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.The R-code to run all the analyses of the study (using the raw data in the tables S1-S4) is provided. A .tree file corresponding to the phylogenetic tree of the 29 species of Pomacentridae investigated is also provided as necessary to run the phylogenetic-corrected analyses.Raw data: The dataset contains four tables with the raw data of the study (excel file tables S1-S4). I) The table S1 contains the mouth closing force and speed in various species of Pomacentridae. The force and velocity have been measured thanks to a dynamic biomechanical model. For more details about how the model works see: Van Wassenbergh, S., P. Aerts, D. Adriaens, and A. Herrel. 2005. A dynamic model of mouth closing movements in clariid catfishes: the role of enlarged jaw adductors. Journal of Theoretical Biology 234: 49-65. Doi: 10.1016/j.jtbi.2004.11.007. Different groups were compared, the "Group 1" variable opposes the grazing to the non-grazing species, and the "Group 2" variable opposes the species with and without the cerato-mandibular ligament. To calculate the mouth closing force and speed with the biomechanical model, sixteen variables were measured by dissection on the specimens. See the study abovecited for more details about each variable. II) The table S2 contains the mouth closing speed measured in vivo in various species of Pomacentridae thanks to a high-speed camera (500 to 1000 fps). III) The table S3 contains the mouth closing speed and duration in various species of actinopterygians. These data were collected from the literature, the references are indicated below the table. For each species, the proportions of nekton and hard item preys in their diet habit are indicated. These latter data were collected from Fishbase. IV) The table S4 contains the closing mechanical advantage (MA closing) in various species of actinopterygians. These data were collected from the literature, the references are indicated below the table. For each species, the proportions of nekton and hard item preys in their diet habit are indicated. These latter data were collected from Fishbase. Supplemental tables: Two supplemental tables are also provided (word file tables S5-S6) and give additional information to the table 1 and 2 published in the study in The American Naturalist