Feeding behaviour in a ‘basal’ tortoise provides insights on the transitional feeding mode at the dawn of modern land turtle evolution

Abstract

Almost all extant testudinids are highly associated with terrestrial habitats and the few tortoises with high affinity to aquatic environments are found within the genus Manouria. Manouria belongs to a clade which forms a sister taxon to all remaining tortoises and is suitable as a model for studying evolutionary transitions within modern turtles. We analysed the feeding behaviour of Manouria emys and due to its phylogenetic position, we hypothesise that the species might have retained some ancestral features associated with an aquatic lifestyle. We tested whether M. emys is able to feed both in aquatic and terrestrial environments. In fact, M. emys repetitively tried to reach submerged food items in water, but always failed to grasp them—no suction feeding mechanism was applied. When feeding on land, M. emys showed another peculiar behaviour; it grasped food items by its jaws—a behaviour typical for aquatic or semiaquatic turtles—and not by the tongue as generally accepted as the typical feeding mode in all tortoises studied so far. In M. emys, the hyolingual complex remained retracted during all food uptake sequences, but the food transport was entirely lingual based. The kinematical profiles significantly differed from those described for other tortoises and from those proposed from the general models on the function of the feeding systems in lower tetrapods. We conclude that the feeding behaviour of M. emys might reflect a remnant of the primordial condition expected in the aquatic ancestor of the tortoises.

Eocene North American Testudinidae and Geoemydidae (Reptilia, Testudines): A Re-Evaluation of Their Alpha Taxonomy, Ecology, and Origin

“…Basal testudinids have long been assumed to have an ecology similar to extant testudinids. This assumption is challenged by Manouria emys, the most basal extant testudinid, which has a distinct ecology [7], including a unique mode of food apprehension, breeding behavior, and a greater willingness to attempt subaqueous food capture. The histology of Hadrianus is that of a semi-aquatic to aquatic turtle [8].…”

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

“…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).…”

Patterns of morphological evolution in the skull of turtles: contributions from digital paleontology, neuroanatomy and biomechanics

“…Crown turtles evolved a great flexibility of their neck, which, as compensation, enables fast and elaborated nutrition strategies (Herrel et al 2008). As such, neck mobility and feeding behavior seem to be strongly connected (Natchev et al 2015). In some forms, particularly in chelids, the neck may be longer than the shell, and many taxa, including trionychids and kinosternids, are able to stretch their heads completely over the carapace for defense or hunting purposes.…”

“…followed by the closure of the jaw holding the prey (Natchev et al 2015). Some aquatic turtles have the suction mechanism extremely well developed, swallowing the food item without grabbing it with their jaws (e.g., Chelus fimbriatus and Apalone spinifera; Lemell et al 2002;Anderson 2009), but most turtles use only a weak suction flow and, hence, holding the prey with the closure of jaws is an important part of the feeding behavior (Natchev et al 2015).…”

“…However, the exclusive terrestrial tortoises (Testudinidae) developed a different way to grab food items in which they first touch the food with their tongue ("tongue prehension"), and then they bring them to the mouth (Wochesländer et al 1999;Bels et al 2008). Natchev et al (2015) proposed a four-stage scenario in which this terrestrial feeding behavior might have originated from an aquatic ancestor. First, amphibious but predominantly aquatic turtles might have explored terrestrial environments and taken food items with their jaws, but would have to drag the food into the water to swallow it (as seen in some emydids; Weisgram 1985;Stayton 2011).…”