Unprecedented biting performance in herbivorous fish: how the complex biting system of Pomacentridae circumvents performance trade-offs

It is well accepted that the complexity of functional systems may mitigate performance trade-offs. However, data supporting this theory is hard to find because it needs to be based on a functional system with different complexity levels in closely-related species. The Pomacentridae (damselfishes) provide an excellent opportunity to test the hypothesis because most of the species have two mouth-closing systems: the first using the adductor mandibulae, as in all teleost fishes, and a second one relying on the cerato-mandibular ligament (cmd), a synapomorphic trait of the family. Interestingly, some pomacentrids have secondarily lost the cmd ligament during evolution and therefore have a less complex mouth-closing system. Using dissection, kinematic analysis, and mathematical modeling, we demonstrated that the possession of two mouth-closing systems enabled grazing damselfishes to have a forceful and extremely fast bite. This combination challenges a major functional trade-off in fish jaw dynamics, as systems better suited for force transmission are usually less suited for speed transmission, and vice versa. The combination of grazing behavior, small and robust lower jaws (conferring high biting force), and an ultra-fast bite is unusual within actinopterygians. These attributes and their associated performance seem to be required conditions to colonize the ecological niche of farming, i.e., the maintenance of small filamentous algae crops serving as both food and storage.