bs_bs_banner Biological Journal of the Linnean Society, 2013, 108, 3–21. With 4 figures REVIEW ARTICLE Bone histology of aquatic reptiles: what does it tell us about secondary adaptation to an aquatic life? ALEXANDRA HOUSSAYE* Steinmann Institut für Geologie, Paläontologie und Mineralogie, Universität Bonn, Nussallee 8, 53115 Bonn, Germany Received 29 May 2012; revised 5 July 2012; accepted for publication 5 July 2012 Aquatic reptiles are very diversified in the fossil record. The description and pooling of certain bone histological features (collagenous weave and vascular network) of the various groups of aquatic reptiles highlight what this histological information can tell us about the process of secondary adaptation to an aquatic life. Notably, they show the absence of interaction between these histological features on the one hand and body size, mode of swimming, type of microanatomical specialization and phylogeny on the other. These histological features in aquatic reptiles seem to essentially provide information about the growth rate and basal metabolic rate of these taxa. The growth rate seems to have been rather high in most marine reptiles, when compared with terrestrial ectotherms. Moreover, distinct metabolic abilities are suggested. Indeed, various groups probably displayed a peculiarly high body temperature, and some show trends towards endothermy. This study also emphasizes the crucial need for homologous comparisons in histology and shows that much remains to be done to better understand the relationship between histological features, growth rate and metabolism in extant taxa in order to make inferences in the fossil groups. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 108, 3–21. ADDITIONAL KEYWORDS: collagenous weave – growth rate – metabolism – vascular network. INTRODUCTION 2005; Erickson et al., 2009; Sanchez et al., 2010). His- tological features have been analysed in several Extant aquatic reptiles are rather scarce, especially if aquatic reptile taxa (see below). However, these we consider only the essentially (spending much of studies have generally focused on a single group (see their time in water), or even exclusively, aquatic taxa, below). It is of particular interest to review these consisting of the highly aquatic turtles and snakes various data in order to better understand what bone (the marine iguana being essentially terrestrial). histology can tell us about the process of secondary However, they were much more diverse in the fossil adaptation to an aquatic life. This is the object of this record, especially during the Mesozoic. Indeed, study, which focuses on two main histological fea- various groups of reptiles illustrating distinct mor- tures: (1) the organization of the collagenous weave phologies and degrees of adaptation to an aquatic life [to distinguish between lamellar, parallel-fibred and were secondarily adapted to aquatic environments fibrous (woven-fibred) bone]; and (2) the organization (cf. Mazin, 2001; Fig. 1). of the vascular network. The terminology follows Bone histology is one of the major sources of infor- Francillon-Vieillot et al. (1990). The histological fea- mation about life history traits (e.g. Sander & Klein, tures described for the various aquatic reptiles (based on adult specimens, except when precised; cf. Fig. 1) are listed in order to be interpreted, based on phylo- *E-mail: [email protected] genetic, functional and physiological perspectives. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 108, 3–21 3 4 A. HOUSSAYE BONE HISTOLOGY OF AQUATIC REPTILES made up of lamellar bone with lines of arrested MESOSAURIDAE growth (LAGs); it is poorly vascularized with longi- tudinally oriented simple vascular canals and a few Histological data on mesosaurs are rather scarce. primary osteons (Fig. 2A, B), which were described as They are based on the analysis of thin sections and organized in concentric rows by Nopcsa & Heidsieck fragments of a few ribs (Nopcsa & Heidsieck, 1934; (1934). The medullary region is occupied by a spon- Kaiser, 1960; de Ricqlès, 1974), and of one long bone giosa made of rather thick, irregularly oriented (? tibia), carpals and tarsals (de Ricqlès, 1974). In trabeculae of lamellar bone and of intertrabecular both the ribs and the long bone, the cortex is thick (as remains of calcified cartilage (de Ricqlès, 1974; a result of pachyosteosclerosis). Periosteal bone is Fig. 2A). In carpals and tarsals, the microstructure is Figure 1. Consensual phylogeny illustrating the relationships between the various groups of marine reptiles. From Modesto & Anderson (2004), Tsuji & Müller (2009) and Scheyer, Klein & Sander (2010). ᭤ Figure 2. A, Mesosaurus brasiliensis. Rib transverse section (TS) in natural light (NL). From de Ricqlès (1974). B, Mesosaurus rib TS in NL. From Kaiser (1960). In both (A) and (B), the cortex is at the top and the medullary cavity is at the bottom. C, Claudiosaurus germaini. Rib TS in polarized light (PL) (left) and NL (right) (Personal photograph). Note the clear limit between the compact primary cortex and the medullary cavity. D, E, Champsosaurus (Choristodera) adult femur TS (D) and detail of the transition between the cortex (top) and the medullary region (bottom) in NL (E). From de Buffrénil et al. (1990). F, Ichthyosaurus humerus TS in NL. Cortex. From de Buffrénil & Mazin (1990). G, Ichthyosaurus humerus TS in PL. Cortex. (Personal photograph) H, I, Dermochelys coriacea. H, Tibia TS. From Kriloff et al. (2008). I, Femur cortex. From de Ricqlès et al. (2004). Abbreviations: cc, calcified cartilage; ds, dense spongiosa; fb, fibrous bone; lb, lamellar bone; lzb, lamellar-zonal bone; po, primary osteon; sb, secondary bone; svc, simple vascular canal. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 108, 3–21 BONE HISTOLOGY OF AQUATIC REPTILES 5 similar, except that the cortex is thin and avascular. CLAUDIOSAURUS A few secondary osteons occur in the perimedullar region of the long bone as a result of remodelling (de de Buffrénil & Mazin (1989) described the bone his- Ricqlès, 1974). tology of limb bones (humerus, femur and tibia), ribs © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 108, 3–21 6 A. HOUSSAYE and vertebrae of this taxon. Their primary periosteal the ontogenetic stage, as a result of additional sec- bone consists of lamellar bone with LAGs and with a ondary lamellar bone deposits during remodelling, limited vascular supply made up of thin simple vas- which fill the cavities and intertrabecular spaces in cular canals, mainly longitudinally oriented (Fig. 2C). Simoedosaurus (de Buffrénil et al., 1990). These bones are characterized by osteosclerosis caused by excessive deposits of secondary lamellar bone during intense remodelling, which mainly occurs HUPEHSUCHIA in the medullary region of long bones and ribs, and in No data on the histology of Hupehsuchia are the core of the vertebral centrum, as well as in the available. inner cortex (Fig. 2C). Secondary osteons are numer- ous in these regions. ICHTHYOSAURS Histological features of ichthyosaurs are known from YOUNGINIFORMES the study of limb bone, vertebra and rib sections of Within Younginiformes (although the monophyly of five taxa: Omphalosaurus, Stenopterygius, Ichthyo- the group is questioned; Bickelmann et al., 2009), two saurus, Platypterygius and Mixosaurus (Kiprijanoff, taxa are adapted to a marine environment and are 1881–1883; Fraas, 1891; Seitz, 1907; Gross, 1934; de thus taken into consideration here: Tangasaurus and Buffrénil, Mazin & de Ricqlès, 1987; de Buffrénil & Hovasaurus (Carroll, 1988). No histological data are Mazin, 1990; Lopuchowycz & Massare, 2002; Kolb, known for these taxa. Sánchez-Villagra & Scheyer, 2011). Periosteal bone is spongious with a zonal organization of circumferen- tial rows of numerous simple vascular canals and CHORISTODERA primary osteons, with a mainly longitudinal, but also The histology of the vertebrae, femora and ribs of radial and sometimes oblique, orientation, giving Champsosaurus and Simoedosaurus has been studied the bone a plexiform aspect (de Buffrénil & Mazin, (Nopcsa & Heidsieck, 1934; de Ricqlès, 1976a; de 1990; Kolb et al., 2011; Fig. 2F). Periosteal bone cor- Buffrénil et al., 1990; Katsura, 2010). In these bones, responds to fibrous bone at rapid stages of growth the cortex is essentially made up of parallel-fibred (Fig. 2G) and to parallel-fibred bone much later in bone – associated with lamellar bone in the vertebrae ontogeny. In large specimens, the periphery of the – with LAGs and a few simple vascular canals cortex consists of a thin layer of compact bone dis- (Fig. 2D, E). Fibrous bone generally occurs in the core playing a few, longitudinally oriented simple vascular of the bones. Vascular canals are very scarce and canals and primary osteons (de Buffrénil & Mazin, radially oriented in the vertebrae. In femora and ribs, 1990; Kolb et al., 2011). In the cortical region, the vascularization is more extensive and displays a lon- trabeculae consist of a core of fibrous bone covered by gitudinal orientation in the deep cortex; vascular platings of lamellar bone (Fig. 2G). In the medullary density decreases in the periphery, where the canals region, trabeculae are rather thin and mainly formed are rather radially oriented. The medullary region of by secondary lamellar bone deposits, as a result of the ribs and femora, which is much larger in adults intense