Protosuchus haughtoni (Busbey & Gow, 1984)

Cowgill, Thomas, Young Fls, Mark T, Schwab, Julia A, Walsh, Stig, Witmer, Lawrence M, Herrera, Yanina, Dollman, Kathleen N, Turner, Alan H & Brusatte, Stephen L, 2023, Cephalic salt gland evolution in Mesozoic pelagic crocodylomorphs, Zoological Journal of the Linnean Society 197 (3), pp. 812-835 : 818-823

PROTOSUCHUS HAUGHTONI

The nasal cavity in Protosuchus haughtoni (BP/1/4770) is almost complete, with only the right dorsolateral portion missing ( Fig. 2 ). The naris and nasal vestibule are oriented anteriorly, and the nasal cavity proper is relatively short compared to more derived crocodyliforms because of the shorter, dorsoventrally tall rostrum. The olfactory region comprises a relatively larger portion of the nasal cavity and shows greater dorsoventral than mediolateral expansion. Ventral to the olfactory region the nasal cavity opens ventrally into a single choana, homologous with the primary choana in mesoeucrocodylians. Lateral to the choana, the antorbital cavity opens laterally from the nasal cavity to create an external antorbital fenestra surrounded by the maxilla dorsally and ventrally and the lacrimal posteriorly ( Fig. 2B ). The dorsal surface of the nasal cavity exhibits a shallow depression ventral to a descending process of the nasals that medially separates two shallow dorsal expansions; at the olfactory region these expansions are significantly deeper ( Fig. 2C ).

Using the Extant Phylogenetic Bracket method, Witmer (1995, 1997) hypothesized that the plesiomorphic archosaur morphology of the nasal gland was positioned dorsally or dorsolaterally within the rostrum and excavated grooved internal surfaces of the bones close to the nasomaxillary suture. A shallow concave internal surface around the nasomaxillary suture is present in Protosuchus ( Fig. 2D ) across the posterior half of the rostrum but is more poorly defined than in the extant crocodylians. The dorsal expansions of the nasal cavity are located dorsomedially to the nasomaxillary suture and are unlikely to be associated with the nasal gland. Instead, they most likely indicate the dorsal surface of the cartilaginous nasal capsule with the descending nasal process inferring the location of the nasal septum.

THALATTOSUCHIA

The nasal cavity reconstructions in the thalattosuchian skulls comprise only the posterior half of the nasal cavity, with the exception of Cricosaurus araucanensis (MLP 72-IV-7-1) where the whole rostrum and nasal cavity is preserved.

The basal thalattosuchian Plagiophthalmosuchus gracilirostris (NHMUK PV OR 15500) shows a nasal cavity morphology comparable to that of extant crocodylians with a tubular nasal cavity proper with an expanded olfactory region at the posterior end of the rostrum ( Fig. 3A, B ). The antorbital cavity opens laterally into a reduced external antorbital fenestra (preserved on the right side of the skull) compared to Protosuchus , which is bordered by the lacrimal dorsally and maxilla ventrally. The nasals comprising the anterodorsal walls of the nasal cavity are missing and the boundaries between the fossilized bones and sedimentary matrix are poorly defined around the olfactory region ( Fig. 3C ), particularly on the dorsal surface, so it is not possible to identify any osteological correlates for either nasal glands comparable to crocodylians or enlarged nasal salt glands in metriorhynchids.

The olfactory region of the nasal cavity is better preserved in the teleosauroid skulls ( Fig. 3 D-I). In Macrospondylus bollensis the olfactory region of both NHMUK PV OR 14436 ( Fig. 3 D-F) and MCZ VPRA-1063 ( Fig. 3 G-I) exhibits two small dorsal expansions ventral to the nasals and medial to the lacrimals, separated by a shallow midline depression ( Fig. 3F, H ), concurring with the previous endocranial reconstruction of MCZ VPRA-1063 by Wilberg et al. (2021). This morphology is better demonstrated in MCZ VPRA-1063 where the whole olfactory region is preserved, whereas only the posterior portion is present in NHMUK PV OR 14436. Despite their occurrence in the olfactory region, when compared to metriorhynchid natural endocasts these expansions are located further dorsally in the olfactory region than the dorsolaterally positioned salt glands ( Fernández & Gasparini, 2000, 2008; Herrera et al., 2013; Fernández & Herrera, 2021). However, their location is comparable to the small olfactory region expansions present in Protosuchus . It is also consistent with shallower dorsal convexities of the natural endocasts identified as part of the olfactory region of the cartilaginous nasal capsule ( Herrera et al., 2013). Therefore, we cannot confidently infer salt glands were present in Macrospondylus from the endocranial reconstructions, and the observed dorsal expansions likely correspond to the nasal capsule instead. The antorbital cavity of Macrospondylus is preserved in MCZ VPRA-1063 and, as with Plagiophthalmosuchus , opens laterally through a small antorbital fenestra. The antorbital fenestra is bordered by the lacrimal dorsally, the maxilla anteriorly and (unlike Plagiophthalmosuchus ) the anterior process of the jugal ventrally.

In the basal metriorhynchoid Pelagosaurus typus (NHMUK PV OR 32599), the olfactory region differs from crocodylians and teleosauroids by possessing a deep ridge on the ventral surface of the nasals, creating a V-shaped depression on the dorsal surface of the olfactory region that separates the shallow dorsolateral expansions on the internal surface of the prefrontals and lacrimals ( Fig. 4 A-E). Such nasal cavity expansions have previously been reported in Pelagosaurus endocranial reconstructions ( Pierce et al., 2017) and, unlike the more dorsally oriented expansions in teleosauroids, the morphology present in Pelagosaurus more closely corresponds to the dorsolateral position of salt glands preserved in natural endocasts of metriorhynchids ( Fernández & Gasparini, 2000, 2008; Herrera et al., 2013; Fernández & Herrera, 2021). Therefore, we concur with Pierce et al. (2017) and can infer that nasal salt glands were present in Pelagosaurus typus from such olfactory region expansions, which may have occupied the lateral portion of these expansions while the dorsal portion (as with the teleosauroid expansions), was likely occupied by part of the nasal capsule. The size of the olfactory region expansions suggests the salt glands of Pelagosaurus were smaller than those observed in metriorhynchid natural endocasts. The posterior end of the nasal cavity bears a shallow dorsolateral groove ventral to the prefrontal that separates the olfactory region expansions into dorsal and lateral portions ( Fig. 4D ) similar to the shallow dorsal groove separating the glands and nasal capsule in metriorhynchid natural endocasts ( Herrera et al., 2013) and likely indicates the same morphology here, with salt glands occupying the lateral portions of the expansions and the nasal capsule occupying the dorsal portions. The antorbital cavity in Pelagosaurus shares with Plagiophthalmosuchus and the teleosauroids a lateral opening through a reduced antorbital fenestra bordered by the lacrimal and maxilla. Dorsal to the antorbital fenestra, a novel antorbital duct is present that opens anteriorly into the nasal cavity through the maxilla anterior to the fenestra ( Fig. 4E ). It is currently unknown what system occupied this duct, but we do not regard this duct as either an extension of the antorbital cavity, as it does not communicate with the antorbital fenestra or as a rudimentary salt duct to facilitate drainage of the salt glands because no posterior opening into the olfactory region is observed.

In Eoneustes gaudryi (NHMUK PV R3263), the expansions of the olfactory region are further enlarged compared to Pelagosaurus , with two bulbous dorsolateral concave depressions on the prefrontals and lacrimals ( Fig. 4 F-H), corresponding to the salt gland location in metriorhynchid natural endocasts ( Fernández & Gasparini, 2000, 2008; Herrera et al., 2013) and the prefrontal depressions reported by Gandola et al. (2006). Thus, we infer that large, hypertrophied nasal salt glands comparable in size to those reported in metriorhynchids were present in Eoneustes . As in Pelagosaurus , a deep ridge on the ventral surface of the nasals and the corresponding V-shaped nasal cavity depression medially separates the two dorsolateral expansions of the olfactory region. In Eoneustes , there is a fenestra in the typical position for an antorbital fenestra. This region of Eoneustes includes a long, obliquely oriented fossa on the external surface of the nasal, maxilla and lacrimal leading to an internal fenestra bordered by the nasal dorsally and lacrimal ventrally. Each fenestra is connected to the nasal cavity by short ducts running posteriorly from the fenestra to the dorsolateral expansions of the olfactory region, comparable to ducts preserved in metriorhynchid natural endocasts ( Fernández & Herrera, 2009). As was reported by Cowgill et al. (2021), no antorbital cavity could be differentiated from the nasal cavity. However, given that antorbital cavities are present in both basal thalattosuchians and more derived metriorhynchids and the closest homologous location of the antorbital cavity is immediately posterior to the dorsal alveolar canal, ventral to the fenestra, we conclude that it was likely present in Eoneustes as well. The ducts connecting the fenestrae to the nasal cavity do not extend to the likely location of the antorbital cavity; thus, there is no evidence that the external fenestra and antorbital cavity are connected, and as such, we refer to it as a pre-orbital fenestra ( Fernández & Herrera, 2009; Leardi et al., 2012).

Among the metriorhynchids, the reconstructed nasal cavity morphology in Cricosaurus araucanensis (MLP 72-IV-7-1) is concordant with the observed internal rostral morphology in natural endocasts from the same species ( Fernández & Gasparini, 2000, 2008; Herrera et al., 2013). The olfactory region shows bulbous dorsolateral expansions expressed as broad depressions on the internal surfaces of the prefrontals with partial extension onto the lacrimals ( Fig. 5A, B, G ) and a shallow dorsolateral ridge separating the inferred location of salt glands from the nasal capsule ( Fig. 5H ). Identical nasal cavity morphologies are present in both Thalattosuchus superciliosus (NHMUK PV R11999) ( Fig. 5C, D, I, J ) and TorƲoneustes coryphaeus (MJML K1863) ( Fig. 5E, F, K, L ). However, in Cricosaurus schroederi (MM unnumbered) no bulbous expansions of the olfactory region are present. The olfactory region itself is dorsoventrally narrow and the nasopharyngeal ducts and antorbital cavities located ventral to this region are larger compared to the other metriorhynchids ( Fig. 6 ). The lack of any dorsoventral compression in the rest of the skull demonstrates this was not a deformation artefact. However, two small lateral expansions of the olfactory region are present medial to the prefrontals in Cricosaurus schroederi and correspond to the salt gland locations in natural casts.

Unlike Pelagosaurus and Eoneustes , no medial V-shaped depression of the nasal cavity occurs in the metriorhynchids, and the olfactory region expansions are instead separated by a smaller ridge on the ventral surface of the nasals creating a shallower depression. The depth and breadth of this depression varies among the sample; in Cricosaurus araucanensis and Thalattosuchus this depression extends across the medial third of the dorsal surface of the olfactory region, but in Cricosaurus schroederi and TorƲoneustes it is limited to a small medial ridge marking the dorsal surface of the cartilaginous nasal septum. The metriorhynchids all have a fenestra in the classic antorbital fenestra position of archosaurs sharing a near identical morphology with each other and Eoneustes , including an oblique external antorbital fossa leading to the internal fenestra. The inferred antorbital cavities of all the metriorhynchids are internalized and do not connect to the fenestrae; at their closest point, the anterior of the antorbital cavity is ventromedial to the fenestra. In Cricosaurus schroederi , short ducts located dorsal to the antorbital cavity connect the fenestra to the lateral expansions of the olfactory region ( Fig. 6C ). Thus, as with Eoneustes , we consider the fenestra in these metriorhynchids to be a pre-orbital fenestra.

Figures

Figure 2. Internal rostral anatomy of Protosuchus haughtoni (BP/1/4770) showing the nasal cavity and antorbital fenestra. A, B, dorsal (A) and left lateral (B) views with skull rendered transparent. C, D, transverse CT slices of nasal cavity showing the concavities where the nasal glands are inferred (C) and small dorsal expansions of the olfactory region (D). Internal reconstruction colours: nasal cavity, yellow; antorbital fenestra, green. Scale bars equal 10 mm (A, B) and 5 mm (C, D).

Figure 3. Internal rostral anatomy of basal thalattosuchian Plagiophthalmosuchus gracilirostris [NHMUK PV OR 15500 (A-C)] and teleosauroid Macrospondylus bollensis [NHMUK PV OR 14436 (D-F) and MCZ VPRA-1063 (G-I)]. A, B, Plagiophthalmosuchus in dorsal (A) and anterodorsal views (B). C, transverse CT slice of nasal cavity olfactory region. D, E, NHMUK PV OR 14436 in dorsal (D) and anterodorsal views (E). F, transverse CT slice of nasal cavity olfactory region showing small dorsal expansions where of the olfactory region where the nasal capsule is inferred. G, H, MCZ VPRA-1063 in dorsal (G) and anterodorsal views (H). I, transverse CT slice showing dorsal expansions of the olfactory region. All skulls are rendered transparent. Internal reconstruction colours: nasal cavity, yellow; antorbital fenestra, green. Scale bars equal 50 mm (A, B, D, E, G, H) and 10 mm (C, F, I).

Figure 4. Internal rostral anatomy of basal metriorhynchoids Pelagosaurus typus [NHMUK PV OR 32599 (A-E)] and Eoneustes gaudryi [NHMUK PV R 3263 (F-H)]. A-C, Pelagosaurus in dorsal (A), anterodorsal (B) and left lateral views (C) with the skull rendered transparent. D, E, transverse CT slices of nasal cavity olfactory region showing dorsal expansions where salt glands are inferred, the dorsolateral groove separating the inferred positions of salt glands and the nasal capsule (D) and the nasal ridge creating a V-shaped depression of the olfactory region ventral to the nasals (E). F-G, Eoneustes in dorsal (F) and left lateral views (G) with the skull rendered transparent. H, transverse CT slice of nasal cavity olfactory region showing the left salt duct, larger dorsolateral expansions where salt glands are inferred and ridge on the ventral surface of the nasals. Internal reconstruction colours: nasal cavity, yellow; nasopharyngeal ducts, pale yellow; antorbital fenestra, green; preobrital fenestra, light green. Scale bars equal 50 mm (A-C, F, G) and 10 mm (D, E, H).

Figure 5. Internal rostral anatomy of metriorhynchids Cricosaurus araucanensis [MLP 72-IV-7-1 (A, B, G, H)], Thalattosuchus superciliosus [NHMUK PV R 11999 (C, D, I, J)] and TorƲoneustes coryphaeus [MJML K1863 (E, F, K, L)]. A, B, Cricosaurus araucanensis in dorsal (A) and left lateral view (B). C, D, Thalattosuchus in dorsal (C) and left lateral view (D). E, F, TorƲoneustes in dorsal (E) and left lateral view (F). G-L, transverse CT slices of nasal cavity olfactory region of Cricosaurus araucanensis (G, H), Thalattosuchus (I, J) and TorƲoneustes (K, L) showing the pre-orbital fenestra external opening (G, I, K) and dorsolateral expansions of olfactory region where salt glands are inferred (H, J, L). All skulls are rendered transparent. Internal reconstruction colours: nasal cavity, yellow; nasopharyngeal ducts, pale yellow; antorbital cavity/sinus, green; preobrital fenestra, light green. Scale bars equal 50 mm (A-F). and 10 mm (G-L).

Figure 6. Internal rostral anatomy of Cricosaurus schroederi (MM unnumbered). A, B, dorsal (A) and left lateral views (B) with the skull rendered transparent. C, D, transverse CT slices of the nasal cavity olfactory region showing salt ducts (C) and small lateral olfactory region expansions where salt glands are inferred (D). Internal reconstruction colours: nasal cavity, yellow; nasopharyngeal ducts, pale yellow; antorbital cavity/sinus, green; preobrital fenestra, light green. Scale bars equal 50 mm (A, B) and 10 mm (C, D).