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- MATERIAL AND METHODS
- LITERATURE CITED
- Supporting Information
The New Zealand tuatara, Sphenodon, has a specialized feeding system in which the teeth of the lower jaw close between two upper tooth rows before sliding forward to slice food apart like a draw cut saw. This shearing action is unique amongst living amniotes but has been compared with the chewing power stroke of mammals. We investigated details of the jaw movement using multibody dynamics analysis of an anatomically accurate three-dimensional computer model constructed from computed tomography scans. The model predicts that a flexible symphysis is necessary for changes in the intermandibular angle that permits prooral movement. Models with the greatest symphysial flexibility allow the articulation surface of the articular to follow the quadrate cotyle with the least restriction, and suggest that shearing is accompanied by a long axis rotation of the lower jaws. This promotes precise point loading between the cutting edges of particular teeth, enhancing the effectiveness of the shearing action. Given that Sphenodon is a relatively inactive reptile, we suggest that the link between oral food processing and endothermy has been overstated. Food processing improves feeding efficiency, a consideration of particular importance when food availability is unpredictable. Although this feeding mechanism is today limited to Sphenodon, a survey of fossil rhynchocephalians suggests that it was once more widespread. Anat Rec, 2012. © 2012 Wiley-Periodicals, Inc.
- Top of page
- MATERIAL AND METHODS
- LITERATURE CITED
- Supporting Information
Oral food processing can be defined as: “Any behavior during which the size, shape, and (or) structural integrity of the [food or] prey item was changed via contact with the tongue, palate, jaws, and (or) teeth” (McBrayer and Reilly,2002; p 884). Under this definition virtually all lepidosaurs (tuatara, lizards, and snakes) process food orally to some extent (e.g. Günther,1867; Throckmorton,1976; Schwenk,2000; Reilly et al.,2001; McBrayer and Reilly,2002; Ross et al.,2007a,b,2010) with specific behaviors including puncture crushing, palatal crushing, and side-to-side movements (McBrayer and Reilly,2002). Sphenodon (the tuatara of New Zealand; Parkinson,2002; Hay,2003,2010) in particular has a highly specialized feeding action whereby the lower jaw closes between two upper rows of teeth (marginal and palatal) before sliding forward to tear food apart with a shearing action analogous to that of a draw cut saw (Günther,1867; Farlow,1975; Robinson,1976; Gorniak et al.,1982; Whiteside,1986; Schwenk,2000). Nothing comparable is known amongst other living amniotes, including within Squamata: lizards and snakes (Schwenk,2000; Reilly et al.,2001).
The feeding apparatus of Sphenodon includes a number of components: a large fleshy tongue; teeth that are fused to the crest of the jaw bone and are generally not replaced; marginal tooth rows that are relatively close to the midline; an enlarged chisel-like premaxillary tooth; anterior caniniform teeth on the maxilla, dentary and palatine; an enlarged palatine tooth row parallel to the maxillary row; prominent posterior flanges on maxillary and palatine teeth; small anterolabial and anterolingual flanges on dentary teeth; relatively thin enamel; and an articulation surface of the articular that is elongate by comparison with the quadrate-articular surface (Günther,1867; Howes and Swinnerton,1901; Gray,1931; Robinson,1976; Schwenk,1986,2000; Reynoso,1996; Jones,2008,2009; Kieser et al.,2009; Jones et al.,2009a,b,2011; Curtis et al.,2010a,b). An elongate wear facet on the labial surface of the dentary below the tooth row is sometimes present in adult animals reflecting tooth on bone contact coupled with proal jaw movement (Robinson,1976).
In the wild, Sphenodon takes a variety of prey items including ants, moths, caterpillars, spiders, beetles, snails, frogs, and lizards (Walls,1981; Ussher,1999; Parkinson,2002), and large individuals are known to bite or saw the heads off sea birds (Walls,1978,1981; Dawbin,1982; Gans,1983; Cartland-Shaw,1998; Cree et al.,1999). Direct observations of feeding have been described by several authors (e.g. Farlow,1975; Walls1981; Gorniak et al.,1982; Schwenk,2000), with Gorniak et al. (1982) using electromyography to record jaw muscle activity. Feeding involves five stages: acquisition (prey capture), immobilization, processing, transport, and swallowing (De Vree and Gans,1989). If the food item is small the tongue may be used to bring it into the mouth, but with larger prey the caniniforms and large chisel-like premaxillary teeth may be important for capture and immobilization (Gorniak et al.,1982). As the adductor muscles contract and the jaws close (during prey processing), the three tooth rows (two upper, one lower) allow three point bending to be applied to food items regardless of how worn the teeth are (Fig. 1, Table 1; Evans,1980). This mechanism is particularly useful for dealing with stiffer but more brittle food items such as beetles with highly sclerotised shells (Lucas and Luke,1984). Once the jaws are closed the large pterygoideus muscle contracts pulling the lower jaw forward (Fig. 2; Farlow,1975; Robinson,1976; Gorniak et al.,1982; Whiteside,1986; Curtis et al.,2010a; not backwards as inferred by Günther,1867; p 601). Material held or impaled by the teeth is sheared between the anterior flanges on the dentary teeth and the posterior flanges on the maxillary and palatine teeth (Robinson,1976; Gorniak et al.,1982; Jones,2009). The jaw is reopened and the tongue may be used to position the food before another shearing stroke (Walls,1981; Gorniak et al.,1982, personal observation). This protraction of the lower jaw therefore involves “draw cutting” (Frazzetta,1988; Abler,1992) and although it is often referred to as propaliny (e.g. Jones,2008) it is more specifically proal jaw movement because the power stroke is anteriorly directed (a posteriorly directed power stroke is termed palinal movement: Krause,1982). Following a number of cycles that may vary according to prey type and size, the food is swallowed (Gorniak et al.,1982).
Figure 1. Three-point bending on stiff or brittle materials as suggested by Evans (1980). (A) A planar food item is held between the upper and lower tooth rows. (B) The dentary teeth press food against the two upper rows of teeth. (C) Dentary continues to rise until the food item fractures because of tension on its dorsal surface. For abbreviations see Table 1.
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Table 1. Anatomical abbreviations
|art.sur||Articulating surface of the articular|
|cpd||Coronoid process of the dentary|
|den.can.t||Dentary caniniform tooth|
|den.t||Dentary additional tooth|
|ltf||Lower temporal fenestra|
|mAMEM||m. Adductor mandibulae externus medialis|
|mAMEP||m. Adductor mandibulae externus profundus|
|mAMES||m. Adductor mandibulae externus superficialis|
|mAMP||m. Adductor mandibulae posterior|
|mDM||m. Depressor mandibulae|
|mPstP||m. Pseudotemporalis profundus|
|mPstS||m. Pseudotemporalis superficialis|
|mPtAt||m. Pterygoideus atypicus|
|mPtTyML||m. Pterygoideus typicus (middle lateral part)|
|mPtTyMM||m. Pterygoideus typicus (middle medial part)|
|mPtTyV||m. Pterygoideus typicus (ventral part)|
|mx.can.t||Maxillary caniniform tooth|
|mx.t||Maxillary additional tooth|
|pal.can.t||Palatine caniform tooth|
|sbs||Secondary bone skirt|
|sym||Medial surface of the symphysis|
Disagreement remains over some aspects of the shearing movement. After examination of anatomical material, both Günther (1867; p 600) and Robinson (1976; p 54) reported that the jaw symphysis was maintained by a fibrous ligament with no involvement of Meckel's cartilage. Both reasoned, as did Schwenk (2000; p 189), that the jaw joints and flexible symphysis accommodated a movement between the right and left mandibles that is necessary for their forward shearing movement (Günther,1867; p 601; Robinson,1976; p 53-54). However, based on observations of feeding in captive Sphenodon, Gorniak et al. (1982; p 337) disputed this suggestion and reported that they found no evidence that the lower jaws moved laterally or could “rotate about their long axes” during the jaw cycle. They argued that the lower jaw was constrained to move “parallel to the upper tooth rows” Gorniak et al. (1982; p 345) because of the narrow gap between those rows and the proximity of the mandibular coronoid process to the pterygoid flanges on the palate. Perhaps correspondingly, Schwenk (2000) also described the lower dentition as fitting “precisely” into the gap between the upper tooth rows.
Because of its limited distribution and iconic status in New Zealand, Sphenodon is listed in CITES Appendix 1 (CITES,2011) and subject to conservation efforts (Parkinson,2002; Ramstad et al.,2009; Besson and Cree,2010). Potential for invasive in vivo work is therefore restricted and the work of Gorniak et al. (1982) would be difficult to replicate today.
However, computer modeling approaches such as multibody dynamics analysis (MDA) provide an alternative means of investigating feeding behavior (Curtis et al.,2008,2010a,b,c; Moazen et al.,2008a,b; Curtis,2011). It allows the interaction of the three-dimensional geometries of the feeding apparatus, muscle forces, and contact forces to be recorded and visualized in detail during jaw movement. An MDA model of Sphenodon has previously been used to illustrate muscle arrangement (Curtis et al.,2009; Jones et al.,2009) as well as investigating muscle activation and function (Curtis et al.,2010a), bite force (Curtis et al.,2010c), potential for mechanoreception at the jaw joints (Curtis et al.,2010b), and the distribution of strain under feeding loads (Curtis et al.,2011). Here we use this model to investigate the movement of the lower jaws in Sphenodon during proal shearing to test the feasibility of three different restrictions on mobility at the mandibular symphysis. Museum specimens were also examined for jaw anatomy and wear patterns associated with this feeding behavior.