Creepy-crawly personality, pain and emotion

I hope you’re a dog person. Failing that, you might be a cat person, which is alright to. One thing I would be very surprised at is if you are say, a spider or cockroach person. If identifying yourself as a cat or dog person says things about your personality, then what would hitching your wagon to the legion of things that don’t have backbones say? Compared to typical pets such as cats and dogs, and other mammals , birds and even reptiles, invertebrates (insects, spiders, crustaceans, molluscs etc) are generally thought of as a bit weird, and quite disgusting .

cockchafer
b-e-a-utiful

 

Sometimes its not hard to see why. For instance, did you hear the one about the females who store sperm from a single mating for over a decade? Or perhaps see the spines and spikes on the penis of Callosobruchus maculatus.

090225-03-spiky-beetle-genitals_big
unpleasant to say the least

Maybe you did, or maybe you didn’t know that ladybirds are cannibals who will think nothing of consuming eggs that would contain brothers and sisters.  I think my favourite is how in some species of spider the females get so hungry they can eat a prospective mate before they mate. Don’t think I’ve ever been that hangry.. The general media coverage of spiders, wasps and the like in peoples’ houses also seems to follow this trend.

express spider headline
Skull and cross-bones warning sign and anti-immigration slant optional extras

Whereas its not the same for our more furred friends. These guys are out there playing with children, helping the less-able, and starring in various internet memes (e.g. grumpy cat, pun dog, anti-joke chicken).

Again, this is hardly surprising. Everyone who has had a pet knows they each have a unique personality, like we do, with quirks and habits, both good and bad. E.g. some squirrels are nutters (OK, no more terrible puns), some are cool as cucumbers. Yet its hard to see personality, consistent behavioural differences, between one worker ant and the next, or this grasshopper and that grasshopper. Or at least, that’s what we used to think.

Recently however, there has been a surge in interest in personality traits in animals. Why they exist when evolution should drive everything to have the same, optimal behaviour, and what large scale consequences they have are now hot topics. The interest has filtered down to those who study invertebrate behaviour, with a raft of studies (reviewed here) investigating whether they have personalities, and what this might mean. And the answer to the first question seems to be a unanimous “Yes!”.  Pretty much everywhere we have looked, scientists are finding that some “creepy-crawlies” are bolder, more active, more aggressive or more explorative than others of their species, and this is consistent over time. For instance, some work I’ve done has shown that field crickets (think a flightless grasshopper than lives in a burrow in the ground and sings beautifully in the early summer) show consistently different levels of activity, exploration and boldness over their adult lives. In fact the differences among-individuals even increase over time. This increased consistency is in fact something that is well-known in humans. So, crickets get stuck in their ways, much like Bert with his pipe or Maud with her 4 O’clock Archers and lemonade.

It goes further. Remember the spiders that eat their mates I mentioned earlier? Well it turns out this is linked to their early life behaviour. Female that were most aggressive and voracious as juveniles are the most successful, so this trait is selected for by evolution. However, they cannot dial down their level of aggression once they become adults. This consistency then means that occasionally, they get carried away and chomp a hopeful male before he gets chance to copulate. Poor bugger.

 

m-f spider
Female left, male separately on the right. Presumable for his own good

OK, so perhaps we’ve got these differences among-individual in their behaviour, but that’s not a big deal. Not all plants of one species look the same, so why should all invertebrates of a certain species act the same? There are other traits we share with cats and dogs and the like which makes them so much like us, unlike the scuttlers, wormers and spinners.

For instance their ability to feel pain. Dogs hate going to the vet, why, because they give them injections and prod places that hurt. Every trodden on your cats paw? Well from the look they give you for days after you know that hurt. But do crickets, bees and slugs feel like that? Based on the fact that they seem to troop on pretty determinedly even when missing a leg, or how the locust in your school dissection class kept kicking even when its head was gone, you would think not. This is a view backed up by the ethics board you need to go to before any research on animals is approved. If its on vertebrates (or octopuses*) you must indicate how you will minimise the number of animals, reduce the chance of them ever suffering, and generally treat them exceptionally well. This is all well and good. If your research involves invertebrates however, you don’t even need to fill in a form. Just go for it. Breed them, use them, freeze them, there is no one to report to. Of course the vast majority of scientists are empathetic people who do not want to see an animal harmed, but there are no official restrictions.

This is interesting, as a recent review has highlighted that in fact studies on invertebrates do in fact suggest they feel pain. A difficulty for studies like this is ascertaining pain in organism you cannot communicate with. There is no chance the hermit crab is putting an X on the 1-10 pain scale when you put it in a vice to crack open its current abode. But you can still look for various things to infer the feeling of pain. For instance, does the animal move away after the potentially pain-causing action occurs? Do they show attention to the site of the injury? Do they change their behaviour afterwards? To they learn to avoid that stimulus? Will they pay some kind of cost to get pain-relieving substances?

 

03_morphine
I think I still prefer calpol

On these counts, the general consensus is that invertebrates fulfil most of the criteria. For example, hermit crabs that receive a single shock show an extended desire to get out of that shell and enter a new one. Furthermore, they will rub the areas of their abdomen which had been shocked, a response coherent with the idea that the area is painful. In fact, electric shocks have been used in many studies on learning in insects as a negative reinforce, something we would happily interpret in humans and mammals as evidence of pain.

Certainly, it seems clear how the feeling of pain would be adaptive, stopping an animal from repeating a behaviour that damages it. From a purely behavioural perspective then, it seems that, although they may deal with it differently (do you keep working when you’ve lost a limb? Does the worker bee? They are tough cookies….) invertebrates can feel pain.

The barriers appear to be coming down then. They are individuals, and they probably feel pain. What more do they need to do to make us like them?

 

insect circus
probably not this

One key dimension of human behaviour that allows us to strongly relate to each other is quite simply how we feel. Are you happy – that makes me happy too; are you sad – is there anything I can do about it? Emotions are a complex, yet utterly essential part of what makes us human. Do other animals, vertebrates as well as invertebrates, have emotions like us?

We again a problem here in finding out what is going on inside an animal’s head. No language, little ability to fill in surveys and only mild insights into their psyche on Twitter.  Instead we must investigate something called their “affective state”. Simply, after training on a set of signals that either indicate rewards or no rewards, what do they do when given an ambiguous stimuli? Do they act optimistically, and expect a reward, or pessimistically, and assume its not their day? As its been shown in humans, this tells us whether an individual is in a good mood (and so acts optimistically) or in a bad or depressed state of mind (and so act pessimistically). This has been investigated in rats, dogs, rhesus monkeys and starlings (reviewed here), and in the majority of cases the biases following negative or positive stimuli were as predicted. Animals exposed to rewards treated ambiguous stimuli more positively, while those exposed to punishment treated the same stimuli more negatively. So this seems a pretty neat way of assessing emotional state.

So, I hear you cry, does this extend to insects, crustaceans and other invertebrates? Well as this is a relatively young area of research, we can’t say for sure they all do. But if you want to look for complex behaviour in an invertebrate, look to the bees. And lo, they did, and the bees did come up with the goods. Bees that recently had the tube they were in vigorously shaken reacted more negatively to an ambiguous stimuli than bees that were un-shaken (and, presumably, not stirred either). Shaken bees also showed lower levels of serotonin, dopamine and octopamine, hormones related to cognitive processes. Check out that research and a nice video explaining it here. This is directly analogous to the earlier research in vertebrates.

OLYMPUS DIGITAL CAMERA
well done bees!

Now, bees are pretty awesome, so we will have to wait for this to be extended to other types of invertebrate before we can mark off emotion alongside personality and probably pain-sensitivity as general traits of those without backbones**. But I wouldn’t bet against a positive finding. This raises a lot of questions. Should there be proper ethics for work in invertebrates? Should we be a bit more circumspect when we reach for the salt to get those slugs or the swatter to splat that fly? At least, we should look again at the little guys that share our world and often our homes.

 

* Octopuses have been shown to play and probably feel pain, and so claim exalted status as an invertebrate that you need ethical approval before working on.

 

** Although Darwin seemed convinced: “Even insects express anger, terror, jealousy and love, by their stridulation” from The expression of emotions in man and animals (1872), p. 347, via doi: 10.1016/j.cell2014.03.003

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