Bite force performance of the last rhynchocephalian (Lepidosauria: Sphenodon)

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1 Journal of the Royal Society of New Zealand ISSN: (Print) (Online) Journal homepage: Bite force performance of the last rhynchocephalian (Lepidosauria: Sphenodon) Marc E. H. Jones & A. Kristopher Lappin To cite this article: Marc E. H. Jones & A. Kristopher Lappin (2009) Bite force performance of the last rhynchocephalian (Lepidosauria: Sphenodon), Journal of the Royal Society of New Zealand, 39:2-3, 71-83, DOI: / To link to this article: Published online: 22 Feb Submit your article to this journal Article views: 280 View related articles Citing articles: 16 View citing articles Full Terms & Conditions of access and use can be found at Download by: [ ] Date: 09 January 2018, At: 10:26

2 71 Journal of the Royal Society of New Zealand, Volume 39, Number 3, September, (Online); (Print)/3902/ The Royal Society of New Zealand 2009 Bite-force performance of the last rhynchocephalian (Lepidosauria: Sphenodon) Marc E. H. Jones 1 and A. Kristopher Lappin 2 Abstract We present the first empirical measurements of bite-force performance from adult Sphenodon (Rhynchocephalia), the only extant non-squamate lepidosaur. Using raw bite-force data, we calculated maximum bite forces at the anterior and posterior extremes of the lower tooth row: 81.8 N and N (female) and N and N (male). Combining our results with published data from juvenile animals, we calculated scaling coefficients of bite force on linear morphometrics of body and head size as c. 2.7 (anterior) and c (posterior). These exceed isometric scaling predictions (2.0), yet are similar to those for other non-avian reptiles. This supports previous views that Sphenodon cannot bite as hard as agamidlizards. We discuss the role of bite force in the behavioural ecology of Sphenodon, propose that the lower temporal bar, unique among extant lepidosaurs, does not necessarily constrain bite force, and evaluate possible effects of other morphological characteristics on bite-force performance. Keywords Rhynchocephalia; skull morphology; ontogeny; feeding; tuatara INTRODUCTION One of New Zealand's most iconic animals is the tuatara (Sphenodon) (Parkinson 2002). It is the largest endemic non-avian reptilian and has significant cultural importance for Maori (Sharell 1966; Mot 1997; Ramstad et al. 2007). Currently restricted to approximately 35 small islands and the subject of concerted conservation efforts (Daugherty et al. 1990; Mlot 1997; Gaze 2001; Parkinson 2002; Mitchell et al. 2008), Sphenodon is of great scientific significance because it is the only extant member of the Rhynchocephalia, a group that was diverse and globally distributed during the Mesozoic (Apesteguia & Novas 2003; Evans 2003; Jones 2008; Jones et al. 2009). Being the closest living relative (sister group) to Squamata (lizards, snakes, amphisbaenians; Rest et al. 2003; Evans 2003), Sphenodon has been the subject of much research and has played an essential role as an outgroup taxon in comparative studies of squamate biology (e.g., Schwenk 1986, 2000; McBrayer & Reilly 2002; Vitt et al. 2003; Herrel et al. 2007; Evans 2008; Jones et al. in press). There has been a long-standing interest in numerous aspects of Sphenodon biology, including its dietary ecology and social behaviour, as well as the unique morphology of this taxon's feeding apparatus. The diet of Sphenodon is diverse and comprises ants, moths, caterpillars, 1 Research Department of Cell and Developmental Biology, Gower Street, UCL, University College London, London, WCIE 6BT, United Kingdom. Author for correspondence: marc.jones@ucl.ac.uk. 2 Biological Sciences Department, California State Polytechnic University, Pomona, CA , USA. aklappin@csupomona.edu R09002; Received 9 March 2009; accepted 20 August 2009; Online publication date 4 September 2009

3 72 Journal of the Royal Society of New Zealand, Volume 39, 2009 beetles, spiders, snails, frogs, lizards, flightless orthopterans, and fledgling sea birds (Günther 1867; Buller 1877; Dawbin 1962; Farlow 1975; Walls 1981; Markwell 1998; Ussher 1999; Crée et al. 1999; Parkinson 2002). Sphenodon is sexually dimorphic with males attaining larger size (Buller 1877; Robb 1977; Crée et al. 1995, 1999; Tracy 1997; Nelson et al. 2004). This is associated with territoriality and fighting among males (Gans et al. 1984; Gillingham étal. 1995). In lizards, bite force is related to feeding biology (e.g., Herrel etal. 1999; Lappin 1999; Herrel et al. 2001a; Verwaijen et al. 2002), and significant positive relationships have been identified between bite-force performance and male territoriality, combat, dominance (Lailvaux et al. 2004; Lappin & Husak 2005; Husak et al. 2006), and reproductive success (Lappm & Husak 2005; Husak et al. 2009). The feeding apparatus of Sphenodon is sophisticated and includes an enlarged palatine tooth row, acrodont marginal teeth, large incisiform teeth on the premaxilla, and a pro-oral shearing action that involves a forward powerstroke of the lower jaw following jaw closure (Robinson 1976; Gorniak et al. 1982; Whiteside 1986; Jones 2008). This unique combination of morphological characteristics and specialised function of the jaws may have implications for bite-force performance. In particular, it has been proposed that the lower temporal bar, absent in extant squamates and early fossil relatives of Sphenodon (e.g., Whiteside 1986; Evans 2003; Jones 2008), constrains bite force in Sphenodon (Schaerlaeken et al. 2008). Recently, bite-force performance in juvenile Sphenodon was empirically measured (Schaerlaeken et al. 2008). Here we report the results of the first bite-force experiments performed on adult Sphenodon. We examine scaling relationships between bite force and morphology in Sphenodon, based on the published data combined with that presented herein. We then compare these relationships with published information on the scaling of bite-force performance in squamates and archosaurs, which all show a well-supported pattern of positive allometry of bite force on measures of body and head size. Finally, we discuss the results of our bite-force performance experiments in light of the unique behavioural ecology and cranial morphology of Sphenodon. MATERIALS AND METHODS We studied two animals from the Dallas Zoo, a female (SpFl/927483) and amale (SpM/04F378). The male belonged to Professor Carl Gans prior to being donated to the Dallas Zoo and was 33 years old when we performed the experiments. The female was 21 years old. They are housed in a large naturalistic enclosure in which the temperature and humidity are controlled to mimic conditions in their native New Zealand habitat. Data collection was carried out in August 2008, when the photoperiod was set to provide 11 h of daylight and the ambient temperature was maintained at 15.5 C. Snout-vent length (SVL) and body mass were recorded as measures of body size. Head length was measured from the jaw joint, as determined by palpation, to the tip of the snout. This measurement was made parallel to the coronal and sagittal planes of the head to avoid the confounding effects of angular head measurements being used as metrics of head size (Lappin & Swinney 1999). Linear measurements were made with digital calipers to the nearest 0.1 mm, and mass was measured to the nearest 1.0 g with a digital scale. Bite-force performance was measured in newtons (N) with a custom-designed piezoelectric isometric force transducer (Type 9203, Kistlerlnc, Switzerland) connected to a charge amplifier (Type 5995, Kistler Inc., Switzerland) and fitted with bite plates (Herrel et al. 2001a,b; Lappin & Husak2005; Husak et al. 2006; Lappin et al. 2006a,b; Fig. 1). To define a bite point such that transducer calibration and bite-force measurements were comparable, and importantly to avoid damaging the animal's teeth, the transducer was prepared by gluing a strip of leather at the end of each plate's outer surface (see Lappin 1999; Lappin & Husak 2005; Fig. 2).

4 Jones & Lappin Bite force in tuatara (Sphenodon) 73 Fig. 1 Female Sphenodon (SpF1/ from Dallas Zoo) biting force transducer in lateral view. Fig. 2 Leather pads at ends of force transducer bars showing bite marks made by the male Sphenodon (SpM/04F378). A, Marks made by upper jaw. B, Marks made by lower jaw. To calibrate amplifier output to reflect the bite forces applied to the same area, a series of weights was suspended on the leather strip with fishing line. The calibration factor was calculated as the regression coefficient of the linear relationship between the masses of the weights (converted to N) and the corresponding amplifier outputs (Lappin & Husak 2005). As previously reported, it was easy to encourage the animals to bite vigorously (Farlow 1975; Walls 1981), and once biting commenced the tuatara would maintain its grip with considerable reluctance to release (Schmidt 1953; Daugherty & Cree 1990). The number of trials performed with the female and male were two and eight, respectively. Using an in-lever:out-lever calculation, bite forces were standardised for variation in the position along the jaw line at which bites were applied to the transducer bars (see Lappin & Husak 2005 for methods). Bite positions (i.e., placement of bites on leather padded transducer bars) were recorded using a video camera viewing the lateral aspect of the animal. We calculated standardised bite forces at the two possible extremes, namely for a bite point at the tip of the lower jaw and for a bite point positioned at the posteriormost teeth, which was estimated as the midpoint between the lower jaw tip and quadrate-articular jaw joint. For each individual, the

5 74 Journal of the Royal Society of New Zealand, Volume 39, 2009 greatest standardised bite force value at each bite point was assumed to represent maximum voluntary bite-force performance (see Losos et al. 2002) and was used in the analysis. Biteforce trials were conducted immediately following the removal of each Sphenodon from its enclosure, such that body temperature reflected that of the ambient temperature in the enclosure (15.5 C). We calculated scaling coefficients of bite force versus body size (i.e., SVL) and head length by combining our data with that presented by Schaerlaeken et al. (2008). Assuming isometric growth, and employing a linear model fitted to log-transformed data, bite force should scale on any linear morphometric with a coefficient of 2.0 (e.g., see Erickson et al. 2003). This prediction is based on the fact that the primary gross predictor of muscle force is the cross-sectional area of the muscle in question, and that measurements of anatomical areas scale on linear anatomical dimensions (e.g., body length, head length) with a coefficient (i.e., slope) of 2.0. Because information on bite points was not available in the published account of juvenile bite forces (Schaerlaeken et al. 2008), our method provided low and high end estimates of scaling coefficients based on bite forces at the lower jaw tip and most posterior teeth, respectively. In doing so, we considered variation in adult bite forces related to bite point, but we made no assumption as to the bite points in the juvenile trials. RESULTS The maximum standardised bite forces for the female Sphenodon (SpF1/927483: SVL = mm, mass = 590 g, head length = 51.6 mm) were 81.8 N at the jaw tips and N at the posterior teeth. For the male (SpM/04F378: SVL = mm, mass = 778 g, head length = 62.0 mm), the maximum standardised bite forces were N and N. An average bite force of 8.7 N for juvenile Sphenodon specimens averaging 96 mm SVL was reported by Schaerlaeken et al. (2008), but no information was provided as to the bite point at which forces were measured. Therefore, we calculated scaling coefficients based on these values combined with our results for bites at the tip of the lower jaw as well as for bites at the posterior-most teeth, assuming that the published values represented bite forces at the corresponding bite points (i.e., juvenile bite force assumed at anterior teeth for low end estimate of coefficient and at posterior teeth for high end estimate). Using adult bite-force performance at the lower jaw tip, the scaling coefficient of bite force on SVL was Using adult bite forces at the posterior bite point, the scaling coefficient increased to Using the published plot of bite force versus head length in a range of agamid lizards and juvenile Sphenodon (Schaerlaeken et al. 2008, fig. 3), we estimated an average bite force of 10 N for Sphenodon approximating 25 mm in head length. Based on this information, scaling coefficients were 2.78 and 3.76 for the anterior and posterior positions, respectively. DISCUSSION Assuming isometric growth, and employing a linear model on log-transformed data, scaling predictions indicate that bite force should scale on linear morphometrics with a coefficient (i.e., slope) of 2.0 (e.g., Erickson et al. 2003). This prediction is based on the fact that the primary gross predictor of muscle force is the cross-sectional area of the muscle in question. Despite this straightforward prediction, the results of all studies of non-avian reptilians to date are that bite force scales with significant positive allometry (i.e., slope of >2.0) on linear measures of body and head size (e.g., Cnemidophorus (New World scleroglossan lizard) = 3.8 (Meyers et al. 2002); Sceloporus (New World iguanian lizard) = 4.6 (Meyers et al. 2002); turtles = >3.0 (Herrel et al. 2002), and Alligator mississipiensis = >2.6 (Erickson et al. 2003, 2004)). Bite force in agamid lizards (87 individuals of 9 different unspecified species), the group with which juvenile Sphenodon were compared by Schaerlaeken et al. (2008), also appears to

6 Jones & Lappin Bite force in tuatara (Sphenodon) 75 scale with positive allometry, though an equation for the linear relationship was not provided. The reason for the positive allometric scaling of bite force is perplexing, and a clarifying explanation for the phenomenon has proven elusive (but see Erickson et al. 2003; Herrel & Gibb 2006). In the case of Sphenodon, an allometric increase in bite force during ontogeny is not surprising. Compared to juvenile animals, adults have taller parietal crests, which provide a greater surface area for the origins of major jaw adductor muscles (Fig. 3, 4) (Jones 2008). Adults also possess relatively larger adductor chambers, which house major jaw muscles (Jones 2008). This is illustrated by comparing the relative length of the postorbital region of the skull (a proxy for adductor chamber volume, Whiteside 1986) in hatchlings versus adults (Fig. 3, 4). In hatchlings, postorbital region makes up c. 30% of the total skull length (e.g., CM , skull length = 12 mm). In juveniles, it consists of c. 40% (e.g., NMNZ RE 5313, skull length = 44 mm) and, in large adults (e.g., LDUCZ x036, skull length = 68 mm), the postorbital region represents >45% of total skull length (Jones 2006a). The orbits themselves are large in Sphenodon (Günther 1867; Jones 2008), disproportionately so in juveniles (Fig. 3), which mirrors the ontogentic change in the size of the jaw-adductor chambers (Jones 2008). In addition, adults possess stronger skulls as evidenced by greater deposits of secondary bone along the jaws which increases their cross-sectional area (Jones 2006a; Jones et al. in press). Skull bones also overlap to a greater degree in adults, providing more rigidity (Jones 2006a, 2007). There are also ontogenetic changes in the dentition, such as the appearance of large caniniform teeth and coalescence of the premaxillary teeth that likely reflect an enhanced Fig. 3 Skull shape in lateral view of hatchling, juvenile, and adult Sphenodon to demonstrate ontogenetic changes in skull proportions. Jugal bone, which comprises the majority of the lower temporal bar, is coloured dark grey. A, Hatchling (skull length = 9.4 mm). B, NMNZRE 0156 (skull length = 28.5 mm). C, OUMNH 908 (skull length = 58.5 mm). D, LDUCZ x036 (skull length = 67.7 mm). (A) redrawn from Howes & Swinnerton (1901). (B), (C), and (D) redrawn from Jones (2008). Scale bars = 10 mm.

7 76 Journal of the Royal Society of New Zealand, Volume 39, 2009 Fig. 4 Skull shape in dorsal view of hatchling, juvenile, and adult Sphenodon to demonstrate ontogenetic changes in skull proportions. Parietal bone is coloured dark grey (left side only). A, Hatchling stage S (skull length = 9.4 mm). B, Hatchling stage T (skull length = 14.5 mm). C, Juvenile (NMNZRE 0156, skull length = 28.5 mm). D, Adult (KCL x12, skull length = 56.5 mm). (A) and (B) redrawn from Howes & Swinnerton (1901). Scale bars = 10 mm. ability to transmit muscle forces during bites (Howes & Swinnerton 1901; Robinson 1976; Jones 2008). Bite force and diet ontogeny and sexual dimorphism A disproportionate increase in bite force during ontogeny in Sphenodon would permit adults to access relatively larger and harder prey than juveniles (Jones 2008), as well as a reduction in prey handling time as found in lizards (Capel-Williams & Pratten 1978; Herrel et al. 2001a; Verwaijen et al. 2002). In fact, differences in diet between juvenile and adult Sphenodon include a tendency for the former to feed on smaller prey items (Ussher 1999). Although Sphenodon preys on a wide range of taxa, comparison between the contents of scat and prey availability show that large, slow invertebrates (e.g., beetles) form a major part of the diet (Walls 1981). This may not be so for juveniles, and they may be able to catch more motile prey than adults (as suggested by Meyers et al for lizards). Juveniles and adults also forage at different times, with juveniles being diurnal and adults crepuscular (Daugherty & Cree 1990), which likely influences the prey available to them. A greater potential dietary niche is advantageous, and researchers should focus future investigations on whether the disproportionate increase in bite force during ontogeny in Sphenodon correlates with greater diversity in prey selection. In addition to ontogentic changes in diet, sexual differences in bite-force performance may permit the larger, harder-biting adult males to more readily access larger and harder prey. Dietary differences between the sexes in sexually dimorphic lizards (i.e., potential niche divergence ) have been documented with several showing that males eat larger prey when they are the larger sex (Schoener 1967, 1968; Schoener & Gorman 1968; reviewed in Vincent & Herrel 2007). Males of a species of Jamaican anole, which are larger and bite harder than females, also eat larger and harder arthropods (Herrel et al. 2006). In other cases, strong sexual differences in size and bite force occur when there are no obvious dietary differences (e.g., Sauromalus, Lappin et al. 2006a). Sphenodon, at least in one significant respect, exhibits a positive relationship between sexual size dimorphism and prey size, in that only large males regularly tackle large vertebrates such as sea bird nestlings (Walls 1981; Cree et al. 1995, 1999; Markwell 1998; Blair et al. 2000; Gaze 2001). Parcelling out the effects of natural (e.g., dietary) and sexual selection on sexual dimorphism has proven challenging. It has been suggested that when sex differences in diet do exist they may be a secondary effect rather than the driving force (Shine 1989; Vincent & Herrel 2007). This view is supported by the fact that sex differences in lizard diets appear to be far less

8 Jones & Lappin Bite force in tuatara (Sphenodon) 77 common than the occurrence of sexual dimorphism. Therefore, although the relatively greater bite-force performance of adult male Sphenodon may permit males to more readily access larger and harder prey, the dietary difference could be a secondary effect of the performance dimorphism resulting from intrasexual selection for high bite force in males. Bite force and intrasexual competition In Sphenodon, males are substantially larger than females in body size, and they have disproportionately larger heads (Dawbin 1962; Robb 1977; Cree et al. 1995, 1999; Tracy 1997). This pattern is similar to that of many lizards, particularly iguanians. In lepidosaurs that exhibit male-biased sexual dimorphism, bite force is advantageous in acquiring and maintaining territories (Lappin & Husak 2005; Husak et al. 2006). For example, in the collared lizard of North America (Crotaphytus), bite-force performance strongly correlates with territory size, the area of which can vary among competing males by nearly an order of magnitude (Lappin & Husak 2005). Corresponding to the relationship between bite force and territoriality in lizards, bite force has been shown to predict reproductive success; the hardest biters enjoy reproductive success nearly four times greater than similarly sized males with the weakest bites (Lappin & Husak 2005; Husak et al. 2009). As with lizards (e.g., Lappin & Husak 2005), Fig. 5 Stereopair of the right lower jaw of Sphenodon specimen LDUCZ x036 (Grant Museum of Zoology at University College London) in lateral view. The bump along the ventral margin (arrow) is a pathology that may have been caused by a bone infection from wounds incurred during intraspecific fighting. Scale bar = 10 mm. confrontations between male Sphenodon can be intense and lead to injuries (Buller 1877; Gans et al. 1984; Gillingham et al. 1995; Seligmann et al. 2008). Pathologies occasionally found on Sphenodon dentaries may be the result of healed wounds or infections from wounds incurred during aggressive territorial encounters (Fig. 5). Given the pattern of sexual dimorphism in Sphenodon, and the combative nature of adult male Sphenodon, it is likely that bite-force performance is an important determinant of fitness for male Sphenodon. Aggressive competition occurs among female Sphenodon for nesting sites on Stephens Island (Nelson et al. 2004). This is similar to aggressive interactions among female Galapagos land iguanas (Conolophus subcristatus), that compete intensely for limited nesting sites in

9 78 Journal of the Royal Society of New Zealand, Volume 39, 2009 their rocky volcanic habitat (Pough et al. 2003). Therefore, bite force may also be an important determinant of fitness for female Sphenodon when nesting sites are limited or of heterogenous quality. Comparison with agamid lizards Juvenile Sphenodon are reported to bite with significantly lower force than (presumably adult) agamid lizards with similarly sized heads (Schaerlaeken et al. 2008). This appears at odds with anecdotal but first hand reports that the bite of Sphenodon is painful and vicelike (Robb 1977, p. 15; Daugherty & Cree 1990, p. 68). However, our results that bite force scales similarly in Sphenodon and lizards lends support to the conclusion of Schaerlaeken et al. (2008) that agamid lizards are relatively stronger biters. Relatively greater bite-force performance in lizards, specifically agamids, is compatible with suggestions that the distribution of rhynchocephalians contracted in the late Mesozoic because of competition with derived lizards (Milner et al. 2000). Available fossil evidence does indicate a change in global lepidosaur communities from those dominated by rhynchocephalians to those dominated by squamates (Evans 1995). The pattern of replacement occurs first in Asia, later in North America, and eventually on the southern continents (Evans et al. 2001, 2004; Apesteguía & Novas 2003; Jones 2006b). Correspondingly, agamids are not found in New Zealand today, and they are absent from the (admittedly limited) New Zealand fossil record (Milner et al. 2000; Mark Hutchinson pers. comm. 2008; Jones et al. 2009; Lee et al. 2009). As previously pointed out, it remains difficult to assess whether this replacement was competitive or opportunistic (Jones 2006b). It is also unknown how the bite force of the modern day Sphenodon compares to that of Mesozoic Rhynchocephalia. It has been suggested that Sphenodon could bite relatively hard compared to some of its fossil relatives (Jones 2008), and bite force within the group as a whole was probably subject to significant interspecific variation (Jones 2008), as it is in Squamata. The degree of morphological and palaeoecological variation now known in Mesozoic rhynchocephalians (Jones 2006a,b, 2008) makes it unlikely that they all went extinct because of competition with one group of lizards. The lower temporal bar and other morphological considerations To explain the difference in bite force between Sphenodon and adult agamid lizards with similarly sized heads, Schaerlaeken et al. (2008) proposed that the lower temporal bar of Sphenodon (Fig. 3), absent in squamates, imposes a physical limitation on the size of the jaw adductor musculature. This follows a previous suggestion that, despite being bowed, the lower temporal bar restricts extension of the m. adductor mandibular superficialis (muscle 1b ) onto the lateral surface of the lower jaw (Rieppel & Gronowski 1981). This is considered to limit the cross-sectional area of the muscle and in turn limit potential bite force. By contrast, squamates without a lower temporal bar are said to be free to extend the attachment of this muscle laterally, thus increasing its size and potential force generation. However, certain considerations warrant a reassessment of this hypothesis. The m. adductor mandibular superficialis was found to have the greatest cross-sectional area among the internal jaw adductors (i.e., housed within the temporal region) of Sphenodon (Schaerlaeken et al. 2008). However, images presented in Rieppel & Gronowski (1981) show that the attachment area of the m. adductor mandibular superficialis on the lower jaw is only marginally larger in Iguana than in Sphenodon, which is due primarily to a difference in its antero-posterior rather than its ventro-lateral extent. Further, the arrangement of the m. adductor mandibular superficialis differs between squamates and Sphenodon. In Sphenodon the muscle originates on the upper temporal bar and the fascia of the lower temporal fenestra (Haas 1973; Gorniak et al. 1982; Jones et al. in press) such that, when the jaws are closed, its

10 Jones & Lappin Bite force in tuatara (Sphenodon) 79 fibres are aligned with only a slight postero-ventrai angulation from the origin (c from the vertical) (Haas 1973). In contrast, in most lizards the muscle originates on the quadrate, and therefore when the jaws are closed it has an antero-ventral inclination that in some cases is >45 from the vertical (Haas 1973; Gomes 1974; Rieppel & Gronawski 1981). This latter arrangement greatly lessens the contribution of this muscle to bite force because its vertical force vector is reduced relative to its total force generation (Rieppel & Gronawski 1981). Thus, the apparent difference in relative bite force between Sphenodon and agamid lizards is not necessarily explained by minor differences in the size of the m. adductor mandibular superficialis. Acquisition of the lower temporal bar in the lineage leading to Sphenodon possibly played a role in stabilising the lateral aspect of the quadrate and, significantly, permitted pro-oral shearing (e.g., Whiteside 1986; Fraser 1988; Rieppel 1993; Wu 2003; Evans 2003; Schaerlaeken et al. 2008). However, presence or absence of a lower temporal bar in fossil lepidosaurs is not tightly linked with pro-oral shearing. Some taxa show clear evidence of translatory jaw movements but lack the bar (e.g., Gephyrosaurus, Priosphenodori), whereas others possessed the bar but had strictly orthal jaw movements (e.g., Clevosaurus, Tianyusaurus) (Jones 2008; Mo et al. 2009). The occurrence of a lower temporal bar is probably related to the general distribution of compressive and tensile forces rather than focused on those generated by the forward power stroke (Gregory &Adams 1915; Adams 1919; Olsen 1961; Frazzetta 1968). Other differences in skull structure between Sphenodon and extant lizards also may contribute to differences in bite-force performance. For example, Sphenodon possesses relatively large eyes, a feature that is associated with foraging during dawn and dusk (Walls 1981 ; Gans 1983; Daugherty & Crée 1990; Meyer-Rochow etal. 2005). For a head of a given size, larger orbits mean a smaller temporal region for housing internal jaw-adductor musculature, a constraint that is expected to compromise bite-force performance. Another example is related to the pro-oral jaw movements observed during feeding in Sphenodon. These movements are facilitated by intra-joint mobility between the quadrate-quadratojugal condyle and articular surface as well as a fibrous joint at the lower jaw symphysis (Robinson 1976; Jones et al. in press). This dynamic behaviour of the jaw joint and symphysis may impose a biomechanical constraint that compromises bite force. Computer models of the Sphenodon feeding apparatus are in development (e.g., Curtis et al. 2009), with the goal of determining the effects of individual anatomical features on skull biomechanics, performance and, ultimately, related aspects of the behavioural ecology of this unique taxon. ACKNOWLEDGMENTS For their supervision, cooperation, and correspondence, we thank Ruston Hartdegen and other staff at the Dallas Zoo, USA. For assistance with transport we are grateful to Louis L. Jacobs, Mike J. Polcyn, and Diana Vineyard, all of Southern Methodist University. For access to skeletal material we thank staff at the Grant Museum of Zoology, UCL, London (UK); Gordon Museum, Kings College London, London (UK); and Museum of New Zealand Te Papa Tongarewa, Wellington (NZ). Travel for MEHJ was supported by a BBSRC research grant awarded to Susan E. Evans (UCL, University College London), Mike Fagan (University of Hull), and Paul O'Higgins (Hull York Medical School). Travel for AKL, and accommodations for MEHJ and AKL, were supported with funding from California State Polytechnic University. We thank Susan E. Evans, Alison Crée, and an anonymous reviewer for comments on an earlier version of this manuscript. REFERENCES Adams LA A memoir on the phylogeny of the jaw muscles in recent and fossil vertebrates. Annals of the New York Academy of Science 28: Apesteguía S, Novas FE Large Cretaceous sphenodontian from Patagonia provides insight into lepidosaur evolution in Gondwana. Nature 425:

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