Morphology of the Braincase of Eocaecilia Micropodia

The holotype of Eocaecilia micropodia (MNA V8066) preserves a virtually complete skull and articulated lower jaws (Figure 1). Micro-computed tomography (µCT) confirms that the braincase of Eocaecilia micropodia consists of two bones (Figure 2A–C), similar in general morphology to the two composite bones comprising the braincase in extant caecilians, i.e., the sphenethmoid and the os basale [32]. The sphenethmoid of E. micropodia has relatively long lateral walls that make up more than 50% of the preserved length of the sphenethmoid (Figure 2A). The dorsal sutural surfaces for connecting to the dermal skull roof appear to be narrow, but it is difficult to determine whether the dorsal margins of the lateral walls are broken or are preserved in their natural state.

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larger image TIFF original image Download: Figure 2. The braincase and middle ear ossicle of Eocaecilia micropodia as revealed by µCT. A–C, three-dimensional digitally segmented braincase of the holotype (MNA V8066) in dorsal, left lateral and ventral views, respectively, with the sphenethmoid (orange) and the os basale (blue). D–E, surface renderings of an isolated braincase referred to E. micropodia (MNA V8063) in dorsal and ventral views, respectively. The alternative hypotheses of foramen identity are depicted in blue and green. F–H, three-dimensional digitally segmented middle ear ossicle of E. micropodia (MNA V8066) in dorsal, left lateral, and ventral views respectively. This element is termed the stapes-quadrate by Jenkins et al. [14] because of the hypothesized fusion of these two elements. Abbreviations: ant., antotic region; ant.w., antotic wall; a.l.p., anterolateral process; d.s., dorsal surface of the otic capsule; f.c.a., foramen for the carotid artery; f.d.v., foramen for a dorsal vein; f.j., jugular foramen; f.s., stapedial foramen; f.v., fenestra vestibuli; f.1, foramen 1 (see text for interpretation); f.2, foramen 2 (see text for interpretation), f.V mx,md , foramen for the maxillary plus mandibular trunk of the trigeminal nerve; f.V op , foramen for the ophthalmic branch of the trigeminal nerve; n.s., nasal septum; oto., otic-occipital complex; o.ca., otic capsule. https://doi.org/10.1371/journal.pone.0050743.g002

The anterolateral corners of the main body of the sphenethmoid bear robust, ossified, anterolaterally-directed processes (a.l.p.; Figure 2A,C) that strongly resemble the condition seen in many extant caecilians [28]. The data acquired from µCT show these to be longer than depicted in the reconstruction of Jenkins et al. [14]. Jenkins et al. [14] identified two foramina located within each anterolateral process of the sphenethmoid in E. micropodia. The first, a large foramen located in the base of the process, was justifiably identified as transmitting the ophthalmic branch of the trigeminal nerve (f.V op ; Figure 2C), based on observations of consistency of this arrangement in extant caecilians [27]. An additional foramen located dorsal to that for the ophthalmic branch of the trigeminal nerve was identified as a foramen transmitting a vessel. This foramen is not visible in MNA V8066, but is present in MNA V8059. The interpreted identity of this second foramen as a vascular foramen is reasonable given the similarity with the condition seen in several extant caecilians [14]. An alternative interpretation may be that the superficial ramus of the facial nerve splits from an anastomosis with the ophthalmic branch of the trigeminal nerve prior to entering the anterolateral process of the sphenethmoid, resulting in a second foramen, as seen in Geotrypetes seraphini and Herpele squalostoma [27], [28].

A dorsomedial process (mesethmoid of some authors [15]) like that of extant caecilians was not seen in the µCT data. If such a process were present, but not preserved in any specimen, the positional relationship between the sphenethmoid and dermal skull indicates it would have been located just deep to the frontals. Because there is no fontanelle between the frontals, dorsal exposure of the sphenethmoid on the skull roof is precluded.

Anteriorly the sphenethmoid is completed by a wall that separates the nasal capsules from the brain cavity, as seen in extant caecilians. The µCT reconstruction reveals that the anterior wall is perforated by two pairs of foramina (f.I D and f.I V ; Figure 3A, B). The paired dorsal and ventral anterior foramina lie close to the midline of the sphenethmoid. These are interpreted here, based on similarity with the condition seen in extant caecilians (Figure 3C), as serving the olfactory nerve. The paired dorsal and ventral foramina suggest the olfactory nerve was bifurcated into dorsal and ventral trunks upon emergence from the brain, as it is in all extant caecilians [27], [33].

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larger image TIFF original image Download: Figure 3. Identification of paired dorsal and ventral foramina, serving the likely transmission of the paired trunks of the olfactory nerve, similar to the condition seen in extant caecilians. A, µCT image of a transverse section through the level of the anterior sphenethmoid in E. micropodia (MNA V8066), showing the location of dorsal and ventral foramina in the anterior wall of the sphenethmoid. B, posterior view of the three-dimensionally segmented sphenethmoid of E. micropodia, further showing the locations of the anterior foramina interpreted here as those serving the dorsal and ventral trunks of the olfactory nerve. C, posterior view of the three-dimensionally segmented sphenethmoid of the extant caecilian Dermophis mexicanus (UMMZ 219030), showing the location of comparable foramina known to transmit the trunks of the olfactory nerve [14]. Abbreviation: f.I D , foramen for the dorsal branch of the olfactory nerve; f.I V , foramen for the ventral branch of the olfactory nerve. https://doi.org/10.1371/journal.pone.0050743.g003

The nasal region is represented by an ossified short, robust nasal septum (n.s.; Figure 2B). It is not known whether the tip of the nasal septum is complete or broken. A broad dorsal sutural surface extends anteriorly from the main body of the sphenethmoid to over the nasal septum. It tapers sharply in width towards the tip (Figure 2A). The ventral margin of the nasal septum is narrow. There is no evidence of sola nasi in E. micropodia.

The antotic walls (or pleurosphenoid of some authors [23]) are long and subparallel in dorsal view in E. micropodia (ant.w.; Figure 2A). The dorsal margins of the antotic walls appear incomplete and therefore the nature of the dorsal sutural surface is unknown. The anterior margins of the antotic walls may also be incomplete in the holotype of E. micropodia, but Jenkins et al. [14] describe a concave anterior margin, likely corresponding to the posterior margin of the optic foramen, as in extant caecilians [28].

Much of the antotic region is poorly preserved in the holotype specimen (ant.; Figure 2B). However, the right side of the specimen consisting of the isolated braincase (MNA V8063) yields some additional information (Figure 2D, E). There are three larger foramina present. Foramen one (f.1; Figure 2E) is located dorsally, just anterior to the otic capsule. A slightly larger second foramen is present ventral to this one (f.2; Figure 2E). The third foramen (f.3, Figure 2E) is located ventral and slightly posterior to the first two, along the anteroventral margin of the otic capsule. The latter two (f.2 and f.3; Figure 2E) were identified by Jenkins et al. [14] as those pertaining to the trigeminal and facial nerves, respectively. The location of foramen one occurs in a similar location to the foramen seen among the extant forms to transmit a dorsal vein [27], which may be the case for E. micropodia as well. An alternative interpretation is one in which the two trunks of the trigeminal nerve, the maxillary plus mandibular trunk and the ophthalmic trunk, exit the braincase from foramen one and two, and the facial nerve from foramen three (Figure 2E). An additional foramen serving a dorsal vein may have been present but is not preserved by the broken dorsal portion of the wall. Given the relative positions and sizes of the foramina, in comparison to those seen in extant caecilians, the latter hypothesis is preferred here and is most similar to the condition seen in rhinatrematid, dermophiid, and siphonopid caecilians (Pattern 1 of Maddin [27]). A small, fourth foramen is present in the antotic region, located anterior to the three just described (f.c.a.; Figure 2E). A groove runs anteriorly from this foramen, and it was reasonably identified as that for the anterior branch of the internal carotid artery [14]. A similarly located foramen serves this function in extant caecilians.

The otic-occipital complex of the braincase (oto.; Figure 2B) is very similar in morphology to that of most extant caecilians. The dorsal surface of the complex forms the roof of the posteriormost portion of the brain cavity (d.s.; Figure 2A). The surface on each side tapers in width towards the midline. In E. micropodia, however, the surface remains relatively broad in comparison with that of most extant caecilians. The dorsal surface of the otic-occipital complex is slightly concave on either side. It is unclear whether the postparietals (plesiomorphic, discrete ossifications posterior to the parietals) contribute to the occipital surface, or if the entire occipital surface is composed only of the braincase, similar to the condition seen in basal caecilians such as Rhinatrema bivittatum and Epicrionops bicolor [28]. It is also unclear from the µCT data whether the anterior margin of the dorsal surface bears a thin sutural surface that receives the postparietals in E. micropodia, similarly to that which receives the parietals in most extant caecilians, where postparietals are presumed lost. The lateral surface of the otic capsule is occupied by a large, laterally facing fenestra vestibuli. The occipital condyles are continuous in profile with the posterior margin of the otic-occipital complex in the holotype specimen (o.ca.; Figure 2B and E). In the isolated braincase the condyles appear somewhat more posteriorly protuberant (Figure 2D), but the incomplete posterior margins of the otic capsules may give an inaccurate appearance of condyle protrusion. The condyles, however, are small in comparison to those of most extant caecilians. A jugular foramen is present between the otic capsule and the occipital condyle (Figure 2E).

The anterior portion of the floor of the os basale is triangular in outline (Figure 2C), similar to the condition seen in Rhinatrema bivittatum. The floor extends to reach the tip of the preserved portion of the nasal septum. Jenkins et al. [14] described the presence of three depressions in the floor of the brain cavity: one posterior depression and a pair of anterior depressions. The posterior depression likely corresponds to that seen in extant caecilians for the hypophysis of the brain, and the anterior pair of depressions likely corresponds to those associated with the large cerebral hemispheres of the brain, also seen in extant caecilians [27]. Well-developed, wing-like basicranial articulations are absent from E. micropodia. Also absent is a well-defined muscle attachment site on the ventral surface of the otic-occipital complex (Figure 2) that is often present in extant caecilians.

The structures of the middle ear are intimately associated with the braincase of tetrapods and are therefore given consideration here. Eocaecilia micropodia possesses an atypical configuration of bones in the middle ear region, making interpretation of the homology of elements difficult. A large element applied to the lateral surface of the otic capsule with a discrete foramen and jaw articulation was interpreted by Jenkins et al. [14] as a fusion of the stapes and quadrate (i.e., the stapes-quadrate; Figure 2F–H). An additional element resembling a small disc-like bone, closely associated with the fenestra vestibuli and stapes-quadrate, was interpreted as an operculum [14]. An alternative hypothesis is one in which the element identified as the operculum is the stapes, and the larger element consists of the quadrate alone [14], [16].