Bone histology of Silesaurus opolensisDzik, 2003 from the Late Triassic of Poland

Bone histology of Silesaurus opolensis Dzik, 2003 from the LateTriassic of Poland

ŁUCJA FOSTOWICZ-FRELIK AND TOMASZ SULEJ

Fostowicz-Frelik, Ł. & Sulej, T. 2010: Bone histology of Silesaurus opolensis Dzik, 2003from the Late Triassic of Poland. Lethaia, Vol. 43, pp. 137–148.

The phylogenetic relationships of Silesaurus opolensis have been the subject of intensedebate since its discovery. Silesaurus possesses some features characteristic ofornithischian dinosaurs, such as the presence of a beak at the front of the lower jaw, yetit lacks a number of important femoral and dental synapomorphies of Dinosauria. Themicrostructure of the long bones (femur, tibia and metatarsal) and ribs of this speciesreveals a relatively intensive rate of growth, comparable with that seen in small dinosaursand the gracile crocodylomorph Terrestrisuchus. Cortical bone formed mainly by perio-steal tissue with fibro-lamellar matrix (in older specimens parallel fibred) shows verylittle secondary remodelling and only in one specimen (large tibia ZPAL Ab III ⁄ 1885)few lines of arrested growth are present in the outermost cortex. The vascularization isrelatively dense, mainly longitudinal and ceases towards the periphery, forming almostavascular parallel fibred bone at the bone surface. This indicates maturation and signifi-cant decrease in the growth ratio in mature specimens of S. opolensis. The delicate trabec-ulae exhibit cores formed by the primary cancellous tissue lined with lamellar endostealbone. The rather intense growth of S. opolensis implies a relatively high metabolic rate.Moreover, evidence from the fibro-lamellar tissue, predominant in the cortex, suggeststhat this kind of rapid bone deposition could be more typical of Archosauria than previ-ously assumed, a prerequisite for the evolution of the very fast growth rates observed inlarge ornithischians, sauropods and large theropods. h Archosauria, Bone histology,Dinosauriformes, Late Triassic, Silesaurus opolensis.

Łucja Fostowicz-Frelik [[email protected]], Institute of Paleobiology PAN, Twarda51 ⁄ 55, PL-00-818 Warszawa, Poland, and Carnegie Museum of Natural History, 4400Forbes Avenue, Pittsburgh, PA 15213, USA; Tomasz Sulej [[email protected]], Instituteof Paleobiology PAN, Twarda 51 ⁄ 55, PL-00-818 Warszawa, Poland; manuscript receivedon 14 ⁄ 7 ⁄ 2008; manuscript accepted on 20 ⁄ 03 ⁄ 2009.

Silesaurus opolensis Dzik, 2003 was discovered in themiddle Keuper claystone beds of Krasiejow, south-western Poland. The phylogenetic position of thisspecies is a matter for some debate (e.g. Dzik 2003;Langer & Benton 2006; Irmis et al. 2007a,b; Butleret al. 2008), particularly following the recent discov-ery of new material that has allowed detailed recon-structions of the skull and sacrum (Dzik & Sulej2007). In the original description of S. opolensis, Dzik(2003) referred this species to Dinosauriformes, andpresented three alternative possibilities for thephylogenetic position of Silesaurus within this group.He stated that, ‘These similarities to herbivorousdinosaurs may mean that Silesaurus: (1) is an earlymember of the ornithischian lineage, (2) belongs tothe lineage leading to both the Ornithischia andProsauropoda, after its emergence from the ancestralcarnivorous stock, but prior to splitting or (3) formsa lineage that developed herbivory independently ofdinosaurs’ (Dzik 2003, p. 573). In a recent review ofthe Krasiejow faunal assemblage Dzik & Sulej (2007)provided a new reconstruction of the sacral region,which consisted of three sacral vertebrae, and of the

skull, based on newly discovered material. Theyemphasized that the beak present at the rostral endof the lower jaw may be homologous with the eden-tulous predentary bone generally considered uniquefor Ornithischia (Norman et al. 2004; Butler et al.2008; see also Ferigolo & Langer 2007). By contrast,recent phylogenetic analyses based upon extensivecladistic data sets place Silesaurus as a sister group toDinosauria (Ezcurra 2006; Langer & Benton 2006;Irmis et al. 2007b). Langer & Benton (2006) notedthat Silesaurus shares some dental apomorphies withOrnithischia. The ornithischian affinities of Silesaurusmay additionally be supported by the presence of:‘sacral vertebrae with transverse processes not cranio-caudally expanded, distal pubis not bulging andsignificantly narrower than the proximal part of theblade and a distal tibia with an acute-angled medio-cranial corner’ (Langer & Benton 2006, p. 347).However, the exact phylogenetic position of Silesau-rus remains unresolved. Nesbitt et al. (2007) statedthat it is best considered a non-dinosaurian dinosauri-form, closer related to Dinosauria than Marasuchus.Butler et al. (2008, p. 17) also excluded it from

DOI 10.1111/j.1502-3931.2009.00179.x � 2009 The Authors, Journal compilation � 2009 The Lethaia Foundation

Dinosauria, classifying Silesaurus as a ‘problematicnon-ornithischian ‘dinosauriform’.

Ours is the first study to document the bone micro-structure of a non-dinosaurian dinosauromorph,phylogenetically one of the closest taxa to Dinosauria.The data on Silesaurus provided herein complementthe recent study by de Ricqles et al. (2008), increasingthe number of the archosaurian taxa for whichdetailed palaeohistological studies have been con-ducted. We discuss also the possible implications ofbone microstructure for the physiology of thisintriguing species.

Materials and methods

The studied bone tissue was sampled from the shaftregion of the long bones (femora, ZPAL Ab III ⁄ 411 ⁄ 4,ZPAL Ab III ⁄ 405, ZPAL Ab III ⁄ 2380; tibiae, ZPAL AbIII ⁄ 1270, ZPAL Ab III ⁄ 414, ZPAL Ab III ⁄ 1885 andmetatarsal ZPAL Ab III ⁄ 1927) and from the ribs(ZPAL Ab III ⁄ 1928, ZPAL Ab III ⁄ 1929 and ZPAL AbIII ⁄ 1286) of several specimens of S. opolensis. The longbones were cross-sectioned either in the middle of theshaft length or as close to this point as possible(Fig. 1), according to the standard procedures. Addi-tionally, some sections present regions placed closer tothe metaphyses to document better the histologicalvariability of Silesaurus.

The thin sections were studied under a light micro-scope in normal and polarized light (de Ricqles 1975;Chinsamy-Turan 2005). All sampled specimens andthin sections are housed in the collection of the Insti-tute of Paleobiology, Polish Academy of Sciences,Warsaw (abbreviated ZPAL).

Bone histology

General features

The transverse sections of all the elements, made inthe vicinity of the mid-length of the shaft, display thecompact cortex of relative thickness of 18–27%. Thepredominant matrix type of the cortex is fibro-lamel-lar bone. In younger (smaller) specimens collagenfibres express frequently the checker-like arrangement,whereas in larger specimens (e.g. ZPAL Ab III ⁄ 411 ⁄ 4or ZPAL Ab III ⁄ 1270) they are arranged in circumfer-ential bundles.

The vascular network is mainly longitudinal, weaklyanastomosing only in the deep cortex region. In smal-ler individuals the canals have almost no osteonaldeposits, whereas only very nascent are visible in thelargest specimens (forming black cross-like pattern inpolarized light).

The interior of the medullary cavity of long bonesis almost empty, whereas the perimedullar regionshows variably developed cancellous bone, formingtrabeculae. In the sections closer to the metaphysealregions, the cancellous tissue fills all the interior spaceof the marrow cavity. Furthermore, in the femur andtibia specimens, an avascular transition zone formingan annular structure can be observed at the border ofthe deepest cortex and medullar region. In the rib sec-tions the perimedullar region displays large erosioncavities and relatively few delicate trabeculae. The tra-beculae, in most cases, have cores of cancellous bonelined with lamellar endosteal deposit.

The secondary remodelling is poorly expressed inthe cortex and there are virtually no secondary ost-eons. Medullar region displays generally endosteal lin-ing of the internal surfaces (margin of the cavity andtrabeculae) and has a well-developed inner circumfer-ential layer, ICL (Chinsamy-Turan 2005).

Ribs

The cross-sections of the ribs of S. opolensis display athick cortical region, surrounding an almost hollowmedullary cavity. The cortex ⁄ medulla border is irregu-lar and wavy, exhibiting large resorption cavities anddelicate mixed structure trabeculae (Fig. 2A), havingcores of the cancellous bone lined with an endosteal

A B

Fig. 1. Location of the cross-sectional planes in the sampled fem-ora and tibiae of Silesaurus opolensis. A, Femora ZPAL AbIII ⁄ 411 ⁄ 4, ZPAL Ab III ⁄ 405 and ZPAL Ab III ⁄ 2380. B, TibiaeZPAL Ab III ⁄ 414, ZPAL Ab III ⁄ 1270 and ZPAL Ab III ⁄ 1885.

138 Ł. Fostowicz-Frelik & T. Sulej LETHAIA 43 (2010)

lamellar bone layer (Fig. 2B–D). The cross-section ofthe medullar region of ZPAL Ab III ⁄ 1286 shows alsostrong secondary remodelling in some of the trabecu-lae, the structure consisting of differently orientedpatches of secondary lamellar bone (Fig. 2C). At themargin of the medullary cavity a thin but distinctinner circumferential layer (ICL) is present as an end-osteal deposit of avascular lamellar bone (Fig. 2B–D).It lines all erosion cavities and main marrow cavity.

The relatively thick cortex, constituting approxi-mately 27% of the total bone diameter, is composedof fibro-lamellar bone showing rather extensive vascu-larization of fine, longitudinally oriented, primarycanals (Fig. 2A–C). They are dispersed almost evenlythroughout the cortex, except for the most externalregions where the canals are less frequent and smallerin diameter (Fig. 2A), and not anastomosing. The pri-mary canals have only nascent layer of osteonal lamel-lar bone, recognizable under polarized light (Fig. 2B).

The cross-section of the rib does not show any signsof interrupted growth such as lines of arrested growth(LAGs) or annuli; however, the bone matrix of theexternal cortex display discrete ‘zonation’ marked bythe plies of condensed osteocyte lacunae (Fig. 2A).

Femur

Three femora were sectioned for this study, the largestone, ZPAL Ab III ⁄ 2380 is equal in size to the femur ofthe holotype specimen (ZPAL Ab III ⁄ 361), which isone of the largest individuals found in Krasiejow. Twoother femora used for this study are larger than thefemur associated with the second well-preserved skele-ton of S. opolensis (ZPAL Ab III ⁄ 1930).

The cross-section of the femoral shaft shows a corti-cal region composed of compact bone and a largemarrow cavity. The medullary region either lacks can-cellous tissue completely, in the case of sections takencloser to the mid-diaphyseal region (the specimensZPAL Ab III ⁄ 405 and ZPAL Ab III ⁄ 2380) or is filledwith intensely remodelled cancellous tissue (Figs 3, 4).This latter type of tissue forms delicate trabeculae inthe specimen ZPAL Ab III ⁄ 411 ⁄ 4, which was sec-tioned closer to the metaphyseal region (Fig. 4). Thetrabeculae consist predominantly of secondary cancel-lous bone and fill the entire medullar region displayedin this section (Fig. 4B). The cortical wall in this speci-men is thin and formed by poorly vascularized parallelfibred bone deposit with scarce primary osteons and afew nascent secondary osteons (Fig. 4).

The cortex of both ZPAL Ab III ⁄ 405 and ZPAL AbIII ⁄ 2380 is of uniform thickness along the entire cir-cumference and amounts to 18–19.5% of the totalshaft diameter. The compacta is densely vascularizedand consists of fibro-lamellar bone, which shows no

A

B

D

C

Fig. 2. Structure of rib of Silesaurus opolensis. A–C, cross-sectionof ZPAL Ab III ⁄ 1928 showing the compact and richly vascularizedcortex and almost hollow marrow cavity. B, C, internal circum-ferential layer (ICL), lining surface of the marrow cavity. D, thetrabecular structure of ZPAL Ab III ⁄ 1286, showing a core of thecancellous bone (cb) lined with the endosteal layer (el). C, D,polarized light.

LETHAIA 43 (2010) Bone histology of Silesaurus opolensis 139

interruption by LAGs or annuli, and virtually notraces of haversian remodelling (Fig. 3A–C). Thefibres show some spatial organization, especially in theexternal part of the cortex, where they group intoshort bundles, mostly oriented circumferentially andparallel to one another (Fig. 3A) or, less frequently,oriented radially, together with the circumferentialbundle creating a net surrounding the primaryosteons. Most vascular canals are oriented longitudi-nally and anastomose poorly, mainly in the mid-cortex region (Fig. 3). Similar to the rib cross-section,a gradient of vascularization decreasing peripherally isevident throughout the cortical region. The mostexternal parts of the cortex are significantly less vascu-larized (Fig. 3B, C) and the primary canals are smallerthan these in the deeper parts of the cortex. The

periphery of the cortex also shows markedly lessercondensation of the osteocyte lacunae and the pre-dominance of the parallel circumferentially orientedcollagen fibres in the bone matrix (Fig. 3B, C; see alsoFig. 4B).

In the outermost part of the cortex of ZPAL AbIII ⁄ 405 there is a small swelling (Fig. 3D) with a radialpattern of canals, representing the distal part of thefourth trochanter. The innermost part of the cortex atthe perimedullar region in specimens ZPAL AbIII ⁄ 405 and ZPAL Ab III ⁄ 411 forms an annular avas-cular transition zone (Figs 3A, B, 4B, C ), character-ized by a condensation of large globular osteocytelacunae (Fig. 4C). The fibres of this annular structureare oriented at an oblique angle to the radius of thebone (not parallel to the circumference as in typical

A B

C D

Fig. 3. Structure of femur ZPAL Ab III ⁄ 405 of Silesaurus opolensis. A–C, cortex formed by fibro-lamellar densely vascularized bone; theperimedullar region with avascular annular transition zone (atz) and internal circumferential layer (ICL) formed by the endosteal tissue.D, orientation change in vascular canals in the base of the trochanter of ZPAL Ab III ⁄ 405. A, polarized light.


annuli) and lie parallel to one another forming, in thepolarized light, a homogenous dark band (Figs 3A,4B). The internal surface of the avascular transitionzone contacts a thin layer of endosteal lamellar bone(ICL), which lines the internal surface of the compacta(Figs 3A, 4B). The contact surface between the transi-tion zone and the ICL represents a reversal line divid-ing two different directions of the bone deposition.This reversal line is best exhibited in the stronglyeroded parts of the cortex of ZPAL Ab III ⁄ 411 ⁄ 4,where the trabeculae with cores formed of a cancellousbone, extensively lined with secondary lamellar tissue,

are compressed against the remains of the cavernedfibro-lamellar cortex (Fig. 4A).

Tibia

Three tibiae of S. opolensis were sectioned for the pur-pose of this study, the specimen ZPAL Ab III ⁄ 1270being one of the largest assigned to this species andmatching the size of the bone (160 mm long) associ-ated with the holotype ZPAL Ab III ⁄ 361. Two othersectioned specimens, ZPAL Ab III ⁄ 414 and ZPALAb III ⁄ 1885, are slightly smaller but similar in size

A C

B

Fig. 4. Structure of femur ZPAL Ab III ⁄ 411 ⁄ 4 of Silesaurus opolensis. A, the reversal line (arrows) in the heavily caverned perimedullar regionof marking the cortex ⁄ medulla transition. The trabeculae exhibit core consisting of the cancellous bone (cb) and the endosteal lining (el). B,cross-section in the metaphyseal region, showing compacta formed by parallel-fibred bone and denser trabecular arrangement; note the avas-cular annular transition zone (atz) in the perimedullar region and ICL. C, structure of the cortex; note the lessening of vascularization in themost peripheral region and condensation of lacunae in the transition zone; the scarce small secondary osteons (so) can be distinguished inthe medullar part. A, B, polarized light.


(ca. 140 mm long) to the bones associated with skel-eton ZPAL Ab III ⁄ 1930. The specimens ZPAL AbIII ⁄ 1270 and ZPAL Ab III ⁄ 414 were sectioned in thediaphyseal region but relatively close to the proximalextremity, whereas specimen ZPAL Ab III ⁄ 1885 wassampled in the mid-diaphyseal region. The cross-sec-tion of the shaft is oval with the cortex occupyingapproximately 20% of the shaft diameter in all studiedspecimens. The cortical tissue of ZPAL Ab III ⁄ 414 andZPAL Ab III ⁄ 1885 consists of fibro-lamellar bone(Fig. 5), exhibiting some ordering in the arrangementof the fibres, particularly in the most external regionswhere it turns into parallel-fibred bone (Fig. 5B). Thevascular network is generally longitudinal, with someweak anastomoses in the deeper cortex (Figs 5A, 6A,B frame). By contrast, the most external part of thecortex shows a decrease in vascularization. In speci-men ZPAL Ab III ⁄ 1885, a few LAGs are observed inthis part marking thin zones (Fig. 5A). Both speci-mens (ZPAL Ab III ⁄ 414 and ZPAL Ab III ⁄ 1885) havecompletely hollow medullar cavity lined with ICL,which in ZPAL Ab III ⁄ 1885 is thick and has zonalstructure, including two LAGs (Fig. 5).

In ZPAL Ab III ⁄ 1270, the structure of the cortex issimilar, except for the part of the circumference,

where the innermost region is sharply separated fromthe perimedullar region consisting of cancellous bone,by a ring-shaped avascular transition zone formed of adense bone rich in large lacunae and parallel fibres ori-ented obliquely to the radius of the bone (Fig. 6D, E).In the part of the circumference of the cross-section ofZPAL Ab III ⁄ 1270 where the transition zone is lessdefined (Fig. 6G) or not present (Fig. 6F), the borderbetween the cortex and the perimedullary region iswavy, showing traits of intense remodelling. The innersurface of the avascular transition zone forms a line ofreverse growth (as is also seen in the femur ZPAL AbIII ⁄ 414 ⁄ 4; Fig. 4A–C), marking a change in the direc-tion of bone accretion. The spongiosa seen in the peri-medullar region of the ZPAL Ab III ⁄ 1270 consists of asecondary cancellous bone. There are no traces of cal-cified cartilage, but some of the trabeculae have theremains of the primary bone in their cores. In someregions of the circumference of ZPAL Ab III ⁄ 1270there are fragments of the ICL preserved. The patchesof cancellous bone are sandwiched between the inter-nal cortex and the ICL in regions where annulus isdiffused (Fig. 6G). Such an arrangement in cross-sections of the regions closer to metaphysis is inter-preted as a result of bone drift. The insertions ofcoarse cancellous bone are remnants of the porousbone tissue placed close to the epiphysis early inontogeny, and later incorporated into the shaft duringgrowth (Chinsamy-Turan 2005).

Metatarsal bone

The microstructure of the metatarsal of S. opolensisresembles that of the femur and tibia, but the com-pacta is thicker, forming approximately 27% of thediameter of the shaft.

The cortex is formed by densely vascularized fibro-lamellar bone, but the vascularization weakenstowards bone periphery (Fig. 7). In the outer cortexthere is a poorly developed zone of avascular bone,visible in normal light as a darker layer with con-densed osteocyte lacunae, and a single row of longitu-dinal canals overlying it externally (Fig. 7A). Furtherexternally, the decrease in vascularization towards thebone perimeter can be observed. Internally, themedullar cavity and erosion cavities in the perimedul-lar region are lined with a thin layer of lamellar endos-teal bone, forming the ICL (Fig. 7A–C).

The marrow cavity is completely hollow (Fig. 7A,B), without traces of trabeculae, but in the perimedul-lar region small erosion cavities occur (Fig. 7C). Theinternal cortex in the perimedullar region is cancellousand, apart from the evidence of remodelling, showssigns of a bone drift, with patches of secondary cancel-lous tissue preserved between the periosteal cortex

A

B

Fig. 5. Structure of large tibia ZPAL Ab III ⁄ 1885. A, note LAGs inthe outer cortex (arrows) and thick inner circumferential layer(ICL) lining medullar cavity. B, the view in polarized light elucidatesparallel arrangement of the collagen fibres in the most externalcortex, forming ‘ill-defined’ external fundamental system (EFS).


and the endosteal inner circumferential layer(Fig. 7D). The transition zone in these specimens hasmore diverse morphology and although it surroundsmost of the medulla perimeter, it does not form sucha regular ring as in femur or tibia. In the parts close tothose with signs of a bone drift the transition zonebecomes significantly wider, dispersed and also vascu-lar (Fig. 7C). In the remainder of its perimeter it isstill avascular and much thinner.

Discussion

Age of the individuals

Archosaurs display a wide spectrum of differentgrowth strategies and tempos of maturation withmarked differences between crurotarsans and

dinosauromorphs (de Ricqles et al. 2003a,b, 2008;Irmis 2007). Although the bone structure can be, tosome extent, an excellent source of information aboutthe age of the individuals (Chinsamy & Hillenius2004), data from skeleton morphology are comple-mentary and important tools (Irmis 2007). In archo-saurs, the most helpful tool to determine theontogenetic status, apart from the histology itself, isthe structure of the vertebrae, in particular the closingof the neuro-central suture. Although the closure ofthe neuro-central suture is not an ultimate proof ofmaturation, for many groups of archosaurs it isassumed to be a morphological indicator of adult age(Brochu 1996; Irmis 2007). However, the exactsequence in which the closing of this suture occurswithin the vertebral column is not uniform in archo-saurs (e.g. Irmis 2007). As demonstrated by Brochu(1996) the closure of the neuro-central sutures in

A

D E F G

B C

Fig. 6. Structure of tibia of Silesaurus opolensis. A–C, the cortical region of ZPAL Ab III ⁄ 414; A, close-up of the internal cortex (inset in B),visible anastomosing vascular canals and net pattern of the fibres; C, the external cortex showing decrease in the vascularization and more cir-cumferential arrangement of the fibres (turned 180� anticlockwise). D–G, cross-section of the ZPAL Ab III ⁄ 1270; D, E, the internal cortexwith well-developed avascular transition zone (atz) and trabeculae with the periosteal core lined with lamellar tissue. F, G, cross-sections ofthe metaphyseal region showing the irregular line of remodelling (F) and bone drift with the cavernous trabecular part sandwiched betweenthe cortex and the internal circumferential layer (ICL). D, normal light.


crocodilians proceeds from caudal to cranial verte-brae. The same pattern is known for phytosaurs, aeto-saurs, and is surmised, but not fully confirmed, insome groups of dinosaurs (Irmis 2007). However, it isproven that at least some representatives of Ornithis-chia, Sauropoda (Camarosaurus) and Theropoda (e.g.Nqwebasaurus and birds) do not share the postero-anterior direction in the suture closing, but quite theopposite, at least in some parts (cervical-dorsal) of theskeleton (Irmis 2007).

The age assignment of the bones of S. opolensissectioned for this study was not based solely on thespecimen size, although generally we selected the larg-est individuals, but also on the comparison of theirsize with other limb bones associated with parts ofvertebral columns showing closed neuro-centralsutures. There are a few well-preserved specimens ofSilesaurus with much of the vertebral column present(Dzik 2003; Dzik & Sulej 2007). The holotype speci-men, ZPAL AbIII ⁄ 361, is one of the largest specimensin the whole sample (the length of the third sacral andthe first caudal vertebrae alike is 24 mm), andincludes cervical, dorsal, sacral and caudal vertebraeall displaying closed neuro-central sutures (Dzik 2003,figs 2, 8). Similarly, a smaller specimen, ZPAL AbIII ⁄ 1930, with a first caudal vertebral length of 21 mmand 18 mm anterior centrum height, also displayscompletely closed neuro-central sutures in articulatedcervical, dorsal and caudal vertebrae (Dzik & Sulej2007, fig. 18). The same holds true for ZPAL AbIII ⁄ 364 which includes cervical and dorsal regions ofthe vertebral column (Dzik 2003, fig. 4). The smallestknown sacral vertebra ZPAL Ab III ⁄ 1274 (20 mm inlength and 15 mm posterior centrum height) has anunclosed suture between the sacral rib and vertebralcentrum, but the neuro-central suture is closed.

Thus, to sum up, all specimens of S. opolensis thatpreserved larger parts of the vertebral column show aclosed condition of the neuro-central sutures in allvertebral regions. Apart from extant birds, which closeneuro-central sutures either prior to hatching or soonafter hatching (Irmis 2007), the complete fusion of theneuro-central suture marks adulthood in most archo-saurian groups. Even if S. opolensis exhibits the reverseof the condition in crocodilians, i.e. the antero-poster-ior direction of the suture closure or the selective typeof the fusion, as was observed in Typothorax (Irmis2007), the existence in the same skeleton of cervicaland caudal vertebrae with closed sutures indicatesmature or close-to-adult ontogenetic status.

We are aware that taphonomy can bias the fossilrecord, especially the taphocenose structure (e.g. byeliminating some age groups entirely from therecord), thus the size cannot be the only criterion ofthe age. Nevertheless, a strong selection on size was

A B

C

D

Fig. 7. Structure of metatarsus of Silesaurus opolensis, ZPAL AbIII ⁄ 1927. A, B, cross-section in the diaphyseal region, visibledensely vascularized cortex with a single poorly developed con-densation zone (con) and the internal circumferential layer(ICL) lining medullar cavity. C, D, cross-sections taken closer tothe metaphyseal region; note signs of bone drift with cancellousremodelled bone packed between the cortex and the ICL, andthe vascular transition zone (trz) in the perimedullar region. A,normal light.


not detected for any of the vertebrate taxa present inthe Krasiejow assemblage, apart from the absence ofthe smallest individuals of metoposaurs (Sulej 2007).Furthermore, it is true for all vertebrates, even thosehaving indeterminate growth pattern, that growthslows down with age, and that slowing is reflected inthe bone histology. There are some important histo-logical traits marking this process: reduced vasculari-zation, predominance of longitudinal canals (lack ofanastomoses), narrowing of the zones depositedbetween successive LAGs, an occurrence of the ICLlining the margins of the marrow cavities and forma-tion of an external fundamental system at the boneperimeter (Padian & Horner 2004). All these featuresare present in the material studied herein. The well-developed ICL is clearly visible in most of the cross-sections studied (Figs 2B–D, 4B, 5, 6G, 7), there is asignificant decrease in vascularization of the outercortex (Figs 3A–C, 5, 6B–C, F, 7A–B), and there areclosely placed LAGs (Fig. 5).

Although in most cases it is impossible to establishthe age of the animal with absolute certainty, in thecase of the specimens of S. opolensis studied here, themost plausible assumption, supported both by themorphological and histological evidence is that allstudied specimens were close to maturity.

Another possible interpretation is that the neuro-central sutures in S. opolensis closed relatively early inthe ontogeny as was supposed for some phytosaursfrom the Otis Chalk beds, Upper Triassic, DockumGroup, Texas (Irmis 2007), and the slowing in bonedeposition in the outer cortex may reflect some sea-sonal effects. However, this possibility must be treatedwith caution because it would be highly unlikely thatSilesaurus alone among all other Triassic archosaursexpressed the pattern known only from recent birds,whereas the whole range of archosaurian groupsexpresses either the crocodilian (Brochu 1996) or thereverse pattern strongly correlated with age (Irmis2007). The unclosed suture between the sacral rib andcentrum found in the smallest known sacral vertebra(ZPAL Ab III ⁄ 1274) corroborates that Silesaurus wasno exception among the archosaurs and the closing ofthe neuro-central sutures as well as the sacral rib–cen-trum sutures were age-related processes.

Growth pattern

The documentation of growth patterns amongstarchosaurs represents a major area of active research(e.g. Horner et al. 2000; Starck & Chinsamy 2002;Padian et al. 2004; Erickson 2005). Multiple patternsof bone growth are observed amongst archosaursranging from relatively slow-growing crurotarsans (0–5 lm per day) to fast-growing large dinosaurs (over

20 lm per day; Padian et al. 2004). It has beensuggested that growth rates within Archosauria aregenerally not closely related to phylogenetic relation-ships. Instead, it was proposed that the growth ratesreflect metabolic rate and overall physiological adapta-tions, in agreement with the Amprino’s Rule (Padian& Horner 2004; de Ricqles et al. 2008), particularlyamongst sauropodomorphs and the largest ornithis-chians, which attained mature body sizes within a fewyears of intense growth (Padian et al. 2001, 2004).However, the bone tissue can express considerabledevelopment plasticity and the results obtained fromstudies on extant birds should be applied to the dino-saurian life strategies and termoregulation with cau-tion (see Starck & Chinsamy 2002; Chinsamy &Hillenius 2004). Despite that, a ‘typically dinosaurian’growth pattern has been identified on the basis of anumber of features generally considered characteristicof fast growth (Padian et al. 2001). These include thedense vascularization with longitudinal, concentricand radial canals, fibro-lamellar bone with a woven-fibred matrix, collagen fibres arranged not onlycircumferential (as in most pseudosuchians sensuPadian et al. 2004) but also in other directions,zonation developing either late in the ontogeny or notexpressed at all. However, it is obvious that theoccurrence and expression of these features vary at thegeneric level and that not all of these features arepresent in some small dinosaurs (Chinsamy-Turan2005).

The bone tissue of S. opolensis suggests fast growthrate, exceeding that observed in most crurotarsans orpseudosuchians (sensu de Ricqles et al. 2003a, 2008),with the exception of Terrestrisuchus and Postosuchus,which exhibit more rapid bone deposition (de Ricqleset al. 2003a, 2008; Padian et al. 2004). However, thebone tissue of Silesaurus is considerably less vascular-ized than that of larger, fast-growing dinosaurs, suchas Maiasaura or even slightly larger Coelophysis (seeHorner et al. 2000; Padian et al. 2004), and vascularcanals in Silesaurus are arranged mainly longitudi-nally, with the short circumferential anastomosingcanals present mainly in the deep cortex of the tibia ofZPAL Ab III ⁄ 414 (Fig. 5A, B). In general appearance(matrix type and canal arrangement) it resembles alsothe tissue of Lesothosaurus (de Ricqles et al. 2008, pl.3, fig. 3), but the canal diameters are significantlysmaller and density of vascularization lower inSilesaurus than in that early ornithischian.

The predominant bone type in Silesaurus is fibro-lamellar tissue with a woven-fibred matrix and small,but well-defined, primary osteons. That type of bonetissue (i.e. with a random arrangement of the fibres)indicates a high ratio of deposition, which is commonin juvenile tetrapods (Chinsamy 1995), as well as in


dinosaurs (e.g. Chinsamy-Turan 2005). In smallerspecimens, a characteristic arrangement of collagenfibres is observed, forming a network of short parallelsets of fibres positioned perpendicularly to oneanother (Fig. 5A), with primary osteons formed in themeshes of this net. However, in the largest specimens,the arrangement of the fibres in the outer cortexbecomes parallel and vascularization almost disap-pears (e.g. Figs 3A–C, 5, 6C, F, G), forming a tissuethat resembles the structure observed in Erythrosuchusas ‘an ill-defined external fundamental system’ (deRicqles et al. 2008, p. 63, pl. 1, fig. 3).

The external fundamental system (EFS, called alsothe outer circumferential layer, OCL; Chinsamy-Turan 2005) signals the maturation and slowing ofthe tempo of bone deposition (Chinsamy-Turan2005). The well-developed EFS is typical of animalswith terminate growth (e.g. birds and mammals) buthas also been observed in smaller dinosaurs, such asScutellosaurus, Orodromeus, Confuciusornis and the‘Victorian hypsilophodontid’ (Chinsamy et al. 1998;Padian et al. 2004; Chinsamy-Turan 2005). A typicalEFS consists of either lamellar or lamellated bone, iscompletely avascular and may or may not have LAGsor annuli (Chinsamy-Turan 2005). In S. opolensis, theinstances of this structure are atypical and poorlyexpressed, and the outermost regions of the cortex arenot completely avascular, although the diameter ofthe canals lessens dramatically (Figs 2A, 3B, C, 4B, C,5, 6C, F, 7A) in a manner similar to that in Erythro-suchus (de Ricqles et al. 2008). There are no distinctannuli in the outer cortex of S. opolensis; however, thetissue shows more regular arrangement of the fibres,typical of parallel-fibred matrix. Moreover, the exis-tence of a few well-defined LAGs in the outermostcortex, divided by thin poorly vascularized zones,found in the large tibia ZPAL Ab III ⁄ 1885 (Fig. 5)supports the interpretation that the growth ratio instudied specimens was slowing down considerably asanimals reached maturity (Chinsamy et al. 1998; deRicqles et al. 2003a, 2008; Padian et al. 2004;Chinsamy-Turan 2005).

Lines of arrested growth and haversianremodelling

The typically developed cortical LAGs are very rare inS. opolensis and appear only in largest specimen, in thecross-section of the mid-diaphyseal region (Fig. 5).Moreover, the poorly developed zone of condensedavascular tissue, marked by the accumulation of theosteocyte lacunae in the cortex of rib and metatarsus(Figs 2A, 7A) can reflect the influence of seasonal fac-tors, such as food or water accessibility. This is espe-cially the case where it is followed by a single layer of

larger canals, indicating the subsequent ameliorationof the environment conditions. Nevertheless, thesestructures were not developed into a typical LAG,indicating that the changes in habitat were not sodrastic and the growth was not stopped, but only itsrate was decreased.

In Silesaurus, the secondary osteons are generallyabsent in the cortex and appear in this region only inthe largest of the studied tibiae (ZPAL Ab III ⁄ 1270)and femora (ZPAL Ab III ⁄ 411 ⁄ 4), mainly as isolatednascent forms in the most internal parts. In the me-dullar region also a few small secondary osteons occurincidentally (Fig. 4A, C).

The secondary osteons and haversian remodellinghave been used as the indicators of maturity. Never-theless, recent studies have shown that the appearanceof the haversian bone varies within species dependingon age, sex, the anatomical region from which thebone sample comes and possible physical stresses dur-ing the animal’s life (Chinsamy-Turan 2005). Second-ary osteons were observed in the young specimens ofDryosaurus (Chinsamy 1995), and were reported asvery rare in adult Coelophysis (Chinsamy-Turan2005). They are absent in Lesothosaurus (de Ricqleset al. 2008). The density and location of the secondaryosteons within the compacta were variable in Baro-saurus, interpreted in terms of sexual dimorphism(Sander 2000). Thus, the absence of secondary osteonsmay suggest that in Silesaurus the haversian remodel-ling occurred late in ontogeny and was not so intense,similar to that seen in some small dinosaurs (e.g. Coel-ophysis, Herrerasaurus and Lesothosaurus), and thefast-growing crocodylomorph Terrestrisuchus (deRicqles et al. 2003a, 2008; Chinsamy-Turan 2005).

Nevertheless, the signs of the intense haversianremodelling are common in the medullar region,where the trabeculae are frequently heavily remodelledand all of them are lined with endosteal deposits. Inmost of the studied sections, apart from these takenclosest to the mid-diaphyseal region a well-developedtransition zone occurs. In the majority of the studiedindividuals of Silesaurus the transition zone is avascu-lar and has an annular shape (Figs 3A, B, 4B, C, 6D,E) contrary to the structures illustrated by Nesbittet al. (2006, fig. 2d, h, l) of the metaphyseal region ofthe femur of Hesperosuchus and Coelophysis, whichdid not circle entire medullar cavity, but appeared ascurved or straight (respectively) structures. The transi-tion zone in most of the studied specimens of Silesau-rus is avascular like in Hesperosuchus, but the sectionof the metatarsal shows more diversified structure,with inflated vascularized parts (Fig. 7C). The struc-ture of the transition zone and its shape seems to bestrongly related to its closeness to the epiphysis, andoccurrence of the bone drift-related structures.


Conclusions

Bone microstructure is not the best tool to determinephylogenetic relationships within Archosauria. How-ever, recent research has demonstrated that bonemicrostructure can give insights into physiology andmetabolic rates (e.g. Padian et al. 2004; de Ricqleset al. 2008). The latter issue was discussed by Chins-amy (1995) and Chinsamy et al. (1998), who sug-gested that the rapid and sustained pattern of bonedeposition, and the general rate of growth observed inDryosaurus may indicate that this genus, as well as the‘Victorian hypsilophodontid’, were capable of main-taining body temperature at high levels by endoge-nous means. Moreover, a similar pattern amongstMesozoic ornithurine birds suggests that they were en-dotherms (Chinsamy 2002).

The zonal–lamellar pattern and flexible growthstrategy have been proposed as primitive charactersfor Archosauria (de Ricqles et al. 2003a; Chinsamy-Turan 2005). However, bone microstructure highlysimilar to that observed in small dinosaurs has alsobeen demonstrated amongst basal crocodylomorphs,such as Terrestrisuchus, and erythrosuchians, indicat-ing a rate of growth higher than in most crurotarsans(pseudosuchians sensu de Ricqles et al. 2003a, 2008).These observations call into question previous identi-fications of the primitive characters of bone micro-structure and growth rate in Archosauria. In the lightof a recent study by de Ricqles et al. (2008), itbecomes more obvious that archosaurs attained a rela-tively fast growth rate early in their evolutionary his-tory. It is not clear which type of bone deposition wasbasal, the fibro-lamellar complex or the lamellar–zonalcomplex, or the condition varied and each type of thetissue development appeared more than once in eachgroup (de Ricqles et al. 2008). Nevertheless, some ofthe archosaurian groups (many pseudosuchians)express relatively low rates of growth, whereas others(some dinosaurs, pterosaurs and birds) even furtherincreased the already high rate (known already in Tri-assic representatives, e.g. Erythrosuchidae).

According to that scenario, the fastest growth rateshave evolved independently at least thrice: in largepterodactyloid pterosaurs, large derived ornithopodornithischians and saurischians.

The evidence presented here suggests that growthrates in Silesaurus were relatively fast in studied speci-mens, that the growth was restricted in mature indi-viduals, and that they grew probably in a non-cyclicalmanner, especially at earlier ontogenetic stages. It isplausible that an individual of Silesaurus achieved fullsize during its first year and then its growth slowedrapidly allowing for the formation of the almost

avascular lamellated external layer. However, there isinsufficient evidence to propose endothermy forSilesaurus. The bone microstructure, as well as themorphology depicts Silesaurus as a member of thegroup of active, agile archosaurs and small dinosaurs,such as Terrestrisuchus (Padian et al. 2004), Confuciu-sornis (de Ricqles et al. 2003b), the polar ‘Victorianhypsilophodontid’ (Chinsamy 1995) and basalornithischians, such as Scutellosaurus and Orodromeus(Padian et al. 2004) or Lesothosaurus (de Ricqles et al.2008). From a palaeoecological point of view, suchforms would profit from a higher metabolic ratio,because it would allow quicker reactions either inescape or pursuit.

Acknowledgements. – We thank Magdalena Borsuk-Białynickaand Jerzy Dzik (Institute of Paleobiology, PAN, Poland) for manyhelpful comments at the earlier stages of the research. We alsoexpress our gratitude to Anusuya Chinsamy-Turan (University ofCape Town, Rondebosh, South Africa) for critically reading thefirst version of the manuscript and for many helpful suggestions.We are deeply grateful to Richard Butler (Museum of Natural His-tory, London) for kind and constructive criticism and to an anony-mous reviewer for focusing our attention on some aspects of thepalaeohistology. Ted Daeschler (Academy of Natural Sciences ofPhiladelphia, USA) kindly checked the final version of the MSlinguistically. Zbigniew Strak (Institute of Paleobiology, PAN,Poland) prepared the thin sections for this study. The study wassupported by the Foundation for Polish Science (Warsaw, Poland)grants to both authors.

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Bone histology of Silesaurus opolensisDzik, 2003 from the Late Triassic of Poland

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