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Reflexions, le site de vulgarisation de l'Université de Liège Fish that have discovered electricity 10/23/14 Several species of catfish (Mochokidae) are capable of producing sounds and electricity, probably for communication. This has just been observed by researchers at the University of Liege. Having studied five species of these fish, the researchers have established that a single muscle which has evolved in different ways is specialized in both properties. Between two extreme cases, one where the fish produce sound and no electricity or vice versa, an intermediate group of species have kept both means of communication. This is an important study which aims to understand how certain fish have been able to discover electricity during the course of evolution. It is public knowledge today that many fish emit sounds for communication purposes, defending their territories or as part of the mating ritual. They have also developed an efficient auditory system for communication. But sometimes, this function is not sufficient and can be rendered useless by the environment. Some species have developed other means of communication and have evolved in such a way that they can emit electric signals by means of electrocytes. Everyone has heard of electric eels, for example, but these are not the only creatures to have played at being the Benjamin Franklin of the aquatic environment. Indeed, many species have yet to reveal their secrets with regard to this subject. Among them are certain catfish such as Synodontis. Eric Parmentier, lecturer and head of the Functional Morphology and Evolutive Morphology Unit at the University of Liege, requested Kelly Boyle, who at the time was a post-doctoral researcher in his unit, to carry out a study of these species. The result is a fascinating work on the morphological evolution of electricity-producing fish (1). From sound to electricity "We have been working on the emission of sounds by fish for more than ten years", explains the researcher. "In the context of this study, we initially wanted to compare the production of sounds in certain species of Synodontis. They presented anatomical differences and we wanted to establish how these variations could interfere in the production of sounds. Something intrigued me about one of the species. It showed all the anatomical elements necessary for the production of sounds, and yet we heard no sounds at all while the other fish were a lot more communicative. At the same time, we had read in a publication dating from the 1990s that certain catfish produced electricity, but without any further details. We decided to place electrodes in the aquarium and everything became more interesting from that point on". Although the fish seemed more © Université de Liège - http://reflexions.ulg.ac.be/ - 16 June 2017 -1- Reflexions, le site de vulgarisation de l'Université de Liège disposed to producing sound, they actually emitted electrical discharges. Intrigued by the theory that certain catfish could possess both properties, Kelly Boyle observed a group of five species of Synodontis. One of them emitted no sound but did emit a lot of electrical discharges. In contrast with this, another species only emitted sounds. Three of the species were capable of both properties. This was evidence of a varied evolutionary group for species of the same genus. "Being able to emit electricity is a very singular property and here we had the opportunity to discover a biological pathway that showed how this was possible". One muscle for two functions Quite quickly, the young post-doctoral researcher noticed that the fish posessing both properties could not emit both of them at the same time. Either they produced a noise or they produced an electric signal but never simultaneously, as Eric Parmentier recalls. "We therefore imagined that the muscle which produced the sound could also be used for producing electricity and this proved to be the case. By blocking the activity of this muscle in some individuals, we noticed that they no longer emitted electricity". In Synodontis, the muscle responsible for the production of sound is the protractor muscle . This rapid muscle, which can contract and relax up to one hundred times a second is connected to a bony plate located at the front of the swim bladder. Just as in a balloon or a buoy, this bladder is an air-filled pocket whose function is to stabilize the fish in the water. When the muscle contracts the bladder stretches and when the musle relaxes the bladder returns to its initial shape. The rapid alternation between the cycles of contraction and relaxation produce the sounds... Not all fish produce sound in this way but it is the process that has been developed by the Synodontis studied here. In order to verify that the protractor muscle was also behind the electric discharges, and especially in order to understand the process, it was necessary to observe the ultrastructure of samples under the electron microscope. "A typical muscle is composed of cells that are mostly covered in myofibrils, which cause the contractions. The more myofibrils there are, the greater the strength of the muscle will be. We observed that in fish that produced only sound, the myofibrils took up less place than on a typical muscle but were present in greater proportion in the cell overall". On the other hand, the fish that is incapable of producing sound but can produce electricity had very few myofibrils. © Université de Liège - http://reflexions.ulg.ac.be/ - 16 June 2017 -2- Reflexions, le site de vulgarisation de l'Université de Liège It is therefore the protractor muscle that also produces electricity. "We also constantly produce electricity with for example each beat of our hearts", explains Eric Parmentier. We do so at a lower voltage; the electricity is produced by the transfer of ions between the cells. For example, it is because muscles create electricity that the hammer-headed shark is able to detect prey, even when they are immobile, hiding in the sand. Its large snout is packed with electrosensitive cells. And the fish that is hidden in the sea bed continues to produce electricity with the beating of its heart despite the fact that it is not moving. The shark can then locate it". © Université de Liège - http://reflexions.ulg.ac.be/ - 16 June 2017 -3- Reflexions, le site de vulgarisation de l'Université de Liège Several different evolutions within the same species The study is unique in that it shows that the same muscle equipped with different ultrastructures has been able to acquire different properties. "In other fish", explains Eric Parmentier, "such as eels or elephant-fish, we have known for a long time that electrocytes were myogenic (of muscular origin). However, these species have never revealed a similar evolutionary process to that of Synodontis, because they are all exclusively electric. There are no longer any intermediate stages existing within their groups". This new knowledge comletes other research, carried out on piranha fish in this instance (2). This study of specimens of different ages made it possible to establish that the muscles capable of producing sound were located in the back muscles. In the youngest specimens, the cells of the sound-producing muscles contain a large nucleus and few myofibrils which develop with age. At a point during growth of the muscles, the development of myofibrils is blocked and they specialize in the emission of sounds. "This observation only concerns piranhas", admits the researcher. "But it is possible to imagine that this property extends to other species and put forward the theory that, while they are growing, Sydontis develop a sound-emitting muscle. By blocking deeper this developmental process, they create a muscle capable of emitting electricity". This is only a theory, because such observations have not been carried out on catfish. It remains a plausible theory nonetheless. The electricity fairy, still full of mystery This raises the question as to why, during their evolution, certain species needed to develop an electric muscle. "Here too, we can only offer theories because we are not studying ethology. We are not trying to understand why they use such a property, but we are theorizing as to the evolutionary process. We cannot even attest that the production of electric discharges is the evolution of sound production, even though I think this is more plausible than the opposite because among catfish , other groupes of fish are capable of sound production. It is always easier to take a pre-existing structure and transform it in order to give it a new function than to create a new organ. Normal development of a muscle favors the production of myofibrils. In this case, a simple malfunction during growth would have blocked this production. This modification in development, probably coupled with others, would have led to the development of muscles capable of emitting electricity in a voluntary manner. Certain species are specialized in this way while others have kept the dual function of the protractor muscles. But in order to definitively attest that electricity is an evolution of sound in catfish, we need to carry out phylogenetic studies". In the case where electric discharges are the evolution of the ability to produce sounds, this would mean that the species experienced limitations in its attempts to communicate. "When fish live in muddy or turbulent waters like the rivers of Africa for example, the natural habitat of Synodontis, their visibility is strongly altered. They must therefore develop other senses if they want to locate each other for reproductive purposes or to detect their prey or predators. The production of sound is a first alternative. Yet we have noticed that the sounds emitted by the different species studied were relatively similar and could be easily confused (see illustration below). Since the environment is also noisy, the fish therefore have more difficulty finding each other". The lack of visibility and noise are therefore two factors which could have led Synodontis to use electricity. Synodontis emit different electric waves according to the species. They are therefore capable of recognizing each other better by means of elecricity than by sound. © Université de Liège - http://reflexions.ulg.ac.be/ - 16 June 2017 -4- Reflexions, le site de vulgarisation de l'Université de Liège The ambition of the researchers was to discover electricity emission in Synodontis and to understand its workings. The objectives were reached. But a great number of questions remain unanswered. Is it really an evolution of sound? Does electricity perform a simple function of communication or rather does it enable the fish to find its way like a radar? Are these fish devoid of electrosensitive cells on their skin which would allow them to receive these signals? Electricity in fish remains charged with mystery. "Its a mystery because it is a sense that we cannot understand", concludes Eric Parmentier. "Hearing and sight we can understand but not electricity. We can measure the emission of electricity in an aquarium with the help of electrodes, we can analyze the physical characteristics of these signals. But thereafter we have absolutely no idea what the animal uses this sense for. A lot more studies need to be conducted". (1) Kelly Boyle, Orphal Colleye, Eric Parmentier, Sound production to electric discharge : sonic muscle evolution in progress in Synodontis spp. catfishes (Mochokidae), Proceedings of the Royal Society, 2014. © Université de Liège - http://reflexions.ulg.ac.be/ - 16 June 2017 -5- Reflexions, le site de vulgarisation de l'Université de Liège (2) Millot S, Parmentier E (2014) Development of the ultrastructure of sonic muscles: a kind of neoteny? BMC Evolutionary Biology 14: 24 © Université de Liège - http://reflexions.ulg.ac.be/ - 16 June 2017 -6-