Evidence for a novel cranial thermoregulatory pathway in thalattosuchian crocodylomorphs

Palatal structures in crocodylomorpha

The presence of palatal grooves is one of the defining characteristics of Thalattosuchia (Andrews, 1913; Parrilla-Bel et al., 2013; Foffa & Young, 2014; Johnson et al., 2019; Johnson, Young & Brusatte, 2020; Aiglstorfer, Havlik & Herrera, 2020; Young et al., 2020a, 2021). As we note herein, these grooves are not found in extant crocodylians, irrespective of their ontogenetic stage. Given that no other mesoeucrocodylian taxon with a maxillopalatine secondary palate has been observed to have palatal grooves, we posit that they are synapomorphies of Thalattosuchia. This is in agreement with phylogenetic analyses that have found these features to be explicit thalattosuchian synapomorphies (e.g., Johnson, Young & Brusatte, 2020; Young et al., 2020a, 2021).

Some notosuchians are known to have prominent palatal openings. Paired foramina are present at the maxilla-palatine boundary in species referred to Notosuchidae and Sphagesauridae, namely: Notosuchus terrestris (Andrade & Bertini, 2008a; Barrios et al., 2018), Mariliasuchus amarali (Andrade, Bertini & Pinheiro, 2006; Zaher et al., 2006), Llanosuchus tamaensis (Fiorelli et al., 2016), and Caipirasuchus mineirus and Caipirasuchus stenognathus (Pol et al., 2014; Martinelli et al., 2018). Curiously, these openings are absent in some sphagesaurids, including Caipirasuchus montealtensis and Caipirasuchus paulistanus (Andrade & Bertini, 2008b; Iori et al., 2013; Pol et al., 2014; Martinelli et al., 2018), and in Sphagesaurus huenei and Yacarerani boliviensis (Pol et al., 2014). Referred to as ‘maxillo-palatine fenestrae’ in the notosuchian literature, openings are often larger than the foramina described herein for thalattosuchians, especially for Caipirasuchus mineirus where these openings are very large (see Martinelli et al., 2018: figures 17 and 32). The ‘maxillo-palatine fenestrae’ seen in notosuchids and some sphagesaurids are in a similar position to the palatal foramina of thalattosuchians (see Fig. 1B). However, the notosuchian fenestrae are noticeably larger, and lack associated palatal grooves. Moreover, it appears that the ‘maxillo-palatine fenestrae’ seen in notosuchids and in two species of the sphagesaurid genus Caipirasuchus evolved independently (given their absence in all other sphagesaurid species). As such, the palatal foramina of thalattosuchians and the ‘maxillo-palatine fenestrae’ of sphagesaurian notosuchians do not share a common origin.

In the notosuchian Simosuchus clarki, Kley et al. (2010: 38, figures 3B and 8F) described paired palatal fossae on the anterior palatal rami of the maxilla, at the premaxilla-maxilla boundary. Within each deep fossa is a palatal foramen. However, given their anterior position and lack of palatal grooves we do not consider them to be homologous to the palatal canals found in thalattosuchians. In the same location, large foramina are also found in the allodaposuchid Lohuecosuchus megadontos, however there is no surrounding fossa (Narváez et al., 2015). Interestingly, mid-way along the maxilla there are paired foramina close to the skull midline in Lohuecosuchus megadontos (Narváez et al., 2015). However, these palatal foramina are not found in any other species of allodaposuchid (Narváez et al., 2015: 25).

Shartegosuchoids are another clade of fossil crocodylomorphs with a curious palate. At the skull midline, there is often a large opening referred to as the anterior palatal fenestra (Dollman et al., 2018; Dollman & Choiniere, 2022). In early-diverging shartegosuchoids, the anterior palatal fenestra, the nasopharyngeal duct and the internal choana are all continuous; however, in Fruitachampsa and Shartegosuchus the anterior palatal fenestra became isolated from the internal choana due to the formation of secondary bony palatal shelves (Dollman & Choiniere, 2022: 9). The morphology of the shartegosuchoid palatal fenestra is radically different from the palatal foramina seen in thalattosuchians, and the shartegosuchoids lack palatal grooves.

Palatal grooves in aquatic mammals and oral vascularisation

While no crocodylomorph clade shares the paired longitudinal palatal grooves seen in Thalattosuchia, curiously fossil and extant cetaceans do. A very similar morphology is present in the semi-aquatic remingtonocetid Remingtonocetus harudiensis (Bajpai, Thewissen & Conley, 2011: figure 1.3), the semi-aquatic protocetid Aegyptocetus tarfa (Bianucci & Gingerich, 2011: figure 3), and in fully aquatic forms, including the early-diverging mysticete Aetiocetus weltoni (Ekdale & Deméré, 2022: figure 2A), the early-diverging odontocetes Simocetus rayi (Fordyce, 2002: figure 4) and Echovenator sanderi (Churchill et al., 2016: figures 1F and 1G), and the beluga-like odontocete Bohaskaia monodontoides (Vélez-Juarbe & Pyenson, 2012: figure 3). The same morphology has also been described and figured for the extant gray whale (Eschrichtus robustus) and finback whale (Balaenoptera physalus) (see Ekdale, Deméré & Berta, 2015), and is also present in the humpback whale (Megaptera novaeangliae) (Fig. 9). There are four striking parallels between thalattosuchians and cetaceans: (1) the presence of anteroposteriorly aligned (longitudinal) grooves, present along most of the maxilla with their posterior terminus either on the palatines (as in thalattosuchians) or at the maxilla-palatine suture (cetaceans); (2) the longitudinal grooves have a large foramen at their posterior terminus; (3) in both clades the morphology is present in both semi-aquatic and fully aquatic forms; and (4) the grooves are closer to the skull midline in the semi-aquatic forms (see Pelagosaurus herein and Remingtonocetus in Bajpai, Thewissen & Conley, 2011), whereas in the fully aquatic forms the grooves are much more widely spaced (see the metriorhynchids herein, and Aetiocetus in Ekdale & Deméré, 2022; Simocetus in Fordyce, 2002; Echovenator in Churchill et al., 2016 and Bohaskaia in Vélez-Juarbe & Pyenson, 2012). Intermediate morphologies also appear in cetacean evolution, such as in Aegyptocetus (Bianucci & Gingerich, 2011).

In extant whales, the greater (or descending) palatine artery exits through the palatal foramen and continues anteriorly via the longitudinal groove/sulcus (Deméré et al., 2008; Ekdale, Deméré & Berta, 2015). This has also been hypothesised for fossil cetaceans (e.g., Bajpai, Thewissen & Conley, 2011; Vélez-Juarbe & Pyenson, 2012; Ekdale & Deméré, 2022). Although there has been a long discussion on whether the greater palatine artery is associated with the evolution of baleen in mysticetes, this hypothesis seems to have been falsified (see Ekdale, Deméré & Berta, 2015; Ekdale & Deméré, 2022). Two further hypotheses have been suggested for the expansion of the palatine vasculature in cetaceans, positing that it is either a consequence of rostral elongation (Ichishima et al., 2008) or for thermoregulation (Ekdale, Deméré & Berta, 2015). Ekdale, Deméré & Berta (2015: 699), however, noted that similar structures are not found in other mammals with elongate snouts (although the palatine foramina, and some form of palatal grooves, are). Within Crocodylomorpha there are numerous long-snouted groups, both extinct and extant, but none show evidence of palatal grooves. Moreover, among extant species long-snouted taxa do not have expanded rostral vasculature compared to broader snouted species (e.g., Bowman et al., 2022).

Mysticetes have highly vascularised oral cavities, with the mouth being an important site for thermoregulation (e.g., Ford & Kraus, 1992; Werth, 2007; Ford, Werth & George, 2013; Ekdale, Deméré & Berta, 2015). This is unsurprising given that mysticetes bulk filter feed, which involves the mouth being repeatedly exposed to (often cold) sea water. However, odontocetes seem to lack vascular adaptations for thermoregulation within the oral cavity (Werth, 2007). This is supported by the palatine foramen being greatly reduced, or almost closed, in extant delphinoid odontocetes (although the foramina are greatly enlarged in the fossil genus Odobenocetops, see de Muizon, Domning & Ketten, 2002), although the grooves are present in the killer whale (Orcinus orca) and Cuvier’s beaked whale (Ziphius cavirostris) (Fig. 10). Werth (2007) suggested that for odontocetes there was either less need to prevent oral heat loss, or that other regions of the body were more important sites for thermoregulation.

During their land-to-sea transition, pinnipedimorphs (seals and their close fossil relatives) evolved a similar morphology (Fig. S4). In early-diverging forms such as Enalioarctos, the palatal grooves originating from the palatine foramina are relatively short (Berta, 1991). During phocid (‘true seals’) evolution, however, the grooves became increasingly broader and more elongated (Dewaele, Lambert & Louwye, 2018; Rule et al., 2020; Koretsky & Rahmat, 2021).

Many other amniote groups have a venous plexus within the soft tissues of the palate. In birds, the palatal plexus and the rete ophthalmicum help maintain eye and brain temperature (Kilgore, Boggs & Birchard, 1979; Midtgård, 1983, 1984; Porter & Witmer, 2016), while in extant crocodylians there is an extensive palatal plexus (Porter, Sedlmayr & Witmer, 2016). In extant archosaurs the palatal plexus is supplied by the palatine artery (Figs. S5 and S6); however, the palatine arteries travel through the soft tissue of the secondary palate (see Porter & Witmer, 2016; Porter, Sedlmayr & Witmer, 2016), unlike in cetaceans where they pass through the bony palate. Moreover, in extant archosaurs the palatine arteries are situated laterally in the rostrum (see Fig. S5; Porter & Witmer, 2016; Porter, Sedlmayr & Witmer, 2016), not medially as in cetaceans. We propose an osteological correlate for the palatine vessels in thalattosuchians: the groove that originates at the anterior margin of the suborbital fenestra (Fig. 1: SOG). This groove is consistent with location of the palatine vessels in extant crocodylians (Porter, Sedlmayr & Witmer, 2016).

Based on the striking similarity between thalattosuchian palatal canal/groove system and those of cetaceans (particularly the fossil semi-aquatic and aquatic species), and the known routes and positions of extant crocodylian cranial vasculature, we hypothesise the following:

1. The thalattosuchian palatal canal/groove system transmitted the medial nasal vessels (artery and vein) or a novel branch thereof, and possibly also some of the rostral nerves. In all extant diapsids, the medial nasal vessels branch off from nasal vessels at the posterodorsal aspect of the nasal cavity. The medial nasal vessels then descend anteroventrally on either side of the median cartilaginous internasal septum to run on the floor of the nasal cavity (e.g., Figs. S5 and S6; Porter & Witmer, 2015, 2016; Porter, Sedlmayr & Witmer, 2016). Therefore, the paramedian/parasagittal position of the palatal canal/groove system in thalattosuchians is consistent with the medial nasal vessels.

2. Early in thalattosuchian evolution, the medial nasal vessels (or a ventral branch thereof) pierced the bony palate to emerge on to the roof of the oral cavity. If thalattosuchians are a non-crocodyliform clade (e.g., see Wilberg et al., 2023) then the formation of the secondary bony palate occurred independently within Thalattosuchia, and therefore nasal vessels would have been enclosed by the palatines during the formation of the maxillopalatine palate.

3. The medial nasal vessels that entered the oral cavity anastomosed with the palatal vascular plexus (which are supplied by the palatine vessels).

4. The large internal osseous canals represent a hypertrophy of the medial nasal vessels.

5. A novel heat exchange pathway was created by linking the palatal plexus to medial nasal vessels. In extant crocodylians, the medial nasal vessels communicate with the encephalic arteries and veins via the ethmoid vessels (Porter, Sedlmayr & Witmer, 2016). The palatal vascular plexus is a critical location of thermal exchange in extant crocodylians (Porter, Sedlmayr & Witmer, 2016). While the palatal plexus is not thought to have a substantial role in thermoregulation of the brain in extant crocodylians, based on our proposed vascular pathway, the palatal plexus would have moderated brain temperatures of thalattosuchians via the ethmoid vessels.

Increased cephalic blood volume in Thalattosuchia

A novel heat exchange pathway to help maintain brain and eye temperatures would have been greatly beneficial for Metriorhynchidae. Not only did metriorhynchids have an elevated metabolism (possibly a poorly homeothermic form of endothermy, see Séon et al., 2020), but they had expanded cerebral hemispheres and orbits relative to extant crocodylians and other thalattosuchians (e.g., see Young et al., 2010; Herrera, Leardi & Fernández, 2018; Schwab et al., 2021). An obvious question is why would semi-aquatic thalattosuchians also have had a novel heat exchange pathway? One of the defining features of Thalattosuchia is the enlarged cerebral carotid foramina on the occipital surface of the cranium, being found in both semi-aquatic and fully aquatic species (Andrews, 1913; Pierce & Benton, 2006; Jouve, 2009; Pol & Gasparini, 2009; Fernández et al., 2011; Young et al., 2012, 2013, 2020b; Herrera & Vennari, 2015; Brusatte et al., 2016; Johnson, Young & Brusatte, 2020). Note, the cerebral carotid foramina become even larger in the clade Zoneait + Metriorhynchidae (Wilberg, 2015; Herrera, Leardi & Fernández, 2018), while they become smaller in some freshwater teleosauroids (Herrera, Leardi & Fernández, 2018). In mammals, larger encephalic arteries are associated with higher rates of blood flow, as flow (perfusion) is proportional to the radius of the arterial lumen raised to an exponent of approximately 2.5 (Seymour et al., 2019). In extant crocodylians, the cerebral carotid arteries supply blood to the brain, eyes, nasal cavities, and the rostral sinuses (Porter, Sedlmayr & Witmer, 2016). Therefore, it is possible that these vessels supplied a greater volume of blood to these regions in thalattosuchians compared to extant crocodylians.

Further, these enlarged foramina do not represent the full extent of vascular hypertrophy observed in thalattosuchian skulls. The cerebral carotid vessels enter the greatly enlarged pituitary fossa chamber, another thalattosuchian synapomorphy, which in extant crocodylians houses the cavernous venous sinus (Porter, Sedlmayr & Witmer, 2016) and was possibly hypertrophied in thalattosuchians. Exiting the anterior margin of the pituitary fossa chamber are two ossified canals thought to transmit the orbital arteries (Brusatte et al., 2016), with these canals being almost as wide as the cerebral carotid canals (Brusatte et al., 2016; Pierce, Williams & Benson, 2017; Herrera, Leardi & Fernández, 2018; Wilberg et al., 2022). Within Crocodylomorpha, only thalattosuchians and the dyrosaurid Rhabdognathus (Erb & Turner, 2021) are known to have the orbital arteries contained within ossified canals. Further, the midbrain and hindbrain of thalattosuchians are very poorly delineated in their endocasts due to the hypertrophy of the longitudinal and transverse dural venous sinuses, the latter being continuous with the hypertrophied stapedial canals (Wharton, 2000; Fernández et al., 2011; Brusatte et al., 2016; Pierce, Williams & Benson, 2017; Herrera, Leardi & Fernández, 2018; Schwab et al., 2021; Wilberg et al., 2022). Collectively, this implies that thalattosuchians had increased encephalic blood volumes and potentially increased perfusion rates relative to extant crocodylians. As such, maintaining stable brain and eye temperatures may have required more extensive heat exchange mechanisms.

Unfortunately, we do not know the timing of these internal changes. All thalattosuchians that have been subject to CT scanning show the same suite of vascular characters outlined above, and the palatal groove/canal system described herein. It is unclear whether encephalic vascular evolution in Thalattosuchia was stepwise and gradual, or whether one of these characteristics was a ‘key adaptation’ that triggered rapid change within the thalattosuchian skull. Only new fossil discoveries, of taxa basal to the teleosauroid-metriorhynchoid split, will allow us to understand this radical reorganisation.

Regardless of what selection pressures drove basal thalattosuchians to evolve these encephalic vascular characteristics, we posit that within Metriorhynchoidea, as the clade became increasingly aquatic, these characteristics made possible the evolution of larger orbits, larger cerebral hemispheres, and an elevated metabolism. An elevated metabolism and a pathway to help maintain stable brain and eye temperatures would also have made feeding below the thermocline viable, especially in a group considered to be primarily vision-based hunters (Massare, 1988; Martill et al., 1994; Young et al., 2010; Bowman et al., 2022). Isotopic analyses suggest that belemnites lived below the thermocline during the Jurassic (e.g., Jenkyns et al., 2012; Xu et al., 2018), and an abundance of belemnite hooklets have been found within the body cavity of Middle Jurassic metriorhynchids from the Oxford Clay Formation of the UK (Martill, 1986). While the evolution of hypertrophied salt glands has been cited as an example of how physiological changes expanded the metriorhynchid prey envelope, to include osmoconforming species (Fernández & Gasparini, 2000, 2008; Cowgill et al., 2022a), thermophysiological changes were undoubtedly also exceptionally important. The suite of vascular characters outlined herein are unique to thalattosuchians, and no other crocodylomorph clade contained a lineage that evolved to become fully aquatic. Perhaps these changes in cranial vasculature were a necessary precursor for the development of the fully aquatic metriorhynchids.

Well-developed palatal grooves are only found in Early Jurassic teleosauroids (e.g., Johnson et al., 2019; Johnson, Young & Brusatte, 2020), whereas in Middle and Late Jurassic taxa the grooves became extremely shallow or were possibly absent (e.g., Johnson et al., 2018; Johnson, Young & Brusatte, 2020; Foffa et al., 2019). It is possible that as teleosauroids adapted to a ‘sit and wait’ ambush ecology, the selection pressures that necessitated maintaining stable brain and eye temperatures were no longer as strong. However, CT scans of Middle and Late Jurassic teleosauroids will be needed to determine whether the internal palatal canals were present or not. It is possible that the grooves themselves simply became shallower in these taxa, perhaps somewhat like in extant odontocete whales—with the oral cavity becoming a less important site of thermoregulation.