Functional morphology and kinematics of terrestrial feeding in the largescale foureyes (Anableps anableps)

Abstract

A major challenge for aquatic vertebrates that invade land is feeding in the terrestrial realm. The capacity of the gape to become parallel with the ground has been shown to be a key factor to allow fishes to feed on prey lying on a terrestrial surface. To do so, two strategies have been identified that involve a nose-down tilting of the head: (1) by pivoting on the pectoral fins as observed in mudskippers, and (2) curling of the anterior part of the body supported by a long and flexible eel-like body as shown in eel-catfish. Although Anableps anableps successfully feeds on land, it does not possess an eel-like body or pectoral fins to support or lift the anterior part of the body. We identified the mechanism of terrestrial prey capture in A. anableps by studying kinematics and functional morphology of the cranial structures, using high-speed video and graphical 3D reconstructions from computed tomography scans. In contrast to the previously described mechanisms, A. anableps relies solely on upper and lower jaw movement for re-orientation of the gape towards the ground. The premaxilla is protruded anteroventrally, and the lower jaw is depressed to a right angle with the substrate. Both the lower and upper jaws are selectively positioned onto the prey. Anableps anableps thereby uses the jaw protrusion mechanism previously described for other cyprinodontiforms to allow a continued protrusion of the premaxilla even while closing the jaws. Several structural adaptations appear to allow more controlled movements and increased amplitude of anterior and ventral protrusion of the upper jaw compared with other cyprinodontiforms.

Dining dichotomy: aquatic and terrestrial prey capture behavior in the Himalayan newtTylototriton verrucosus

“…The sample size used in this study is comparable with previously published work on feeding kinematics in vertebrates (e.g. Deban, 1997; Deban and Richardson, 2011; Heiss et al, 2013a; Konow et al, 2013; Michel et al, 2015a; Van Wassenbergh, 2013) and therefore deemed appropriate for our approach.…”

“…In fact, there are only a few vertebrates that can handle the challenges associated with a switch between media to capture prey in both environments (e.g. Deban and Marks, 2002; Heiss et al, 2013a, 2015; Lauder and Shaffer, 1988; Michel et al, 2015a,b; Natchev et al, 2010, 2015; Reilly, 1996; Stayton, 2011; Van Wassenbergh, 2013; Van Wassenbergh et al, 2006). When animals feed in both environments they can use the same set of movements, however they will perform suboptimally in at least one of the two environments; alternatively they can alter their feeding behavior to increase efficiency (Bramble, 1973; Stayton, 2011).…”

Terrestrial capture of prey by the reedfish, a model species for stem tetrapods

“…The length of the head relative to the body (i.e., head length divided by total length) was measured on preserved specimens for E. calabaricus (N = 6) and for the other terrestrially feeding fish Anableps anableps (N = 3; specimens from Michel, Aerts, Gibb, & Van Wassenbergh, 2015) and Periophthalmus barbarus (N = 4; specimens from Michel, Heiss, et al, 2015) and measured on anatomy drawings for the eelcatfishes Channallabes apus and Gymnallabes typus (Cabuy, Adriaens, Verraes, & Teugels, 1999;Devaere, Adriaens, Verraes, & Teugels, 2001). Head length was measured as the distance between the anterior tip of the jaws and the posterior margin of the opercle.…”

Aquatic–terrestrial transitions of feeding systems in vertebrates: a mechanical perspective

“…Instead of lifting the trunk up and rotating the head down as in the catfish and reedfish ( Fig. 4A-C, Table 1), the largescale foureyes entirely relies on the kinematics of its jaws to pick up food from the ground (Michel et al, 2015a). The tooth-bearing part of the upper jaw, the premaxilla (see Glossary), first performs mainly a forward translation while the lower jaw is depressed (resembling typical upper jaw protrusion) (Fig.…”

“…The latter action can be performed seemingly independently from lower jaw adduction by the other jaw adductor muscle divisions, allowing more precise 'picking' of food from the bottom compared with other (i.e. non-cyprinodontiform) fishes (Hernandez et al, 2008(Hernandez et al, , 2009Michel et al, 2015a). Michel et al (2015a) proposed that the increased amplitude of ventral protrusion (i.e.…”