Phosphotriton sigei, Tissier & Rage & Boistel & Fernandez & Pollet & Garcia & Laurin, 2016

Tissier, Jérémy, Rage, Jean-Claude, Boistel, Renaud, Fernandez, Vincent, Pollet, Nicolas, Garcia, Géraldine & Laurin, Michel, 2016, Synchrotron analysis of a ‘ mummified’ salamander (Vertebrata: Caudata) from the Eocene of Quercy, France, Zoological Journal of the Linnean Society (Zool. J. Linn. Soc.) 177 (1), pp. 147-164 : 150-158

PHOSPHOTRITON SIGEI SP. NOV.

Holotype

An incomplete ‘mummified’ body of a salamander ( MNHN.F. QU17755 ).

Type locality

Unknown locality of the Phosphorites du Quercy, southwestern France.

Horizon

Likely Eocene (late Middle or Late Eocene).

Etymology

After Bernard Sigé, one of the main contributors of the Quercy campaigns.

Diagnosis

A non-elongate, lunged caudate amphibian referred to Pseudosauria, based on the presence of a median process on the ischium, clearly separated para- and diapophyses on trunk vertebrae, spinal nerves exiting intravertebrally in caudal vertebrae, and in lacking articulated ribs in the caudal region. Tentatively referred to Salamandridae on the basis of having a paired sacral rib, a median notch in the posterior border of the neural arch, neural spines low on trunk vertebrae, neural spines present on caudal vertebrae, a bony lamina connecting para- and diapophyses, and spinal nerves exiting intravertebrally in posterior trunk vertebrae. Differs from other Pseudosauria by the presence of an anterior interzygapophyseal ridge, a dorsal alar process extending between the parapophysis and prezygapophysis and amphicoely of centrum, an association of characters that is unique within the clade.

Description

External morphology

The fossil ( Fig. 2 ) shows body proportions that are fairly primitive for tetrapods, and that are retained among extant taxa in many urodeles and squamates. It is approximately 60 mm long, about 2 cm wide anteriorly, and its thickest part is slightly more than 1 cm. The head, anterior part of the thorax, and anterior limbs are lacking. The posterior limb and the tail are incomplete. The specimen is globally fusiform, except for the hindlimb fragments that emerge from the pelvic area and are directed anteriorly. The caudalmost part is much thinner (<0.5 cm wide) than the anterior part. The specimen is best preserved on its left side.

The skin does not show any scales, which suggests that it is a salamander, rather than a squamate. In dorsal view ( Fig. 2A ), the vertebral column and some ribs can be distinguished beneath the skin. At least five costal grooves appear on the left side of the mummy, in dorsal view. They are found on most caudates, with different counts according to the species. A longitudinal fold, going from the level of the pelvic girdle to the anterior part of the specimen, is visible on the ventral face ( Fig. 2B ), and may result from the position of the animal on the substratum during fossilization. A longitudinal slit of a few millimeters long, posterior to the hindlimbs, probably represents the cloaca. It is not to be confused with the small square damaged area just anterior to it, which is a missing fragment of skin. Cranially, pisoliths (mineral concretions) are visible where the inside of the thorax once was.

Skeleton

Tomography revealed that the whole skeleton of the actual part of the animal is preserved and is in anatomical position ( Fig. 3A ). Six trunk vertebrae (v3– v8) are complete, each being articulated to a complete rib on both sides of the specimen. Two other, more anterior vertebrae are incomplete, here labeled v1 and v2. Throughout this description, the position of vertebrae refers to the specimen in its current state, not as if it were complete, i.e. v1 is the anteriormost preserved vertebra, not the atlas. This is necessary because the number of missing vertebrae is uncertain. The first preserved vertebra (v1) is connected to a complete rib on the left side, but the right side is missing. v2 is connected to a complete rib on the left and to an incomplete rib (the proximal end is not preserved) on the right. The left rib-bearer is incomplete. Two other rib fragments are also present anterior to v1, for which the proximal extremities are missing: they must have been connected to two other unpreserved vertebrae, anterior to v1. Seventeen trunk ribs are preserved (at least partially): ten on the left and seven on the right.

The sacrum (v9) is preserved and articulates to v8 anteriorly and to the first caudosacral vertebra ( CS 1). Rib-bearers are more massive than on the other vertebrae, and each articulates to a sacral rib. These ribs are shorter than trunk ribs, but stouter. v9 presumably articulated (through cartilaginous tissues) to the ilium, but the connection is not preserved (in fact, no cartilage is preserved at all in this specimen). The ilium articulates to the ischium, which connects to its mate ventrally. The pubis is not preserved. The femur is incomplete on both sides: it articulates to the ilium; its distal extremity is broken off.

Two caudosacral vertebrae and three caudals are preserved and complete to subcomplete. Shrunken ribbearers are present but no ribs articulate with them. In addition, a fragment of a caudal vertebra (C4) is connected to the last caudal vertebra but it is very poorly preserved. Therefore, the specimen possessed at the very least 11 trunk vertebrae (sacrum included) and six caudal vertebrae, but obviously more because the tail and trunk region are very incompletely preserved ( Fig. 4 ).

Vertebral column

The vertebrae display the overall morphology that occurs in short-bodied, four-limbed urodeles ( Estes, 1981; Ratnikov & Litvinchuk, 2007; Fig. 3B–F ). All vertebrae are amphicoelous. There are neither subcentral keels nor basapophyses. In ventral view ( Fig. 3C ), the centrum is hourglass-shaped. The shape, size, and number of subcentral foramina are highly variable along the vertebral column. A median notch indents the neural arch posteriorly, which therefore forms two posterior rounded projections ( Fig. 3B and C ); the posterior part of the neural spine is also affected by the notch. The neural canal is wide, high, and its cross section is pentagonal. Within the neural canal there are no visible spinal cord supports ( Skutschas & Baleeva, 2012), but because these structures are very thin and difficult to see on tomograms (P.P. Skutschas, pers. comm., 2014) they cannot be definitely regarded as absent. Furthermore, a little prominence is in fact visible on some vertebrae, on the ventrolateral part of the neural canal, which could be interpreted as the base of such sup- ports. The articular facets of the prezygapophyses and postzygapophyses are circular. The anterior borders of the prezygapophyses protrude beyond the anterior limit of the centrum ( Fig. 3B ). The posterior edges of the postzygapophyses extend beyond the posterior extremity of the centrum. In posterior view, the articular surfaces of the postzygapophyses make an angle of approximately 23° with the horizontal ( Fig. 3E ).

Each rib-bearer comprises a dorsal and a ventral process. These processes are here referred to as the diapophysis (dorsal) and parapophysis (ventral), following Skutschas (2013), although homology with the diapophyses and parapophyses of other tetrapods is not demonstrated ( Wake & Lawson, 1973). The ribbearers are directed posterolaterally: the angle between them and the vertebral axis (the ‘transverse process angle’ or ‘TPA’ in Babcock & Blais, 2001) is around 108° ( Fig. 3B ). The dia- and parapophysis are widely separated, and they are connected by a bony lamina that extends along most of their length ( Fig. 3E and F ). The diapophysis is slightly posterior to the parapophysis, and is more slender. The articular surfaces for ribs are circular.

The anterior and posterior interzygapophyseal ridges are well developed and horizontal ( Fig. 3B and C ). The weak posterior ventral crest forms a horizontal ridge ( Fig. 3C, D and E ). The vertebrae lack an anterior ventral crest, but an oblique crest joins the parapophysis to the prezygapophysis. It is analogous (but perhaps not homologous) to the dorsal alar process ( Gardner, 2003) that occurs in the Sirenidae ; for the sake of convenience, we call this crest ‘dorsal alar process’, as that of sirenids ( Fig. 3D and F ). Between this dorsal alar process and the anterior interzygapophyseal ridge is a deep fossa (which we call the lateral fossa) in which opens a large foramen ( Fig. 3D ). Aside from sirenids, the dorsal alar process appears to exist only in pleurodeline salamandrids ( Bailon, Rage & Stoetzel, 2011).

Trunk vertebrae

These vertebrae are very homogeneous in size and shape. The centrum measures approximately 5.7 mm long, and the vertebrae are between 6.4 (v8) and 6.0 (v3) mm wide (rib-bearers included); their width increases caudally.

The neural arch is moderately vaulted and its position is rather elevated with regard to the centrum: the angle formed between the posterodorsal end of that arch and the zygapophyseal plane is 16° for the anteriormost ( Fig. 5A ) and 10° for the posteriormost vertebrae ( Fig. 5B ). The anterior margin of the neural arch is concave between the two prezygapophyses ( Fig. 3B ). The neural arch bears a neural spine. The latter is thin and poorly developed, and it is strongly reduced on the posteriormost trunk vertebra (v8) ( Fig. 3A ). When present, it does not extend to the anterior extremity of the neural arch, but only halfway.

In anterior view ( Fig. 3F ), a large foramen (termed the anterior foramen here) is present on each side, laterodorsal to the anterior cotyle; it pierces the base of each prezygapophyseal buttress. It is connected to the subcentral foramen (where present; Fig. 3C ). In posterior view, a paired fossa ( Fig. 3E ) is present on the posteroventral face of the posterior part of the neural arch, mediodorsal to the postzygapophyses. It is shallow and ellipsoid. A notochordal canal is present at the centre of the cotyles and is rather small ( Fig. 3E and F ).

The parapophysis is horizontal, whereas the diapophysis is directed slightly dorsally. The space and bony lamina extending between the dia- and parapophysis are narrower on v8 than on the more anterior vertebrae.

Caudal to the rib-bearers and between the posteri- or interzygapophyseal ridge and the posterior ventral crest a foramen for the spinal nerve is present ( Fig. 3D ). The foramen is small on the anteriormost vertebrae and becomes very large on the last trunk vertebra (v8).

Sacrum

A single sacral vertebra (v9) is present. It is much more robust and depressed than the other vertebrae ( Fig. 6A ). It is also wider across the rib-bearers than long. The neural arch is clearly depressed, with an angle of 10° between the zygapophyseal plane and the posterior end of the neural arch. The neural spine is reduced to a very weak, almost vestigial ridge. There are three nearly circular subcentral foramina.

The spinal nerve foramen is located on the same position as in the other vertebrae, but is larger than on v8 ( Fig. 6B ). Two other foramina are present, dorsal and ventral to this spinal nerve foramen; these may represent vascular foramina, and/or roots for the spinal nerve. The dorsalmost foramen is smaller than the ventralmost foramen, and both are much smaller than the spinal nerve foramen. The dorsal foramen is connected to the neural canal, whereas the ventral foramen is connected to one of the subcentral foramina. The ventral foramen was therefore probably a vascular foramen, whereas the dorsal foramen may have been used by an unidentified nerve.

In addition, this vertebra differs from the others by the shape and size of its rib-bearers: they are longer and thicker ( Fig. 6A ). The diapophysis and parapophysis are in contact with each other on most of their length, but the bony lamina is still present between their distal portions. In dorsal view, the right rib-bearer is longer than the left rib-bearer, because of an outgrowth on the diapophysis. Finally, the sacral vertebra differs from other vertebrae in the absence of a notochordal canal. Caudal region

At least six postsacral vertebrae are preserved, but the last one (C4) is very incomplete ( Fig. 6C ). The general morphology of these vertebrae is quite variable. The first two vertebrae ( CS 1 and CS 2) are termed caudosacral: they differ from the more posterior vertebrae, i.e. the caudal vertebrae, in lacking haemal arches ( Ratnikov & Litvinchuk, 2007). CS 1, CS 2, and the first caudal, C1, are wider (rib-bearers included) than long, whereas C2 and C3 are as long as wide. The global size and the width of the neural arch of these vertebrae diminish caudally: CS 1 is twice as wide as C3. The neural spine, which is strongly reduced on v8 and on the sacral vertebra, is developed in the caudal region, except for CS 1. The angle between the posterodorsal edge of the neural spine and the zygapophyseal plane varies between 18° (on C1, the highest vertebra) and 13° (on C3), but it does not decrease in a regular way.

Contrary to the other vertebrae, no ribs articulate to the postsacrals, even though rib-bearers are still present. On CS 1, the diapophysis and parapophysis remain distinct distally, and their extremities still form round facets. On CS 2, dia- and parapophysis are still separated distally, but their extremities are compressed anteroposteriorly and they no longer form facets. In the three well-preserved caudals (C1–C3), the dia- and parapophysis merge distally and form a single, vertically compressed extremity. The size of the ribbearers decreases posteriorly. The neural spine is thinner and higher than on trunk vertebrae. The spinal nerve foramen of CS 1 and CS 2 is nearly the same size as on the sacral vertebra; it becomes smaller on the more posterior vertebrae. Other small foramina are present anteroventral and anterodorsal to this foramen, and are irregularly distributed. Several other unidentified foramina are present on these vertebrae. The notochordal canal is open.

The haemal arches are at least partly preserved on C1, C2, and C3. They are deeply curved posteriorly (at least on C1, on which it is almost complete; it is too incomplete on the other vertebrae to assess this). The distal extremity does not seem completely ossified.

Ribs

Fourteen well-preserved presacral ribs are in anatomical position (eight on the left side and six on the right side), and three others are fragmentary (two on the left side and one on the right side; Fig. 3A ). They are all bicapitate, as in most urodeles, and the articular facets are circular. Compared with other urodeles, the ribs are relatively long ( Fig. 4 ), although their length does not reach 10 mm and are weakly curved to almost straight.

Presacral ribs

The ventral articular head (which connects to the parapophysis) is usually larger than the head articulating to the diapophysis ( Fig. 6D ). The diameter of each rib is constant for all of the rib length (the rib does not taper distally; Fig. 3A ), except for the articular heads, which are broader. Rib curvature and (even more) length are generally greater cranially than caudally, and the last presacral ribs are nearly straight.

Sacral ribs

One sacral rib is connected on each side of the sacral vertebra. They are shorter and more robust than presacral ribs ( Fig. 6E ). The right one is in anatomical position, whereas the left is slightly disarticulated. The distal extremity of these ribs was connected to the ilia. The three articular facets (for the parapophysis, diapophysis, and ilium) are circular. A short uncinate process is present posterodorsally.

Pelvis and femora

The paired ilium and ischium are preserved almost in anatomical position ( Fig. 7 ); the ischium appears to be slightly shifted posteriorly with regard to the ilium. The femur is broken on both sides; only the proximal ends are preserved ( Fig. 7A ). It is directed anteriorly. The pubis, which ossifies only in some urodele taxa, is not preserved. There is no trace of an epipubis (ypsiloid cartilage).

The ilium comprises two portions ( Fig. 7B ): the acetabular portion, which articulates ventrally to the femur and the ischium, and a posterodorsally direct- ed shaft, which articulated to the sacral rib. The shaft is straight and it scarcely expands posterodorsally. It lacks crests and its cross section is approximately oval. The median surface of the acetabular region is smooth, as in most urodeles (Roček et al., 2012), and flat. The ventral limit of the ilium is convex; it forms the sutural surface for the pubis and ischium. The anterior area of the sutural surface is broad and semicircular, whereas the posterior part is elongate and clearly narrowed. At least the anterior part of the broad area was in contact with the pubis, whereas the narrow area was sutured to the ischium. The acetabulum is subtriangular and shallowly concave; its anterior margin is parallel with the shaft axis. The articular surface occupies almost the entire acetabular portion. The margins of the acetabulum are not clearly distinct; they do not project laterally, except in their dorsal portion, where they form a marked tubercle. The latter tubercle is not homologous to the ventrolateral tuberosity that occurs in some extant and extinct urodeles ( Gardner et al., 2010). The ventrolateral tuberosity is distinct from the acetabular margin, whereas in P. sigei gen. et sp. nov. the tubercle is a part of the margin. Ventrally, the articular surface of the acetabulum was completed by the ischium.

The ischium is a thin plate in which the anterior part is only lightly ossified ( Fig. 7C ). The caudal part produces a short posteromedial process and an elongate, slender posterolateral process. The anterior edge of the ischial plate forms a gutter, which indicates the insertion of the cartilaginous pubis. A medial cartilaginous symphysis probably joined the two plates, but it is not visible on the tomograms. The ventral part of the articular surface of the acetabulum is located anterolaterally on the ischium; it protrudes laterally.

On the femur, the femoral crest (crista trochanterica; Venczel, 2008; Skutschas & Gubin, 2012) is well developed ( Fig. 7A ). It extends to the greater trochanter, which forms a strong projection directed posteroventrally on the ventral face, close to the proximal extremity of the femur. The outline of the distal extremity of the trochanter is ovoid. The trochanter diverges sharply from the femoral shaft. Between the base of the trochanter and the proximal extremity of the femur, extends the marked trochanteric groove ( Vasilyan & Böhme, 2012) that appears to be present in most (all?) urodeles with non-reduced limbs. The cartilaginous cap of the proximal extremity of the femur is not preserved ( Fig. 7D ).

Lung

Several types of soft tissues are preserved and may be identified on the tomograms. A histological study will be undertaken to determine their nature. One organ is discussed here, however, because it is of significant interest for our phylogenetic study: the lung.

The lung is present at the anteriormost part of the specimen ( Fig. 7E ). It is triangular in ventral view, with its tip directed caudally, and flattened in cross section ( Fig. 7F ). The cranial part of the lung is missing, which makes identification difficult. Nevertheless, the position of this organ in the body, its shape, and its ‘honeycombed’ internal structure suggest that it is a lung ( Francis, 1934; M. Laurin, pers. observ.).

Figures

Figure 2. Photograph of MNHN.F.QU17755, holotype of Phosphotriton sigei gen. et sp. nov. in dorsal (A) and ventral (B) views. The old collection number (1903–20) is partially visible. CG, costal groove; cl, cloaca; d, damaged area; f, fold; hl, hindlimb; pis, pisolith; r, rib; vc, vertebral column.

Figure 3. A, skeleton of MNHN.F.QU17755 in dorsal view. B–F, trunk vertebra (v6) in dorsal (B), ventral (C), left lateral (D), posterior (E), and anterior (F) views. G–J, trunk vertebrae in posterolateral view, illustrating a type-III disposition of the spinal nerves (Edwards, 1976) in Paramesotriton deloustali (Bourret, 1934) (G), Pseudobranchus striatus (LeConte, 1824) (H), Ambystoma opacum (Gravenhorst, 1807) (I), and Bolitoglossa mexicana Duméril, Bibron and Duméril, 1854 (J). Abbreviations: ac, anterior cotyle; af, anterior foramen; air, anterior interzygapophyseal ridge; bl, bony lamina; c, centrum; d, diapophysis; dap, dorsal alar process; f, fossa; lf, lateral fossa; LF, left femur; LI, left ilium; Lis, left ischium; mn, median notch; na, neural arch; nc, neural canal; noc, notochordal canal; nsp, neural spine; p, parapophysis; pc, posterior cotyle; pir, posterior interzygapophyseal ridge; po, postzygapophysis; pr, prezygapophysis; pvc, posterior ventral crest; rb, ribbearer; RF, right femur; RI, right ilium; Ris, right ischium; s, sacrum; scf, subcentral foramen; snf, spinal nerve foramen.

Figure 4. Three-dimensional reconstruction of the skeleton of Phosphotriton sigei gen. et sp. nov. (B), scaled to the same length as other Eurasian urodeles: a European plethodontid, Hydromantes italicus Dunn, 1923 (A), and two salamandrids, Hypselotriton orientalis (David, 1873) (C) and Salamandra salamandra (Linnaeus, 1758) (D).

Figure 5. A, v1 in left lateral view with value for the angle between the posterior end of the neural arch and the zygapophyseal plane. B, v8 in left lateral view, with value of the same angle.

Figure 6. A, sacrum in anterior view (left, 3D reconstruction; right, labelled drawing), with abbreviations as defined in the legend to Figure 3. B, sacrum in posterolateral view, illustrating the spinal nerve foramen. C, articulated caudosacral and caudal vertebrae in left lateral view. D, left trunk rib articulating on v3 in anterior view. E, sacral rib in posterior view. Legend: da, dorsal articulation; ha, haemal arch; pa, posteroventral articulation with ilium; up, uncinate process; snf, spinal nerve foramen; va, ventral articulation.

Figure 7. Three-dimensional reconstructions of various parts of the skeleton (A–D) and of the lung (E, F). A, right and left femora in lateral and proximal views. B, left ilium in medial and lateral views. C, left and right ischia in dorsal view. D, pelvic bones in dorsal (top) and ventral (bottom) views; green (light grey in print), femur; light blue (medium grey in print), ischium; and dark blue (dark grey in print), ilium. E, virtual cross section of the anteriormost part of MNHN.F.QU17755, showing part of the preserved lung. F, three-dimensional reconstruction of the preserved part of the lung, in ventral view. Abbreviations: ac, acetabulum; ama, anterior margin of the acetabulum; Ant., anterior; ct, crista trochanterica; gt, greater trochanter; plp, posterolateral projection; pmp, posterior median process; sh, shaft; tb, tubercle; trg, trochanteric groove; Vent., ventral.