The retroarticular process, streptostyly and the caecilian jaw closing system
Introduction
Caecilians are fossorial, limbless amphibians with a circumtropical distribution (Taylor, 1968). The architecture of the caecilian skull appears particularly well suited to burrowing, exhibiting tight sutures and fusion of skeletal elements (Wake, 1993). In spite of their robust skull there is a surprising degree of cranial kinesis (streptostyly) in the quadrate-squamosal apparatus (Wake and Hanken, 1982), and though the quadrate does not rotate to any great degree, it may be relatively free to do so (Fig. 1). Streptostyly has evolved several times in tetrapods, serving to increase gape in lizards and snakes, and also allowing the lower jaw to move relative to the origin of the adductor muscles in order to alter the leverage of these jaw closers (Gans, 1961, Gans, 1966; Herrel et al., 2000). The development and functional significance of streptostyly in caecilians has been speculated on (Marcus et al., 1933; Wake and Hanken, 1982; Straub, 1985; Wilkinson and Nussbaum, 1997; summarized by Wake, 2003), but specific tests of the effects of streptostyly have not been done.
Neither of the two reasons mentioned above for the evolution of streptostyly would seem to pertain to caecilians: most do not eat particularly large prey items (they are elongate, but not large in cross-section; see Gaborieau and Measey, 2004; Measey et al., 2004; O’Reilly, 2000; Presswell et al., 2002; Wake, 1980, Wake, 1983, and references therein) and their jaw adductors are relatively small, with origin and insertion quite close to the jaw joint (Bemis et al., 1983; Nussbaum, 1983; O’Reilly, 2000). However, Wilkinson and Nussbaum (1997) suggest that a habitat shift, from burrow-dwelling sit and wait predators to a free-swimming active predatory lifestyle, may be involved in the evolution of the unusually kinetic skull of Atretochoana.
The jaw adductors of caecilians are constrained in size by the maxillopalatine and squamosal bones that close over the entire ‘cheek’ area, restricting the adductors to rather narrow channels medial to these two bones (Bemis et al., 1983; Nussbaum, 1983; Straub, 1985; O’Reilly, 2000; Wake, 2003). Small jaw closing muscles are at odds with the strong sharp teeth and robust jaws of these active predators (Fig. 1). However, caecilians have an alternative method of exerting closing force that involves two unique characters – an unusually pronounced retroarticular process (RA) of the lower jaw, and a hypaxial muscle, the interhyoideus posterior (IHP), that exerts a ventro-posteriorly directed force on the RA (Bemis et al., 1983; Nussbaum, 1983). The lower jaw is composed of two compound elements, the pseudoangular, bearing the articular facet and the retroarticular process, and the pseudodentary, the dentigerous component. Force exerted by the IHP on the RA, which forms a significant rearward projection of the pseudoangular bone of the lower jaw (compared to that of reptiles, including fossil taxa – see Gans, 1966), acts to close the jaws by rotating the lower jaw about the quadrate–articular joint. The RA is variable in both its length and its angle relative to the body of the pseudoangular and the pseudodentary (see Wake, 2003). Thus, variation in RA will likely have consequences for the biomechanics of jaw closure.
The force of jaw closure is an important biomechanical determinant of trophic niche, limiting a predator to prey that it can reduce between its jaws (Hernandez and Motta, 1997; Wainwright, 1987). Variation in bite force can be so closely tied to dietary niche that it has been used to explain the small divergences in diet within a single lizard species with a sexually dimorphic head shape (Herrel et al., 1996, Herrel et al., 1999, Herrel et al., 2001). There are no published bite forces for caecilians, but in spite of data from some species suggesting that they eat small prey (Gaborieau and Measey, 2004; Measey et al., 2004), caecilians are opportunistic, and larger species can and will consume mammals and lizards. The lack of dietary analyses for the vast majority of species makes it difficult to guess the importance of a strong bite; but in some cases difficult prey is consumed (e.g. Dermophis eating lizards; Moll and Smith, 1967). The unique morphology of the caecilian head allows some insight to be gained by simple biomechanical modeling of the jaw closure forces. The aims of this paper are three-fold: (1) to model the effect of changing RA angle and length on the jaw closure force exerted by the IHP; (2) to model the effect of a mobile quadrate (streptostyly) on jaw closure force; and (3) to determine whether there is appreciable variation in expected force output for a variety of actual caecilian morphologies.
Section snippets
Modeling
Jaw closure force was modeled using the MatLab mathematical analysis environment. The simplest model assumed: (1) closure forces due to the IHP muscle were directed purely posteriorly (any inclination of this muscle would be equivalent to a change in the angle of the RA); (2) no contribution to closure force from the jaw adductor muscles; (3) IHP muscle force did not vary with gape; and (4) no rotational freedom at the quadrate–articular joint. Closure force was calculated for gape angles
Simple model (no streptostyly)
With the RA angle held at 0° (in line with the PD) the force at the tip of the jaws (output force) is maximized when the jaws are open to 90° and decreases to 0° as the jaws close (Fig. 2c). Output force scales with RA/PD, a larger RA relative to PD leads to increased output force. Changing the angle of the RA decreases the gape angle of maximum output force to a 90°-RA angle. Peak output force is input force multiplied by RA/PD, and so it never exceeds 50% of the force generated by the IHP
Discussion
Our models of jaw function imply new interpretations of the functional significance of the RA and the streptostylic jaw joint of caecilians. The RA is thought to have been the site of insertion for a jaw opening muscle that originated on the posterior of the skull in extinct amphibian and reptilian lineages including nectrideans, captorhinomorphs and goniorhynchids (Carroll, 1988). In caecilians the RA has a nearly opposite function, serving as an insertion for a hypaxial jaw closing muscle (
Acknowledgements
MHW thanks Enrique Lessa for previous collaboration on caecilian jaw closing mechanisms and the National Science Foundation, currently IBN 0212027, for support of research; APS thanks the Miller Institute for Basic Research and the National Science Foundation. We also appreciate Nicole Danos’ assistance in taking measurements of caecilian jaws and gape angles.
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