Smell the fear

With Halloween just around the corner it seemed appropriate to have a fear-themed post.

How do frightened – or even apprehensive – people respond to bees?

And how do bees respond to them?

Melissophobia is the fear of bees. Like the synonym apiphobia, the word is not in the dictionary 1 but is a straightforward compounding of the Greek μέλισσα or Latin apis (both meaning honey bee) and phobos for fear.

Melissophobia is a real psychiatric diagnosis. Although people who start beekeeping are probably not melissophobic, they are often very apprehensive when they first open a colony.

If things go well this apprehension disappears, immediately or over time as their experience increases.

If things go badly they might develop melissophobia and stop beekeeping altogether.

Even relatively experienced beekeepers may be apprehensive when inspecting a very defensive colony. As I have discussed elsewhere, there are certain times during the season when colonies can become defensive. These include when queenless, during lousy weather or when a strong nectar flow ends.

In addition, some colonies are naturally more defensive than others.

Some could even be considered aggressive, making unprovoked attacks as you approach the hive.

A defensive response is understandable if the colony is being threatened. Evolution over eons will have led to acquisition of appropriate responses to dissuade natural predators such as bears and honey badgers.

I’m always careful (and possibly a little bit apprehensive) when looking closely at a completely unknown colony – such as these hives discovered when walking in the Andalucian hills.

If Carlsberg did apiaries ...

Apiary in Andalucia

How do bees detect things – like beekeepers or bears – that they might need to mount a defensive response against?

Ignore the bear

Bees have four senses; sight, smell, touch and taste. Of these, I’ve briefly discussed sight previously and they clearly don’t touch or taste an approaching bear 2 … so I’ll focus on smell.

Could they use smell to detect the scent of an approaching human or bear that is apprehensive of being stung badly?

Let’s forget the grizzly bear 3 for now. At over 200 kg and standing 2+ metres tall I doubt they’re afraid of anything.

Let’s instead consider the apprehensive beekeeper.

Do bees respond to the smell of a frightened human (beekeeper or civilian)?

This might seem a simple question, but it raises some interesting additional questions.

  • Is there a scent of fear in humans?
  • Can bees detect this smell?
  • Have bees evolved to generate defensive responses to this or similar smells?

If two beekeepers inspect the same colony and one considers them aggressive and the other does not, is that due to the beekeepers ‘smelling’ different?

I don’t know the answers to some of these questions, but it’s an interesting topic to think about the stimuli that bees have evolved to respond to.

The scent of fear

This is the easy bit.

Is there a distinctive scent associated with fear in humans?

The Scream by Edvard Munch (1895 pastel version)

Using some rather unpleasant psychological testing researchers have determined that there is a smell produced in sweat secretions that is associated with fear. Interestingly, the smell alone appears not to be detectable. The female subjects tested 4 were unable to consciously discriminate the smell from a control neutral odour.

However, the ‘fear pheromone’ alone caused changes in facial expression associated with fright and markedly reinforced responses to visual stimuli that induced fear.

Females could respond to the fear pheromone produced by males (and vice versa) and earlier MRI studies (involving significantly less unpleasant experiments) had shown that this smell was alone able to induce changes in the amygdala, the region in the brain associated with emotional processing.

So, there is a scent of fear in humans. We can’t consciously detect it, but that doesn’t make it any less real.

Can bees detect it?

Can bees smell the scent of fear?

This is where things get a lot less certain.

I’m not aware that there have been any studies on whether bees can definitively identify the fear pheromone produced by humans.

To conduct this study in a scientifically-controlled manner you would need to know precisely what the pheromone was. It would then be tested in parallel with one or several irrelevant, neutral or related (but different) compounds. In each instance you would have to identify a response in the bee that indicated the fear pheromone had been detected.

All of which is not possible as we don’t definitely know what the fear pheromone is chemically.

We do know it’s present in the sweat of frightened humans … but that’s about it. This makes the experiment tricky. Comparisons would also have to be made with sweat secretions present in the same 5 human when not frightened.

And what response would you look for? Usually bees are trained to respond in a proboscis extension test. In this a bee extends its proboscis in response to a recognised smell or taste.

But, as none of this has been done, there’s little point in speculating further.

So let’s ask the question the other way round.

Would bees be expected to smell the scent of fear?

Smell is very significant to bees.

They have an extremely sensitive sense of smell, reflected in their ability to detect certain molecules as dilute as one or two parts per trillion. Since many people struggle with visualising what that means it’s like detecting a grain of salt in an Olympic swimming pool 6.

Part of the reason we know that smell is so important to bees is because evolution has provided them with a very large number of odorant receptors.

Odorant receptors are the proteins that detect smells. They bind to chemical molecules from the ‘smell’ and these trigger a cellular response of some kind 7. Different odorant receptors have different specificities, binding and responding to the molecules that are present in one or more odours.

Odorant receptor diversity and sensitivity

Bees have 170 odorant receptors, more than three times the number in fruit flies, and double that in mosquitoes. Smell is clearly very important to bees 8.

This is perhaps not surprising when you consider the role of odours within the hive. These include the queen and brood pheromones and the chemicals used for kin recognition 9.

In addition, bees are able to find and use a very wide range of plants as sources of pollen and nectar and smell is likely to contribute to this in many ways.

Finally, we know that bees can detect and respond to a wide range of other smells. Even those present at very low levels which they may not have been exposed to previously. For example Graham Turnbull and his research team in St Andrews, in collaborative studies with Croatian beekeepers, are training bees to detect landmines 10 from the faintest ‘whiff’ of TNT they produce. This deserves a post of its own.

So, while we don’t know that bees could detect a fear pheromone, there’s a good chance that they should be able to.

Evolution of defensive responses

We’re back to some rather vague arm waving here I’m afraid.

In a rather self-fulfilling manner we don’t know if bees have evolved a defensive response to the fear pheromone of humans as – for reasons elaborated above – we don’t actually know whether they do respond to the fear pheromone.

We could again ask this question in a slightly different way.

Might bees be expected to have evolved a defensive response to the fear pheromone?

Long before we developed the poly nuc or the fiendishly clever Flow Hive, humans have been attracted by honey and have exploited bees to harvest it.

The ancient Egyptians kept bees in managed hives over 5000 years ago.

However, we can be reasonably certain that humans provided suitable nesting sites (which we’d now call bait hives) to attract swarms from wild colonies well before that.

But we’ve exploited bees for tens or hundreds of thousands of years more than that.

The ‘Woman(Man) of Bicorp” honey gathering (c. 8000 BC)

There are examples of Late Stone Age (or Upper Paleolithic c. 50,000 to 10,000 years ago) rock art depicting bees and honey from across the globe, with some of the most famous being in the Altamira (Spain) cave drawings from c. 25,000 years ago.

Survival of the fittest

And the key thing about many of these interactions with honey bees is that they are likely to have been rather one-sided. Honey hunting tends to be destructive and results in the demise of the colony – the tree is felled, the brood nest is ripped apart, the stores (and often the brood) are consumed.

None of this involves carefully caging the queen in advance 🙁

This is a strong selective pressure.

Colonies that responded earlier or more strongly to the smell of an apprehensive approaching hunter gatherer might be spared. These would survive to reproduce (swarm). Literally, the survival of the fittest.

All of this would argue that it might be expected that bees would evolve odorant receptors capable of detecting the fear pheromone of humans.

There’s no fire without smoke

There are (at least) two problems with this reasoning.

The first problem is that humans acquired the ability to use fire. And, as the idiom almost says, there’s no fire without smoke. Humans were regularly using fire 150-200,000 years ago, with further evidence stretching back at least one million years that pre-humans (Homo erectus) used fire.

And, if they were using fire you can be sure they would be using smoke to ‘calm’ the bees millenia before being depicted doing so in Egyptian hieroglyphs ~5,000 years ago.

It seems reasonable to expect that the use of smoke would mask the detection of fear pheromones, in much the same way that it masks the alarm pheromone when you give them a puff from your trusty Dadant.

The other problem is that it might be expected that the Mesolithic honey hunters had probably ‘got the job’ precisely because they weren’t afraid of bees. In extant hunter gatherer communities it’s known that there are specialists that have a particular aptitude for the role. Perhaps these beekeepersrobbers produce little of no fear pheromone in the first place?

What about other primates?

It’s well know that non-human primates (NHP’s), like chimpanzees and bonobo, love honey. They love it so much that they are responsible for an entire research area studying tool use by chimps.

Bonobo ‘fishing’ for termites using a tool (I couldn’t find a suitable one robbing honey)

Perhaps NHP’s produce a fear pheromone similar to that of humans? Since they haven’t learned to use fire (and they are very closely related to humans) bees may have evolved to respond to primate fear pheromone(s), and – by extension – to those of humans.

However, chimpanzees and related primates prefer to steal honey from stingless bees like Meliponula bocandei. The only information I could find suggested they avoided Apis mellifera, or “used longer sticks as tools“.

Perhaps not such a strong selective pressure after all …

More arm waving

A lot of the above is half-baked speculation interspersed with a smattering of evolutionary theory.

Bees clearly respond in different ways to different beekeepers. I’ve watched beekeepers retreat from a defensive colony which – later on the same training day – were beautifully calm when inspected by a different beekeeper.

Trainee beekeepers

Trainee beekeepers

Although this might have been due to differences in the production of fear pheromones, it’s clear that the bees are also using other senses to detect potential threats to the colony.

Look carefully at how outright beginners, intermediate and expert beekeepers move their hands when inspecting a colony.

The tyro goes slow and steady. Everything ‘by the book’. Not calm, but definitely very controlled.

The expert goes a lot faster. However, there’s no banging frames down, there are no sudden movements, the hands move beside the brood box rather than over it. Calm, controlled and confident.

In contrast, although the “knowing just enough to be dangerous” intermediate beekeeper is confident, they are also rushed and a bit clumsy. Hands move back and forwards over the box, movements are rapid, frames are jarred … or dropped. A bee sneaks inside the cuff and stings the unprotected wrist. Ouch!

“That’s an aggressive colony. Better treat it with care.”

You see what I mean about arm waving?

I strongly suspect movement and vibration trigger defensive responses to a much greater extent than the detection of fear pheromones in humans (if they’re detected at all).

Closing thoughts

You’ll sometimes read that bees respond badly to aftershave or perfumes. This makes sense to me only if the scent resembles one that the bees have evolved a defensive response against.

Don’t go dabbing Parfum de honey badger behind your ears before starting the weekly inspection.

Mellivora capensis – the honey badger. Believe me, you’re not worth it.

But why would they react aggressively to an otherwise unknown smell?

After all, they experience millions of different – and largely harmless – smells every day. Bees inhabit an environment that is constantly changing. One more unknown new scent does not immediately indicate danger. There would be an evolutionary cost to generating a defensive response to something that posed no danger.

And a final closing thought for you to dwell on …

Humans have probably been using fire to suppress honey bee colony aggression for hundreds of thousands of years.

Why haven’t bees evolved defensive responses to the smell of smoke? 11

Happy Halloween 🙂


 

Footnotes

  1. At least, it’s not in the Oxford English Dictionary.
  2. Or it’s a bit late if they do.
  3. Ursus arctos horribilis … how appropriate.
  4. Females have a better developed sense of smell and so make better test subjects for these types of studies.
  5. Just in case humans smell different … which, of course, they do. What’s more, different classes of humans smell different. For example, single men (as opposed to partnered men) smell different to women.
  6. Except you can’t smell salt of course. D’oh!
  7. Richard Axel and Linda Buck shared the 2004 Nobel Prize in Physiology or Medicine for the discovery of odorant receptors. Axel had one of the most impressive views from his office window overlooking Manhattan and the Hudson River in New York.

    New York, New York

  8. For comparison, humans have about 400 odoratory receptors and can theoretically distinguish about 1 trillion different smells.
  9. As an aside, bees have a reduced number of taste (gustatory) receptors, only ~15% those found in fruit flies or mosquitoes.
  10. Biological Method (Bees) for Explosive Detection by Gillanders, R. N. & Turnbull, G. A., 2019, in Explosives Detection: Sensors, Electronic Systems and Data Processing. Capineri, L. & Turmus, E. (eds.). 1 ed. Springer, (NATO Science for Peace and Security Series B: Physics and Biophysics).
  11. After all, they can clearly smell it. I don’t need answers on a postcard to this Q. Remember that bees are a forest/tree dwelling animal where forest fires would be expected. A defensive response to a forest fire is unlikely to be of any evolutionary benefit.

12 thoughts on “Smell the fear

  1. Paul Honigmann

    I’ve thought a lot on this too.

    I’ve noticed inconsistent responses to smells, some said to trigger bees.

    My working theory is that bees respond defensively to a sudden CHANGE in odours. This alerts them that something large is nearby, for example an animal crushing vegetation. Thus if I weed vetch near my hives, its pungent sap brings guards out. But if a visitor wearing perfume approaches hives SLOWLY the bees ignore them.

    I worked with gas sensors a lot. Biological ones tend not to be absolute (1ppm = consistent signal), they tend to be differential. Ever noticed how your nose gets used to some background smells with time?

    Reply
    1. David Post author

      Hello Paul

      Interesting … however, how would you interpret the use of air freshener when uniting colonies. I discussed doing this a few weeks ago. The few gentle squirts of air freshener certainly represent a rapid change in odour, but I’ve not noticed any immediate increase in aggression of colonies treated like that. Perhaps the smell is so all-enveloping they don’t get a chance to mount any sort of response?

      It’s something I’ll think about next season …

      Cheers
      David

      Reply
  2. Paul Lindstrom

    Reading the article make me remember a visit recently by a young man and his father. The father wanted to see our bees, and I took him down to the hives. We stayed at a safe distance since I didn’t want to bother to put on the bee suits. His son, scared of bees (he admits to this freely) eventually came down towards us to have a look, despite his fear. It didn’t take many seconds before a bee flew straight at him, chasing him away. I don’t remember the wind direction, so can’t say for sure, but it was uncanny that the bee flew straight to him, ignoring us. So I think there is something in what you say/speculate on.

    Reply
    1. David Post author

      Interesting Paul … we do some collaborative work with a group in Aberdeen. When we visit the apiary one of their team always gets stung, even when we’re all working on the same hive. He’s taller than the rest of us. Whether that’s the reason is unclear, but once the sting pheromone is in your suit or gloves you know you’re going to keep on getting unwanted attention 🙁

      Cheers
      David

      Reply
  3. Steve Donohoe

    I love walking in the Andalusian hills 🙂

    I wonder if dark features can make bees more prone to attack. I went with Randy Oliver to inspect bear damage; the bees ignored him and had a dig at me. We were in t-shirt & jeans. It could have been the stench of walrus OR the fact that I have dark hair despite being in my late 50s (no dye, honest) whereas Mr Oliver is grey. He says his sons get pinged much more often than him too.

    Reply
    1. David Post author

      Hi Steve

      Dark colours also tend to result in more robust responses. I presume this is evolutionary pressure due to bears. Height also influences the response as well. We collaborate with another research group and, when we visit their apiary, one of their scientists is taller than anyone else present. Without exception he gets the most attention.

      Very useful 😉

      Cheers
      David

      Reply
  4. Helen Tworkowski

    As ever an intriguing post. Some thoughts on your post:

    The more i work at being a “good” beekeeper, the better my bees behave. Year on year on year. You reap what you sow. Maybe it is the breeding. Maybe they do not live their lives in a hypervigilent state, like battered famies waiting for a drunk abuser to come home. Epigenetics?

    I try to stop and prepare before i open a colony. To go into “the zone”. To focus on them, and them alone. I am sure that carbon dioxide plays a role in all of this. We definitely know they can sense it. Bees have a prediliction to sting on the face. The more hyped you are the more you huff and puff. So calm quiet beekeepers produce less CO2. Less than a big brown bear.

    Thank you

    Reply
    1. David Post author

      Hello Helen

      They certainly can detect CO2 … and I regularly take advantage of that when looking for eggs on an overcrowded frame. I bring it up to my veil and blow very gently and the bees tend to move away in a relatively orderly manner. It’s even gentler than gently shifting them aside with a finger. I rarely if ever get an aggressive response.

      The experience and confidence that comes from opening hundreds of hives is itself calming. I certainly never achieve the sort of Zen-like state (or anything close) seen if you accompany a bee inspector or good beefarmer, where they can ‘read’ the hive almost without opening it, but at least I have something to aspire to in my beekeeping 🙂

      Best Wishes
      David

      Reply
  5. Dave McManis

    Hello David,
    I’ve been keeping bees for five years now and am certainly more relaxed when handling bees than I was in the ‘early years’, when every inspection was adventure.
    I now use much less smoke and have developed the habit of talking to ‘my girls’ as the inspection progresses. Whether this calms the bees or the bee-keeper is debatable, but it does appear to help. Even during the June gap when they can be quite tetchie on a cold wet summer day it seems to take my mind focussed on the task in hand and not the cloud of irritated bee surrounding my visor.

    Reply
    1. David Post author

      Hello Dave

      You’re not the first person I’ve heard of that talks to their bees. I also know some who name individual queens. There’s nothing wrong with either practice though it’s not something I do. However, it’s not unusual for me to mutter to myself during an inspection … Where’s the queen? Are there any eggs? Where are my glasses? etc., interspersed with the occasional Sorry! if I’m struggling to return the supers to an overflowing brood box.

      And I suspect you’re right … the talking probably helps the beekeeper (focus, stay calm, remember or whatever) more than the bees.

      Cheers
      David

      Reply
  6. Paul H

    Re: air freshener, I imagine it as being equivalent to some effect which instantly robs a crowd of humans of their sense of hearing – the inability to communicate. Effective yes, but I assume the bees are distressed by it, so I prefer the slower “newspaper” method of uniting.

    Reply

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