Leap of faith

A frillfin goby. Image from Wikimedia.

I have two different ways to start this post: one from a comparative psychology perspective and one from an ecological perspective. Since I’m a bad editor, I can’t pick one, so I’ve given you both. The psychology one is on the left, the ecology on the right. You can read them in whichever order you want, but you should read both to follow the rest of the post.

One fundamental challenge we all face is finding our way around. Members of almost any species have to find where food is, find a mate, or find their way back home. Animals use a variety of cues to do this, such as remembering landmarks (things that can be seen from far away and are close to, or somehow relate to, the place you are looking for) or path integration (remembering the route you took so you can redo it in reverse; think Hänsel and Gretel). For a long time, there was a debate about whether animals learn to use each of these kinds of cues independently or form what is called a cognitive map, which contains all the cues and allows you to do cool things like take novel shortcuts and plan routes to multiple destinations. Most people would argue that this debate is now over and that many species, from bees [1] to bats [2] find their way around using cognitive maps (there are, however, some interesting dissensions from this opinion [3]).

Most animals live in challenging environments, where they face intense competition for things like mates and food. One way to minimize this competition is to move somewhere less desirable (much like the process that drives house prices: location, location, location). Partly by this process, various species have colonized almost every ecological niche imaginable. One type of challenging environment, for a fish, is in places that only have water in them some of the time, like small ponds that evaporate away in the summer or intertidal pools, which are areas along the coast that are underwater at high tide but out of the water, except for a few small pools, at low tide. If a fish gets stuck in a small intertidal pool, there might not be enough food or even oxygen in the water to sustain it until the next high tide (or it might not have anywhere to run or hide from a predator; or it might just feel claustrophobic). In this case, the fish needs to leave.

There are quite a few species of fish that live in intertidal areas and they have a range of adaptations to survive there. One of the most extreme is possessed by the mudskipper. Mudskippers solve their lack-of-water problem by breathing air instead of water (most fish breathe water, through their gills; they cannot breathe in air). Mudskippers don’t have lungs (though some fish species do) but breathe through their skin (and gills), which they therefore need to keep moist. When the tide is out, they dig themselves a burrow in the mud where they can stay moist and breathe. Who could ask for more? Mudskippers have adapted so well to this method of breathing that they actually can’t breathe in water any more (they are fish that can drown in water). When the tide is in, they hole up in their burrows where they store a small bubble of air, so that they can breathe. Fish out of water, indeed. Mudskippers do a number of other crazy things like climbing trees, jumping in the air (to impress the ladies), and having epic battles (between the males, over the good burrow sites, ultimately also to impress the ladies).

This post, however, is about a closely related fish to the mudskipper, the frillfin goby (see picture at top; both fish are from the goby family). Gobies also live in intertidal areas and, when the tide goes out, may find themselves stuck in a small pool. Unlike mudskippers, gobies do need to be underwater to breathe and they solve their real-estate problem by moving: If they find themselves in a pool that is too small, they leap out of the water and into a larger pool.

This is where their cognitive challenge lies, as shown in the diagram below. At high tide (on the left), there are no pools, just one flooded area with different depths of floor. At low tide (on the right), when jumping between pools, the fish can’t see one pool from the other. A fish that wants to get from the small pool on the left into the larger pool on the right has to already know where that larger pool is. Otherwise, it runs the risk of jumping in the wrong direction, landing on bare rock, and possibly drying out (or being eaten by one of evolution’s handmaids). In other words, the fish needs a cognitive map.

Of course, in order to have a map of their rocky shore, the fish need to visit different areas of it in advance, so they can learn what’s where. In a classic series of studies, Lester Aronson [4,5] found that they do this during high tide, when they can freely swim around all the ‘pools’. During this exploration they form their map, to be used at low tide later on, without ever having ‘practiced’ the route (though Aronson did suggest – half in jest, I think – that they might practice their jumps when it was raining and the intervening rocks were wet and slippery).

The key feature of a cognitive map, in this context, is that the map is independent of where you are on it (which makes it what is called an allocentric map) which allows you to plan new routes between places on the map. Say, for example, that construction season has started* and your regular route home is blocked. If you have a good map of the roads in the area, you should be able to plan a new route home – even if you’ve never taken that route before. This is called taking a novel shortcut and was, for a long time, considered the ultimate test of cognitive maps [6] because it was assumed that you couldn’t plan such a shortcut unless you had a ‘proper’ cognitive map with all the mental bells, whistles, and horns that play “La Cucaracha”.

Two of the main problems in testing for novel shortcuts are ensuring that the animal isn’t using some other cue, like a prominent landmark, to find its way around, and making sure that the shortcut is really novel – that the animal has never taken this route before. The goby’s pool-hopping, therefore, presents an excellent natural experiment that avoids most of these problems. Aronson brought gobies into his lab and built them a fake rock-pool environment in which he could raise and lower the water level. The fish were given the opportunity to explore this space at ‘high tide’ and then forced to jump between the pools (Aronson poked them with a stick) at ‘low tide’. This neatly solves both of the problems noted above: the fish had never been in this environment before; at the time of taking their great leap into the unknown, they had never experienced the space at low tide; and they certainly couldn’t see any cues outside their current pool that could indicate which way to jump (like those helpful signs the construction people put up that just say “detour”). The fishes’ jumps were much more accurate after exploring the space at high tide, compared to a set of earlier jumps they had made before exploring. In other words, it looks like they formed a cognitive map of the space while exploring it at high tide. The fish also seemed to remember their maps when tested again up to a month later [5].

Aronson’s experiments also hint at another potential spatial skill of the goby. The appearance of the rock-pool environment changes drastically between high and low tide. Goby cognitive maps could be sufficiently flexible that they could adjust to these changes in water level. For example, if the water level has gone down a little or a lot might determine how far the fish has to jump (how much dry land is in between the pools) and even which pools are still viable options (very shallow pools might be almost gone if the water has gone down a lot). As far as I know, no-one has explicitly tested whether the fish can do this. Aronson only use two levels of water (high and low) and his experiments have rarely been repeated and never (that I’ve been able to find) with more than two levels of water.

There is another interesting aspect to these experiments, which I’ll just briefly mention. Being able to do complicated things with your brain, like cognitive mapping and language and calculus, has a cost: you need to have a larger and more sophisticated brain. This means that you should only evolve (or retain) skills that you actually need. You could think of this as an evolutionary version of “use it or lose it”. There are lots of species of gobies and not all of them live near rocky beaches. Some of them live near sandy beaches where they can just retreat into the open ocean when the tide goes out. It’s possible that these fish won’t have the same mapping skills as the frillfins, because they wouldn’t ever need them. In fact, Aronson tested this and found that it was true: the fish from sandy-shore areas learned much less than the fish from rocky-shore areas.

Aronson’s experiments are not very widely known and rarely come up in discussions of cognitive maps, despite having been published 45 years ago and being better controlled than many other examples. Recently, however, there has been one more attempt to figure out what kinds of cues the gobies use [7]. Four species of gobies were used: two from rocky-shores and two from sandy-shores. The researchers built a fake rock-pool, a lot like Aronson’s, that had 4 pools. Two were shallow, one was deep, and the fourth looked deep but had a hole near the bottom that meant that it only retained a small amount of water at ‘low tide’. Two of the pools also had large very visible rocks on one side which could be used as landmarks at low tide to figure out which way to jump. Like Aronson, the researchers found that the rocky-shore fish easily found the deep pool and stayed there. One of the two species moved to a different (shallow) pool when the researchers moved the rocks – which suggests that they were using the rocks to find the correct pool (the other rocky-shore species did not change pools when the rocks moved, though). The sandy-shore fish tended to end up in the ‘fake deep’ pool. So it looks like all the gobies can do some mapping of their space, but the ones that live in rock-pool areas are much better at it and can incorporate more types of cues into their maps. In fact, the brain areas that seem to do spatial learning are larger in rocky-shore species than in sandy-shore species [8].

The frillfin goby is under 5 cm long and has a brain about one seventh the size of a pea (about 9 mm cubed, if you care). For comparison, your brain is about 150,000 times larger. And yet, these fish can navigate their complex and constantly changing environments every bit as well as bees (which, admittedly, have even smaller brains), bats, or us. Think about that the next time you get lost at the seashore.


* For non-Canadians: there is a long-standing joke that in Canada we have two seasons: winter and construction. This is not quite as funny to live through.

1. Cheeseman JF, et al. (2014). Way-finding in displaced clock-shifted bees proves bees use a cognitive map. PNAS, 111:8949-8954.
2. Geva-Sagiv M, Las L, Yovel Y, Ulanovsky N (2015). Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation. Nature Reviews Neuroscience, 16:94-108.
3. Cheung A, et al. (2014). Still no convincing evidence for cognitive map use by honeybees. PNAS, 111:E4396-E4397.
4. Aronson LR (1951). Orientation and jumping behavior in the gobiid fish, Bathygobius soporator. American Museum Novitates, no. 1486.
5. Aronson LR (1971). Further studies on orientation and jumping behavior in the gobiid fish, Bathygobius soporator. Annals of the New York Academy of Sciences, 18:378-392.
6. Bennett ATD (1996). Do animals have cognitive maps? The Journal of Experimental Biology, 199:219-224.
7. White GE, Brown C (2014). A comparison of spatial learning and memory capabilities in intertidal gobies. Behavioral Ecology and Sociobiology, 68:1393-1401.
8. White GE, Brown C (2015). Microhabitat use affects brain size and structure in intertidal gobies. Brain, Behavior and Evolution, 85:107-116.