Microanatomical and Histological Features in the Long Bones of Mosasaurine Mosasaurs (Reptilia, Squamata) – Implications for Aquatic Adaptation and Growth Rates

Abstract

BackgroundDuring their evolution in the Late Cretaceous, mosasauroids attained a worldwide distribution, accompanied by a marked increase in body size and open ocean adaptations. This transition from land-dwellers to highly marine-adapted forms is readily apparent not only at the gross anatomic level but also in their inner bone architecture, which underwent profound modifications.Methodology/Principal FindingsThe present contribution describes, both qualitatively and quantitatively, the internal organization (microanatomy) and tissue types and characteristics (histology) of propodial and epipodial bones in one lineage of mosasauroids; i.e., the subfamily Mosasaurinae. By using microanatomical and histological data from limb bones in combination with recently acquired knowledge on the inner structure of ribs and vertebrae, and through comparisons with extant squamates and semi-aquatic to fully marine amniotes, we infer possible implications on mosasaurine evolution, aquatic adaptation, growth rates, and basal metabolic rates. Notably, we observe the occurrence of an unusual type of parallel-fibered bone, with large and randomly shaped osteocyte lacunae (otherwise typical of fibrous bone) and particular microanatomical features in Dallasaurus, which displays, rather than a spongious inner organization, bone mass increase in its humeri and a tubular organization in its femora and ribs.Conclusions/SignificanceThe dominance of an unusual type of parallel-fibered bone suggests growth rates and, by extension, basal metabolic rates intermediate between that of the extant leatherback turtle, Dermochelys, and those suggested for plesiosaur and ichthyosaur reptiles. Moreover, the microanatomical features of the relatively primitive genus Dallasaurus differ from those of more derived mosasaurines, indicating an intermediate stage of adaptation for a marine existence. The more complete image of the various microanatomical trends observed in mosasaurine skeletal elements supports the evolutionary convergence between this lineage of secondarily aquatically adapted squamates and cetaceans in the ecological transition from a coastal to a pelagic lifestyle.

Osteohistology of the Early Triassic ichthyopterygian reptile Utatsusaurus hataii: Implications for early ichthyosaur biology

“…The vascularization pattern in the ribs is similar to that described for hydropelvic mosasauroids (Houssaye and Bardet 2012;Houssaye et al 2013), considered to be gigantothermic (Motani 2010). However, whereas mosasauroids essentially display parallel-fibered bone, Utatsusaurus displays a bone tissue comparable with the fibrolamellar complex, which changes into parallel-fibred bone only later in ontogeny.…”

Investigations of a Cretaceous limestone with spectral induced polarization and scanning electron microscopy

“…Following a review of the grinded powder results, samples from three levels were selected for a more detailed thin section analysis. Dried rock samples were embedded in epoxy resin, and thin sections were made according to the method described in Houssaye et al (2013). The thin sections were examined at variable magnification in a petrographic microscope (Nikon Eclipse E400 POL) and the carbonate textures of the rock samples were determined according to the widely used Dunham classification system (see Dunham 1962) via point counting (300 points).…”

Turtle humeral microanatomy and its relationship to lifestyle

“…Evidence for bone mass increase has been found in, for example archaeocetes (de Buffrénil et al, 1990a;Gray et al, 2007), fossil sirenians (de Buffrénil et al, 2010), basal desmostylians (Hayashi et al, 2013), aquatic folivorans (Amson et al, 2014), shallow-marine squamates (Houssaye, 2013), mesosaurs (de Ricqlès, 1974), choristoderes (de Buffrénil et al, 1990b;Katsura, 2010), non-plesiosaur sauropterygians (e.g. On the other hand, Desmostylus (Hayashi et al, 2013), derived species of mosasaurs (Sheldon, 1997;Houssaye et al, 2013), most plesiosaurs (Wiffen et al, 1995;Liebe & Hurum, 2012), and ichthyosaurs (de Buffrénil & Mazin, 1990;Kolb, Sánchez-Villagra & Scheyer, 2011;Nakajima, Houssaye & Endo, 2014) show signs of an osteoporotic-like state. On the other hand, Desmostylus (Hayashi et al, 2013), derived species of mosasaurs (Sheldon, 1997;Houssaye et al, 2013), most plesiosaurs (Wiffen et al, 1995;Liebe & Hurum, 2012), and ichthyosaurs (de Buffrénil & Mazin, 1990;Kolb, Sánchez-Villagra & Scheyer, 2011;Nakajima, Houssaye & Endo, 2014) show signs of an osteoporotic-like state.…”