The pterosaur tongue bone… and others, too

I did not give the pterosaur tongue much thought
until Li, Zhou and Clarke 2018 discussed it. They report, “Pterosaurs show convergent evolution of traits linked to tongue protrusion and mobility in birds (narrow midline element [achieved through fusion] and elongate, paired and rostrally positioned ceratobranchials).”

Figure 1. Scaphognathus (holotype) with hyoid traced in magenta.

Figure 1. Scaphognathus (holotype) with hyoid traced in magenta.

“We find pterosaurs similarly show lightly-built single pairs of ceratobranchial elements.

“Here, we bring together evidence from preserved hyoid elements from dinosaurs and outgroup archosaurs, including pterosaurs, with enhanced contrast x-ray computed tomography data from extant taxa.” (That means crocs and birds. Pterosaurs are not outgroup archosaurs, but fenestrasaur tritosaur lepidosaurs. Only taxon exclusion and academic suppression prevents this from being widely accepted.)

“The absence of direct and cranially-extensive support from bony elements make crocodilian tongue incapable of significant independent motion. Relative to outgroup lepidosaurs and other tetrapods the bony structure in crocodilians and surveyed basal archosaurs is uniformly simple and small with a single pair of ceratobranchials and no well-mineralized midline element or fusion.” 

“Elongation of hyobranchial elements co-occurs with increased ossification of a midline element (i.e., in paravians) and ceratobranchial fusion on the midline (i.e. pterosaurs). It is also well mineralized in some primarily quadrupedal, herbivorous ornithischians dinosaurs (e.g., ankylosaurids and hadrosauroids.) Within testudines, increase ossification of the midline element is seen in terrestrial taxa with an increase role for intraoral manipulation of food by the tongue.” Quoted verbatim. Ornithischia hyoids from Pinacosaurus are shown in figure 7.

Ludodactylus.

Figure 2. Click to enlarge. Ludodactylus, with rare pterosaur hyoid.

Li, Zhou and Clarke conclude
“In lepidosaurs, which show remarkable diversity in hyoid shape, there remains a primary respiratory function for the hyoid elements. The hyobranchial elements (multiple sets of ceratobranchials) show a primarily dorsoventral movement that is deployed during buccal pumping. The hyoid structure shows strong muscular links to the pectoral girdle that are lost in archosaurs and any tongue protrusion is via attached fleshy extensions rather than bony components. Perhaps not true in fenestrasaurs, which have a bird-like hyoid. See below.

“In Archosauria, the evolution of novel respiratory mechanisms apparently drove a simplification of the tongue that was retained in most taxa. Only with the evolution of flight (birds and pterosaurs) and in select quadrupedal herbivores was tongue structure elaborated.” By convergence, one must assume. Otherwise, what is the common thread?

Li, Zhou and Clarke did not realize
pterosaurs are lepidosaurs, not archosaurs. Anyone can test this by adding more relevant taxa to any relevant cladogram.

Figure 4. Sphenodon hyoids in two views.

Figure 3. Sphenodon hyoids in two views from Jones et al. 2009

Phylogenetic bracketing
using Sphenodon (Schwenk 1986) and Iguana (both with a fleshy tongue and posteriorly branching hyoids) should give tritosaur pterosaurs a fleshy tongue, too… except pterosaurs are highly derived and volant tritosaurs. Only the juvenile Huehuecuetzpalli, otherwise identical to the adult except in size, preserves hyoids. These are only visible posterior to the jaw. “According to their position, the anterior element was identified as the first ceratobranchial and the posterior element as the epihyal. The latter one, however, may be the hyoid cornu.” (Reynoso 1998). Tanystropheus and Macrocnemus have simple slender hyoids that approach one another anteriorly.

Figure 3. Longisquama in situ with hyoids identified.

Figure 4. Longisquama in situ with straight lateral and Y-shaped central hyoids identified.

Overlooked by Li, Zhou and Clarke,
a flightless lepidosaur and pterosaur outgroup taxon, Longisquama (Fig. 4) shares the pterosaur hyoid morphology. Sharovipteryx (Fig. 5) and Kyrgyzsaurus may as well. However in the lateral two taxa the lateral hyoids are so large they appear to have been able to spread laterally and so produce a cobra-like fleshy strake from otherwise loose neck skin and so introduce another aerodynamic membrane. Skull material prevents seeing a central hyoid if present.

Figure 4. Sharovipteryx in situ with hyoids identified. Note the expansive neck skin. Much has been said about the wasp-like insect in the left orbit, but Sharov was an insect collector first and there are many other insects, particularly beetles, all over the matrix.

Figure 5. Sharovipteryx in situ with hyoids identified. Note the expansive neck skin. Much has been said about the wasp-like insect in the left orbit, but Sharov was an insect collector first and there are many other insects, particularly beetles, all over the matrix.

Very few pterosaurs preserve hyoids.
The few that do have bird-like, y-shaped central hyoids (Figs. 1, 2) and sometimes straight lateral hyoids (Fig. 4), as Li, Zhou and Clarke correctly reported.

Yet another bunch of overlooked lepidosauriforms,

  1. Megalancosaurus has a Y-shaped central hyoid, unknown in other drepanosaurs.
  2. Stem chameleon (Early Cretaceous from amber) has a large central element split anteriorly
  3. Chlamydosaurus and kin use the hyoid elements for stretching the dermal skin, whether neck, like the Triassic Sharovipteryx (see above) or throat, as in the anole, Polychrus.
  4. Earliest reptile hyoids I have found: Diplovertebron (Fig. 6, a basal archosauromorph (in the LRT) from the Westphalian, but with its genesis in the Viséan.
Figure 3. Reconstruction of G. watsoni as a distinctly different genus, nesting with Eldeceeon rather than G. bohemicus.

Figure 6. Reconstruction of Diplovertebron (= Gephyrostegus watsoni) showing paired hyoids, the earliest I have seen on a reptile (Westphalian, Late Carboniferous, 300 mya)

Conclusions:
Hyoids vary greatly in size and shape in tetrapods. The basal/typical tetrapod tongue is boneless, fleshy and anchored by hyoids (see Sphenodon (Schwenk 1986), Caiman, Homo or Iguana). A few tongues are modified with an internal Y-shaped element for prey apprehension or reduced mobility, as in Melanerpes and Trioceros. This is found in various lepidosaurs (including pterosaurs) and birds by convergence. Mammals that use their tongues for prey/nectar apprehension do not have hyoids inside the tongue.

Figure 7. A selection of hyoids from Hill et al. 2015 with a focus on the ornithischian, Pinacosaurus.

Figure 7. A selection of hyoids from Hill et al. 2015 with a focus on the ornithischian, Pinacosaurus.

References
Hill RV, D’ Emic MD, Bever GS and Norell MA 2015. A complex hyobranchial apparatus in a Cretaceous dinosaur and the antiquity of avian paraglossalia. Zoological Journal of the Linnean Society 175: 892–909.
Jones et al. 2009. The head and neck muscles associated with feeding in Sphenodon (Reptilia: Lepidosauria: Rhynchocephalia). Palaeontologia Electronica 12(2).
Li Z, Zhou Z and Clarke JA 2018. Convergent evolution of a mobile bony tongue in flghted dinosaurs and pterosaurs. PLoS ONE 13(6):e0198078. https://doi.org/10.1371/journal.
Reynoso V-H 1998. Huehuecuetzpalli mixtecus gen. et sp. nov: a basal squamate (Reptilia) from the Early Cretaceous of Tepexi de Rodríguez, Central México. Philosophical Transactions of the Royal Society, London B 353:477-500.
Schwenk K 1986. Morphology of the tongue in the tuatara, Sphenodon punctatus (Reptilia: Lepidosauria), with comments on function and phylogeny. J Morphol. 1986; 188: 129–156. pone.0198078

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