Do bumblebees know when ants are in?

Bombus terrestris queen visiting Digitalis flowers with ants outlined
Bombus terrestris queen visiting Digitalis flowers with ants outlined

I took a few photos of a large Bombus terrestris bumblebee (queen I think) visiting foxglove flowers in St. James Park, London on a fine day last week. When I looked closely at the images I noticed a few ants within individual foxglove flowers.

Bombus terrestris queen visiting Digitalis - ant outlined
Bombus terrestris queen visiting Digitalis – ant outlined

Lasius niger worker ants – and other species presumably – often tend aphids on foxglove flowers (Digitalis purpurea) and may forage for nectar on the flowers (1). But ants are not always welcome visitors to the flowers; they are detrimental to their fitness for a number of reasons (2). Firstly, they are usually too small to be much good as pollinators and secondly, their aggressive behaviour may put off more useful pollinators! They are ‘nectar thieves’ taking nectar without providing any mutual benefit for the plant, and also potentially diminishing the appeal of the flower to hard-working pollinators such as bees, which might stay away. Some plants try to keep ants away by using physical or chemical barriers, or offering them an alternative source of nectar, via extrafloral nectaries – EFNs (3). Foxgloves also have guard hairs to deter smaller bees from entering the flower (4), but it seems that ants can easily pass through these.

Bombus terrestris queen visiting Digitalis - with ant on flower rim
Bombus terrestris queen visiting Digitalis – with ant on flower rim

Does the presence of the ants affect the behaviour of the bees? Bumblebees can apparently detect whether another bee has visited a particular flower recently and thereby avoid wasting time by visiting a depleted nectar source. Do they do the same with ants? Ants do leave scent markings – e.g. pheromone trails marking a source of food – and laboratory experiments have shown that bumblebees potentially could avoid ant-visited flowers (1), if they put their minds too it! But they do not seem to use this ability much in the wild. Perhaps the ants are not taking very much nectar, so it is still worthwhile for the bee to visit the flower. Also, the bumblebees are in and out so quickly, and there are so many individual flowers clustered together on a foxglove inflorescence that it is not worth taking the time to sniff out whether ants had been in or not!

Bombus terrestris queen visiting Digitalis flowers
Bombus terrestris queen visiting Digitalis flowers

Would the bumblebee avoid a flower with an ant sitting in it? Perhaps big bumblebees like this one are not bothered by ants? Or do the ants get out of their way? Anyway, my observation was that the bumblebees were in and out of the flowers so quickly it was very hard to tell whether they avoided flowers containing individual ants. Perhaps they just steam rollered over them! Someone way know the answer to this?

  1. Ballantyne, G., & Willmer, P. (2012). Floral visitors and ant scent marks: noticed but not used?. Ecological Entomology, 37(5), 402-409.
  2. Willmer, P.G., Nuttman, C.V., Raine, N.E., Stone, G.N., Pattrick, J.G., Henson, K. et al. (2009) Floral volatiles controlling ant behaviour. Functional Ecology, 23, 888–900.
  3. https://rcannon992.com/2016/05/20/be-my-bodyguard-and-have-a-drink-said-the-vetch-to-the-ant-2/
  4. https://rcannon992.com/2015/10/25/bumbler-bees-and-foxgloves/

The big decision!

Crested-black macaque looking surprised or astonished?
Crested-black macaque looking surprised or astonished?

Just 9 days to go to the UK’s EU referendum. Voters are being asked to vote on whether Britain should leave or remain in the European Union. It’s a big decision which will affect the lives of ourselves and our descendants for generations to come. Many people – bombarded by seemingly contradictory information and so-called facts – are undecided.

Asian small-clawed otters (Aonyx cinerea) fortunatley they do not have to vote!
Asian small-clawed otters (Aonyx cinerea) fortunately they do not have to vote!

Give us the facts they cry! But there are no hard and fast facts. We are being asked to choose the outcome of two possible futures. No one can predict the future. All we can do is shape possible scenarios or outcomes, and compare and contrast them.

lar or white-handed gibbon (Hylobates lar) looking pensive.
lar or white-handed gibbon (Hylobates lar) looking pensive.

Better in or out? Who knows! Why are you asking me say some people. Others are confused and fed up with having to decide something so difficult and momentous.

Agile or black-handed gibbon (Hylobates agilis) looking fed up in Chiang Mai zoo.
Agile or black-handed gibbon (Hylobates agilis) looking fed up in Chiang Mai zoo.

If you want my opinion – which you probably don’t but here it is anyway! – leaving is probably a bigger gamble than staying. At least from a short to medium term perspective. Short term gains – keeping the money we pay to the EC (8 billion) – might be outweighed by the losses (a contracting economy).

But it’s not just about jobs and the economy, it’s also about who we are and what we aspire to be. Since I take the view that we would be better off with no national borders or boundaries at all on earth – at least in theory! – I can understand the motives of people wanting to forge a unified Europe. Even though getting there will not be easy. Secondly, in such a precarious and rapidly changing world that we now live in, I think we would be better forming alliances and unions with our friends and allies, not fragmenting. This argument was well put by a fellow blogger I follow: A C Stark (1).

  1. https://adamcharlesstark.wordpress.com/2016/04/09/in-out-shake-it-all-about/

Slugfest

Arion rufus ¼ adult (probably) feeding on flower
Arion rufus ¼ adult (probably) feeding on flower

No, it’s not a MMA slugging match but a wet day in Scarborough! Slugs (and snails) love a damp summer day, with a shower or two to keep the vegetation moist so they can glide around the garden!

Common Garden Slug (Arion distinctus) side view showing mantle, and stripy skirt running along the bottom of the foot
Common Garden Slug (Arion distinctus) side view showing mantle, and stripy skirt running along the bottom of the foot

Here (below) are a group of slugs feeding on fallen leaves; they almost look like they are at a food bar! Notice the tiny little grey-black sluglet – not the small one on the left – below the third slug at the bottom of the image. So these slugs are doing something useful – helping me tidy up fallen leaves! They also feed on a wide range of rotting organic matter, processing it through their bodies and enriching the soil.

Slugs feeding

OK they do feed on garden plants and flowers (!) although that has never bothered me. Here (below) is one feeding on a yellow poppy. You can see the slug’s mouth (radula) through the flower.

Common Garden Slug (Arion distinctus) feeding on yellow poppy flower
Common Garden Slug (Arion distinctus) feeding on yellow poppy flower

This particular Garden slug (next three images) was very acrobatic, hanging onto the end of a stem and moving about trying to locate another flower to feed on.

Common Garden Slug (Arion distinctus) hanging from stem
Common Garden Slug (Arion distinctus) hanging from stem

There are two tiny dots of reflected light on the two optical tentacles: the light-sensitive eye-spots. What did I look like to the slug?

Garden slug optical tentacles with eye-spots
Garden slug optical tentacles with eye-spots

Here is another shot (below) showing both the optical and sensory tentacles as the animal searches for another plant. The fluidity of its movement is amazing; all whilst holding onto the end of a tiny flower stalk.

Garden slug showing optical and sensory tentacles
Garden slug showing optical and sensory tentacles

All that action needs energy and like us they need to breathe. Slugs take in air through a hole in their mantle called a pneumostome. The sides of this ‘blow-hole’ appear blue in this garden slug (below). They are also said to have green blood.

Common Garden Slug (Arion distinctus) with pneumostome
Common Garden Slug (Arion distinctus) with pneumostome

There is a lot more to say about slugs – such as how they move, their mucus, their hermaphroditic sex life and so on – but for now, I am pleased to have had a damp day on which to appreciate these amazing animals.

“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.