An oyster for an amplifier

The turquoise waters of the coral reefs are packed with species that still harbour many secrets. This is the case of Onuxodon, small fishes that live inside the shells of pearl oysters. An unusual and discreet shelter that makes any behavioural studies rather difficult. And yet, recent research conducted at the University of Liège has established that they emit sounds from dusk till dawn. A nocturnal activity that complicates observations, but has led scientists to assume that this is a call for a mate during reproduction cycles. One convenient yet surprising particularity seems to be the role of the amplifier, played by the oyster shells.

There’s no need to dive into the oceans’ murky depths to reveal the mysteries of the underwater world. Take Eric Parmentier and Loïc Kéver, from the Functional and Evolutionary Morphology Laboratory at the University of Liège, for instance; they stopped at the coral reefs of French Polynesia. These tropical waters are shared by a good many species, with some of the shyer ones remaining very discreet. This is the case of Onuxodon which belong to a group of fish more commonly known as pearlfish. "They were given this name because certain remains of dead fish were found on the oyster shell valves, completely surrounded by mother-of-pearl", Eric Parmentier tells us. "But not all species from this group live in oysters. Other species from the Carapidae family are also capable of penetrating and living inside echinoderm hosts such as sea cucumbers or starfish. Other ones have a free lifestyle and don’t depend on a host."

Besides this particular behaviour, we know that certain species of Carapidae leave their refuge at night to feed, while others display parasitic behaviour and eat their host’s genitals. In the case of Onuxodon, and many others, what they eat remains a mystery. They seem capable of eating small worms (annelids) and small crustaceans. If the prey is found inside the oyster, the behaviour would be of mutual benefit (the fish cleans the host, the bivalve protects the fish). However, we can’t exclude the possibility that the fish feeds off the host’s tissues, thus making it a parasite. Or, if the fish hunts its prey outside the host, this can be seen as commensalism (the oyster protects the fish but doesn't get anything in return). A study in progress should provide more information, by comparing the carbon and nitrogen isotopes of the fishes and the oysters. However, in this particular study, the two scientists focused on another characteristic of this delicate fish: its ability to produce sound.    

Extensive underwater research

Eric Parmentier had the chance to study the morphology of Onuxodon and conclude that these fish must be capable of producing sounds. This idea was further reinforced by the recording of species found in sea cucumbers. In addition to several missions dedicated to other research in French Polynesia, he went looking for these fish in their natural environment, only to return empty-handed for several years. "One day", Loïc Kéver remembers, "the head of diving at a centre Eric Parmentier knew well, left on a mission in the atolls of the Tuamotu Archipelago.  During a dive in the Makemo atoll, he collected several pearl oysters. When they were opened, he discovered Onuxodon and sent them to us. We studied and identified them, and we went on a mission in November and December 2011."

The first oysters collected weren’t inhabited. The scientists turned their research to passes, places where the ocean’s waters communicate with those of the lagoon. The fish return here to set up home when they reach adulthood. "That’s where we found them. Approximately 30% of oysters were infested. We collected them so we could put them in an aquarium. But the change of pressure was too accelerated and too great for the Onuxodon. They were all dead by the time we reached the surface. We had to find a gentler way of bringing them up." The oysters and their discreet landlords could finally be placed in an aquarium.

The hypothesis of a reproductive function

Waterproof microphones, known as hydrophones, were placed in the aquariums at the same time as the cameras. But no sounds were recorded in the first few days. "We attempted several manipulations, for instance, encouraging several fish to go into the same oyster, to observe their reactions." But to no avail. The Onuxodon remained silent. Up until the day when the researchers left the microphone on at nightfall. "That’s when we detected the sounds. There were even a lot of them, at certain moments. The fact that these sounds were emitted at dusk is probably related to a reproductive function or, in any case, a call to attract a mate that was outside the oyster." When sound production has this function in fish, it is not unusual for it to occur predominantly at night. Because according to the reproductive cycle, if mating takes place in the early hours, so will the egg-laying. Thus, the eggs will reach the open sea when it is dark. They will be protected from the danger of predators who use sight to hunt. This hypothesis concerning reproduction is all the more likely since several species close to Onuxodon, which are already better known, produce sounds for this purpose.

A morphology tailored to produce sound

The biological mechanism at the origin of this sound producion is quite original and bears witness to the ability of tissue to adapt when subject to certain constraints. In Onuxodon, the front of the swimbladder has been "transformed" into a mineralised structure (rocker bone). It sits at the front of this bladder a bit like a cork on a bottle of champagne. A pair of muscles link the eye’s upper orbit to the rocker bone. The contraction of the sonic muscles pull the rocker bone forwards. When the muscle relaxes, the bony part quickly draws back into the swimbladder initiating  a sound.

Nocturnal activity and its limits for the observer

While nearly all the sounds recorded were emitted at night, leading the researchers to believe that their function relates to the reproduction cycle, the specific time at which the sound is produced presents a major inconvenience. "We have no idea whatsoever what happens when they produce these sounds", the young researcher regrets. "We can’t define any associated behaviour since we can’t observe them. We were able to catch the emission of a sound during the day, from the inside of an oyster.  However, we don’t know whether they also produce sounds in open water, for instance." Another grey area is linked to a subsequent discovery concerning the morphology of these fish. The morphology of the rocker bone varies according to gender. It is smaller in females, has a different shape, and the sonic muscle isn't attached to the same points of the bony structure as in males. "The differences are very subtle but lead us to believe that the mechanism doesn’t function in exactly the same way. And yet, we didn’t record a variety of different sounds. We did notice variations in the pulses, but it was always the same type of sound". Observations that lead to two hypotheses. Either the morphological differences between the two sexes don’t have any particular effect on the characteristics of the sounds emitted, or only one of the two genders emitted sounds during the recording. In which case, the researchers will have to conduct further missions to collect other types of sounds.

"Now we have to carry out further investigations concerning behaviour and sound production. But to achieve this, we have to be able to observe them." The operation may appear simple. Just put infrared cameras in position at night time, and there you have it! An easy enough system to set up in a laboratory, but far more difficult to do on an isolated atoll in the middle of the Pacific Ocean. And bringing back live fish isn’t any easier either. Only eight centimetres long and no more than one centimetre wide, Onuoxodon is far from being the most robust underwater species. It would be rather complicated to inflict such a long journey on so a fragile fish.

From the limits of the aquarium to widespread propagation in the lagoon 

The studies carried out in an aquarium did have certain advantages. In particular, it allowed the researchers to attribute the sounds emitted to the species studied without a doubt. But, above all, they demonstrated their limits. They don’t reflect the true conditions of the fishes’ environment, or the way they evolve in it. "And the aquarium poses real problems concerning resonance, since there is a constant and distorted background noise", Loïc Kéver points out. "This is what encouraged Eric Parmentier to return to Makemo the year after our mission, and subsequently make a recording in the lagoon".

In particular, the operation allowed the researchers to confirm that Onuxodon emitted sounds from dusk till dawn, but not only then. The biologists also observed that the peaks recorded were followed by a second set of weaker, yet similar, peaks. By taking into account the depth at which the oysters were to be found (some twenty metres), and the speed of the sound’s propagation in the water, i.e. 1500 metres per second, they were able to deduce that the amount of time between the two recorded peaks was the time it took for the sound to reach the surface from the place where it was emitted, and return back again. "The first sound recorded therefore came directly from the fish. But the sound spreads in all directions. It doesn’t just go towards the hydrophone. When it reaches the surface, the majority of it is reflected, a bit like light off a mirror, then returns in the other direction, and is then recorded a second time. What was surprising, for so small a fish, was that the sound emitted was sufficiently powerful to cover such a distance, i.e., some forty metres."

Oyster shells acting as amplifiers   

The most plausible hypothesis to explain this power of diffusion is also the most amusing.  The oysters may not only be a source of shelter; they may also serve as an amplifier, thus amplifying the sounds emitted by Onuxodon, and therefore increasing their chances of being heard by their fellow pearlfish. "It’s a tentative idea", Loïc Kéver adds carefully. "Because, once again, we don’t know if they only emit sound from inside the oyster or also outside their host. We also don’t know if they use the bivalves as amplifiers, and if this behaviour has a decisive role in terms of calling or reproducing. In any case, we sent shells to Marco Lugli, an Italian researcher and co-author of the publication. He kept the shells in a half-open position which is close to the natural position. He placed a diffuser in them that emitted a white noise, whereby all the frequencies are at the same intensity, and a microphone. He noticed that the sound emitted was amplified by the oysters, particularly regarding the frequencies close to those that we found mainly in the sounds collected in Onuxudon."

 
These are encouraging initial results, that nevertheless require more in-depth research. The oyster can indeed amplify the sound emitted by Onuxodon. But is this particularity useful to these fish, or is it superfluous, calculated, or are they unaware of it? Another question whose answer shall depend on more in-depth behavioural studies. Even if the fact that the oyster shells can facilitate the propagation of sound in an environment as noisy as the coral reefs appears to be particularly useful. This ingenious discovery, whether accidental or not, has helped this branch of species to evolve. However, these initial experiments on oysters were carried out in an aquarium. And the propagation of sound is still a tricky phenomenon to understand and study, since it varies greatly depending on the environment. Nothing allows the researchers to confirm that these properties are just as efficient in the depths of the lagoons. Thanks to the studies in the aquarium, it was possible to elaborate plausible and appealing hypotheses. Nevertheless, the nocturnal activity of these fish and the time they spend hidden in their oysters make it difficult to study them and requires new experiments to be carried out in the field.

(1) Loïc Kéver, Orphal Colleye, Marco Lugli, David Lecchini, Franck Lerouvreur, Anthony Herrel, Eric Parmentier, Sound production in Onuxodon fowleri (Carapidae) and its amplification by the host shell, The Company of Biologists, 2014