-probing. Zoomorphology, 118(1), 23-30.

Minnich, D. E. 1922. The chemical sensitivity of the tarsi of the red admiral butterfly, Pyrameis atalanta Linn. J. Exp.
Zool. 35: 57-81

Ômura, H., Honda, K., Asaoka, K., & Inoue, T. A. (2008). Tolerance to fermentation products in sugar reception: gustatory adaptation of adult butterfly proboscis for feeding on rotting foods. Journal of Comparative Physiology A, 194(6), 545-555.

Romeis, J. O. R. G., Städler, E., & Wäckers, F. L. (2005). Nectar-and pollen-feeding by adult herbivorous insects. Plant-Provided Food for Carnivorous Insects: A Protective Mutualism and its Applications. Cambridge University Press, Cambridge, UK, 178-219.

Silva, D. S., Barp, E. A., Kucharski, L. C. R., & Moreira, G. R. P. (2017). Sensing the Plant Surface Prior to Feeding and Oviposition: Differences in External Ultrastructure and Function Among Tarsi of Heliconius erato. Neotropical entomology, 1-11.

Weis, I. (1930). Versuche über die Geschmacksrezeption durch die Tarsen des Admirals, Pyrameis atalanta L. Zeitschrift für vergleichende Physiologie, 12(2), 206-248.

Wolfe, J. M., Oliver, J. C., & Monteiro, A. (2011). Evolutionary reduction of the first thoracic limb in butterflies. Journal of Insect Science, 11(1), 66.