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By slamming their oral jaws shut, damselfishes produce noise and use it to defend their territory or to attract partners during courtship displays. For most of these species, the mechanics of this action are linked to the cerato-mandibular ligament. Located in the mouth, it enables the jaws to slam shut rapidly thereby producing sound. This ligament does not only have an acoustic function. It enables the fish to select algae with surgical precision and to feed on the cultivated algae. Some species have therefore been able to adopt “farming” behavior and occupy a unique position in coral ecosystems and reefs throughout the world. This morphological particularity is therefore directly behind this ecological behavior that is unique in fishes. Two studies conducted at the Functional and Evolutionary Morphology Laboratory of the University of Liege have just revealed how a morphological trait was able to shape the evolution of damselfishes.
During dives along coral reefs, an attentive eye can observe small parcels of algae that are around one meter squared in size. These are small carefully arranged fields that look like well-manicured lawns. As soon as the diver approaches, the damselfishes try to hunt him away by slamming their jaws shut in a very deliberate way. These “farmer” fish are the owners of such parcels and spend many hours tending to their food store. They remove algae that are not to their liking and cultivate those they prefer. No intruders are tolerated and their tiny size in comparison with the divers does not seem to dampen their protective ardor. Even though this behavior has been known for a long time in damselfish, it is still not understood why they are capable of it (Read the article : The evolution of damselfishes).
The sound produced which in this instance is an actual defense reflex, is emitted by means of a slamming of the jaws and is perfectly audible to humans. It is produced by means of the cerato-mandibular ligament which links hyoid bar to the mandibles, and which enables the jaws to very quickly. One of the aims was to know whether this same slamming of the jaws was produced during the trimming of algae. The other was to understand whether this ligament completely or partly influenced the diversification of damselfishes during their evolution. In order to do this, two studies were jointly conducted; one was morpho-functional and behavioral studying a “farmer” species of damselfishes(1), and the other using phylogeny and comparing morphology of 124 species (2). Among these, it was noticed that some do not have this ligament and have adopted a diet consisting mainly of zooplankton.
The presence of this ligament in damselfishes has been known since 1981. But at that time, nobody really knew what it was used for. In 2007, Eric Parmentier, a researcher at the Functional Evolutionary Morphology Laboratory of the University of Liege, discovered its function in the production of clownfish (these belong to the family of damselfishes) and had an intuition that this slamming noise was initially the result of a mechanism at work during feeding. Following these observations, Damien Olivier, a PhD student in the same laboratory, supervised by Bruno Frédérich, a postdoctoral researcher at the F.R.S.-FNRS, extended the research to the entire family of damselfishes (Pomacentridae). He attempted to understand how the biomechanics of this oral ligament could influence their feeding, their diet and therefore their ecological role within coral reefs.
A first article summarizes part of the thesis of Damien Olivier. In this study, the young researcher focusses on a damselfish species, Stegastes rectifraenum. A “farmer” fish that rarely wanders far from reef substrate and which ardently defends its ‘plot’ of algae. “It was an ideal candidate because I wanted to understand to what extent the presence of this cerato-mandibular ligament influenced the feeding habits of the damselfishes”. |
For this purpose, he went to Mexico where he captured several specimens and also took pieces of rock with algae, their favorite food. He placed them in an aquarium, recreated their environment and filmed them by using a high-speed camera (up to 1000 images per second). For the first time, a researcher analysed in detail the movement of the damselfishes’ head when it was eating or defending its territory. The movement is identical in both cases. The ligament allows the fish to quickly close the mouth in order to capture filamentous algae without doing much damage to the substrate that supports the crop of algae.
“It is a high-precision work”, explains the young doctoral researcher. “Some of these algae are very small, around one millimeter in size. The fish must therefore act with precision in order to avoid ingesting undesirable elements or damaging the cultivations”.
During a second phase, without damaging the specimens, he cut the cerato-mandibular ligament and put them back in the aquarium. “They were then incapable of carrying out the observed movement. It was therefore a mechanism that was determined by the presence of the ligament. They no longer emitted any noise and did not compensate with the adductor mandibulae muscles which are normally used by other fish to close the mouth. But the most astonishing thing was that they no longer ate any algae either. They did not even try. It was as though they knew they would be unable to grasp it. However, they were volunteers and they were hungry. When I placed other types of food that can be found in the water column, like zooplankton, they ate what I gave them without hesitation. This was where the link between the presence of the ligament and the handling of algae was observed. I had suspected that it was an important factor but I didn’t expect it to be indispensable to this extent”.
While all damselfishes studied to date produced sound, not all of them have the ligament in question. This was an evolutionary particularity which the two biologists were not expecting and which they did not observe by chance, as a prelude to the research for the thesis of the young doctoral student. “For his thesis work”, explains Bruno Frédérich, “Damien firstly dived in the Mediterranean Sea to capture specimens of Chromis chromis. It is one of the species of damselfish that doesn’t live in a coral environment. While dissecting them, he did not observe this famous cerato-mandibular ligament. At the outset, we thought that it was a handling error and then we had to recognize that this species was lacking the ligament”. While the PhD student was beginning his thesis, Bruno Frédérich was in the United States in order to gather as much data as possible on the jaws of a maximum of damselfish species. It was a real godsend. Damien Olivier’s observation brought a new dimension to the two research programs conducted simultaneously. If the ligament was necessary in order for the fish to feed, why did some of these fish lose that trait during the course of their evolution? Bruno Frédérich scoured museums, laboratories and aquariums. Each time he dissected a fish, he noted the presence or absence of this ligament. For the 124 species studied, 19 did not have the ligament.
“We therefore began the phylogenetic studies and tried to find out if the common ancestor of these 124 species was lacking the ligament. During their evolution, at three different times at least, some lineages lost the ligament. What is remarkable is that they continue to produce noise but they do so with the cheek muscles”, says Bruno Frédérich.
The researchers underline that the loss of this ligament is not linked to a change of life with regard to the proximity of the reef area. Some species which do not have the ligament do not wander far from the reef, like most damselfishes. “And even so, when we are talking about species that live in the water column, they remain quite close to the reefs, do not wander more than a few meters from it and only develop in shallow water. At night, they return to sleep among the coral reefs or rocky anfractuosities. The morphological evolution is therefore not linked to a change of habitat but to a dietary specialization”, continues Damien Olivier. Usually, damselfishes are quite opportunistic when it comes to eating as the observations of the young researcher have shown in the context of his thesis. According to the species, they have developed three different types of diet. The first consists of algae attached to the substrate, a second, consists of zooplankton in the water column, and a third which groups together a series of intermediate species. “What we noticed, however, was that all the species lacking the ligament are exclusively zooplanktivorous. Among the species with the ligament, the three types of diet were observed. During the course of evolution, some lineages went from being zooplanktivorous to algivorous and vice versa. Once they lost the ligament however, they no longer ate algae. It seems that there was no going back after the loss of the ligament”.
So how did the ligament disappear during evolution? The question remains without a definitive answer even though the logic of the mechanics of evolution makes it possible to put forward plausible theories. “Just because a fish began to feed itself exclusively with zooplankton does not cause the loss of the ligament during the evolution”, Damien Olivier interjects. “There is no causality of this type. On the other hand, what is possible is that at a given time and due to genetic mutation, a fish was born without this ligament and survived by continuing to catch zooplankton, and that it transferred its genes during reproduction thus introducing a new phenotype without the ligament. By adopting a new morphology during the course of evolution, this made them better hunters of zooplankton, the species without the ligament would have been able to perpetuate their line and diversify. This is one theory which we are attempting to verify by means of a new study” Bruno Frédérich continues, “Or there may have been a sexual selection made linked to sound. Perhaps certain females were more attracted by another acoustic sound linked to the absence of the ligament that the species reproduced more often and this phenotype was able to perpetuate”.
The discovery of the ligament and its role in the feeding habits of damselfish makes it possible to identify its presence as a veritable functional adaptation. It was a key innovation which enabled damselfishes to forge a place in the coral reefs by adopting this ‘farming’ behavior. Within fifty million years, the damselfishes successfully radiated in the modern coral reef ecosystems. This success can be partly explained by this morphological trait.
Bruno Frédérich and Damien Olivier also demonstrate that this ligament acts as a constraint to a morphological evolution of the jaws and prevents, for example, an adaptation for maximizing the capture of zooplankton. “It is important to note that the zooplanktivorous species have several strategies for capturing prey. One of these consists of creating a protrusion of the mouth. The upper jaw can slide forward. The mouth then forms an actual tube which enables the fish to capture its prey without approaching its body which would otherwise create disturbances in the water alerting the prey which could then escape. We have observed that those damselfishes which have lost the cerato-mandibular ligament have morphological adaptations for capturing zooplankton. In other words, the disappearance of the ligament has made hyperspecialization possible for zooplanktivory, explains Bruno Frédérich.
How did they draw this conclusion? In this publication, the authors have divided the 124 species into two groups according to the presence or non-presence of the cerato-mandibular ligament. By means of methods of evolutionary modelling in molecular biology coupled with fossil data, they were able to trace their phylogeny (see evolutionary tree above). Once this time-tree was completed they were able to test a whole series of theories. “We wanted to verify whether the disappearance of the ligament modified the rate of evolution of the groups studied. In the first instance, we looked at whether the ligament influenced the speed of speciation and therefore the multiplication of species. But there was no evolutionary burst, an explosion of species within the different lineages which lost their ligament. This would have been plausible”. On the other hand, while carefully looking at the rate of morphological diversification for the body and the two mouth pieces: the upper jaw (premaxilla) and the mandible, they observed an important difference. The morphology of the species without the ligament evolved very rapidly, that is to say up to three times faster than the basic morphological variation of the other species, to optimize zooplankton hunting. This discussion is based on ecomorphological theory but the researchers will tend to demonstrate their hypotheses in a future publication.
The articles of Bruno Frédérich and Damien Olivier have two different approaches. One deals with comparative methods in morphology and phylogeny and embraces a large number of species whereas the other studies the behavior and functional morphology of only one species. Finally, both have the same objective; that of understanding the diversification within the same family of fish, observing the causes and consequences of the appearance of certain phenotypes and analyzing the way the morphology of fish has been a determining factor for their evolutionary success.
(1) Damien Olivier, Bruno Frédérich, Milton Spanopoulos-Zarco, Eduardo F Balart and Eric Parmentier (2014) The cerato-mandibular ligament: a key functional trait for grazing in damselfishes (Pomacentridae). Frontiers in Zoology, 11: 63.
(2) B. Frédérich, D. Olivier, G. Litsios, M.E. Alfaro and E. Parmentier. 2014. Trait decoupling promotes evolutionary diversification of the trophic and acoustic system of damselfishes
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