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Keywords:

  • chewing;
  • shearing;
  • Sphenodon;
  • symphysis;
  • teeth;
  • tuatara;
  • mandible;
  • mastication

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIAL AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. Acknowledgements
  9. LITERATURE CITED
  10. 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.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIAL AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. Acknowledgements
  9. LITERATURE CITED
  10. 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).

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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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Figure 2. Basic jaw movement in Sphenodon as observed by Gorniak et al. (1982) in left lateral view. Skull modified from Robinson (1976).

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Table 1. Anatomical abbreviations
ANANGULAR
ant.lab.flAnterolabial flange
ant.lin.flAnterolingual flange
apexApex
art.surArticulating surface of the articular
constrConstraint
cpdCoronoid process of the dentary
cvex.depConvex depression
DDENTARY
COCORONOID
den.can.tDentary caniniform tooth
den.tDentary additional tooth
ECPTECTOPTERYGOID
fasFascia
lab.flLabial flange
lat.lobLateral lobe
lat.riLateral ridge
lin.flLingual flange
ltfLower temporal fenestra
MMAXILLA
mAMEMm. Adductor mandibulae externus medialis
mAMEPm. Adductor mandibulae externus profundus
mAMESm. Adductor mandibulae externus superficialis
mAMPm. Adductor mandibulae posterior
mDMm. Depressor mandibulae
med.lobMedial lobe
mk.grMeckelian groove
mPstPm. Pseudotemporalis profundus
mPstSm. Pseudotemporalis superficialis
mPtAtm. Pterygoideus atypicus
mPtTyMLm. Pterygoideus typicus (middle lateral part)
mPtTyMMm. Pterygoideus typicus (middle medial part)
mPtTyVm. Pterygoideus typicus (ventral part)
mx.can.tMaxillary caniniform tooth
mx.tMaxillary additional tooth
ntchNotch
orbOrbit
PPALATINE
pal.can.tPalatine caniform tooth
pal.tPalatine tooth
pathPathology
po.lin.flPosterolingual flange
po.med.flPosteromedial flange
PREPREARTICULAR
pt.flPterygoid flange
qu.cotQuadrate cotyle
sbsSecondary bone skirt
symMedial surface of the symphysis
tTooth
we.fctWear facet

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.

MATERIAL AND METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIAL AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. Acknowledgements
  9. LITERATURE CITED
  10. Supporting Information

Material

Skeletal material of Sphenodon sp. was sampled from a number of collections, including the Grant Museum of Zoology, University College London, UK (LDUCZ); Natural History Museum, London, UK (BMNH); Southland Museum and Art Gallery, Invercargill, New Zealand (SMAG); and the personal collection of Dr. David Gower, Natural History Museum, London (DGPC): LDUCZ x036, x146, x343, x721, x723, x1176; BMNH 1972.1499, 1985.1212; SMAG Mackay collection 35, 54; DGPC 1, 2.

A Sphenodon skull and lower jaws (specimen LDUCZ x036) were subjected to microcomputed tomography (micro-CT) at the University of Hull, UK, using a X-Tek HMX 160 scanner and the following scan parameters: Beryllium target, 93 kV; uA 17; aperture 75%; 1,000 projections averaging out 32 frames per projection. To reduce beam hardening the X-rays were filtered through a 0.1 copper plate. Using image segmentation and analysis software (Amira 4.1, Mercury Computer Systems Inc, and Avizo 6.3, Visualization Sciences Group), the micro-CT dataset was used to generate a geometrically accurate three-dimensional model of the skull, lower jaws, and joint surfaces.

Comparative Anatomy

The jaws, teeth, and articular surfaces were examined using a Wild stereo binocular microscope, paying particular attention to tooth shape and tooth wear facets.

A contour visualization of the articular and quadrate cotyle morphology was generated by segmenting the respective CT models into layers of equal thickness (0.48 mm, exact value restricted by voxel size). Each layer is parallel to the horizontal plane between the ventral tips of the quadrate long axis of the skull and was assigned a different color.

Multibody Dynamics Analysis

The three-dimensional geometries of the skull elements were imported into ADAMS multibody dynamics analysis software (MSC Software Corp), as previously described (Curtis et al.,2009,2010a,b). The CT models of the lower jaws were imported as two separate geometries, attached at their anterior symphysis by an assigned constraint within the multibody software (Fig. 3A). Mass and inertial properties of all geometries were calculated automatically within the software, based on volumes and tissue density (of 1,050 kg/m3). Muscles were represented by 110 spring elements positioned according to observations of dissected material (Curtis et al.,2009,2010c; Jones et al.,2009a). These included eight elements representing the m. depressor mandibulae, 48 representing the external adductors, 10 representing the posterior adductors, and 44 representing the internal adductors (Fig. 3B,C).

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Figure 3. The multibody model. (A) The model of the lower jaw showing the position of the anterior constraint. (B and C) The muscle representation in (B) oblique dorsolateral view and (C) oblique ventrolateral view.

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Vertical and horizontal movement components of a biting cycle, comparable to that discussed in Gorniak et al. (1982), were assigned to motion markers within the multibody software. Following the dynamic geometric optimization (DGO) method (Curtis et al.,2010a,c), the muscles were activated so as to move the lower jaws along the motion path observed in captive living animals (Farlow,1975; Gorniak et al.,1982; personal observation). Thus, DGO varies the force within each individual muscle “spring,” based on its instantaneous orientation to move the lower jaws in line with the desired motion markers (see Curtis et al.,2010a for a more comprehensive explanation of this method). This muscle activation method does not constrain the movements of the two lower jaws in relation to one another. These movements are instead influenced primarily by the constraint at the mandibular symphysis and the contact geometries within the skull, i.e. the quadrate-articular jaw joints and the teeth. The skull was also fixed in space at the neck during all simulations since these investigations were focused on lower jaw movements only.

Contact was specified between the articulating surfaces of the quadrates on the skull and the articulars of the lower jaws, the pterygoid flanges and coronoid bones, the premaxillary teeth and lower jaw tips, as well as between corresponding teeth. To remove noise from subtle differences between the left and right jaw joints a mirrored version of the right quadrate cotyle and articular was used for the left side. Motion paths defined a movement that aimed to open the lower jaws to a gape of approximately 30 degrees, during which the lower jaws would translate backwards so that the quadrate cotyles contacted the anterior edges of the articular joint surfaces (Fig. 1A) (Supporting Information 1 and 2). The lower jaws would then close while maintaining this joint contact position until the teeth of the upper and lower dentitions came into contact. The motion path then aimed to move the lower jaws forward to replicate the proal shear observed in live animals. To allow the lower jaws to follow the defined motion paths the jaw muscles were activated in an appropriate sequence as defined by the DGO muscle model (Curtis et al.,2010c).

To test the influence of symphysis flexibility on lower jaw kinematics and feeding mechanics in Sphenodon the model was run with three different setups with respect to the anterior mandibular symphysis. Setup 1 assigned a fixed constraint that rigidly attached the two lower jaws and prevented any relative movements between them. Setup 2 assigned a hinged constraint that permitted medial-lateral flaring movements (i.e. rotation about the z-axis only, see Fig. 3), while setup 3 assigned a spherical joint that permitted free rotation about all three axes (i.e. rotation about the x, y, and z axes, see Fig. 3).

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIAL AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. Acknowledgements
  9. LITERATURE CITED
  10. Supporting Information

Tooth Shape

Tooth shape was consistent with previous descriptions (e.g. Robinson,1976; Gorniak et al.,1982; Jones,2008,2009; Jones et al.,2009a,b). The dentary teeth vary in shape according to the degree of wear. Before wear, the main dentary teeth of Sphenodon (the posterior additional teeth) are usually described as resembling smooth anterodorsally directed cones without sharp edges (e.g. Robinson,1976; Reynoso,1996). This observation is usually correct but some Holocene jaws referred to Sphenodon possess dentary teeth that bear true flanges (anterolabially, anterolingually, posterolabially, and posterolingually) and show no sign of wear (Fig. 4B). Wear facets on the dentary teeth first appear on the labial and lingual surfaces and eventually also become apparent on the anterior surface (Reynoso,1996; Jones et al.,2009a,b). This gives worn teeth the appearance of a pyramid with a rectangular base, four definite corners, and an anteriorly located apex (Fig. 4A,B). Further wear leads to the teeth being labiolingually narrower with an anteroposterior crest replacing the apex (Reynoso,1996; Jones et al.,2009a,b). The degree of tooth wear tends to be greater anteriorly because these teeth are older; additional teeth are added to the rear of the jaw bone during growth (Harrison,1901; Robinson,1976). Anteriorly there is also a large conical anterior caniniform tooth within a row of small and usually worn hatchling teeth (Robinson,1976).

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Figure 4. The teeth of Sphenodon. (A) Stereopair of the dentary tooth row in labial, apical and lingual views; (B) stereopair of the two posterior dentary teeth; (C) stereopair of the two upper tooth rows in an articulated specimen; (D) the maxillary tooth row in lingual and labial view; (E) a complete lower jaw in labial view; (F) close up of the anterior alveolar margin in lingual view. (A, B) Specimen SMAG Mackay collection 35; (C) specimen DGPC2; (D) specimen SMAG Mackay collection 54; (E, F) specimen LDUCZ ×146. Scale bar = 5mm.

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The posterior additional maxillary teeth are conical with a posterolingual flange that extends beyond the anterior edge of the following tooth (Fig. 4C,D). The palatine teeth are slightly smaller but are essentially mirror images of the maxillary teeth (Fig. 4C; Robinson,1976): conical with posterolabial flanges. In both the maxillary and palatine teeth there is some alternation in size anteriorly. Wear on the maxillary teeth may be limited to the posterolingual edge or more commonly includes the entire lingual surface (Fig. 4D). Similarly, wear on the palatine teeth can be located at the posterolabial edge but usually includes most, or all, of the labial surface. Wear on opposing maxillary and palatine teeth is often broadly comparable but, as with the dentary teeth, the wear on the anterior teeth is often greater than that on the posteriormost additional teeth (Fig. 4C). The anterior-most dentition of the maxilla may include a large conical caniniform and a group of smaller conical successional teeth. A conical caniniform tooth is also present at the front of the palatine tooth row.

The anterior alveolar margin of the dentary in some individuals is polished (Fig. 4D; e.g. LDUCZ x146; LDUCZ x343; Reynoso,1996), probably from contact with the posterior surface of the chisel-like premaxillary teeth during shearing (Robinson,1976; Jones et al.,2009a). A similar wear facet can be found on the posteroventral surfaces of the premaxillary teeth (e.g. LDUCZ x036). As previously described and figured, the palatine tooth row is near-parallel with the longer tooth row of the maxilla (e.g. Fig. 4C; Robinson,1976; Gorniak et al.,1982; Jones et al.,2009). The gap between the upper tooth rows (“groove” of Robinson,1976; “trough” of Gorniak et al.,1982) is about 1.5 mm wide, wider than the labiolingual dimensions of the dentary tooth bases, which tend to be closer to 1 mm (LDUCZ x036; Jones2009).

The Symphysis of the Lower Jaw

The osteological component of the lower jaw symphysis is located at the anteromedial end of the dentary associated with a small ventral chin-like projection. It is comma-shaped with a smooth medial surface (Fig. 5A) and lies ventral to a notch at the anterior tip of the jaw (Fig. 5B; Jones et al.,2009a). According to Robinson (1976) ligamentous soft tissues span the gap between the right and left notches, as well as the short gap beneath the symphysis. The Meckelian groove runs along the lingual surface of the dentary just above the ventral margin and terminates at the posteroventral boundary of the symphysis (Fig. 5A). Overall it appears as though that the lower part of the symphysis would be more rigid than the upper part.

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Figure 5. The osteological component of the symphysis in an adult Sphenodon. (A) Medial view of the right dentary of specimen LDUCZ x146 (reversed). (B) Anterior view of a CT model based on the lower jaws of LDUCZ x036. The ventral margins are asymmetric because of a local pathology on the right ramus (previously figured in Jones and Lappin, 2010). Scale bars = 2 mm in (A) and 10 mm in (B).

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Articular and Quadrate Articulation

Although the articulation surface at the base of the quadrate has been referred to as a condyle (e.g. Jones et al.,2009a) it is probably better referred to as a cotyle. It is bilobate in posterior view with the medial lobe being slightly larger and extending further ventrally (Fig. 6A,B). The articulating surface of the articular is somewhat saddle-shaped, comprising a long rounded ridge laterally and a convex depression medially (Fig. 6D,E). These features are oriented along a similar axis to the dorsal process of the surangular, coronoid process, and tooth row, and are both approximately twice the length of the surface on the quadrate cotyle. The convex depression of the articular narrows anteriorly so that contact between the articular and quadrate is greatest at the end of the proal shear phase, just before the jaws open.

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Figure 6. The jaw joint in an adult Sphenodon (LDUCZ x036). (A) A posterior view of the skull. (B,C) The quadrate cotyle in (B) posterior and (C) ventral view. (C, D) The posterior part of the lower jaw in (D) posterior and (E) dorsal view. Each layer of the contour models is 0.48 mm thick. Scale bars in (A) = 10 mm and (B–E) = 5 mm.

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The Coronoid and Pterygoid-Flange

The pterygoid flange is formed by the lateral process of the pterygoid and the ventral process of the ectopterygoid and is located at the posterolateral corner of the palate (Günther,1867; Jones et al.,2009a,2011). At least in large adult specimens (skull length = >45 mm) it projects further ventrally than either the premaxillary tooth or quadrate cotyle (Fig. 2; e.g. DGPC 2, LDUCZ x036). The lateral surface is very subtly convex so that the ventral most tip is slightly medially inclined. The coronoid is a large essentially flat bone that contributes to the medial surface of the lower jaw posterior to the tooth row and anterior to the adductor fossa (Günther,1867; Jones et al.,2009a). The lateral surface of the coronoid contacts the dentary whereas its ventral end meets the angular anteriorly and prearticular posteriorly. Posteriorly the coronoid bifurcates and envelops the lateral process of the surangular. In medial view the pterygoid flange and medial face are most closely aligned when the jaws are closed and the quadrate cotyles are positioned on the posterior ends of the articular surfaces. At this point the pterygoid flange extends ventral to the coronoid bone, adjacent to the prearticular and angular (e.g. DGPC2).

Multibody Dynamics Model

Jaw movement, as predicted by MDA, was notably different for each of the three symphysial setups. The fixed constraint (setup 1) restricted jaw movement considerably. During proal shearing only 1 mm of anterior movement is possible and gape is constrained to about 10 degrees (Supporting Information 3). This is due to the geometric constraints between the two conforming surfaces of the jaw joint. During jaw opening the medial lobe of the quadrate cotyle prevents posterior movement of the lateral ridge of the articulation surface of the articular.

The hinged constraint (setup 2) restricted rotation of the lower jaws about their long axes, but did permit relative medial-lateral movements between the two lower jaws. During jaw opening the lower jaws slide backwards by approximately 4 mm so that the front of the articulation surface of the articular is located beneath the quadrate cotyle (Supporting Information 4). This position is maintained until the onset of proal shearing. Also, as the jaws open the anterior angle between the lower jaws increases by approximately 4 degrees because the articulars move laterally away from each other as their surfaces pass along the quadrate cotyle. This movement is permitted by the hinged symphysis. During jaw closing the wider angle between the lower jaws is maintained. On closure the lower jaws slide forwards approximately 4 mm and the angle between the lower jaws reduces as they return to their original position.

The spherical constraint (setup 3) behaves somewhat similarly to the hinged constraint (setup 2). During jaw opening there is a comparable 4 mm posterior translation of the lower jaw (Fig. 7A,B) (Supporting Information 5). There is also an increase in the symphysial angle of approximately 4 degrees (Fig. 7C,D). However, in contrast to setup 2, relative movement between the lower jaws is not limited to just one plane. There is also a 10-degree long axis rotation of each of the lower jaws as the lateral ridge of the articular rotates within the groove of the quadrate cotyle (Fig. 7C–H) (Supporting Information 6). As the jaws translate anteriorly during proal shearing the dorsal edge of each jaw rotates medially and the dorsoventral jaw axis becomes more vertical. This in turn brings the anterodorsal tips of the lower jaws closer together (Fig. 8A,B) and also alters the mode of interaction between the lower and upper dentition. At the beginning of the shearing phase, the most intimate shearing contact occurs between the anterolabial flanges on the dentary teeth and posterolingual flanges of the maxillary teeth (Figs. 7E,G and 8E,G), but toward the end of the shearing phase it is between the anterolingual flanges of the dentary teeth and the posterolabial flanges of the palatine teeth (Figs. 7F,H and 8F,H).

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Figure 7. Movement predicted by MDA in the model with a spherical constraint at the symphysis (setup 3). Relative positions of the lower jaws at the (A, C, E, G) beginning, and (B, D, F, H) end of proal jaw movement. (A, B) The skull in lateral view, (C, D) ventral view, (E–H), and dorsal view with a transparent cranium. (G, H) A close up of the left posterior dentary teeth and left palatine tooth row. (A–D) The cranium is transparent but the lower jaws are opaque. (E, F) The right lower jaw and portion of the left dentary are opaque, most of the cranium is transparent but one portion across the palate (including parts of the maxilla, palatine, jugal, and pterygoid) is relatively less transparent. All scale bars = 10 mm.

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Although the medial surface of the lower jaw and the lateral surface of the pterygoid flange are generally in close proximity the flanges do not appear to restrict forwards or backwards movement of the lower jaw in any of the models. Usually the point of closest proximity is between the ventral tip of the flange and the boundary between the coronoid bone and angular, but at the end of the shearing phase in setup 3 it is between the midpoint of the flange and the central part of the coronoid.

DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIAL AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. Acknowledgements
  9. LITERATURE CITED
  10. Supporting Information

Jaw Symphysis Flexibility

The analysis described above using the multibody model of Sphenodon demonstrates that flexibility at the mandibular symphysis is necessary to replicate the jaw movements observed in the living animal. For the lower jaw to move backwards at jaw opening and forwards after jaw closure the saddle-shaped joint surface of the articular has to pass along the labiolingually concave quadrate cotyle. For this to be possible, the symphysial angle between the lower jaws must change. This point can be illustrated by representing the lower jaws as an open triangle with the apex at the mandibular symphysis. The two long edges of this triangle are straddled by two fixed constraints distal to the apex (i.e. the large medial lobes of the quadrate cotyles). For the apex of this triangle to move backwards, the angle between the two long edges must increase and for the tips to move forwards the angle must decrease. Without the potential for symphysial hinging, backwards translation of the lower jaws is restricted and both normal gape and subsequent proal shearing are inhibited. This supports previous inferences that the anterior symphysis is mobile in Sphenodon (Günther,1867; Robinson,1976; Schwenk,2000).

Gorniak et al. (1982; Fig. 6) reported the anterior translational movement of the lower jaw to be about 2.3 mm. As this was recorded from an individual approximately 20% smaller than the one modeled here (see Curtis et al.,2010c), we might expect translational movement in the MDA model to be at least 2.75 mm. This is much greater than the 1 mm permitted by the setup with the fixed symphysis (setup 1) but is easily accommodated by the hinged and spherical joints (setup 2 and setup 3) which both allowed 4 mm of movement. Note, the MDA model lacks ligaments around the jaw joints so that the movements are restricted only by the geometry of the articulating surfaces, as well as the pterygoid flanges and tooth rows. Therefore, the extent of movement exhibited by a model should be viewed as the maximum amount achievable without the presence of soft tissues. Relative movement between the jaws appears to be possible because the symphysis is held together mainly by fibrous connective tissue (Günther,1867; Robinson,1976).

The osteological component of the symphysis in lepidosaurs has received relatively little direct attention although variation clearly exists (Evans et al.,2002; Evans,2008; Zaher et al.,2009). The morphology observed in Sphenodon certainly differs from that of Varanus and many snakes where there is no clear bony symphysial surface (Rieppel and Zaher,2000; Evans,2008; Holliday et al.,2010). Sphenodon also differs from many squamates, including most agamids, pleurodont iguanians, lacertids, skinks, geckos, and Lanthanotus where the bony symphysis tends to be ovoid, dorsally located and without a dorsal notch (e.g. Pregill,1984; Rieppel and Zaher,2000; Evans et al.,2002; Evans,2008; Hollenshead, et al.,2011). Amongst squamates, the greatest similarity to the symphysis of Sphenodon seems to be with certain chameleons (e.g. Chamaeleo) where both a dorsal notch and ventral chin may be present (Čerňanský,2010). Understanding the functional significance of this variation in the bony symphysis requires a more detailed examination of the relationship between anatomy (bone and soft tissues) and mandibular movement.

The soft tissue anatomy of the squamate symphysis has been surveyed by Young (1998; snakes) and Holliday et al. (2010; lizards). Holliday et al. (2010) found that the lizard symphysis was usually divided into dorsal and ventral components. The dorsal part contained a fibrocartilaginous pad and tightly packed parallel fibers whereas the jaws were joined ventrally by more loosely connected woven fibers and, in some taxa, fusion of the left and right Meckel's cartilage. They concluded that intermandibular movement was possible in most squamates with rotation (or hingeing) occurring between the anterodorsal tips of the dentaries. The degree of intermandibular flexibility may be linked to the degree of intracranial flexibility, the most flexible symphyses being found in snakes which also possess intramandibular hinges and highly mobile cranial joints (Young,1998; Lee,1999; Rieppel and Zaher,2000). Sphenodon has little cranial flexibility (Jones et al.,2011) and yet setup 3 of our multibody analysis suggests that rotational movements (around the long axis of the lower jaw) also occur in Sphenodon. However, in contrast to lizards the centre of rotation is located anteroventrally rather than anterodorsally (Figs. 8–10). The notched upper part of the symphysis, supported by soft tissue, splays during jaw opening and retraction but closes slightly during jaw protraction (proal movement) (Figs. 8A,B and 9D,H,L). A detailed histological examination of the symphysial joint is required to assess the exact nature of the fibers in Sphenodon and to determine how they may be related to these movements.

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Figure 8. Movement predicted by MDA by the model with a spherical constraint at the symphysis (setup 3). Relative positions of the lower jaws at the (A, C, E, G) beginning, and (B, D, F, H) end of proal jaw movement. (A, B) The skull in anterior view and (C–F) anterolateral view. (G, H) A close up of the left posterior dentary teeth and left palatine tooth row in cross-section. (A, B) The cranium is transparent but the lower jaws are opaque. (E–H) Most of the cranium is transparent whereas the entire right lower jaw and a portion of the left dentary and cranium (including parts of the maxilla, palatine, jugal, and pterygoid) are opaque. All scale bars = 10 mm.

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Figure 9. Schematic summary diagram of the lower jaw movements in Sphenodon as suggested by the MDA model with greatest freedom for the quadrate to follow the articulation surface of the articular (setup 3). (A) The skull in lateral view. Relative positions of the feeding apparatus at the (B–E) beginning, (F–I) middle, and (J–M) end of proal shearing: (B, F, J) the articular relative to the quadrate cotyle, (C, G, K) dentary tooth rows relative to the upper tooth rows; (D, H, L) the right and left tips of the lower jaws; (E, I, M) the long axes of the right and left lower jaws (intermandiblar angle).

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Figure 10. A schematic diagram illustrating the changes in the position of the tooth blades during shearing in Sphenodon. (A) At jaw closure and the start of the shearing phase. (B) At the end of the shearing phase. Maxillary, palatine, and dentary teeth are shown in ventral view but the dentary teeth are shown as if semitransparent.

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Although the Meckelian cartilages are fused anteriorly in the Sphenodon embryo (de Beer,1937; Schwenk,2000), this is apparently not the case in adults (Günther,1867). Holliday et al. (2010) suggested that fused Meckel's cartilages stabilized the joint between the lower jaws in squamates such as iguanians and geckos that use their tongue for prey capture or drinking, respectively (although a more apomorphic behavior in geckos may be eye licking, Daza, personal communication, March 2012). As Sphenodon uses its tongue for prey capture (Gorniak et al.,1982; Schwenk,2000) it does not fit this pattern. Flexibility of the symphysis in Sphenodon has implications for jaw mechanics during unilateral biting (Schwenk,2000; Evans,2008) which is known to occur in this genus (Gorniak et al.,1982; Curtis et al.,2010a). This is because compliance between the jaws would inhibit the transfer of forces between the working and balancing sides (Crompton and Hylander,1986; Holliday et al.,2010). The frequency and importance of unilateral biting in other lepidosaurs has yet to be systematically surveyed.

Shearing in Sphenodon

The lower jaws of Sphenodon are analogous to a serrated blade characterized by a series of high and low points that fragment compliant material such as food by “gripping and ripping” (Abler,1992). During jaw closure, penetration of food material is made easier by the blades running along the apicobasal axis of the teeth and near-parallel to the arc of jaw closure (Freeman and Leman,2006; Jones,2009). Some food is also cut because the blades on the lower and upper jaw meet obliquely with different approach angles (Evans and Sanson,2003). The arrangement of the teeth (in series) provides a series of notches for trapping compliant food as found in mammalian carnassial teeth (Butler1946; Lucas and Luke,1984; Abler,1992; Evans and Sanson,2003; Anderson and LaBarbera,2008; Anderson,2009). Food that is not cut is gripped and held. During proal shearing, trapped food is cut (or ripped) between the anterior blades on the dentary teeth and posteroventral blades on the upper dentition. For such a draw-cutting system to be effective there is no need for the horizontal (forward) motion to be greater than the distance between the blades as once the blades have moved this distance there should (in theory) be nothing left to cut (Frazzetta,1988; Abler,1992). When the blades are subject to wear and the material to be cut is heterogeneous the situation can be more complex. Nevertheless, the distance that the lower jaws move forward during proal shearing (about 2–3 mm) corresponds with the length of most marginal teeth and hence the distance between the cutting edges on each tooth (e.g. Jones,2009).

There is obvious disagreement as to the sophistication of the shearing mechanism in Sphenodon. In a review of food processing, Reilly et al. (2001) described it as “formidable” and “one of the best shearing jaws in amniotes.” By contrast, Robinson (1976) characterized occlusion in Sphenodon as “poor” and Gorniak et al. (1982; p 345) stated that Sphenodon lacked occlusion comparable to mammals, speculating (1982; p 352) that tooth wear was “as likely to reflect” food-on-tooth wear as tooth-on-tooth wear. The results of our analyses question these latter assertions. Although the gap between the upper teeth is larger than the labiolingual dimensions of the dentary teeth, the orientation of the dentary teeth within the gap may change dynamically during jaw movement.

The MDA model with the spherical joint (setup 3) permits the greatest flexibility, thus allowing the articulation surface of the articulars to follow the contours of the quadrate cotyle without restriction. During proal shearing, the lower jaws also undergo a long axis rotation that engenders a subtle dynamic form of occlusion between the dentary, palatine, and maxillary teeth (at least at the rear of the jaws). As the jaws close the anterolabial flanges on the dentary teeth cut against the posterolingual flanges of the maxillary teeth whereas toward the end of the shearing phase the anterolingual flanges of the dentary teeth cut against the posterolabial flanges of the palatine teeth. In life this would promote close contact between opposed blades and enhance the shearing action by focusing the cutting force between particular blades in turn (Figs. 8G,H, 9, and 10) (Lucas and Luke,1984; Evans and Sanson,2003). That Gorniak et al. (1982) did not note these movements may simply reflect the difficulty of perceiving subtle intracranial movements in a relatively small living animal, particularly when those movements may be masked by the skin and other soft tissues.

As mentioned above, shearing mechanisms can be disrupted by heterogeneous material that offers uneven resistance, leading to irregular movements of the cutting tools. Such problems may be reduced by stabilizing or compensatory movements, in this case controlled by modifications to muscle activity (Curtis et al.,2010a), but also through physical constraints (in addition to those of the jaw articulation). The short distance between the pterygoid flange and medial surface of the lower jaw supports the hypothesis that the pterygoid flange acts as a brace to limit medial displacement of the lower jaw (Fig. 11; Iordansky,1964; Taylor,1992; Jones et al.,2011; Porro et al.,2011). Therefore, as well as being important for dealing with struggling prey this medial buttress may also help guide the jaws and ensure smoother shearing of heterogeneous food material. It is possible that the convex lateral surface of the pterygoid flange is shaped to maintain a consistent relationship with the flat surface of the coronoid during the 10-degree long axis rotation of the lower jaw (Figs. 9C,G,K and 11B,D) during shearing. The closer anteroposterior alignment of the coronoid and pterygoid flange just before jaw opening suggests that this is the time when guidance or support from the flange is most important (Fig. 10C,D). Nevertheless, the ventral extent of both the flange and coronoid bone ensure support is also provided at jaw closure and during shearing (Fig. 11A,B). The large chisel-like teeth may also serve as a constraint to jaw movement providing an anterior obstruction to the jaw tips as well as helping to retain food in the mouth. The wear facets on the dentaries and premaxillary chisel-like teeth demonstrate that contact certainly occurs between these elements.

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Figure 11. A schematic diagram illustrating the relationship between the pterygoid flange and coronoid process based on results from setup 3. (A, B) At jaw closure and at the start of the shearing phase. (C, D) At the end of the shearing phase. In medial view (A and C) and anterior view (B and D). Of the cranium (light grey) only parts of the palatine, pterygoid, ectopterygoid, and quadrate are visible. Asterisk on the pterygoid flange indicates point of closest proximity. Scale bar = 10 mm.

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Oral Food Processing

Oral food processing is particularly complex in mammals and involves an integration of elaborate dentitions, three-dimensional occlusion, and highly rhythmic chewing strokes (e.g. Hiiemäe and Crompton,1985; Evans and Sanson,2003; Ross et al.,2007a,b,2010). Thus, although lepidosaurs are considered to “chew” it has been argued that the term “mastication” should be restricted to mammals (Ross et al.,2007a; p 133). Because the most sophisticated oral food processing is found in mammals it has been strongly linked to the evolution of endothermy or at least the maintenance of a high metabolic rate and activity level (e.g. Lumsden and Osborn,1977; Lucas and Luke1984; Crompton and Hylander,1986; Reilly et al.,2001; Kemp,2005; Fritz et al.,2010; see also footnotes 1 and 2). In a review of lepidosaur feeding, Herrel et al. (2001) wrote that “a true mammalian-like power stroke” is found only in Sphenodon. However, Sphenodon does not have a particularly high metabolic rate (Thompson and Daugherty,1998) and it is generally considered to be a sit-and-wait predator (e.g. McBrayer and Reilly,2002). Although Sphenodon does not “comminute” food to the same extent as many mammals, it certainly does process food to a greater degree than other lepidosaurs, including squamates such as Varanus that are considered to be particularly active (Schwenk,2000; Clemente et al.,2009). This suggests the link between food processing and high metabolism (and certainly endothermy) has been overstated.

Oral food processing is advantageous for at least three reasons besides facilitating endothermy. First, it increases the surface area available for chemical breakdown (Bjorndal et al.,1990; Reilly et al.,2001). This in turn allows more efficient digestion and reduces the length of intestines or gut passage time needed to digest the same amount of food (Lucas and Luke,1984). Surface coatings and internal structures that may be resistant to chemical breakdown can be opened or fractured mechanically (Hiiemäe and Crompton,1985; Lucas,2004). This is particularly important for herbivores and, as a result, food processing is also associated with increased omnivory and herbivory (e.g. Throckmorton,1976; Throckmorton et al.,1981; Hiiemäe and Crompton,1985; Bjorndal et al.,1990; Modesto,1995; Sues and Reisz,1998; Barrett,2000; Reilly et al.,2001; Cooper and Vitt,2002; Barrett and Upchurch,2007; Upchurch et al.,2007). Although plant material can represent 14% of the material in Sphenodon scats its intake is probably accidental during prey capture (Walls,1981; Cooper and Vitt,2002). Second, oral processing allows tighter food packing as spaces within the food item are compressed. In addition, a limited space can accommodate a greater volume of material if that material is heterogeneous rather than homogenous in shape and size (Beckett,2000; p 72). This again reduces the length of intestine required to deal with the same food intake. Finally, oral processing allows small pieces to be removed from a larger food item so that they fit inside the mouth and can be swallowed. This allows access to larger food items (Robinson,1973; Lucas,2004; Jones,2008). All three factors help an animal when food is limited, either by allowing it to make the most of the food that is available or by widening dietary range.

Robinson (1973) discussed shearing in Sphenodon (and other rhynchocephalians) as a means of accessing large food items. She referred to cranial kinesis in squamates as an alternate strategy to the same ends. Whether kinesis in squamates is linked to feeding on large food items is contentious (Schwenk,2000; Metzger,2002; Evans,2008) and Sphenodon mainly eats small or medium sized arthropods (Walls,1978,1981; Ussher,1999). However, “average,” “modal,” or “preferred” diet is not necessarily useful for interpreting the relationship between form and function because diet may change at times of hardship when selection pressures are at their greatest (Grant and Grant,1993; Robinson and Sloan Wilson,1998). Large adult Sphenodon are certainly known to eat vertebrate material (notably seabird chicks), particularly during periods when other sources of nutrients and water are scarce (Walls,1978,1981). Sphenodon populations have probably only been restricted to their current habitus for the past few hundred years (Hay et al.,2003) and it is unlikely that Sphenodon or its ancestral lineage evolved alongside sea birds (Crook,1975). However, the ability to take a range of prey would have been advantageous in any resource challenged environment (Evans and Jones,2010; Apesteguía and Jones,2012). Sphenodon provides an example in which specialization of the feeding mechanism appears to permit a broader diet (Pregill,1984).

Evolutionary Perspective

Historically, Sphenodon was considered to be representative of the ancestral reptilian condition (e.g. Williston,1917; Crook,1975) and Robb (1977) referred to Sphenodon as the “most primitive and unspecialized reptile in existence.” However, more recent research contradicts this (e.g. Gorniak et al.,1982; Gans,1983; Whiteside,1986; Thompson and Daugherty,1998; Evans,2003; Jones,2006,2008,2009; Jones et al.,2009a,2011; O'Meally et al.,2009; Evans and Jones,2010). The level of sophistication observed in the feeding mechanism described here further demonstrates that Sphenodon is not a generalized amniote: it is the only living amniote to possess a feeding mechanism that involves a propalinal (or proal) power stroke and bladed teeth on both the maxilla and palatine (Schwenk,2000; Reilly et al.,2002). However, Sphenodon is also the only living member of the Rhynchocephalia (the sister taxon to Squamata, Evans,2003; Rest et al.,2003), with all other named genera known exclusively from the Mesozoic (Jones,2008; Evans and Jones,2010).

Several anatomical features associated with the Sphenodon-mode of shearing are found in its Mesozoic fossil relatives (Fig. 12). The enlarged palatine tooth row is present in all Rhynchocephalia and represents a diagnostic character for the clade (Evans,2003; Jones,2008). The elongate articulation surface of the articular is found in the most plesiomorphic members of the clade such as Diphydontosaurus and Gephyrosaurus from the Late Triassic and Early Jurassic of England and Wales respectively (Evans,1980; Fraser,1982; Whiteside,1986; Jones,2008), as well as in herbivorous eilenodontines from the Late Jurassic and Early Cretaceous of North America (Throckmorton et al.,1981; Rasmussen and Callison,1981; Reynoso,1996; Foster,2003; Apesteguía and Novas,2003). However, some derived taxa such as Clevosaurus hudsoni (Triassic, UK, Fraser,1988) and possibly the pleurosaur Palaeopleurosaurus (Late Jurassic, Europe, Carroll,1985) have a short articulation surface on the articular indicative of a different feeding mode.

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Figure 12. A simplified cladogram of Rhynchocephalia plotted against time. Black bars represent the known fossil record, grey bars represent ghost ranges, faded grey bars indicate uncertain ghost ranges, and white bars indicate ghost lineages. The status of three characters associated with proal shearing found in Sphenodon are plotted next to taxa. A filled circle indicates state present, a line indicates absent, and a question mark indicates unknown. Clade names: A = Lepidosauria; B = Rhynchocephalia; C = derived rhynchocephalians; D = Sphenodontinae. Information taken from Evans (1980,1990); Rasmussen and Callison (1981); Throckmorton et al. (1981); Fraser (1982,1988); Carroll (1985); Carroll and Wild (1994); Reynoso (1993,1996,2005); Evans et al. (2001,2002); Apesteguía and Novas (2003); Jones (2008); Evans and Borsuk-Bialynicka, 2009; Jones et al. (2009a,b). Please note that Tikiguania is no longer considered to represent a Late Triassic squamate (Hutchinson et al., in press), thus making material from the Early Jurassic of India potentially the oldest record for this clade (Evans et al.,2002).

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In Sphenodon the complete lower temporal bar probably serves to brace the quadrate and it has thus been considered associated with the proal shearing in this taxon (e.g. Whiteside,1986). However, Gephyrosaurus which lacks a complete temporal bar demonstrates that it is not essential for proal jaw movement (Evans,1980; Jones,2008). Similarly, Clevosaurus and the fossil squamate Tianyusaurus show that a complete bar may be present when proal jaw movement is not permitted by the jaw articulation (Fraser,1988; Mo et al.,2010; Jones and Lappin, 2010). The majority of fossil Rhynchocephalia for which skull material is known lack a complete lower temporal bar (Jones,2008).

The structure of the symphysis is highly variable within Rhynchocephalia (Evans et al.,2002). In the most plesiomorphic taxa, it is relatively large and has a posterior cleft that may have housed an anterior extension of Meckel's cartilage (Evans,1980,2008; Holliday et al.,2010). A somewhat similar symphysis is also found in Cynosphenodon and Sphenovipera from the Early Jurassic of Mexico (Reynoso,1996,2005) whereas Clevosaurus and eilenodontines lack a cleft but the symphysis is deep (Throckmorton et al.,1981; Fraser,1988). Presumably both of these arrangements would constrain mobility between the lower jaws. Other Mesozoic rhynchocephalians possess a notched symphysis which may have conferred greater flexibility, like that of Sphenodon. These genera include Rebbanasaurus and Godivarisaurus from the Jurassic of India (Evans et al.,2001); Opisthias from the Jurassic of North America and, reportedly, Mexico, and from the Early Cretaceous of the UK (Throckmorton et al.,1981; Evans and Fraser,1992; Reynoso,1993).

The teeth of the most plesiomorphic taxa are conical or columnar and lack obvious flanges (Evans,1980; Whiteside,1986; Jones,2009). Therefore, although the most plesiomorphic Triassic rhynchocephalians probably used some form of propalinal movement during food processing, they lacked the dental and symphysial specializations found in Sphenodon. More derived taxa possess stouter teeth (Jones,2008,2009) with blades or flanges arranged in a variety of ways (e.g. Throckmorton et al.,1981; Fraser,1986,1988; Jones2009). Taxa with teeth and wear facets most similar to those of Sphenodon include Cynosphenodon and Sphenovipera (Reynoso,1996,2005; Jones,2006,2009); Godivarisaurus (Evans et al.,2001); Opisthias (Throckmorton et al.,1981); and an unnamed form from the Middle Jurassic of the UK (Evans,1992). These animals are known almost exclusively from partial jaw material. Nevertheless, they demonstrate that although proal shearing is rare today, a similar kind of food processing was likely more widespread in the Jurassic and may have become established in the lineage leading to Sphenodon as long as 190 million years ago.

CONCLUSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIAL AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. Acknowledgements
  9. LITERATURE CITED
  10. Supporting Information

Using a multibody dynamics computer model we show that flexibility at the mandibular symphysis in Sphenodon is essential for proal shearing to occur. This flexibility allows the jaws to move backwards during jaw opening and forwards after jaw closure. Concomitantly the intermandibular angle increases and decreases. The model with most flexibility at the symphysis, and therefore also the model with the most freedom at the quadrate-articular joint, suggests that long axis rotation of each mandibular ramus facilitates tooth-on-tooth shearing, initially between the dentary and maxillary teeth and later between the dentary and palatine teeth. By localizing the cutting action of the teeth the effectiveness of the processing is maximized. These observations clearly demonstrate that complex oral food processing can be found in some nonmammalian ectothermic amniotes. Moreover, although a proal mode of shearing is today restricted to Sphenodon, the fossil record of Rhynchocephalia suggests that this type of oral food processing was more common during the Mesozoic and that relatively sophisticated oral food processing was the norm rather than the exception in this clade. Such food processing may have been advantageous in environments where food availability was unpredictable, as may be the case for Sphenodon today.

Acknowledgements

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIAL AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. Acknowledgements
  9. LITERATURE CITED
  10. Supporting Information

For CT scanning of LDUCZ x036 the authors thank Sue Taft (University of Hull). For the opportunity to observe feeding in live Sphenodon, the authors thank Ruston Hartegan (Dallas Zoo) and Richard Gibson and Isolde McGeorge (Chester Zoo). For access to skeletal material the authors thank Jack Ashby, Mark Carnall, Emma-Louise Nicholls (all of the Grant Museum of Zoology, UCL), Colin McCarthy, David Gower (both of the Natural History Museum, London), and Jennifer Hay (formerly Massey University, Auckland), and Lindsay Hazley (Southland Museum and Art Gallery, Invercargill, New Zealand). A Sylvester Bradley (Palaeontological Association) award to Marc E. H. Jones helped support a data collection trip to New Zealand. We also thank Juan D. Daza (Villanova University, USA), Casey M. Holliday (University of Missouri), and one anonymous reviewer for helpful comments that improved the manuscript.

  • 1

    The pressence of endothermy in birds that lack extensive oral food processing is excused because of the internal food processing performed by the gizzard (Reilly et al., 2001).

  • 2

    Abler (1992) also speculated that the more complex jaw movements involved in sophisticated oral food processing might also be linked to the evolution of mammalian intelligence. Despite possessing jaw movement that is relatively more complex than many non-avian reptiles tuatara appear to be no more intelligent (Northcutt and Heath, 1973).

LITERATURE CITED

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIAL AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. Acknowledgements
  9. LITERATURE CITED
  10. Supporting Information
  • Abler WL. 1992. The serrated teeth of tyrannosaurid dinosaurs, and biting structures in other animals. Paleobiology 18: 161183.
  • Apesteguía S, Novas FE. 2003. Large Cretaceous sphenodontian from Patagonia provides insight into lepidosaur evolution in Gondwana. Nature 425: 609612.
  • Apesteguía S, Jones MEH. 2012. A Late Cretaceous “tuatara” (Lepidosauria: Sphenodontinae) from South America. Cretac Res 34: 154160.
  • Anderson PSL. 2009. The effects of trapping and blade angle of notched dentitions on fracture of biological tissues. J Exp Biol 212: 36273632.
  • Anderson PSL, LaBarbera M. 2008. Functional consequences of tooth design: effects of blade shape on energetics of cutting. J Exp Biol 211: 36193626.
  • Barrett PM. 2000. Prosauropods and iguanas: speculation on the diets of extinct reptiles. In: Sues, H-D, editor. Evolution of herbivory in terrestrial vertebrates. Cambridge: Cambridge University Press. p 4278.
  • Barrett PM, Upchurch P. 2007. The evolution of feeding mechanisms in early sauropodomorph dinosaurs. Sp Pap Palaeontol 77: 91112.
  • de Beer 1937. The development of the vertebrate skull. Oxford: Oxford University Press.
  • Beckett ST. 2000. The science of chocolate. Cambridge: RSC Paperbacks.
  • Besson AA, Cree A. 2010. Integrating physiology into conservation: an approach to help guide translocation of a rare reptile in a warming environment. Anim Conserv 14:2837.
  • Bjorndal KA, Bolten AB, Moore JE. 1990. Digestive fermentation in herbivores: effect of food particle size. Phys Zool 63: 710721.
  • Butler PM. 1946. The evolution of carnassial dentitions in the Mammalia. Proc Zool Soc Lond 116: 198220.
  • Carroll RL. 1985. A pleurosaur from the lower Jurassic and the taxonomic position of the Sphenodontida. Palaeontol Abt A 189: 128.
  • Carroll RC, Wild R. 1994. Marine members of the Sphenodontia. In: Fraser NC, Sues H-D, editors. In the shadow of the dinosaurs: early Mesozoic tetrapods. Cambridge: Cambridge University Press. p 7083.
  • Cartland-Shaw LK, Cree A, Skeaff CM, Grimmond NM. 1998. Differences in dietary and plasma fatty acids between wild and captive populations of a rare reptile (the tuatara. Sphenodon punctatus). J Comp Physiol B 168: 569580.
  • Čerňanský A. 2010. A revision of chamaeleonids from the Lower Miocene of the Czech Republic with description of a new species of Chamaeleo (Squamata, Chamaeleonidae). Geobios 43: 605613.
  • CITES. 2011 Appendices I, II and III. Available at: http://www.cites.org/eng/app/appendices.pdf. Last accessed on 22 December 2011.
  • Clemente CJ, Withers PC, Thompson GG. 2009. Metabolic rate and endurance capacity in Australian varanid lizards (Squamata: Varanidae: Varanus). Biol J Linn Soc 97: 664676.
  • Cooper WE, Vitt LJJr. 2002. Distribution, extent, and evolution of plant consumption by lizards. J Zool Lond 257: 487517.
  • Cree A, Lyon GL, Cartland Shaw L, Tyrrel C. 1999. Stable isotope ratios as indicators of marine versus terrestrial inputs to the diets of wild and captive tuatara (Sphenodon punctatus). NZ J Zool 26: 243253.
  • Crompton AW, Hylander WL. 1986. Changes in mandibular function following the acquisition of a dentary-squamosal jaw articulation. In: Hotton NIII, Mchean P, Roth J, Roth E, editors. The ecology and biology of mammal-like reptiles. Washington: Smithsonian Institute. p 263282.
  • Crook IG. 1975. The tuatara. In: Kuschel G, editor. Biogeography and ecology in New Zealand. New Zealand: Junk. p 331352.
  • Curtis N. 2011. Craniofacial biomechanics: an overview of recent multibody modelling studies. J Anat 218: 1625.
  • Curtis N, Jones MEH, Evans SE, O'Higgins P, Fagan MJ. 2009. Visualising muscle anatomy using three-dimensional computer models—an example using the head and neck muscles of Sphenodon. Palaeontologia Electr 123.7T: 118.
  • Curtis N, Jones MEH, Evans SE, O'Higgins P, Fagan MJ. 2010a. Feedback control from the jaw joints during biting: an investigation of the reptile Sphenodon using multibody modelling. J Biomech 43: 31323137.
  • Curtis N, Jones MEH, Evans SE, Shi J, O'Higgins P, Fagan MJ. 2010b. Predicting muscle activation patterns from motion and anatomy: Modelling the skull of Sphenodon. R Soc Interface 7: 153160.
  • Curtis N, Jones MEH, Lappin AK, Evans SE, O'Higgins P, Fagan MJ. 2010c. Comparison between in vivo and theoretical bite performance: using multi-body modelling to predict muscle and bite forces in a reptile skull. J Biomech 43: 28042809.
  • Curtis N, Jones MEH, Shi J, O'Higgins P, Evans SE, Fagan MJ. 2011. Functional relationship between skull form and feeding mechanics in Sphenodon, and implications for diapsid skull development. PLoS One 6: e29804.
  • Curtis N, Kupczik K, O'Higgins P, Moazen M, Fagan M. 2008. Predicting skull loading: applying multibody dynamics analysis to a macaque skull. Anat Rec 291: 491501.
  • Dawbin WH. 1982. The tuatara Sphenodon punctatus (Reptilia: Rhynchocephalia): a review. In: Newman DG, editor. New Zealand herpetology. New Zealand: Wildlife Service Occasional Publications 2. p 149181.
  • De Vree F, Gans C. 1989. Functional morphology of the feeding mechanisms in lower tetrapods. Fortschritte der Zool 35: 115127.
  • Evans AR, Sanson GD. 2003. The tooth of perfection: functional and spatial constraints on mammalian tooth shape. Biol J Linn Soc 78: 173191
  • Evans SE. 1980. The skull of a new eosuchian reptile from the Lower Jurassic of South Wales. Zool J Linn Soc 70: 203264.
  • Evans SE. 1992. A sphenodontian (Reptilia: Lepidosauria) from the Middle Jurassic of England. Neues Jahrb Geol Paläontol Abh 1992: 449457.
  • Evans SE. 2003. At the feet of the dinosaurs: the early history and radiation of lizards. Biol Rev 78: 513551.
  • Evans SE. 2008. The skull of lizards and tuatara. In: Gans C, Gaunt AS, Adler K, editors. Biology of the reptilia. Vol. 20, Morphology H: The skull of Lepidosauria. Ithaca, New York: Society for the Study of Amphibians and Reptiles. p 1344.
  • Evans SE, Borsuk-Bialynicka M. 2009. A small lepidosauromorph reptile from the Early Triassic of Poland. Palaeontol Pol 65: 179202.
  • Evans SE, Fraser NC. 1992. A sphenodontid jaw (Reptilia: Lepidosauria) from the Upper Jurassic of Dorset. Proc Dorset Nat Hist Soc 1992: 199200.
  • Evans SE, Prasad GVR, Manhas BK. 2001. Rhynchocephalia (Diapsida: Lepidosauria) from the Jurassic Kota Formation of India. Zool J Linn Soc 133: 309334.
  • Evans SE, Prasad GVR, Manhas BK. 2002. Fossil lizards from the Jurassic Kota formation of India. J Vertebr Paleontol 22: 299312.
  • Evans SE, Jones MEH. 2010. The origin, early history and diversification of lepidosauromorph reptiles. In: Bandyopadhyay S, editor. New aspects of Mesozoic biodiversity, 27 Lecture notes in earth sciences 132. London: Springer. p 2744.
  • Farlow JO. 1975. Observation on a captive tuatara (Sphenodon punctatum). J Herpetol 9: 353355.
  • Foster JR. 2003. New specimens of Eilenodon (Reptilia, Sphenodontia) from the Morrison formation (Upper Jurassic) of Colorado and Utah. BYU Geol Stud 47: 1722.
  • Fraser NC. 1982. A new rhynchocephalian from the British Upper Trias. Palaeontology 25: 709725.
  • Fraser NC. 1986. New Triassic sphenodontids from South West England and a review of their classification. Palaeontology 29: 165186.
  • Fraser NC. 1988. The osteology and relationships of Clevosaurus (Reptilia: Sphenodontida). Philos Trans R Soc Lond B Biol Sci 321: 125178.
  • Frazzetta TH. 1988. The mechanics of cutting and the form of shark teeth (Chondrichthyes, Elasmobranchii). Zoomorphology 108: 93107.
  • Freeman PW, Lemen C. 2006. Puncturing ability of idealized canine teeth: edged and non-edged shanks. J Zool 269: 5156.
  • Fritz J, Hummel J, Kienzle E, Streich WJ, Caluss M. 2010. To chew or not to chew: fecal particle size in herbivorous reptiles and mammals. J Exp Zool 313: 579586.
  • Gans C. 1983. Is Sphenodon punctatus a maladapted relic? In: Rhodin AGJ, Miyata K, editors. Advances in herpetology and evolutionary biology. Cambridge, MA: Harvard University Press. p 613620.
  • Gorniak GC, Rosenberg HI, Gans C. 1982. Mastication in the Tuatara, Sphenodon punctatus (Reptilia: Rhynchocephalia): Structure and activity of the motor system. J Morphol 171: 321353.
  • Grant BR, Grant PR. 1993. Evolution of Darwin's finches caused by a rare climatic event. Proc R Soc B 251: 111117.
  • Gray JE. 1931. Note on a particular structure in the head of an Agama. Zool Misc 1: 1314.
  • Günther A. 1867. Contribution to the anatomy of Hatteria (Rhynchocephalus, Owen). Philos Trans R Soc Lond 157: 134.
  • Hay JM, Daugherty CH, Cree A, Maxson LR. 2003. Low genetic divergence obscures phylogeny among populations of Sphenodon, remnant of an ancient reptile lineage. Mol Phylogenet Evol 29: 119.
  • Hay JM, Sarre SD, Lambert DM, Allendorf FW, Daughery CH. 2010. Genetic diversity and taxonomy: a reassessment of species designation in tuatara (Sphenodon: Reptilia). Conserv Genet 11: 10631081.
  • Hiiemäe KM, Crompton AW. 1985. Mastication, food transport and swallowing. In: Hildebrand M, Bramble DM, Liem KF, Wake DB, editors. Functional vertebrate morphology. Harvard: Belknap Press of Harvard University. p 262290.
  • Harrison HS. 1901. Development and succession of the teeth in Hatteria punctata. Q J Microsc Sci 44: 161213.
  • Herrel A, Meyers JJ, Nishikawa KC, De Vree F. 2001. The evolution of feeding motor patterns in lizards: modulatory complexity and possible constraints. Am Zool 41: 13111320.
  • Howes GB, Swinnerton HH. 1901. On the development of the skeleton of the tuatara, Sphenodon punctatus; with remarks on the egg, on the hatchling, and on the hatched young. Trans Zool Soc London 16: 186.
  • Hollenshead MG, Mead JI, Swift SL. 2011. Late Pleistocene Egernia group skinks (Squamata: Scincidae) from Devils Lair, Western Australia. Alcheringa 35: 3151.
  • Holliday C, Gardner N, Paesani S, Douthitt M, Ratliff J. 2010. Microanatomy of the mandibular symphysis in lizards. Anat Rec 293: 13501359.
  • Hutchinson MN, Skinner A, Lee MSY. 2012 Tikiguania and the antiquitiy of squamate reptiles (lizards and snakes). Biol Lett, doi: 10.1098/rsbl.2011.1216.
  • Iordansky NN. 1964. The jaw muscles of the crocodiles and some relating structures of the crocodilian skull. Anat Anz 115: 256280.
  • Jones MEH. 2006. Tooth diversity and function in the Rhynchocephalia (Diapsida: Lepidosauria). In: Barrett PM, Evans SE, editors. Ninth International Symposium on Mesozoic Terrestrial Ecosystems and Biota. London, UK: Natural History Museum. p 5558.
  • Jones MEH. 2008. The evolution of skull shape and feeding strategy in Sphenodon and other Rhynchocephalia (Diapsida: Lepidosauria). J Morphol 269: 945966.
  • Jones MEH. 2009. Dentary tooth shape in Sphenodon and its fossil relatives (Diapsida: Lepidosauria: Rhynchocephalia). Front Oral Biol 13: 915.
  • Jones MEH, Lappin AK. 2009. Bite-force performance of the last rhynchocephalian (Lepidosauria: Sphenodon). J R Soc NZ 39: 7183.
  • Jones MEH, Curtis N, Fagan MJ, O'Higgins P, Evans SE. 2011. Hard tissue anatomy of the cranial joints in Sphenodon (Rhynchocephalia): sutures, kinesis, and skull mechanics. Palaeontologia Electr 14.2.17A: 192.
  • Jones MEH, Curtis N, O'Higgins P, Fagan M, Evans SE. 2009a. Head and neck muscles associated with feeding in Sphenodon (Reptilia: Lepidosauria: Rhynchocephalia). Palaeontologia Electr 12.2.7A: 156.
  • Jones MEH, Tennyson AJD, Worthy JP, Evans SE, Worthy TH. 2009b. A sphenodontine (Rhynchocephalia) from the Miocene of New Zealand and palaeobiogeography of the tuatara (Sphenodon). Proc R Soc B 276: 13851390.
  • Kemp TS. 2005. The origin and evolution of mammals. 2nd ed. Oxford: Oxford University Press.
  • Kieser JA, Tkatchenko T, Dean MC, Jones MEH, Duncan W, Nelson NJ. 2009. Microstructure of dental hard tissue and bone in the tuatara dentary, Sphenodonpunctatus (Diapsida: Lepidosauria: Rhynchocephalia). Front Oral Biol 13: 8085.
  • Krause DW. 1982. Jaw movement, dental function, and diet in the Paleocene multituberculate Ptilodus. Paleobiology 8: 265281.
  • Lee MSY, Bell GL, Caldwell MW. 1999. The origin of snake feeding. Nature 400: 655659.
  • Lucas PW. 2004. Dental functional morphology: how teeth work. 1st ed. Cambridge: Cambridge University Press.
  • Lucas PW, Luke DA. 1984. Chewing it over: Basic principles of food breakdown. In: Chivers DK, Wood BA, Bilsborough A, editors. Food acquisition and processing in primates. New York and London: Plenum Press. p 283301. Chapter 12.
  • Lumsden AGS, Osborn JW. 1977. The evolution of chewing: a dentist's view of palaeontology. J Dent 5: 269287.
  • McBrayer LD, Reilly SM. 2002. Prey processing in lizards: behavioural variation in sit-and-wait and widely foraging taxa. Can J Zool 80: 882892.
  • Metzger K. 2002. Cranial kinesis in lepidosaurs: Skulls in motion. In: Aerts P, D'Aou' t K, Herrel A, van Damme R, editors. Topics in functional and ecological vertebrate morphology. Maastricht: Shaker Publishing. p 1546.
  • Mo J-Y, Xu-X, Evans SE. 2010. The evolution of the lepidosaurian lower temporal bar: new perspectives from the Late Cretaceous of South China. Proc R Soc B 277: 331336.
  • Moazen M, Curtis N, Evans SE, O'Higgins P, Fagan M. 2008a. Rigid-body analysis of a lizard skull: modelling the skull of Uromastyx hardwickii. J Biomech 41: 12741280.
  • Moazen M, Curtis N, O'Higgins P, Jones MEH, Evans SE, Fagan MJ. 2008b. Assessment of the role of sutures in a lizard skull: a computer modelling study. Proc R Soc B 276: 3946.
  • Modesto SP. 1995. The skull of the herbivorous synapsid Edaphosaurus boanerges from the Lower Permian of Texas. Palaeontology 38: 213239.
  • Northcutt RG, Heath JE. 1973. T-maze behavior of the tuatara (Sphenodon punctatus). Copeia 1973: 617620.
  • O'Meally D, Miller H, Patel HR, Marshall Graves JA, Ezaz T. 2009. The first cytogenetic map of the tuatara, Sphenodon punctatus. Cytogenet Genome Res 127: 213223
  • Parkinson B. 2002. The tuatara, New Zealand wild series. 2nd ed. New Zealand: Reed Publishing.
  • Porro LB, Holliday CM, Anapol F, Ontiveros LC, Ontiveros LT, Ross CF. 2011. Free body analysis, beam mechanics, and finite element modeling of the mandible of Alligator mississippiensis. J Morphol 272: 910937.
  • Pregill G. 1984. Durophagous feeding adaptations in an amphisbaenid. J Herpetol 18: 186191.
  • Ramstad KM, Paine G, Dunning DL, Geary AF, Keall SN, Nelson NJ. 2009. Effective partnerships between universities and indigenous communities: a case study in tuatara conservation in Aotearoa. J R Soc NZ 39: 229231.
  • Rasmussen TE, Callison G. 1981. A new herbivorous sphenodontid (Rhynchocephalia: Reptilia) from the Jurassic of Colorado. J Paleontol 55: 11091116.
  • Reilly SM, McBrayer LD, White TD. 2001. Prey processing in amniotes: biomechanical and behavioural patterns of food reduction. Comp Biochem Physiol A 128: 397415.
  • Rest JS, Ast JC, Austin CC, Waddell PJ, Tibbetts EA, Hay JM, Mindell DP. 2003. Molecular systematics of primary reptilian lineages and the tuatara mitochondrial genome. Mol Phylogenet Evol 29: 289297.
  • Reynoso VH. 1993. A sphenodontid assemblage from the early Middle Jurassic deposits of Huizachal Canyon, Tamaulipas, Mexico. J Vertebr Paleontol S13:54.
  • Reynoso VH. 1996. A Middle Jurassic Sphenodon-like sphenodontian (Diapsida: Lepidosauria) from Huizachal Canyon, Tamaulipas, Mexico. J Vertebr Paleontol 16: 210221.
  • Reynoso VH. 2005. Possible evidence of a venom apparatus in a Middle Jurassic sphenodontian from the Huizachal red beds of Tamaulipas, México. J Vertebr Paleontol 25: 646654.
  • Rieppel O, Zaher H. 2000. The intramandibular joint in squamates, and the phylogenetic relationships of the fossil snake Pachyrhachis problematicus Haas. Fieldiana 43: 169.
  • Robb J. 1977. The tuatara. 1st ed. Durham: Meadowfield Press Limited.
  • Robinson BW, Sloan Wilson D. 1998. Optimal foraging, specialisation, and a solution to Liem's paradox. Am Nat 151: 223235.
  • Robinson PL. 1973. A problematic reptile from the British Upper Trias. J Geol Soc 129: 457479.
  • Robinson PL. 1976. How Sphenodon and Uromastix grow their teeth and use them. In: Bellairs Ad A, Cox CB, editors. Morphology and biology of the reptiles. London: Academic Press. p 4364.
  • Ross CF, Eckhardt A, Herrel A, Hylander WL, Metzger KA, Schaerlaeken V, Washington RL, Williams SH. 2007a. Modulation of intra-oral processing in mammals and lepidosaurs. Integr Comp Biol 47: 118136.
  • Ross CF, Dharia R, Herring SW, Hylander W-L, Liu Z-J Rafferty KL, Ravosa MJ, Williams SH. 2007b. Modulation of mandibular loading and bite force in mammals during mastication. J Exp Biol 210: 10461063.
  • Ross CF, Baden AL, Georgi J, Herrel A, Metzger KA, Reed DA, Schaerlaeken V, Wolff MS. 2010. Chewing variation in lepidosaurs and primates. J Exp Biol 213: 572584.
  • Schwenk K. 1986. Morphology of the tongue in the tuatara, Sphenodon punctatus (Reptilia: Lepidosauria), with comments on function and phylogeny. J Morphol 188: 129156.
  • Schwenk K. 2000. Feeding in lepidosaurs. In: Schwenk K, editor. Feeding. Form, function, and evolution in tetrapod vertebrates. San Diego: Academic Press. p 175291.
  • Sues H-D, Reisz RR. 1998. Origins and early evolution of herbivory in tetrapods. Trends Ecol Evol 13: 141145.
  • Taylor MA. 1992. Functional anatomy of the head of the large aquatic predator Rhomaleosaurus zetlandicus (Plesiosauria, Reptilia) from the Toarcian (Lower Jurassic) of Yorkshire, England. Philos Trans Biol Sci 335: 247280.
  • Thompson MB, Daugherty CH. 1998. Metabolism of tuatara, Sphenodon punctatus. Comp Biochem Physiol 119: 519522.
  • Throckmorton GS. 1976. Oral food processing in two herbivorous lizards, Iguana iguana and Uromastix aegypticus (Agamidae). J Morphol 148: 363390.
  • Throckmorton GS, Hopson JA, Parks P. 1981. A redescription of Toxolophosaurus cloudi Olson, a Lower Cretaceous herbivorous sphenodontian reptile. J Paleontol 55: 586597.
  • Upchurch P, Barrett P, Xijin Z, Xing Xu. 2007. A re-evaluation of Chinshakiangosauruschunghoensis Ye vide Dong 1992 (Dinosauria, Sauropodomorpha): implications for cranial evolution in basal sauropod dinosaurs. Geol Mag 144: 247262.
  • Ussher GT. 1999. Tuatara (Sphenodon punctatus) feeding ecology in the presence of kiore (Rattus exulans). NZ J Zool 26: 117125.
  • Walls GY. 1978. The influence of the tuatara on Fairy Prion breeding on Stephens Island, Cook Strait. NZ J Ecol 1: 9198.
  • Walls GY. 1981. Feeding ecology of the tuatara (Sphenodon punctatus) on Stephens Island, Cook Strait. NZ J Ecol 4: 8997.
  • Whiteside DI. 1986. The head skeleton of the Rhaetian sphenodontid Diphydontosaurus avonis gen. et sp. nov., and the modernising of a living fossil. Philos Trans R Soc Lond B Biol Sci 312: 379430.
  • Williston SW. 1917. The phylogeny and classification of reptiles. J Geol 25: 411421.
  • Young BA. 1998. The comparative morphology of the intermandibular connective tissue in snakes (Reptilia: Squamata). Zool Anz 237: 5984.
  • Zaher H, Apesteguía S, Scanferla CA. 2009. The anatomy of the upper Cretaceous snake Najash rionegrina Apesteguía & Zaher, 2006, and the evolution of limblessness in snakes. Zool J Linn Soc 156: 801826.

Supporting Information

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIAL AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. Acknowledgements
  9. LITERATURE CITED
  10. Supporting Information

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