Feeding of the megamouth shark (Pisces: Lamniformes: Megachasmidae) predicted by its hyoid arch: A biomechanical approach

Abstract

Studies of the megamouth shark, one of three planktivorous sharks, can provide information about their evolutionary history. Megamouth shark feeding has never been observed in life animals, but two alternative hypotheses on biomechanics suggest either feeding, i.e., ram feeding or suction feeding. In this study, the second moment of area of the ceratohyal cartilages, which is an indicator of the flexural stiffness of the cartilages, is calculated for 21 species of ram- and suction-feeding sharks using computed tomography. The results indicate that suction-feeding sharks have ceratohyal cartilages with a larger second moment of area than ram-feeding sharks. The result also indicates that the ram-suction index, which is an indicator of relative contribution of ram and suction behavior, is also correlated with the second moment of area of the ceratohyal. Considering that large bending stresses are expected to be applied to the ceratohyal cartilage during suction, the larger second moment of area of the ceratohyal of suction-feeding sharks can be interpreted as an adaptation for suction feeding. Based on the small second moment of area of the ceratohyal cartilage of the megamouth shark, the feeding mode of the megamouth shark is considered to be ram feeding, similar to the planktivorous basking shark. From these results, an evolutionary scenario of feeding mechanics of three species of planktivorous sharks can be suggested. In this scenario, the planktivorous whale shark evolved ram feeding from a benthic suction-feeding ancestor. Ram feeding in the planktivorous megamouth shark and the basking shark evolved from ram feeding swimming-type ancestors and that both developed their unique filtering system to capture small-sized prey.

Cartilage of Marine Vertebrates

“…It was hypothesized that stronger suction feeders are expected to have stronger contraction forces of the coracohyoideus coupling because they generate larger negative pressures. It was confi rmed (Tomita et al 2011 ) that "the stiffness of the ceratohyal cartilage is positively correlated with suction feeding".…”

“…Usually, this type of cartilage supports the "tongue" and is made by a pair of rod-shaped cartilages. It articulates with the hyomandibular cartilage at its proximal end, and with the basihyal cartilage at its distal end (Tomita et al 2011 ). As observed by Tomita and co-workers, "the ceratohyal cartilages rotate around the hyomandibuloceratohyal articulations ventrally just after opening the mouth during prey capture.…”

“…Their function is described in following way: "by shortening the coracohyoideus coupling, the basihyal cartilage is pulled posteriorly and the hyoid arch rotates ventrally, expanding the oral cavity. At this time, negative pressure is generated in the oral cavity, and suction-feeding sharks use this negative pressure to suck in the prey into front of its mouth" (Tomita et al 2011 ). It was reported by (Motta et al 2008 ) that contraction forces of the coracohyoideus coupling are able to generate the negative pressure in the oral cavity in the nurse shark Ginglymostoma cirratum up to 2,100 kPa.…”

“…Nurse sharks and bamboo sharks ( Chiloscyllium plagiosum ) can generate among the greatest recorded subambient suction pressures when feeding (Motta et al 2008 ;Wilga and Sanford 2008 ). The feeding behaviour of the cookie-cutter shark ( Isistius brasiliensis ) is described as follow: this predator "remove a plug of fl esh from the body of a cetaceans or some large fi sh with strong suction pressure after cutting the fl esh using its razor-shaped lower teeth," (Tomita et al 2011 ; see for more information Shirai and Nakaya 1992 ). The zebra shark ( Stegostoma fasciatum ) and the nurse shark ( G. cirratum ) are known suction capture small bony fi shes as well as suck out the soft parts of molluscs like moon shells or trumpet shells from their hard mineralized encasements.…”

“…The zebra shark ( Stegostoma fasciatum ) and the nurse shark ( G. cirratum ) are known suction capture small bony fi shes as well as suck out the soft parts of molluscs like moon shells or trumpet shells from their hard mineralized encasements. It was reported about large amounts of moon shell opercula that have been found in the gastric contents of S. fasciatum (Tomita et al 2011 ).…”