Big Bad Flashy Fish (BBFF): the final answer to echolocation

This is -probably- the last of my series of posts on the comparison of vision with echolocation. Previously, I discussed disadvantages of echolocation (here and here).First, an animal using echolocation must send out very loud noises, and in doing so makes its presence known over a much larger distance than at which it can detect objects itself. Second, echolocating animals  have to provide their own signal limiting their range, while sight takes advantage of sunlight or moonlight. Third, sight -and hearing- are passive senses, not betraying the presence of animals using them. Instead, echolocation boils down to shouting "WHERE ARE YOU!?", which probably means that only the Big and the Bad can afford its use.

I ended by assuming that the darkness of the deep sea would make it a perfect habitat for echolocators. Of course whales do exactly that, and they fit the job description of being Big and Bad. But they have not been around all that long, and the seas have been full of fish and squid for much longer, so you would think that they would have had the time to evolve echolocation. So where are the marine echolocators? Nothing. Silence. 

So I asked a biologist, Steve Haddock, who was kind enough to enlist a colleague, Sonke Johnsen. Here is their conversation, Steve Haddock first: "I don't know of any examples. Lots of fish make sound (the midshipman), but it takes a lot of energy and seems to be largely for mating. Maybe the distance between their 'ears' is too small to be effective? Even humans underwater can't tell what direction sound is coming from. That doesn't explain bats, but different speeds of sound in air vs. water? Not sure, but it is an interesting question!"

I had not thought of that, but sound certainly travels faster through seawater than through air. At a depth of 2 km, sound travels at a speed of over 1500 m/s. Compared to about 333 m/s in air at sea level, the speed of sound in the deep sea is about 4.5 times faster. That matters, because you can tell the direction of a sound by measuring the differences in arrival time between two ears. Immersing those ears in water immediately makes the difference in arrival time 4.5 times smaller and therefore more difficult to detect. Could it still work? To find out,  I first assumed a distance between the two ears of 20 cm. With that, a sound coming in from the side will arrive 0.6 ms later at the farthest ear in air, and 0.13 ms later in the deep sea. That does not seem like a lot, but Wikipedia informs us that humans can detect differences in  arrival times of sound of 0.01 ms. So, given some good neural software, it should be possible to use this trick in the deep sea.

Anyway, Sonke Johnson added the following to Steve's reply: "There seems to be no good reason why fish don't echolocate. There are certainly fish and sharks whose heads are wider than echolocating dolphins. It's also not a marine mammal thing, since seals don't echolocate. Many fish and mammals eat the same things, so it's not that either. Cetaceans have great hearing, but that's sort of a chicken-egg thing and there's nothing preventing fish from having better hearing. You can't even say it's a warm-blooded-only club, because certain large fish (e.g. swordfish, tuna) actually heat up their brains and eyes so that the work faster. It's probably just one of those things. One possibility is that early cetaceans may have started in muddy rivers. Muddy river animals sometimes evolve interesting sensory systems (e.g. electroreception) because it's impossible to see. Even today, some cetaceans inhabit murky rivers and lagoons. Of course, many fish do too...." 

I thanked both through email, but would like to repeat my gratitude to them here.

Back to the light

So far, we have to conclude that we do not know why the deep seas are not filled with Big Bad Echolocating Fish (BBEF) or Squid (BBES).

Click to enlarge; from this source

The sea is full of bioluminescent animals, and the image above shows the ways it can be used for offensive purposes, something we will focus on. An amazing array of life forms, from bacteria to many diverse major groups, have bioluminescence. They use it for a wide variety of purposes, that can be basically divided into defensive and offensive ones. Steve Haddock has written a very comprehensive review, that can be obtained free of charge, and which is very readable for non-biologists. There is also an excellent website. I will focus on just one of the many uses of bioluminescence: to illuminate prey using photophores.

Click to enlarge; source here

First, what are photophores? Well, the word simply means 'light bearers', so they are organs producing light. Without ever having studied them, I thought they would be just sacs with bioluminescent chemicals in them. But as the image above proves, showing a squid photophore, they turn out to be much more complicated than that. Perhaps you recall the reasoning that the physics of light quickly led to the evolution of a camera-type eye, with a retina, lens and diaphragm? Well, there are lenses and shutters in photophores as well. There must have been a process very similar to that of evolution of the the eye, but here the question must have been how to produce the best biological flashlight possible. The image above shows a photophore from a squid. At the centre there is a light producing mass, surrounded by a mirror, reflecting light until it exits the photophore through a lens. I have unfortunately not found a review paper comparing the optical design of photophores, but this should be enough to prove how complex they can be.

Click to enlarge. These are 'loosejaw' fish.The one on the top right sends out red light, and is called Malacosteus niger. Note that these animals have various photophores on their heads. The one it is all about is the suborbital one ('so'). 

From: Kenaley CP. J Morphol 2010; 271: 418-437

Now, finally, we are ready for the final twist in the comparison of vision and echolocation. There are fish, shown above, using well-developed photophores as searchlights to find their prey. This use of light is very similar to echolocation: the animals have to provide their own signal, resulting both in a limited range and in becoming rather conspicuous.

Click to enlarge. Photophores from the dragonfish Malacosteus. In the two images, 'c' is the light-emitting core, 'r' is the reflector surrounding it, and 'f' is a filter to give the emitted light a red colour. The light bounces around until it exits the photophore through the aperture 'ap'. Form: Herring and Cope, Marine Biology 2005; 148: 383-394

The fish best known for this behaviour are so-called dragonfish, and their use of photophores involves the kind of wonderful bizarre features that only real evolution produces. These fish send out red light, which is unusual because red light doesn't carry very far in water. Most bioluminescent signals therefore use blue light, and accordingly most animals in the deep sea cannot see red light. They also cannot see the red light emitted by the dragonfish, which is rather cunning and makes the searchlight invisible. The snag is that some dragonfish species do not have a pigment in their retinas to see red light either...

Instead, they use a trick: there is an antenna protein in their eyes that is sensitive to red light, and this transferred the energy to the pigments sensitive to blue and green light that the fish does have. That transfer pigment works like chlorophyll, not a protein you expect in an animal at all. That's because the fish obtain it from their food and somehow transfer it to their retina. All this can be found on the website I mentioned. I certainly would not dare to use such outrageous traits in my fictional animals!

The oceans may not be filled with predatory BBEF, but there aren't many Big Bad Flashy Fish (BBFF) either. Neither option seems to have gained evolutionary prominence. Perhaps their characteristic conspicuousness makes these options too risky. I must say I like the option of equipping animals with flash lights.

Click to enlarge; copyright Gert van Dijk

So here is a quick and rough sketch of a possible Furahan animal with searchlights, which has just spotted a tetropter. Would the edge of better prey detection outweigh the increase in its own predation risk? I do not know. There are other worrying thoughts: why is bioluminescence on Earth so rare outside the oceans? It is hardly found on land, and does not even seem to occur in fresh water either. Are there reasons for that? Is the poor animal shown above doomed already?

The 'lateral fin theory' and mackerel mode

I still have no time for posts that take time to read, think and write; well, more than a hour or two. That is a pity, as some ideas need time to do them justice. For instance, there is a post to write on what happens is photosynthesis is less dramatically imperfect as it is on earth (see here); there is also the final chapter of the 'sight is superior series' (see here), and I have at least one other world builder's creations in mind.   

Those will have to wait; instead, here is a short post on where the six limbs on Furahan hexapods came from. On the 'real life' level the answer is easy: 'six limbs will look exotic and therefore help create an alien ambiance'. Within the Furahan world, the logic of science fiction demands an answer that fits within the concept.

 

Click to enlarge; copyright Gert van Dijk

The sketch above is an old one, and the first that showed the first steps in hexapod ancestry. By now, many of the anatomical features are being overhauled, so the number of eyes is incorrect. The overall scheme is still there though: it all starts with a less than impressive little elongated tube with broad fins at its sides. This 'ULF' (unassuming life form) swims by waves that pass from front to back along the fins. Nothing particularly spectacular here: undulating fins may well be a constant throughout the universe. From that start I assumed that the fins might be divided gradually, to provide greater control and flexibility (you cannot suddenly move a part in one direction if it is fixed to parts in front and behind of it). This greater need for manoeuvrability evolved together with jaws; you cold also say that the jaws and the fins helped one another's evolution: without jaws, there is no speed, and without a better propulsion, the jaws do not provide that much benefit. The third stage shows an animal with fully separated fins, just not necessarily six of them; the reduction to six came afterwards.

The origin of hexapod fins therefore lay in a lateral membrane that split up. Many years later I wondered where Earth vertebrate limbs originated. To my very large surprise, the first explanation I came across was something called the 'lateral-fin theory'.

Click to enlarge; Coates MI. The origin of vertebrate limbs. Development 1994; Supplement 169-180 

The images above show an example of what a hypothetical vertebrate ancestor was supposed to look like: it already had unpaired fins along its back and belly, and lateral (sideways) fins along its sides. The theory, apparently first formulated in 1877, states that these lateral fins later gave rise to limbs. I was first a bit irritated, but later pleased that I had stumbled on a principle that apparently was not altogether fictional. That was until I went back for a closer look at current theories regarding vertebrate limbs. It would appear that the lateral-fin theory is now out of date. Other theories held that limbs evolved out of gill branches, which seemed to make sense as the first forelimbs were attached directly to the skull. That theory apparently also now belongs in the dustbin of history.

                   

Click to enlarge; Coates MI, Cohn MJ. Fins, limbs, and tails: outgrowths and axial patterning in vertebrate evolution. BioEssays 20:371–381, 1998

The image above shows an illustration from a recent paper on limb development. It shows that that unpaired fins in the midline ('median fins') existed well before vertebrates had jaws or lateral fins/limb. When lateral fins appeared, the first to appear were the front pair, with as yet no trace of hind limbs. The two pairs did not evolve together, which you would think, given their similarities. Modern discoveries in the field of 'evo-devo' ( embryonic development in light of evolution) centres on hox genes as a sort of overall conductors of embryo formation. A recent theory holds that the genes responsible for limb formation were co-opted from a previous use, one that involved formation of the gut through the 'lateral plate mesoderm'. The paper from which the image above was taken  mentioned the possibility of a third pair of limbs in vertebrates, the kind of nice exotic happening that we like in speculative biology. Here is what Coates and Cohn wrote:

"Finally, the absence of vertebrates with more than two sets of paired appendages has often been used as an illustration of evolutionary constraint. Developmental mechanisms responsible for this anatomical limitation remain unclear. Arguably, the nearest approach to a third pair of lateral appendages may be the lateral caudal keels of certain fishes, such as tuna and various sharks."


So there are in fact three pairs of lateral, well, outgrowths in vertebrates? Fascinating. But the test continues:

"Even the most elongate lateral fins of primitive fishes terminate in front of the anal level. Clearly, lateral caudal keels can and do emerge, but articulated endoskeletal paired appendages require the lateral plate mesoderm, and this is linked intimately to the extent and pattern of the gut."

Curiouser and curiouser. It does not look as if vertebrates will surprises us by evolving a third pair of legs, though. For three pairs of legs, you need to turn to insects, and for big hexapods, there is always the fictional universe.

But does all this mean I should give up on my 'lateral fin theory'. Actually, I see no reason to do so. In fact, it is rather nice that the lateral fin theory remains in place on Furaha, as the explanation of the origin of six legs in Furahan hexapods.

 

Click to enlarge; copyright Gert van Dijk 

To celebrate that I stole another two hours and used Sculptris to sculpt two quick ULFs. The first is shown above: no jaws, four eyes, two lateral undulating membranes and two long gill tubes running along the belly connected to the sea by a number of spiraculae. I still need to name it, and I think I need something that does justice to its pivotal position in evolution. Suggestions are welcome. Latin or Greek only though, please.

Click to enlarge; copyright Gert van Dijk

And here is its successor. As you can see, the membrane has developed indentations and the animal is longer and bigger. It has six claspers in front that can already deal with soft prey quite well. Note that the body is stiff, very unlike the very flexible body in the old sketch. The body can flex up and down, but sideways movement are almost impossible, thanks to he two stiffening rods that lie buried in the body at the root of each lateral fin. The stiffness is a consequence of this early body plane, and is a feature of all later hexapods.

Click to enlarge; copyright Gert van Dijk

I could not resist quickly daubing one in Sculptris with colour to show one in 'mackerel mode' (I still prefer painting, but the 3D process certainly is a very quick way of producing an illustration).