Contributions to Zoology, 84 (1) – 2015Nicole Klein; Alexandra Houssaye; James M. Neenan; Torsten M. Scheyer: Long bone histology and microanatomy of Placodontia (Diapsida: Sauropterygia)
Discussion

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Histological characteristics

Placodonts share several histological features. Numerous primary osteons occur in all bones that grew with fibro-lamellar bone. Primary osteons are not developed in Psephoderma alpinum and they are rare in Paraplacodus broilii, which both grew with lamellar-zonal bone. All placodonts share immature (i.e. incompletely lined) primary osteons that predominately occur in the inner cortices. Incompletely lined primary osteons are also described for other Sauropertygia such as a pachypleurosaurs and a pistosauroid (Klein, 2010), and for young Alligator mississippiensis (Woodward et al., 2014). There thus might be a correlation between aquatic lifestyle (and an inferred increased growth rate when compared to terrestrial forms; see White, 2011) and incompletely lined primary osteons.

Resorption occurs in all placodont samples. Psephoderma humerus and femur exhibit a perimedullary region in which periosteal bone is resorbed and partially replaced (remodelled). The entire medullary region of Paraplacodus is made of secondary (endosteal) bone, resulting in a very compact centre. Some Placodontia indet. show an extended medullary region filled by secondary trabecels. In fact, the Placodontia indet. sample can be divided into two groups based on the presence of a medullary cavity in some femora (MB.R. 961; MB.R 812; MB.R 814.2; SMNS 54578) and the presence of a large medullary region, respectively (IGWH 9, 23; SMNS 54585; MB.R. 454). The presence of a free cavity in some Placodontia indet. aff. Cyamodus and Placodontia indet. is not typical for aquatic tetrapods (e.g. Quemeneur et al., 2013; Hayashi et al., 2013).

In those samples that grew with fibro-lamellar bone remodelling is always only initiated, which means that secondarily widened (eroded) vascular canals or primary osteons are surrounded by a layer of circumferentially deposited lamellar bone but stay widely open and are not infilled. Mature secondary osteons are very rare and are restricted to the inner cortex of few samples. The absence of large amounts of mature secondary osteons (Francillon-Vieillot et al., 1990; Currey, 2002) in the placodont samples expressing fibro-lamellar bone is atypical. Ricqlès (1976) hypothesized a possible relation between fibro-lamellar bone and remodelling (i.e., the presence and number of secondary osteons), which is true for many extant and extinct vertebrates such as large herbivorous mammals, large birds, dinosaurs, and ichthyosaurs (e.g. Klein and Sander, 2008; Houssaye et al., 2014).

All placodonts, thanks to an inhibition of bone remodelling, have a good and fairly complete growth record preserved, which is the subject of another study (Klein et al., unpubl. data).

Paraplacodus, one humerus of Placodontia indet. aff. Cyamodus, and some humeri of Horaffia show pockets of calcified cartilage at midshaft. Retention of calcified cartilage at midshaft is often coupled with osteosclerosis and is recognized in many secondarily aquatic vertebrates, e.g. in pachypleurosaurs and plesiosaurs (Buffrénil et al., 1990; Ricqlès and Buffrénil, 2001; Hugi et al., 2011; Krahl et al., 2013). It is also described in some armour plates of placodonts (Scheyer, 2007).

Two major histological groups can be distinguished among placodonts, which do not follow the classical phylogenetic distinction into armoured vs. non-armoured Placodontia. The armoured Psephoderma and the non-armoured Paraplacodus both grew with compact, low vascularized or avascular lamellar-zonal bone, indicating a slow growth rate and rather low basal metabolic rate comparable to that of modern amphibians and reptiles. The armoured Henodus, non-armoured aff. Placodus, and the armoured Placodontia indet. aff. Cyamodus grew with plexiform to radiating fibro-lamellar bone tissue, indicating high growth rates and a high basal metabolic rate. For Placodontia indet. and for Horaffia it is unknown if the individuals had carried an armour or not, also grew with fibro-lamellar bone tissue but here the organization is more circumferential, indicating somewhat lower growth rates (Margerie et al., 2004). Fibro-lamellar bone tissue is known from modern birds, dinosaurs, most synapsids, and from other extinct marine reptiles such as ichthyosaurs and plesiosaurs (e.g. Chinsamy-Turan 2005, 2011; Houssaye et al., 2014; Wiffen et al., 1995). Thus, fibro-lamellar bone tissue clearly originated several times within different vertebrate lineages.

The fibro-lamellar bone of placodonts has the typical scaffolding of woven bone surrounded by lamellar bone. However, sometimes the woven bone component is replaced or grades into parallel-fibred bone with specially thick and coarse fibers. Both always contain a high amount of thick and numerous osteocyte lacunae. A replacement or modification of the woven bone component by parallel-fibred bone in the fibro-lamellar tissue was described before for archosaurs (Ricqlés et al., 2003), the ornithopod dinosaur Gasparinisaura (Cerda and Chinsamy, 2012), and the titanosaur dinosaur Ampelosaurus (Klein et al., 2012). An atypical parallel-fibred bone was mentioned for mosasaurs (Houssaye et al., 2013) and for the temnospondyl Plagiosaurus (Konietzko-Meier and Schmitt, 2013), which both did not grow with fibro-lamellar bone. It also occurs within the fibro-lamellar bone of ichthyosaurs (Houssaye et al., 2014).

Locally, a high amount of radial vascular canals occurs within the fibro-lamellar bone of some placodonts. Radial bone tissue reveals according to Margerie et al., (2004:869) in the king penguin chick the highest growth rates. In ichthyosaurs, a radial arrangement of vascular canals was interpreted as a consequence of the insertion of Sharpey’s fibers and thus linked to mechanical reasons (Houssaye et al., 2014). The local radial trabecle-like architecture in the inner cortex of some placodont samples may also indicate mechanical properties in addition to high overall growth rates. The fibro-lamellar bone tissue in combination with the plexiform to radiating organization indicates for Placodontia indet. aff. Cyamodus the highest growth rates among placodonts but also among other Triassic Sauropterygia and is comparable to that of ichthyosaurs (Buffrénil and Mazin, 1990; Houssaye et al., 2014).

In all placodonts that grew with fibro-lamellar bone, primary tissue is in general highly vascularized. Locally it is even spongeous-like or trabecular-like. Primary osteons are secondarily widened by successive resorption processes, resulting in an overall secondary spongeous tissue, which is similar to some ichthyosaurs (Houssaye et al., 2014).

In spite of certain inter- and intraspecific variability within the placodont sample that grew with fibro-lamellar bone, the primary bone tissue is in general very similar to that of ichthyosaurs. Differences include the lack of a medullary cavity, high endosteal and periosteal remodelling, and an overall more spongeous organization, in ichthyosaurs (Houssaye et al., 2014). The similarities are notable, because ichthyosaurs were efficient and sustained swimmers that lived in the open marine sea with a comparable body shape and lifestyle to dolphins or tunas. Placodonts have a cylindrical, sea cow-like body shape (non-armoured forms) or resemble the shape and morphology of flat aquatic turtles (armoured forms).

Long bone histology allows the identification and assignment of isolated bone fragments to Placodontia. Neither the combination of the avascular to low vascularized lamellar-zonal bone tissue of Psephoderma and Paraplacodus nor the special plexiform to radiating fibro-lamellar bone tissue of aff. Placodus, Placodontia indet. aff. Cyamodus, and Henodus or circumfertential fibro-lamellar bone of Placodontia indet. has so far been reported in the here described combinations in any long bone of any other marine reptile (e.g. Sander, 1990; Wiffen et al., 1995; Pellegrini 2007; Klein, 2010; Hugi, 2011; Hugi et al., 2011; Krahl et al., 2013; Houssaye et al., 2014).