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Cranial Performance in Solid and Fenestrated Caecilian Skulls

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Cranial Performance in Solid and Fenestrated Caecilian Skulls 833 The Journal of Experimental Biology 215, 833-844 © 2012. Published by The Company of Biologists Ltd doi:10.1242/jeb.065979 RESEARCH ARTICLE Is solid always best? Cranial performance in solid and fenestrated caecilian skulls Thomas Kleinteich1,2,*, Hillary C. Maddin3, Julia Herzen4, Felix Beckmann4 and Adam P. Summers2 1Christian-Albrechts-Universität Kiel, Department of Zoology – Functional Morphology and Biomechanics, Am Botanischen Garten 1-9, 24098 Kiel, Germany, 2University of Washington, Friday Harbor Laboratories, 620 University Road, Friday Harbor, WA 98250, USA, 3University of Calgary, 2500 University Drive, Calgary, Alberta, T2N 1N4, Canada and 4Helmholtz Zentrum Geesthacht, Institute of Materials Research, Max-Planck-Straße 1, 21502 Geesthacht, Germany *Author for correspondence ([email protected]) Accepted 23 November 2011 SUMMARY Caecilians (Lissamphibia: Gymnophiona) are characterized by a fossorial lifestyle that appears to play a role in the many anatomical specializations in the group. The skull, in particular, has been the focus of previous studies because it is driven into the substrate for burrowing. There are two different types of skulls in caecilians: (1) stegokrotaphic, where the squamosal completely covers the temporal region and the jaw closing muscles, and (2) zygokrotaphic, with incomplete coverage of the temporal region by the squamosal. We used 3-D imaging and modeling techniques to explore the functional consequences of these skull types in an evolutionary context. We digitally converted stegokrotaphic skulls into zygokrotaphic skulls and vice versa. We also generated a third, akinetic skull type that was presumably present in extinct caecilian ancestors. We explored the benefits and costs of the different skull types under frontal loading at different head angles with finite element analysis (FEA). Surprisingly, the differences in stress distributions and bending between the three tested skull types were minimal and not significant. This suggests that the open temporal region in zygokrotaphic skulls does not lead to poorer performance during burrowing. However, the results of the FEA suggest a strong relationship between the head angle and skull performance, implying there is an optimal head angle during burrowing. Supplementary material available online at http://jeb.biologists.org/cgi/content/full/215/5/833/DC1 Key words: caecilian, burrowing, skull evolution, 3-D surface manipulation, amphibian origin. INTRODUCTION Caecilians are a monophyletic group of amphibians with skulls that Marcus et al., 1933; Carroll and Currie, 1975). This view is are thought to be highly specialized for their burrowing lifestyle; supported by the absence of a real suture between the squamosal they are wedge shaped, compact and robust (Wake, 1993). Many and the parietal in the stegokrotaphic skull. However, the discovery bones of the skull have been fused into larger compound elements, of a stem group caecilian with a stegokrotaphic skull, Eocaecilia e.g. the os basale of caecilians comprises all of the bones of the micropodia, has challenged this view and suggests that the skull base [i.e. the parasphenoid, the exoccipitals, and the caudal zygokrotaphic skull in the Rhinatrematidae is a derived condition parts of the neurocranium, including the otic capsules (Wake, 2003) and that stegokrotaphy is ancestral for all caecilians (Jenkins and (Fig.1)]. There are two distinct skull types in caecilians: (1) Walsh, 1993; Carroll, 2000; Jenkins et al., 2007). zygokrotaphic, in which the skull is fenestrated between the Despite coverage of the temporal region by the squamosal in squamosal and the parietal, and (2) stegokrotaphic, in which the the stegokrotaphic caecilian skull type, there is always a narrow skull is completely roofed. gap between the squamosal and the parietal instead of a tight Based on recently published caecilian phylogenies (Roelants et suture (Wiedersheim, 1879; Sarasin and Sarasin, 1887–1890; al., 2007; Zhang and Wake, 2009; Pyron and Wiens, 2011; Peter, 1898; Versluys, 1912; Abel, 1919; Marcus et al., 1933; Wilkinson et al., 2011) (Fig.2), the zygokrotaphic skull has evolved Goodrich, 1958; Lawson, 1963; Taylor, 1969; Nussbaum, 1977; independently several times in caecilians, in the Scolecomorphidae, Nussbaum, 1983; Wake and Hanken, 1982). This gap is supposed Typhlonectidae and Dermophiidae (Brand, 1956; Taylor, 1969; to allow movement of the squamosal and the attached quadrate Nussbaum, 1977; Nussbaum, 1985; Wilkinson and Nussbaum, 1997; and thus plays a role in a complex cranial kinesis (Versluys, 1912; Müller et al., 2009). Zygokrotaphy in the Rhinatrematidae, however, Marcus et al., 1933; Iordansky, 1990; Iordansky, 2000). has usually been considered to be the ancestral condition for the Movement of the squamosal is related to the unique caecilian dual Gymnophiona (Nussbaum, 1977; Nussbaum, 1983; Wake, 2003; jaw closing mechanism that involves an accessory ventral jaw Müller, 2007), and the reduction of bone coverage in the temporal closing muscle (m. interhyoideus posterior) acting simultaneously skull region was considered to be homologous among caecilians, with the primary jaw closing muscles (mm. levatores mandibulae) frogs and salamanders. Thus, the completely roofed stegokrotaphic (Bemis et al., 1983; Nussbaum, 1983). The movement of the skulls of some caecilians were considered to be secondarily derived squamosal during feeding, as revealed by three-dimensional (3- in association with their burrowing lifestyle (Peter, 1898; Goodrich, D) modeling, is a small mediolateral rocking that does not expose 1958; Parsons and Williams, 1963; Nussbaum, 1983; but see a substantial gap in the skull (Kleinteich et al., 2008; Kleinteich, THE JOURNAL OF EXPERIMENTAL BIOLOGY 834 T. Kleinteich and others Fig.1. Caecilian cranial anatomy and regions that were Premaxillary constrained in the finite element model applied herein. Nasal Surface renderings in dorsal (left), ventral (right) and Prefrontal lateral (bottom) view based on the HRCT data for Ichthyophis cf. kohtaoensis. Caecilian skulls are compact Frontal Vomer and wedge shaped. The maxillopalatine and the os basale are compound bones that can be ontogenetically Maxillopalatine derived from separate ossification centers. For finite element analysis, we applied point loads to the area Squamosal around the nasal capsules (highlighted in pink) and Pterygoid prevented the joint areas of the occipital condyles Parietal (highlighted in green) from translation or rotation in either direction. The terms for cranial bones follow Wake (Wake, Os basale 2003). Occipital condyle Parietal 2 mm Point loads Squamosal Os basale Fixed displacements Prefrontal Nasal Premaxillary Occipital condyle Maxillopalatine 2010). The stem group caecilian E. micropodia, however, differs zygokrotaphic dermophiid caecilian Geotrypetes seraphini shows from extant caecilians by having additional bones in the temporal similar burrowing performance to other stegokrotaphic caecilians region (e.g. a presumed tabular) and a different jaw joint that is (Herrel and Measey, 2010). flat instead of a deep groove (Jenkins et al., 2007), which suggests Here, we present an experimental study where we modified the the presence of a different jaw closing mechanism, possibly 3-D geometry of zygokrotaphic and stegokrotaphic caecilian skulls without movements of the squamosal. to artificially render zygokrotaphic skulls stegokrotaphic and vice Understanding the costs and benefits of one skull type over the versa. We further modified the stegokrotaphic skull models to test other is crucial for evaluating amphibian skull evolution because it a third, akinetic skull type. The original and modified skull gives insight into how strongly the biology of a caecilian is affected geometries were tested using finite element analysis (FEA) for their by its skull. The stegokrotaphic skull would, on casual inspection, performance under the frontal loading regime that caecilians appear better suited to burrowing than the zygokrotaphic skull with encounter during burrowing. The skulls were oriented at different the large unroofed region and, for two caecilian groups with angles relative to their anterior–posterior axis to simulate varying zygokrotaphic skulls, there might actually be an ecological link to directions of the frontal loads that caecilians are likely to encounter poorer burrowing performance; rhinatrematids are considered to be by dorso-ventral movements of the head to manipulate the substrate poor burrowers that can be readily trapped during surface activity (Wake, 1993). The aims of this study were: (1) to evaluate the (Nussbaum, 1983; Gower et al., 2010); typhlonectids are mainly sensitivity of the strain distribution in caecilian skulls as the head aquatic species and may therefore be relieved of the constraints of moves through different angles during burrowing; (2) to quantify burrowing (Wilkinson and Nussbaum, 1997). However, the the difference in deformation of zygokrotaphic and stegokrotaphic zygokrotaphic scolecomorphids are considered to be specialized caecilian skulls under frontal loading; (3) to determine whether burrowers (Nussbaum, 1977; Nussbaum, 1983); furthermore, the deflection during burrowing is affected by the state of the skull Table 1. Specimens used in this study, and parameters for HRμCT imaging Total length Preparation for Energy for HRμCT Resolution of HRμCT I.D. Species (mm) Original skull type HRμCT imaging imaging (keV) dataset (μm) MNHN 1999.8360
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