There are no major organism groups that are exclusive to the deep sea, except the monoplacophorans (which were long though to be a fossil only group, but were rediscovered in the 1950s). Many groups are simply more common in the deep sea. These include the pycnogonids (sea spiders), echiurans and the asellotan isopods (who are by far the dominatant crustaceans in the deep sea benthos). Galathaeoids are found in shallow water reefs, but also near hydrothermal vents and on seamounts. Everyone knows sea stars and sea urchins from the beach, but they are much more abundant in the deep sea.
This clear stratification has led to the thought that the deep sea is a refuge for ‘living fossils’. I already mentioned the monoplacophorans. Crinoids have an extremely rich fossil record and were also thought to be extinct, until living ones from the deep were collected in the 1860s. Glypheids are another such case: they have a fossil record stretching from the Triassic to the Eocene, at which point they presumably disappeared. Then in 1908, a living specimen was caught.
This is all suggestive, but doesn’t really stand up to scrutiny. It’s not a matter of uncompetitive organisms having been pushed to the deep sea. It’s simply a matter of biology: these organisms have managed to adapt to their environment and migrated to the deep sea permanently. In that respect, they are as successful as any shallow water organisms, since they’re still surviving. The reason they left the shallow water is most probably climate changes – this is best seen when looking at the Southern Ocean (i.e. Antarctic Ocean), where there have been multiple shifts to and from the deep sea over geological time, all related to the state of the ice caps.
Let’s look at the Asellota as an example. They’re benthic crustaceans belonging to the Peracarida family. They are blind, tiny (few mms) and, like all peracarids, have no planktonic larvae. Basically, they’re not very good at dispersing and spreading around. They have all sorts of adaptations for all sorts of lifestyles, from the bulldozer-like diggers (desmosomatids), the spiny mesosignids, stick-like ischnomesids and even a secondarily-evolved swimming genus (Eurycope).
They are very important components of the abyssal meiobenthos, but can also be found in shallow waters at high latitudes – and even there, they have no eyes. By analysing them genetically, we can reconstruct how they came to colonise the deep sea. It turns out that sometime in the Mesozoic, they migrated there (multiple times) from the polar areas due to changes in the sea level. Once they got down to the deep, they liked it there and stayed, and are now the most successful animals of the ecosystem. They did not get outcompeted in the shallower waters, they simply managed to survive down there.
There are four things all deep-sea life has to be adapted to: low temperature, complete darkness, oligotrophy (low levels of food) and extreme pressure. The adaptations can be small or large, affecting individual proteins or whole structures. The most interesting, in my opinion, are modifications to any sensory organs and the underlying changes in brain structure, since this is an area where natural selection plays a very important role, given the unique ecological characteristics of the deep sea. This includes changes to the visual system (and the emission and reception of bioluminescence), as well as for sensing water movements (in fish, this involves changes in the lateral line). When talking of neurological adaptations, I will only be referring to fish since it’s simpler to tie changes in their brains to ecological adaptations.
Let’s get some generalisations out of the way first. The swimming ability of fish decreases as you go as you go deeper – an adaptation to low metabolism, brought by the lowered amounts of food available. There are two extremes that can develop: the fish, exemplified by the anglerfish, that have a neutral swim bladder (meaning they naturally sink), reduced organs (gills, kidneys, brains), low swimming ability, huge jaws and teeth and an associated strecthy stomach that allows them to eat prey as large as themselves, as well as enhanced sensory perception. They basically float around in the depths and wait for prey to come into their mouths.
However, there are those that retain their swimming ability – but they are the ones that live near seamounts, not the real bathypelagic. This is very telling: namely, it allows us to say with a high degree of certainty that food limitation is the most powerful selection factor in the deep sea, and that everything else revolves around the capture, storage and efficient use of energy.
The deeper you go, the smaller the brains of fishes get. This trend can be seen as reflecting many causes, since correlations between vertebrate brain size and almost anything can be drawn: habitat complexity (reef fish have the largest brains); sharks that chase their prey have brains larger than the more passive ones; the more social the fish, the larger its brain; and so on. Therefore, it has to be tied to behavioural and ecological aspects of the deep sea, and the sure correlations that can be drawn are: low habitat complexity (for fish, it really is quite a featureless habitat), and the passiveness of predation in the deep sea – there are no highly active predators, since they have to conserve their energy and have a very slow metabolism.
Notice the large size of the optic lobes, which is correlated with eye size and complexity. In mesopelagic species, what you also have are reductions in the olfactory areas, whereas in benthic species, they are grossly enlarged; this can be traced directly back to the feeding habits of the fishes in those environments: the pelagic species hunt by sight primarily, benthic species need to smell to detect their prey, since there isn’t going to be much light anyway.
If you look at deep sea pelagic shark brains, you’ll see that they have small brains, a cerebellar corpus that is not split into subregions and a smaller-than-usual telencephalon. The diencephalon, mesencephalon and cerebellum are all variable and there is no set pattern. This brain organisation not a result of phylogeny, as it is different in shallow water sharks – so it must be caused by being in the deep sea.
However, deep sea benthic sharks break from this mould by having significantly larger telencephalons (statisitcally speaking). This suggests that larger telencephalons are related to habitat complexity: the pelagic water column is empty and featureless, the benthos has all sorts of formations.
Another observed correlation is that the medulla was enlarged in deeper pelagic species. This is significant, because it’s in the medulla that the lateral line (organ for sensing water currents) and the electroreceptive organ plug in, as well as the ‘ears’ (I don’t know what they’re called, the accoustic sense organs). The implications and possible reasons for this are clear: they are more sensitive to water currents and are able to detect prey, even in the absence of light.
And that’s a perfect segueway into talking about adaptations to light! Before talking about bioluminescence, let’s think about eyes first. The eyes of deep sea fish are very specialised for seeing in extremely dim light conditions. The retina contains only elongated rod cells (100 µm on average, compared to 26 µm in humans), which are arranged in such a way as to capture the maximum number of photons, and in general are tuned to detect blue wavelengths. The rods have a layer behind them called the tapetum which reflects light back onto the rods, allowing a second chance at absorption.
Deep sea cephalopods and fish have regular camera eyes, but another thing that helps them is their relatively large size, which increases with depth. The fluid in the eyes is very clear to maximise how much light enters them. There are two types of eyes found: the ones found dorsally of benthic organisms, which allow them to spot changes in illumination from above (useful for spotting predators), and the usual eyes on the side of the head.
Deep sea crustaceans have compound eyes similar to nocturnal insects. Between the lens and the retina is a crystalline, transparent space that focuses the light from all the ommatidia to be concentrated on the photoreceptors – there may be more than 2000 lenses per photoreceptor. But the real cool part of crustacean deep sea eyes is their metamorphosis: the planktonic larva has a very different eye than the adult. Sometimes, the adult just has an enlarged larval eye (as in stomatopods); but the majority use only the barebones base of the larval eye and change it drastically – and this results in an amazing diversity of eye types that we see in deep sea crustacean eyes (I will not go into details, but I can do it on request!)
Bioluminescence is a trait present in most organism groups, whether they’re in the oceans or on land, or in the deep sea or the shallow sea. It’s also not uncommon. In fact, the most abundant organisms in the oceans are bioluminescent (whether you count it by number, in which case the bacteria win, or by mass, in which case various fish and crustaceans win). Obviously, it’s a desireable trait, and it’s the only reason bathypelagic and bathybenthic fishes have retained their eyes.
The diagram above shows what wavelengths of light are most often emitted and at what depth. Besides a couple of exceptions (one of which we’ll look at later), all of them are on the blue side of the spectrum, because those shorter wavelengths are most easily transmitted in the deep ocean: as you go deeper, longer wavelengths (green to red) gradually disappear.
Bioluminescence is the result of a chemical reaction during which photons are released as a result of energy input (in this case, breaking chemical bonds) – it’s the same principle as flame tests in inorganic chemistry. By far the most common are various luciferins (with the enzyme catalysing the reaction called luciferase), shown in the diagram above. They are kept within cells (photocytes) which can be arranged into whole organs (photophores). Alternatively, they can be released into the water.
Of course, most of the time, bioluminescence doesn’t come from the organism itself but from symbiotic bacteria. They are not some monophyletic group of bioluminescent bacteria, despite the fact that the light comes from the presence of a single gene family (the lux genes) – it can be imagined that either these genes were lost in many descendants from a last common ancestor, or that they spread by lateral gene transfer. Their luminescence is an integral part of their cellular circuitry and is not just some side-effect feature. It’s tightly controlled by gene expression (especially the lux genes) and the state of the cell, as well as other bacteria around it (through quorum sensing, which is how bacterial colonies communicate and coordinate each other).
These symbioses are not always beneficial and some bacterial strains act as parasites on various crustaceans, causing them to glow and get eaten by their predators. But in the usual cases, the bacteria are ‘cultured’ by the organism in the photocytes/photophores, and the light produced gets modified by various reflectors, absorbers, shutters and whatnot to produce the patterns or special wavelengths. These are achieved by having organic crystals, which bend the light, scattered specifically around the photocyte.
This tight association with animals may be the only reason these bacteria retained their ability to produce light. Another possibility is as a defence from oxygen, as I will describe later. But other than that, the physiological importance of light is a mystery, and the reasons its retention by natural selection have not yet been completely elucidated.
The luciferins are often accompanied by other proteins, which either emit their own light or mess around with the light from the luciferins, achieving different wavelengths and patterns, all of which play a part in the function of bioluminescence in specific organisms. The most famous example of such a protein is the green fluorescent protein (GFP) and related molecules (the ones used in molecular biology to tag cells and molecules).
On a related note, GFPs are what cause pigmentation in corals and other cnidarians. The cool thing about GFPs is that they synthesise themselves just by reacting with molecular oxygen. The difference between GFPs and luciferases is physical: luciferases exhibit luminescence, GFPs exhibit fluorescence. I already explain luminescence above; fluorescence is simply electromagnetic radiation emitted when a specific wavelength of light hits the molecule – there are no breaking bonds or changing energy states here (at least not on any relevant level).
Bioluminescence can be used consciously by an organism in three ways: to find food, to avoid being food and for (sexual) communication. The first two are the coolest, with all sorts of clever applications. For example, squids may release the bioluminescent chemicals into the water to distract predators/attract prey. They can blind their attackers/prey, as squids do. Predators may use it to judge the distance towards a prey visually. Some more cunning animals will leave bioluminescent marks on their predators, so that they will then be attacked by animals higher on the food chain. Those animals that eat bioluminescent organisms often have very densely pigmented stomachs, so that the luciferin glow from their prey doesn’t shine to the outside.
Bioluminescence can play an important role for camouflage. Squid living in the mesopelagic zone are good at doing this: they make their underside blueish, the same hue as the light filtering from above, making them essentially invisible to any fish looking up at them (this technique is called counterillumination).
As for bioluminescent communication, it is limited – unlike in fireflies, where the insects can really talk and inform each other using light flashes. In the deep sea, this hasn’t been observed yet, beyong some light flashes which are used as warnings or attractants (much like pheromones in insects), but no real dialogue takes place. Although it is imaginable that conspecifics use it to signal and coordinate themselves, this so far remains speculative.
Sexual communication is one of the main purposes of this kind of bioluminescence. Females may produce bioluminescent eggs or have shiny ovaries, so that males will know where to plant their sperm (remember, no light down there!) There may be differences in the positions, sizes and activity of the photophores. This can be seen in many species, from various shrimp to cephalopods. In extreme cases only the females have any photophores.
That is best seen in anglerfishes, where the males are dwarfish, parasite-like creatures, while the females are the ‘regular’ fish as in the picture above. The photophore here is called the esca, and it’s attached to the body by the illicium, which is homologous to the first fin ray. The esca itself can be very complex in some species, containing the equivalents of mirrors, various filaments jutting out and other cool effects. The light comes from bacteria living inside it, and the fish can control the emissions.
In anglerfish, the male finds the female and bites into her and starts to rot, losing organ after organ until all that’s left are his gonads pouring sperm into the female. The reason I mention this is because the male doesn’t bite her with teeth, he uses a bone to ‘stab’ her. This bone (called the basal bone) is homologous to the pterygiophore, which is the structure that attaches the illicium to the head.
Lanternfish can also show sexually dimorphic bioluminescence. Here, there may be minor differences in the tail – they have bioluminescent scales that together form the photophores, called the supra- and the infracaudal organs. Note that I am generalising, and that some species do not have these organs and some species don’t exhibit sexual dimorphism in them. But when it does occur, there are all sorts of variations, from one organ missing only in females, to one organ being larger in males, to both organs being present only in males. There are also differences in the head photophores.
But just because there are sexual dimorphisms, it doesn’t mean that the role is necessarily sexual communication, and in fact it is very difficult to rule out other purposes. If, as in squids, the photophores can be very intricately controlled to produce specific wavelengths and patterns, then that makes a role in communication very likely. Anglerfish bioluminescence is almost certainly a sexual signal (as well as a lure for prey) – but this is not always the case, as the males of some species don’t have functional eyes. In lanternfishes, the staggering variability strongly suggests a role in sexual communication, since it allows for individual species to recognise each other, and for the males and females to recognise each other too.
As for the evolution of bioluminescence, the jury is still out. The only thing we’re sure of is that it evolved independently many, many times. The stomiid example we’ll be looking at will show just how pervasive the level of convergence is.
Notice that above, I talked of the three conscious uses of bioluminescence. I did that to differentiate from the biochemical functions of bioluminescence, namely photoprotection. Luciferases are very strong antioxidants, protecting cells from damage caused by oxygen free radicals – this is always useful to have, especially in shallower waters. The way this works is simple: they have a very high affinity for oxygen and so will bind with it before it can react with anything else. As you get deeper into the ocean, the danger posed by them decreases (with a lower metabolic rate, there is less generation of free radicals), letting natural selection act on the bioluminescence, generating the diversity of uses and systems we see today. The photoprotective effect is also largely attributed to GFPs.
Another way in which bioluminescence is useful (albeit only in shallow waters) is in optimising how well photosymbionts work, as in corals with their zooxanthellae, by making sure only the optimal wavelengths suitable for photosynthesis get transmitted.The picture above shows four dragonfishes (Stomiidae), a family of fish specialised for living in the pelagic deep sea and are characterised by their huge mouths and teeth and the multitude of photophores located on the head (the arrows on the picture point to them). Photophores are found in many groups of deep sea fishes, with different arrangements in each. Loosejaw dragonfishes have a suborbital (SO) photophore, which is used to help the eye adjust to the different brightnesses. They have a postorbital (PO) photophore emitting blue-green light (wavelength beneath 500 nm), used for sexual communication. Finally, there is at least one extra accessory orbital (AO) photophore, which is a bit more special.
In specimens B and D above, you can see that they glow along the red side of the spectrum, i.e. a longer wavelength of light. And this is the really cool part: the only wavelengths of light that penetrate to the deep ocean are blue. All the animals living there are therefore adapted to seeing only blue, short-wavelength light. So basically, these guys can shine as much red light around as they want to see ‘clearly’, while their prey is completely oblivious since they can’t see it.
In stomiids, sexual dimorphism is also found: females have no PO photophore, and the other photophores tend to be smaller. Of course, there are exceptions.
Vision is clearly important for deep-sea fishes, as evidenced by the fact that their eyes have not been reduced. However, most eye pigments of deep-sea organisms can only detect short wavelengths. This is in line with what we would expect: they only need to concentrate on any light coming from above, losing the sensitivity to longer wavelengths since they don’t exist in the deep sea. In fact, there are strong correlations between water depth and pigment sensitivity, which show that as you get deeper, the bands of detected light get narrower. Stomiids are an exception, and therefore have a spectrum of light all to themselves – it’s like having a loud party in an appartment building for the deaf. Although in the case of the deep ocean, some animals have developed symbiotic relationships for sensing red light. It’s all part of the predator – prey coevolutionary arms race.
The stomiid AO photophore is a very clever system and is arguably the main reason for their success. But here’s the great part: the AO is not a homologous structure. It came about convergently multiple times during the evolution of the loose-jawed stomiids, as can be seen clearly when looking at how the AO is innervated. If they had inherited it from a common ancestor, we’d expect that the same nerve, or at least the same nerve bundle, would be controlling it. But as can be seen in the picture above, this is not the case.
Now let’s look at pressure. As a general rule, pressure rises by 1 atm every 10 m (consider that the average depth of the ocean is 3500 m). This affects all levels of an organism’s functioning, from its biochemistry to its physiology, so it is a very strong selection factor; most shallow-water organisms cannot survive in the deep-sea because of pressure, and the best way to classify the vertical distribution of marine organisms is by pressure tolerance, since it’s a completely linear relationship with depth.
On the most fundamental level, high pressures affect biochemical reactions (as anyone who’s ever tried to do organic chemistry knows). So the proteins carrying them out have to be adapted, and there are generally two paths for them to take: either they have wide-ranging influence by changing the cell’s chemistry (making it more tolerating of high pressures so that proteins can function normally), or the protein itself changes to cope with the pressure (interestingly, this almost always involves a reduction in the volume a protein takes up – this has been observed even in DNA).
Pressure also alters gene expression and transcription. Pressure, in microorganisms at least, causes the expression of a particular set of pressure shock genes, and genes involved in the regulation of the cell cycle and protein synthesis get down-regulated. Also, since pressure causes everything to pack up close together, this reduces the fluidity of the cell membrane (by bunching up all the lipids that make it up). Another cellular effect is an increase in acidification of the cytoplasm, since at higher pressures, CO2 is absorbed more easily.
That’s why deep sea archaeans and bacteria have specific solutions – slight differences in biochemistry that make all the difference. The adaptations to pressure are so ingrained in many of these organisms that they will not even develop under regular atmospheric pressure (making it hard to study them in the lab, since we can’t set up a nice colony of them in an aquarium).
That said, when considering animals, pressure does not seem to affect their morphology too much and does not act as a particular selection factor – despite the fact that shallow water fish cannot tolerate deep sea pressures – but this goes both ways, and many deep sea species (except those that rise to the surface at night) cannot tolerate shallow water pressures, simply because their biochemistry gets screwed up in the lower pressures. The main visible differences come in muscle development, which is adversely affected by high pressures (and is not helped by the low food levels of the deep sea).
Another thing that is important, especially for, larvae is the temperature. Since it has such a large effect on metabolism, it can slow down development, which is both a blessing and a curse. It’s good because the longer an animal is in the larval stage, the farther it can swim and disperse. On the other hand, larvae are defenceless, sensitive and not so good at surviving.
Animals living near hydrothermal vents (like Bathymodiolus, above) have one completely different problem to deal with: the extreme temperature changes (they have been measured at 5°C/cm/minute) – keeping in mind, of course, that this water is also highly polluted. Staying with animals, it is known that alvinellid worms can colonise the seafloor when it is at 80°C. Some bacteria and prokaryotes can certainly live in higher tempratures, but I will not consider them. But besides exceptional species, animals would prefer not getting cooked.
And indeed, animals will actively avoid swimming in the hotter waters and actively seek out the colder currents, no matter what their maximum heat tolerance is. In fact, a parallel can be drawn with animals living in desert regions, who also have the ability to survive in hotter temperatures, but try to escape from them as fast as possible. But this only applies for mobile species. Sessile animals can’t move, and this brings back the point I mentioned in the previous section about microhabitats: this is an example where selecting the proper microhabitat provides excellent protection.
Another problem facing organisms initially colonising this ecosystem is symbiosis: all the animals here live somehow symbiotically with chemosynthetic bacteria. Associated with this is achieving a tolerance to hydrogen sulphide. Research on mussels (like Bathymodiolus above) suggests an interesting theory: their ancestors may have gone through several transitions, from shallow water, to specialising on floating wood, to whale falls and finally to the hydrothermal vent. It may sound strange, but there are some similarities between whale falls and vents that make this hypothesis likely, as can be seen in the diagram above.
Hydrothermal vents are environments rich in reduced chemicals (sulphides, methane), which bacteria can survive on alone. But animals need oxygen, and that’s present in the water around the vents. So no matter how tightly-bound the symbiosis is, if there is a sudden period of anoxia, the animals will not survive.
These symbioses are found everywhere in the ocean, but are only dominant in vents, since in regular waters photoautotrophy (i.e. photosynthesis) and regular eating are enough to get energy. This is why at whale falls, the dominant organisms are regular meat and sediment eaters, although these symbiotic organisms are also found due to the sulphidic chemicals that also come along with a carcass. Of course, keep in mind that there can be multiple symbioses established within one animal, so it is possible for animals to adapt to more than one feeding environment.
The type of symbiosis varies wildly depending on the host species. Shrimps and nematodes have epibionts, meaning that the bacteria colonise the whole outside of the body (as in nematodes) or just specific parts (feeding appendages and gills in shrimp). Mussels (like Bathymoodiolus) keep their endosymbionts inside the body with their own cells. I mentioned the Riftia oligochaetes with their trophosome in the previous section – they are not the only organisms who have such organs. Another quirky adaptation is in Osedax, a siboglinid worm found standing up straight on whale bones, which is what it specialises on feeding. It actually has ‘roots’ dug down into the bone, with the bacteria housed in them (similar to leguminous plants, come to think of it).
The animals are also clever enough to know that they need to feed their inhabitants. For Osedax, this is no problem. But those animals with trophosomes will go out of their way to make sure the bacteria get their share of sulfides. Mussels will bury themselves in the sulfide-rich sediments to satisfy the bacteria, while keeping their siphon up in the oxygenated water. Other clams build entire Y-shaped burrows that allow them to access the oxygen easily while remaining in the sediment.
This relation to the environment and the habitat is very important, as I’ve stressed multiple times. Let’s look at another example, staying with hydrothermal vents and symbiosis. The picture above shows a community of Rimicaris shrimps on the chimney of a vent, where the hydrothermal fluids mix with the sea water (specifically, this is at the Mid-Atlantic ridge, where the Atlantic Ocean is spreading). It is a relatively warm place, since they position themselves right where the water comes out, at a temperature range between 3 and 18°C.
It’s also a chemical-laden position, with sulphides, methane and various heavy metals (cadmium, lead, copper, zinc) highly concentrated in the water. It’s toxic for any unadapted animal: a few micromolars of hydrogen sulphide is enough to kill a fish, for example. So how do these shrimp tolerate these conditions?
The answer is they don’t really have to. Look again at the diagram showing the symbiosis diagram above, specifically at the shrimp. The symbionts live in the gills of the shrimp, meaning that the water gets filtered and detoxified before entering the animal – not completely, but enough to not cause the shrimp to break down. Not only that, these bacteria also provide the shrimp with its food by breaking down sulphides and methane into organic carbon.
But those bacteria only filter sulphides and methane. What about the heavy metals? Rimicaris also has whole microbial communities covering its legs and its underside, which form real microbial mats. They basically absorb the bulk of the heavy metals.
So as you can see, cooperation is just as important as predation in this environment. These shrimp have only managed to successfully colonise this hazardous habitat because of their bacterial symbionts, not because of any adaptations on its part.
However, there are some organisms in hydrothermal vents that have developed their own particular morphologies. Take the scaly snail above, which has a foot covered with scaled made of iron sulphides. They are also very heavily dependant on their endosymbionts (their digestive system, from radula to digestive tract, are reduced), but the scales are also important: they support a large community of epibionts that provide more food for the snail, so it builds them (they are organised, not just layers of bacterial wastes).
One thing that must be remembered is that there is very little to no oxygen in hydrothermal vents, and one other adaptation is that these organisms have abnormally large concentrations of haemoglobin, hemocyanin or any other respiratory pigments to allow them to capture as much O2 as possible.
As for the bacteria themselves, they are not really related to each other, having evolved independently multiple times. However, the ones researched so far all seem to have descended from various shallow-water anoxygenic sulphur oxidisers, so it’s relatively easy to imagine the transition to the deep sea.
A myth that is associated with hydrothermal vents is that they represent ancient communities – this is the same kind of thought that was once upon a time common about the deep sea. This is simply not true, and it can be proven with the fossil record since hydrothermal vent fossils are found for many time ranges. And the result is very clear: there are big differences and completely different species, genera and families populating modern hydrothermal vents. In fact, many of the modern hydrothermal vent faunas have no fossil record (and this is not an artefact of fossilisation, since similar counterparts are preserved).