Contributions to Zoology, 80 (2) 143-156 (2011) Structure and function of the feeding apparatus in the common musk turtle Sternotherus odoratus (Chelonia, Kinosternidae) Nikolay Natchev1, 3, Egon Heiss1, Katharina Singer1, Stefan Kummer1, Dietmar Salaberger2, Josef Weisgram1 1 Department of Theoretical Biology, University of Vienna, Althanstr. 14, A-1090 Vienna, Austria 2 Campus Wels, Upper Austria University of Applied Sciences, Stelzhammerstr. 23, 4600 Wels, Austria 3 E-mail: [email protected] Key words: feeding behaviour, head morphology, motion analysis, mud turtles, suction Abstract or ‘ingestion’; ‘food transport’ (including manipula- tion); ‘pharyngeal packing’; and ‘swallowing’ (or The present study examined the kinematic patterns of initial mammalian ‘deglutition’ (Smith, 1992)). In turtles, food uptake, food transport, pharyngeal packing and swallow- aquatic prey capture kinematics has been studied in ing in the common musk turtle Sternotherus odoratus. These data are supplemented by morphological descriptions of the pleurodirans (Van Damme and Aerts, 1997; Lemell skull and the hyolingual complex. Although the hyoid is mainly and Weisgram, 1997; Lemell et al., 2002) and in ma- cartilaginous, S. odoratus still use exclusively hydrodynamic rine (including one estuarine) cryptodirans (Bels and mechanisms in prey capture and prey transport. The tongue is Renous, 1992; Bels et al., 1998). To date, food uptake relatively small, with weakly developed intrinsic musculature. kinematics have been analysed in details in only three We propose that the elasticity of the hypoglossum and the hyoid body impacts the capability of S. odoratus to suction feed, but freshwater cryptodirans; Chelydra serpentina (L., allows these turtles to effectively re-position the food items 1758) (Lauder and Prendergast, 1992), Terrapene within the oropharyngeal cavity during transport, manipulation carolina (L., 1758) (Summers et al., 1998) and Cuora and pharyngeal packing. We standardised conditions in all amboinensis (Daudin, 1801) (Natchev et al., 2009). In- feeding events by using food items of the same consistence and formation on the kinematics of all other main phases is size, and by always offering the food at the same position at the bottom of the aquarium. Nonetheless, the measured kinematic scarce (Bels et al., 2008). values varied considerably. The duration of prey capture and The origins and the phylogenetical relationships of prey transport cycles were relatively long in S. odoratus com- stem and crown group turtles are still not completely pared to other freshwater turtles studied so far. The initiation of understood (see Sterli, 2010). The oldest unquestioned hyoid retraction relative to the onset of jaw opening can be stem turtle was an aquatic animal (Li et al., 2008). modulated not only in prey capture but also in prey transport cycles. In the common musk turtle, the jaw and hyoid move- Some other stem turtle groups were terrestrial (Joyce ments apparently have a low level of integration. and Gauthier, 2004; Scheyer and Sander, 2007), so the aquatic origin of the turtle stem is still contentious (see Lyson et al., 2010). Anyhow the feeding apparatus of Contents the recent chelonians is secondarily adapted to aquatic feeding (Lauder and Prendergast, 1992). The turtles Introduction .....................................................................................143 have developed aquatic feeding convergently with Material and methods .................................................................. 144 feeding systems in anamniotes. Lauder and Prender- Results ............................................................................................. 146 gast (1992) point to kinematic similarities in prey cap- Discussion ...................................................................................... 150 ture modes in some bony fishes, salamanders and the Acknowledgements ...................................................................... 153 References ...................................................................................... 154 turtle C. serpentina. These authors explain the analo- Appendix ........................................................................................ 156 gy in the underwater food uptake motoric by hydrody- namic constraints placed on prey capture due to the physical properties of the water as feeding media. The Introduction prey capture mechanism of C. serpentina was defined as ‘ram feeding’ – the prey is not sucked up into the According to Schwenk (2000), the feeding process in oral cavity, but engulfed by the jaws in a rush forward tetrapods consists of four main phases: ‘prey capture’ strike of the cranocervical complex (Lauder and Downloaded from Brill.com09/24/2021 10:18:28PM via free access 144 Natchev et al. – Feeding in the common musk turtle Prendergast, 1992). In tetrapods utilising ‘bidirection- common musk turtle is not able to suck up food items al feeding’ (Reilly and Lauder, 1992), any volume ex- deep within the oropharynx and that the first contact to pansion of the oropharynx will result in a backward the food will involve the jaws. Based on this analysis water flow relative to the skull. Van Damme and Aerts we predict the highest ‘tb’ concentration directly be- (1997) introduced the terms ‘compensatory suction’ hind the horny ‘bills’ of the rhamphothecae. and ‘inertial suction’ for turtles, retaining the term In some turtles that use tongue-based food trans- ‘ram feeding’ only for feeding systems with unre- port underwater, the lingual mucosa exhibits morpho- strained water through-flow. According to Summerset logical similarities to those in purely terrestrial spe- al. (1998), the term ‘compensatory suction’ describes cies. The dorsal lingual surface bears numerous verti- exactly the prey capture mode in cryptodirans, so the cal, high and slender lingual papillae. These increase present study will not use the term ‘ram feeding’ for the tongue surface and the interlocking effect between food uptake. the tongue and the food during transport (see Natchev The neuromotor program of the underwater food et al., 2010). The common musk turtle has a papillated transport is predicted to be conserved in the evolution dorsal tongue surface, but is not able to manipulate or of gnathostome feeding systems (Reilly and Lauder, transport food on land. The papillae are floppy, longi- 1990). In the cyclic model proposed by these authors tudinally orientated and often overlap each other. Be- for anamniotes, the jaw cycle is divided into a ‘fast cause these papillae are highly vascularised, it is pro- open’ and ‘fast close’ phases, as hyoid retraction (ex- posed that the main function of these structures is con- pansion phase) starts simultaneously to the begin of nected to aquatic gas exchange (Heiss et al., 2010). jaw opening. The coincidence between hyoid retrac- One of the main goals of the present study is to inves- tion and jaw opening is regarded as a uniform pattern tigate the role of the papillated tongue of the common throughout tetrapods. This hypothesis is not always musk turtle in the aquatic food transport. Based on the supported for turtles. The transport modes in turtles design and orientation of the lingual papillae, we pro- seem to be extraordinarily variable (Lemell and Weis- pose that they are physically incapable of withstanding gram, 1997; Lemell et al., 2002; Natchev et al., 2010). shear forces. We hypothesise that S. odoratus uses ex- According to Aerts et al. (2001) the underwater trans- clusively hydrodynamic mechanisms to move food port in chelonians combines ‘compensatory suction’ items within the oral cavity and toward the pharynx. and ‘inertial suction’. Both mechanisms are termed According to Bels et al. (1998), turtles with variable ‘intraoral-aquatic hyoid transport’ (Bels et al., 2008). diet exhibit variability in their feeding kinematics and Nonetheless, some chelonians, even completely aquat- we expect the same for the common musk turtle. To ic species, use tongue-based transport, which is termed test this hypothesis, we investigate statistically which ‘intraoral-aquatic lingual transport’ (Bels et al., 2008). variables of food uptake and food transport kinematic Except a brief description of feeding biomechanics profiles exhibit similarities. We also test whether the in Claudius angustatus (Cope, 1985) (Weisgram, kinematic patterns differ on an intra and inter-individ- 1982, 1985) information on the feeding kinematics in ual level. Special focus is devoted to analysing the co- kinosternids is lacking. In this study, we describe the ordination (sensu Wainwright et al., 2008) between the kinematics of the neck, jaws and hyoid complex based neck, hyoid and jaw movements. This is designed to on high-speed film analysis during the whole aquatic test a predicted strength correlation between the move- feeding process in the omnivorous kinosternid Ster- ments of the elements of the feeding apparatus in un- notherus odoratus (Latreille, 1801). These data are derwater food transport in lower tetrapods (Reilly and supplemented by morphological descriptions of the Lauder, 1990). skull and hyolingual complex. According to Heiss et al. (2008), the highest con- centration of taste buds (tb) within the oropharynx in Material and methods turtles is in areas where the first contact to the food occurs. Using the electron microscopic and histologi- The common musk turtle or stinkpot Sternotherus cal techniques, we test this hypothesis in the