Analysis of prey capture and food transport kinematics in two Asian box turtles, Cuora amboinensis and Cuora flavomarginata (Chelonia, Geoemydidae), with emphasis on terrestrial feeding patterns

Natchev, Nikolay; Heiss, Egon; Lemell, Patrick; Stratev, Daniel; Weisgram, Josef

doi:10.1016/j.zool.2008.05.002

Cited by 32 publications

(47 citation statements)

References 43 publications

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“…environments also displayed this same difference between aquatic and terrestrial bites (both in the present study and in others) (Summers et al, 1998;Natchev et al, 2009) (supplemental material Fig. S2), providing support for the idea that these differences are ultimately appropriate for the two environments.…”

Section: Terrapene Carolina Tersupporting

confidence: 86%

“…More common are studies on species that will feed naturally in more than one environment, such as turtles (Summers et al, 1998;Natchev et al, 2009;Natchev et al, 2010), salamanders (Reilly, 1996;Deban and Marks, 2002;Shaffer and Lauder, 1988), snakes (Alfaro, 2002) and even fish (Sponder and Lauder, 1981;Van Wassenbergh et al, 2006), or studies on organisms that make this transition during metamorphosis, such as salamanders (Shaffer and Lauder, 1988;Reilly, 1996;Deban and Marks, 2002). In most of these cases, feeding behaviors and kinematics differ between different environments, usually in ways that are appropriate for the different fluid properties of water and air (Reilly, 1996;Alfaro, 2002;Deban and Marks, 2002;Natchev et al, 2009;Shaffer and Lauder, 1988). However, given that these species naturally feed in both environments, it is expected that they will have evolved appropriate responses to each environment.…”

Section: Introductionmentioning

confidence: 99%

“…In air, T. carolina individuals took longer bites and generated a smaller amount of hyoid depression. Similarly, Cuora amboinensis uses a different pattern of hyoid protraction during aquatic feeding in order to generate compensatory suction (Natchev et al, 2009). In addition to these differences, turtles might also be expected to approach prey more closely before opening their jaws and to more rapidly depress the jaw underwater to maximize water flow velocity when biting (Summers et al, 1998;Reilly, 1996;Deban and Marks, 2002).…”

Section: Introductionmentioning

confidence: 99%

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Terrestrial feeding in aquatic turtles: environment-dependent feeding behavior modulation and the evolution of terrestrial feeding in Emydidae

Stayton

2011

Journal of Experimental Biology

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SUMMARYEvolutionary transitions between aquatic and terrestrial environments are common in vertebrate evolution. These transitions require major changes in most physiological functions, including feeding. Emydid turtles are ancestrally aquatic, with most species naturally feeding only in water, but some terrestrial species can modulate their feeding behavior appropriately for both media. In addition, many aquatic species can be induced to feed terrestrially. A comparison of feeding in both aquatic and terrestrial environments presents an excellent opportunity to investigate the evolution of terrestrial feeding from aquatic feeding, as well as a system within which to develop methods for studying major evolutionary transitions between environments. Individuals from eight species of emydid turtles (six aquatic, two terrestrial) were filmed while feeding underwater and on land. Bite kinematics were analyzed to determine whether aquatic turtles modulated their feeding behavior in a consistent and appropriate manner between environments. Aquatic turtles showed consistent changes between environments, taking longer bites and using more extensive motions of the jaw and hyoid when feeding on land. However, these motions differ from those shown by species that naturally feed in both environments and mostly do not seem to be appropriate for terrestrial feeding. For example, more extensive motions of the hyoid are only effective during underwater suction feeding. Emydids evolving to feed on land probably would have needed to evolve or learn to overcome many, but not all, aspects of the intrinsic emydid response to terrestrial feeding. Studies that investigate major evolutionary transitions must determine what responses to the new environment are shown by naïve individuals in order to fully understand the evolutionary patterns and processes associated with these transitions. Supplementary material available online at

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Section: Terrapene Carolina Tersupporting

confidence: 86%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Terrestrial feeding in aquatic turtles: environment-dependent feeding behavior modulation and the evolution of terrestrial feeding in Emydidae

Stayton

2011

Journal of Experimental Biology

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“…Semi-terrestrial fish species, for example, use slightly modified suction-feeding mechanisms when capturing prey on land (Sponder and Lauder, 1981;Van Wassenbergh et al, 2006). Similarly, aquatic turtles rely on modified aquatic feeding mechanics when grasping food on land (Summers et al, 1998;Natchev et al, 2009;Stayton, 2011). This shows that during invasion of land, vertebrates in general use slightly modified aquatic prey-capture mechanisms, corroborating the importance of behavioral plasticity in aquatic-terrestrial transitions.…”

Section: Discussionmentioning

confidence: 76%

“…In fact, only a few species have evolved mechanisms that allow them to exploit food sources in both environments. Such amphibious feeders are mainly known within lower tetrapods, especially within salamanders and turtles (Reilly and Lauder, 1989;Miller and Larsen, 1989;Miller and Larsen, 1990;Summers et al, 1998;Deban and Wake, 2000;Deban, 2003;Heiss et al, 2008;Natchev et al, 2009;Natchev et al, 2010;Stayton, 2011). Recent studies have shown that the capability to feed in both media is mainly due to behavioral plasticity, where modulatory behavior compensates for morphological constraints (Stayton, 2011).…”

Section: Introductionmentioning

confidence: 99%

Masters of change: seasonal plasticity in the prey-capture behavior of the Alpine newtIchthyosaura alpestris(Salamandridae)

Heiss

Aerts

Wassenbergh

2013

Journal of Experimental Biology

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SUMMARYTransitions between aquatic and terrestrial environments are significant steps in vertebrate evolution. These transitions require major changes in many biological functions, including food uptake and transport. The Alpine newt, Ichthyosaura alpestris, is known to show a 'multiphasic lifestyle' where the adult shifts from a terrestrial to an aquatic lifestyle and then back to a terrestrial lifestyle every year as a result of its breeding activity. These transitions correspond to dramatic changes in morphology, physiology and behavior, resulting in distinct aquatic and terrestrial morphotypes. We hypothesized that these shifts go along with changes in prey-capture mechanics to maintain a sufficiently high performance in both environments. We analyzed the preycapture kinematics in the four possible modes: aquatic strikes in the aquatic phase, terrestrial strikes in the terrestrial phase, aquatic strikes in the terrestrial phase and terrestrial strikes in the aquatic phase. A multivariate comparison detected significant kinematic differences between the phase-specific feeding modes. In both the aquatic and the terrestrial phase, I. alpestris uses a suction-feeding mechanism for capturing prey in water. By contrast, I. alpestris uses a jaw-based grasping mechanism with a kinematic profile similar to the aquatic modes for terrestrial prey-capture in its aquatic phase but an elaborate lingual-based prehension mechanism to capture terrestrial prey in the terrestrial phase. These results exhibit a so-far unknown amount of behavioral plasticity in prey-capture behavior that is tuned to the seasonal demands of performance, and exemplify functional mechanisms behind aquatic-terrestrial transitions in vertebrates.

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The Fish in the Turtle: On the Functionality of the Oropharynx in the Common Musk Turtle Sternotherus odoratus (Chelonia, Kinosternidae) Concerning Feeding and Underwater Respiration

Heiss

Natchev

Beisser

et al. 2010

The Anatomical Record

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In tetrapods, the oropharyngeal cavity and its anatomical structures are mainly, but not exclusively, responsible for the uptake and intraoral transport of food. In this study, we provide structural evidence for a second function of the oropharynx in the North American common musk turtle, Sternotherus odoratus, Kinosternidae: aquatic gas exchange. Using high-speed video, we demonstrate that S. odoratus can grasp food on land by its jaws, but is afterward incapable of lingual based intraoral transport; food is always lost during such an attempt. Scanning electron microscopy and light microscopy reveal that the reason for this is a poorly developed tongue. Although small, the tongue bears a variety of lobe-like papillae, which might be misinterpreted as an adaptation for terrestrial food uptake. Similar papillae also cover most of the oropharynx. They are highly vascularized as shown by light microscopy and may play an important role in aquatic gas exchange. The vascularization of the oropharyngeal papillae in S. odoratus is then compared with that in Emys orbicularis, an aquatic emydid with similar ecology but lacking the ability of underwater respiration. Oropharyngeal papillae responsible for aquatic respiration are also found in soft-shelled turtles (Trionychidae), the putative sister group of the kinosternids. This trait could therefore represent a shared, ancestral character of both groups involving advantages in the aquatic environment they inhabit.

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Analysis of prey capture and food transport kinematics in two Asian box turtles, Cuora amboinensis and Cuora flavomarginata (Chelonia, Geoemydidae), with emphasis on terrestrial feeding patterns

Cited by 32 publications

References 43 publications

Terrestrial feeding in aquatic turtles: environment-dependent feeding behavior modulation and the evolution of terrestrial feeding in Emydidae

Terrestrial feeding in aquatic turtles: environment-dependent feeding behavior modulation and the evolution of terrestrial feeding in Emydidae

Masters of change: seasonal plasticity in the prey-capture behavior of the Alpine newtIchthyosaura alpestris(Salamandridae)

The Fish in the Turtle: On the Functionality of the Oropharynx in the Common Musk Turtle Sternotherus odoratus (Chelonia, Kinosternidae) Concerning Feeding and Underwater Respiration

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