The cerato-mandibular ligament: a key functional trait for grazing in damselfishes (Pomacentridae)

Abstract

Introduction: The success of a taxonomic group can be promoted by a key character that allows the group to interact with its environment in a different way and to potentially occupy new niches. The Pomacentridae possess a synapomorphic trait, the cerato-mandibular (c-md) ligament, which joins the hyoid bar to the inner part of the lower jaw. It has previously been shown that this ligament is a key trait in communication in damselfishes because it enables them to slam the oral jaws shut causing teeth collision and sound production. This specific behavior of mouth closing could, however, also be used for other tasks, such as feeding. Many territorial damselfishes are referred to as farmers, due to their ability to manage algal crops on which they feed. This study hypothesizes that the c-md ligament provides an advantage for grazing filamentous algae, and should thus be considered a key trait for farming behavior. Results: The kinematic patterns associated with sound production and biting filamentous algae or attached animal prey are all based on the same mechanism and are associated with a slam of the oral jaws. We observed that transection of the c-md ligaments makes the fish unable to perform such actions. We also counted biting rates on filamentous algae in fish with and without the c-md ligament and observed a drop of more than 80% in the latter. Conclusion: This study shows that the c-md ligament is a key trait both for sound production and for grazing activities in damselfishes. The buccal jaw slam enables the fish to perform accurate strikes on small filamentous algae. This kind of bite probably plays a major role in farming activity and allows grazing damselfishes to occupy distinct niches, possibly increasing their competitive evolutionary success.

The evolution of jaw protrusion mechanics has been tightly coupled to bentho-pelagic divergence in damselfishes (Pomacentridae)

“…Exclusively morphological studies have shown that damselfish trophic evolution can be characterized as repeated adaptation to planktivory, omnivory and herbivory Frédérich et al, 2016Frédérich et al, , 2013Olivier et al, 2014) and this description is further supported by our combined analyses of both morphological and kinematic data (Table 4). Heavy feeding on detritus has evolved at least three times in herbivorous damselfishes (Stegastes nigricans, Hemiglyphidodon plagiometopon and Dischistodus perspicilliatus; Wilson and Bellwood, 1997) and the four-peak OU model, which included detritivory, had a fit to our data that was nearly as good as OU 3.2 (Table 4).…”

Multiple exaptations leading to fish sound production

“…Beside sound production, the function of the ceratomandibular ligament, a morphological novelty, provides a diversification in the feeding mechanism (Frédérich, Olivier, Litsios, Alfaro, & Parmentier, ; Olivier, Frédérich, Herrel, & Parmentier, ). In the filamentous algae grazer Cortez damselfish ( Stegastes rectifraenum Pomacentridae), the slam occurs during feeding and simultaneously produces sounds (Olivier et al ., ). The same morpho‐functional process occurs in the anemonefish A. clarkii .…”

“…Rapid mouth closure is forced by a synapomorphic ceratomandibular ligament (Stiassny, ) joining the lateral side of the hyoid bar to the medial side of the mandible. Experiments on anesthetized specimens show the jaw slam is caused by the stretched ligament and does not require adductor muscle contraction (Olivier, Frédérich, Spanopoulos‐Zarco, Balart, & Parmentier, ). Further, cutting the ceratomandibular ligaments prevents both feeding and sound production.…”

“…(i) Sounds can be made during feeding and are therefore a by‐product. (ii) In all studied species, a single jaw slam is related to fighting and produces a single pulse; fighting sounds usually occur before elevated aggressive behaviour with biting (Mann & Lobel, ; Olivier et al ., ; Parmentier, Kéver et al ., ). (iii) Biting occurs during foraging activities in Cortez damselfish (Olivier et al ., ).…”

Staging and normal table of postembryonic development of the clownfish (Amphiprion ocellaris)

“…For example, they independently evolved jaw protrusion ability, thus providing one case of this convergent feature, allowing the analyses of how different ontogenetic trajectories reach similar solutions . In addition, they possess peculiar anatomical traits to graze filamentous algae and to produce sounds during numerous social interactions . The clownfish also provide a unique model for the evolution of pigment pattern that allows the study of how ecology and development can permit and constrain the diversification of complex patterns .…”