But recently I read something very interesting about Earth's cephalopods (squids, octopuses, etc) that shines another light on the ability of cephalopod tentacles to function as legs. By the way, the usual term for octopus tentacles is 'arms', and only the two prey-catching appendages of squids are called 'tentacles'; their other appendages are called arms as well. Because I am looking at their function I will stick to 'tentacles' here. My interest was piqued by the following sentence: "... flexible arms, with no joints as fixed reference points, cannot discriminate between shapes, however elaborate the brain." I found this in a section entitled 'What has limited the evolution of cephalopods?' in a book by Janet Moore on Invertebrates (the book is quite interesting for would-be animal designers).
If cephalopods indeed cannot feel well enough to tell shapes apart, that is bad news for having their tentacles turn into functional legs. In man, the ability to sense where our limbs are enables us to walk in the dark and to recognise objects by manipulating them. I will come back to the importance of this sense, called proprioception, later. First I searched for more data on tactile function in cephalopods. Luckily, there is an excellent summary in Scholarpedia, so everyone can read it.
Click to enlarge; sources through link in text
It turns out that octopuses are quite good at feeling the texture of an object, and you can teach them (using rewards etc.) to tell two objects apart that have the same shape but a different texture. In the graph above octopuses were given two different objects, and they had to learn how to tell the two apart. When the two lines with black and open markings diverge, the octopuses managed to learn the difference, but when the lines do not separate, the octopuses hadn't a clue what the humans wanted them to learn. At the top, the octopuses quickly learned that a cylinder with grooves is not the same as one without them. But if you give them cylinders with the same surface texture, but with a different mass because one has a weight hidden in it, they have no idea. They cannot tell a heavy from a light object. The remaining two graphs were control experiments proving the same thing. Other experiments also showed that octopuses are indeed very bad at recognizing shapes. The most likely explanation is that they cannot judge well where the various parts of their limbs are in relation to other parts.
The Scholarpedia review does not go so far as to state, in contrast to the book, that it is the lack of solid parts that is to blame for this, but that does make sense. Consider our limbs, or those of insects for that matter. Telling where the end of the limb is requires two things: the first are sensors to tell the degree to which all joints are bent, and the second item of knowledge is a table containing the lengths of all segments in-between the joints. In fact, working that out does not require more than fairly simple trigonometry. Can an octopus do the same? The lack of joints makes it more difficult. What it would need is some kind of sensor that can tell where it is in relation to another one in theedimensional space: direction as well as distance. Off the top of my head I cannot think of any biological sensors like that. The point is not whether any exist, but that the octopus doesn't seem to have any! One more reminder that alienness can be found on our doorstep.
Do you actually need propriocepsis? Humans do! There are a few people in whom this sense has been wiped out completely by disease, and these people cannot tell the position of their body and their limbs without looking. Most cannot walk, even though their muscles are fine. There are many more examples showing that the ability to feel where your body is in space in extremely important for human, and I would guess vertebrate, control over posture and movement.
What I find hard to understand is how the octopus moves about without such an option. The clip above shows an octopus disguised as some plants walking over the sea floor (on YouTube here). That is impressive, and there are many more video's showing rather impressive feats of movement. Their control over their tentacles must be organised differently from the way we control movement. Again, they're rather alien.
Can all these problems be reconciled with turning tentacles into walking limbs? Well, yes. After all, the Mark II had evolved a series of incompressible elements with joints in between them purely for mechanical reasons. Those elements of the Mark II are shown on the right in the image above. On the left is its successor, a proper leg with a reduced number of segments. The Mark II set-up is just what is needed to allow propriocepsis like ours to evolve; I am assuming here that it is advantageous to have such a sense. If there is a small sensing error in each limb, having a large number of short segments adds up to more uncertainty about where the limb is than having a smaller number of longer segments. Reducing the number of elements was better mechanically anyway, and may also allow a more sophisticated, or at least more reliable sense of position as well. There are probably advantages in the motor control of movements as well, but I think I will skip that (or reserve it for another post, who knows?).