Contributions to Zoology, 80 (2) – 2011Nikolay Natchev; Egon Heiss; Katharina Singer; Stefan Kummer; Dietmar Salaberger; Josef Weisgram: Structure and function of the feeding apparatus in the common musk turtle Sternotherus odoratus (Chelonia, Kinosternidae)

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According to Bever (2007, 2009), features associated with the feeding apparatus are the most variable cranial structures for both continuous and discrete characters in S. odoratus. One explanation for the postnatal morphological variations in the continuous characters of the skull is a potential dietary shift during ontogenetic development (Pritchard, 1979; Bonin et al., 2006; Bever, 2007, 2009). Correlations between dietary shift and ontogenetic changes in the skull morphology and biomechanics are well documented in the loggerhead musk turtle Sternotherus minor (Agassiz, 1857) (Pfaller, 2009; Pfaller et al., 2010). Based on our morphological investigations in S. odoratus using CT, we demonstrate that no major change takes place in the ossification rate of the hyoid complex during transition from juvenile to adult. The hyoid corpus remains largely cartilaginous even in older animals. A heavily ossified hypoglossum and hyoid body are predicted in all turtles using predominantly suction feeding under water (Bramble, 1973; Bramble and Wake, 1985; Van Damme and Aerts, 1997; Lemell et al., 2000, 2002, 2010). A cartilaginous hyoid body (or lingual processus) in extant chelonians is associated with a greater role of the tongue in feeding (Bramble and Wake, 1985; Wochesländer et al., 1999; Richter et al., 2007; Natchev et al., 2009, 2010). According to Pfaller (2009) the durophagous (feeding on hard-shelled snails) loggerhead musk turtle possesses a relatively large, muscular and mobile tongue and a weakly developed hyoid apparatus. That author proposes that the large tongue helps to orally manipulate the snails. The common musk turtle utilises exclusively hydrodynamic mechanisms in prey capture and prey transport, so one could expect more rigid hyoid complex. Our interpretation is that the elastic hyoid body allows these turtles to increase the plasticity in the movements of the hyolingual complex. The common musk turtle feeds on hard prey, including insects, snails and mussels. That kind of hard prey has to be killed, crushed, eventually cleaned or sized, so a bendable hyoid basis would facilitate the rostro-caudal and caudo-rostral reposition of the food item within the oropharynx during the transport (manipulation) phase. We cannot completely exclude that the smaller and elastic hyoid is a remnant of the ancestral state, but as the common ancestor of all extant turtles was an aquatic species (see Joyce and Gauthier, 2004) and a well-ossified hyoid is expected in aquatic living turtles (see Bramble and Wake, 1985), it is logical to propose that the reduced ossification of the hyoid in S. odoratus represents an adaptation. Within kinosternids are found also species with highly ossified hyoid apparati (Weisgram, 1985).

Our prey capture sequences revealed that the common musk turtles actively sucked up the food items by somewhat expanding the oropharyngeal cavity. Initial movement of the food toward the oropharynx was detected as the fish pieces were already within the plane of the gaping mouth. In only one film the initial food uptake event (food ingestion) resembled pure inertial suction – the cranium remained static as the prey moved into the mouth. Herrel et al. (2002) hypothesise a trade-off between the bite performance and the capacity to suction feed in turtles. Those authors report a bite force of 30.72 ± 19.20 N in S. odoratus and include this species in the ‘biters’ group of turtles. Prior to the ‘final head fixation’ (see Lemell and Weisgram, 1997) S. odoratus must approach the food item to a very close distance (several millimetres). Apparently, outside the margins of the jaws, the common musk turtles are unable to create effective suction forces. Although suction performance was not quantified in the present study, these observations seem to support the hypothesis of Herrel et al. (2002), that turtles able to bite hard have a relatively low capacity to suction feed (or at least to capture prey via suction).

Kinematic patterns of the gape and neck varied considerably. We therefore conclude that S. odoratus adjusts its food uptake behaviour to every single feeding situation, depending on the position of the food relative to the jaws. As the pieces of fish used in our experiments usually remained under the ‘beak’ during jaw opening, the animals apparently have no permanent visual contact with the food items. Perhaps the motoric of the feeding apparatus is coordinated in combined response to visual and olfactory feedback, and to the tactile ‘cirri’ (see Winokur, 1982).

In contrast to the most cryptodiran turtles studied to date (Lauder and Prendergast, 1992; Bels et al., 1998; Summers et al., 1998; Bels et al., 2008), hyoid retraction in the common musk turtle starts shortly before or even after reaching peak gape during food uptake (Figures 3, 4). This behaviour [similar to the behaviour described in C. amboinensis (Natchev et al., 2009)] probably reflects the relatively poor capacity of S. odoratus to suction feed. The abrupt retraction of the relatively small and elastic hyoid complex cannot produce the high suction forces found in species like e.g. Chelus fimbriata (Schneider, 1783) (Lemell et al., 2002). The common musk turtle lacks the skinny ‘cheeks’ lateral to the gaping mouth [as found in some turtles specialized in suction feeding (Lemell et al., 2002)], so the water flow cannot be directed so precisely toward the oropharynx. In our interpretation, the maintain of largest possible gape during the initiation of suction and the start of head protraction increase the potential for successful procurement of the food item.

When feeding on fish pieces, the common musk turtle transported the food items using ‘intraoral-aquatic hyoid transport’ (see Bels et al., 2008). The tongue played a subordinate, or perhaps no role in food transport (see Fig. 6). In 72% of our sequences, prey transport involved compensatory suction. As the neurocranium remained fully static in the rest of the food transport events, the turtles apparently relied on pure inertial suction in these cases. Our film sequences reveal no discrete slow phase during jaw opening, but there is variability in the delay of the start of hyoid retraction to the start of gape increase (see Tab. 1; Fig. 5). The beginning of pharyngeal expansion in S. odoratus does not correspond strictly to the start of the jaw open phase as predicted from the model of Reilly and Lauder (1990). In some turtles that can feed under water and have relatively well-developed tongues, hyoid retraction starts shortly before or even after reaching peak gape. The Amboina box turtle C. amboinensis uses its tongue to fix the prey against the palate during jaw opening (Natchev et al., 2009), whereas the Indochinese box turtle Cuora galbinifrons (Bourret, 1939) is able to fix prey to the dorsal tongue surface during gape increase (Natchev et al., 2010). This enables these two species to hold the food items within the oral cavity even at maximum gape. The common musk turtle has a weak intrinsic lingual musculature and the tongue papillae are not designed to support food transport (Heiss et al., 2010), so the tongue cannot be used to fix the food. For prey transport S. odoratus uses exclusively hydrodynamic mechanisms (as demonstrated in Fig. 6). Hyoid retraction must start after the prey is released from the rhamphothecae during jaw opening, but before the prey can escape or float out of the oral cavity. Due to the numerous taste buds on the oropharyngeal surfaces (Fig. 2d), we propose that besides mechanoreceptor input, the chemosensorial feedback helps coordinate the movements of the feeding apparatus during transport. Tb’s are most highly concentrated in the anterior palate and the anterior floor of the mouth. This anterior concentration enables a fast motoneural response of the type ‘eat it or leave it’ (Heiss et al., 2008) because the first prey contact occurs there. In the natural environment, the negative response (rejection) may be crucial: the benefit of avoiding harmful food is self-evident (Schwenk, 1985; Berkhoudt, 1985; Berkhoudt et al., 2001; Heiss et al., 2008).

The omnivorous aquatic turtles studied to date have a very flexible (sensu Wainwright et al., 2008) feeding behaviour (Davenport et al., 1992; Lauder and Prendergast, 1992; Lemell and Weisgram, 1997; Bels et al., 1998). The common musk turtle also exhibited plasticity in food uptake kinematics. It feeds on variety of non-elusive prey and approaches the food items to a close distance prior to ingestion. The construction of the hyolingual complex in S. odoratus restricts the turtle’s ability to ingest food via suction, but benefits its ability to re-position and manipulate food items within the oropharynx. The present study demonstrates that the common musk turtles modulate their feeding behavior even in successive feeding events involving food items which have exactly the same consistence, size and position. The food transport kinematics differed significantly within the three individuals: one of the turtles needed about half as many transport cycles prior to pharyngeal packing as the other two. Interestingly, that was the only individual showing significant correlations between the movement of the hyoid and the head. Further studies will reveal whether this can be interpreted in the context of the learning capacity or cognitive flexibility of cryptodyran turtles (Wilkinson et al., 2007, 2009, 2010. Plasticity in the cognitive capacity of S. odoratus could have strongly affected its ecological potential.