Jun 4, 2012

The culinary adventures of a cuttlefish

Rapid taste aversion learning in adult cuttlefish, Sepia officinalis *

Taste aversion is a physical response to a certain taste, that was formerly associated with nausea and sickness.

Psychologist and author Martin Seligman described this phenomenon as the “Sauce Béarnaise Syndrome” after eating a filet with Sauce Béarnaise and throwing up afterwards, due to a stomach flu. From then on even the smell of the sauce became repelling to Seligman, although the nausea was caused by the flu and not the meal.
Interestingly, only the sauce made Seligman gag, the meat that he ate for his entire live, seemed to be somewhat immune to the conditioning!

An animal study, that became classic for taste aversion, was done by John Garcia:
He gave rats saccharin-sweetened water and exposed them to heavy radiation, which made them sick (rats, like guinea pigs, can’t throw up, though).
He found that his rats would drink much less sweetened water than a control group. Garcia concluded that the rats associated the nausea caused by the radiation with the sweet taste.

The remarkable thing about conditioned taste aversion (CTA) is its super-fast and robust effect: After only one exposure to the radiation Garcia’s rats would build an association of the sweet taste and feeling sick.

Conditioned taste aversion is thought to be a survival mechanism to avoid toxic or poisonous foods.  Cephalopods seem to be mostly predators and not scavengers and – at least under laboratory conditions – can be tough customers when it comes to dead food. It is not uncommon that animals (in our case Octopus vulgaris and Sepia officinalis) would refuse fish or shrimps at the first feeding in the lab after captivation or if the food is from a batch that has gone yucky.

Yet we do not know much about the prey choice and the related learning mechanisms in cephalopods. Although there are some papers out about smell and taste in squids or octopuses, this research is the first conditioned taste aversion investigation in cephalopods ever.

Dude, I really love shrimps. No wait, wait! I really l-o-v-e shrimps!!
[Sepia officinalis, by Bora Zont under creative commons]

The experiments are pretty straightforward: First the authors did a food preference test to see if the cuttlefish like crabs or shrimps better. The preferred food was then coated with a quinine-nail-polish-mix to make it taste bitter and presented to the cuttlefish.
They weren’t too happy about this “improvement” and after catching the bitter package a couple of times and checking it out, the cuttlefish didn’t react to the food presentation anymore.

 Here you can see the average time until the cuttlefishes attacked the prey. 
Over the trials you can clearly see that experiment animals (squares) 
become more and more "meh...", while the controls (triangles) stayed totally “woo-hoo!”

So now the researchers tested the food preference again. They presented shrimps and crabs either 24 hours after the last food presentation or after 72 hours. In the first group, 14 of 18 animals changed their mind and in the second group 12 out of 15!
The researchers successfully killed a cuttlefish’s favorite dish!

Researchers killing kids dreams and cuttlefishes favorite dishes: 
Experiment animals that changed their opinion about the best food ever (black bar) 
and control animals (white bar) in a food preference test 24 hrs and 72 hrs after the last experiment. 
Stars indicate significance.

I liked this experiment since the authors presented a first approach to conditioned taste aversion in cephalopods. Although this entire taste aversion thing is known since the 50s, it wasn’t studied in a huge variety of animals – of course mainly mammals (rats) and only very few invertebrates (e.g. drosophila and the fresh water snail lymnea). So it is really cool to test this learning paradigm in more species, especially in the cool gang of cephalopods.

The ‘but’ lies in the difficulty of the topic definition. Taste aversion has some unique features, which make it so special.

  • One condition is that you need a novel taste. The problem lies in the “lateral inhibition”, which is the filet that wasn’t affected by Seligman’s Béarnaise aversion, because he ate it his entire life. The cuttlefish ate crabs and shrimp all their life long, so since it is not a novel taste, it shouldn’t be taste-aversion-condition-able.
  • Another feature is the super-fast acquisition of the aversion, which could not be seen in this experiment. However, it might be connected to the above problem.
  • Maybe the most important point would be the reoccurring nausea after the conditioning (the feeling to gag, whenever Seligman just smelled Sauce Béarnaise). I don’t know if cuttlefish can vomit (I never saw a cephalopod throwing up, but then again I rarely meet them at bars), but the quinine is just repelling bitter, instead of toxic.
It should be said that quinine is used for taste aversion studies in other animals as well (lymnea and drosophila again), so in my opinion this could be a general problem, especially if we want to generalize our findings and compare it to studies in mammals.

Maybe we could find a back door and just call this paradigm “food aversion” to somewhat circumvent this problem?

I would be happy to hear your opinion!

ResearchBlogging.org Darmaillacq, A., Dickel, L., Chichery, M., Agin, V., & Chichery, R. (2004). Rapid taste aversion learning in adult cuttlefish, Sepia officinalis Animal Behaviour, 68 (6), 1291-1298 DOI: 10.1016/j.anbehav.2004.01.015