Kinematics of aquatic and terrestrial prey capture in Terrapene carolina, with implications for the evolution of feeding in cryptodire turtles.

Studies of aquatic prey capture in vertebrates have demonstrated remarkable con- vergence in kinematics between diverse vertebrate taxa. When feeding in water, most vertebrates employ large-amplitude hyoid depression to expand the oral cavity and suck in water along with the prey. In contrast, vertebrates feeding on land exhibit little or no hyoid depression. In this study we compared the kinematics of terrestrial and aquatic prey capture within one species of turtle, Terrapene carolina, in order to determine whether an individual species can modulate the magnitude of hyoid depression between air and water. High-speed video (250 frames per second) showed that hyoid depression was over three times greater in aquatic than in terrestrial feedings, indicating that T. carolina is able to modulate hyoid depression magnitude depending on the me- dium in which feeding occurs. In addition, we observed medium-dependent modulation of hyoid depression in another turtle, Heosemys grandis, and large-amplitude hyoid depression during aquatic feeding in Kinosternon leucostomum, Platysternon megacephalum, and juvenile Chelydra serpentina. In all of these turtles, hyoid depression produced oral cavity expansion during aquatic feeding, but the earthworm prey were never sucked toward the predators. Prey were captured by neck extension (ram feeding), and we conclude that the function of hyoid depression during aquatic feeding in cryptodire turtles is to prevent the forward motion of the predator from pushing the prey away (compensatory suction). Aquatic feeding is probably the primitive condition for all ex- tant turtles, and thus terrestrial feeding in T. carolina and other turtles is a secondarily derived characteristic. We conclude from this historical pattern that it is not appropriate to use extant turtles in attempts to reconstruct the terrestrial feeding mechanisms of primitive amniotes. J. Exp. Zool. 281:280-287, 1998. © 1998 Wiley-Liss, Inc. Biomechanical studies of feeding in numerous aquatic vertebrates have demonstrated the nearly universal use of suction feeding to acquire prey in the aquatic realm. In suction feeding, depres- sion of the hyoid apparatus expands the oral cav- ity and water is pulled into the mouth. Sharks, ray-finned fishes, lungfishes, larval and adult sala- manders, aquatic turtles, and odontocete whales have all been shown to employ large-amplitude hyoid depression and oral cavity expansion when feeding in water (e.g., Lauder, '80; Bemis and Lauder, '86; Lauder and Reilly, '88; Werth, '89; Lauder and Prendergast, '92; Reilly and Lauder, '92; Motta et al., '97; but see Schwenk and Wake, '88 for an example of aquatic lingual feeding). This remarkable convergence is thought to result from constraints imposed by the high density and vis- cosity of water (Lauder, '85; Liem, '90). If an animal generates no suction when feeding on small prey in water, the prey may be pushed away as the predator approaches. In some cases suction is sufficient only to counter the forward motion of the predator and thus allow it to engulf or grasp the prey in its jaws. This prey capture mechanism has been termed compensatory suc- tion (Van Damme and Aerts, '97) or ram feeding (Norton and Brainerd, '93). In other cases suction is sufficient to pull the prey towards the mouth and has been termed inertial suction (Van Damme and Aerts, '97) or suction feeding (Norton and Brainerd, '93). The existence of these different terms high-