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. 2025 Feb 17;247(3-4):712–727. doi: 10.1111/joa.14229

Palaeobiology and osteohistology of South African sauropodomorph dinosaurs

Fay‐yaad Toefy 1,✉, Emil Krupandan 2, Anusuya Chinsamy 1
PMCID: PMC12397067  PMID: 39960138

Abstract

Several sauropodomorph dinosaurs have been excavated from the Elliot Formation (EF) of Southern Africa which include important taxa such as Massospondylus, Melanorosaurus and Antetonitrus. The study of the bone microstructure of smaller, bipedal Sauropodomorpha and larger, quadrupedal Sauropoda allow us to infer how the growth dynamics changed during the evolution of gigantism. Historically, osteohistological studies of Sauropodomorpha tended to have focused on either early diverging taxa (e.g. Plateosaurus & Massospondylus) or on derived taxa (diplodocids & titanosaurs), whereas studies on the growth dynamics of the transitionary groups (i.e. Sauropodiformes & early Sauropoda) are poorly known. Here, we assess the palaeobiology of two sauropodiformes and an early sauropod by analysing their bone histology. Thin sections of the long bones of two indeterminate sauropodiformes NMQR 3314 and NMQR 1551, and an indeterminate sauropod SAM–PK–K382 were prepared. The general histology of the long bones of all three dinosaurs were similar. Rapid growth through the deposition of fibrolamellar bone tissue characterised their respective ontogenies. Lines of arrested growth (LAGs) were commonly located in the mid and outer cortex signalling the onset of uninterrupted growth. Differences in the histology of these dinosaurs were principally related to the pathological bone tissue evident in the femur of the sauropodiform NMQR 1551 and to the formation of annuli around LAGs in Sauropoda indet., as well as in the location of LAGs in the compacta. The number of LAGs in the cortex varied among the taxa but generally the outer regions of the cortex showed an accumulation of LAGs. The growth dynamics of our three sauropodomorph dinosaurs are similar to early sauropods such as Antetonitrus. It appears that the abundance of fibrolamellar bone tissue and uninterrupted growth at later ontogenetic stages are likely key traits in the early evolution of gigantism in Sauropoda, which supports the occurrence of a mosaic of growth dynamic patterns among transitionary Sauropodomorpha.

Keywords: dinosauria, Elliot Formation, growth dynamics, histology, Sauropodiformes, Sauropodomorpha

We found that the transitionary Sauropodiformes show both the traits of rapid growth of derived Sauropoda as well as interrupted growth of early branching Sauropodomorpha. There appears to be much more variation in growth dynamics of Sauropodiformes than initially thought.

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1. INTRODUCTION

Sauropodomorph dinosaurs ranged from small bipeds to the gigantic, quadrupedal sauropods which roamed the Earth from the middle Triassic to the Cretaceous (Nesbitt et al., 2013). The evolution of gigantism can be studied through their osteohistology by examining the changes in their growth dynamics (e.g. Cerda et al., 2017; Chinsamy, 2023; Chinsamy‐Turan, 2005; Sander, Christian, et al., 2011). Palaeobiological data such as growth rates, bone tissue types, and ontogenetic stages can be directly assessed from their bone microstructure (Chinsamy‐Turan, 2005; Francillon‐Vieillot et al., 1990). How the Sauropodomorpha grew, that is, their growth dynamics, varied substantially (Apaldetti et al., 2018; Cerda et al., 2017; Sander, Klein, et al., 2011).

Early osteohistological research on the Sauropodomorpha (Chinsamy, 1993, 1994; Curry, 1999; De Ricqles, 1983, Sander et al., 2004, Klein, 2005, Klein & Sander, 2007, Sander, Christian, et al., 2011) suggested that non‐sauropodan Sauropodomorpha grew cyclically with the periodic deposition of predominantly parallel‐fibred bone and the occurrence of lines of arrested growth throughout ontogeny. This growth pattern is considered as the ‘typical’ growth of the early branching Sauropodomorpha. The latter researchers (Sander et al., 2004; Klein, 2005, Klein & Sander, 2007; Sander et al., 2011) further suggested that only derived taxa, such as sauropods, grew rapidly with LAGs only forming in the late ontogenetic stages (Klein & Sander, 2007; Sander et al., 2004; Sander, Christian, et al., 2011). This growth pattern of predominant uninterrupted growth prior to LAG deposition is referred to as the ‘typical’ growth of the late diverging Sauropoda (Klein, 2005; Klein & Sander, 2007; Sander et al., 2004; Sander, Christian, et al., 2011). This dichotomy of growth strategies was poorly supported by sparse studies on the early diverging Sauropodomorpha and Sauropodiformes. Recent studies (Apaldetti et al., 2018; Cerda et al., 2017, 2022; Krupandan et al., 2018) show that there is far more variation in the growth dynamics of early sauropodomorphs and sauropods. More specifically, the osteohistology of sauropodiformes such as, Sefapanosaurus (Botha et al., 2022) and Aardonyx (Botha et al., 2022; Yates et al., 2010), as well as the Lessemsauridae show a combination of fast, cyclical growth (Apaldetti et al., 2018; Cerda et al., 2017) suggesting that sauropodan growth traits evolved gradually among sauropodiformes. Subsequently, this shows that rapid rates of bone deposition started occurring before the development of large body size. Furthermore, the comprehensive analyses of the bone histology of the early sauropodomorph, Mussaurus, showed much intraspecific variation in their growth dynamics, which ranged from uninterrupted continuous, rapid growth rates to cyclical, slower rates of growth (Cerda et al., 2017, 2022).

Given that only a few sauropodiform dinosaurs have had their growth analysed through osteohistological studies, here, we describe the histology of the long bones of two sauropodiformes dinosaurs: NMQR 3314 (Figure 1) and NMQR 1551 (Figure 2) (formerly considered to be Melanorosaurus but recently amended as an indeterminate sauropodomorph) (Barrett & Choiniere, 2024), and SAM–PK–K382 which will be subjected to a phylogenetic analysis in this publication in order to provide a phylogenetic framework for comparison of this taxon to the others. A more comprehensive anatomical, taxonomic and phylogenetic assessment of SAM–PK–K382 will be published separately (Krupandan pers. comm. 2024). Since this large‐bodied, indeterminate sauropodomorph was excavated from the Elliot Formation (EF), we hypothesise that it will fall within the Sauropodiformes. Given the prior phylogenetic placement of NMQR 1551 and NMQR 3314 (see Apaldetti et al., 2018; Barrett & Choiniere, 2024), and the likely position of SAM–PK–K382, we hypothesise that these dinosaurs would show the rapid, uninterrupted growth in early ontogeny prior to onset of cyclical deposition of parallel‐fibred bone during late ontogeny as seen in the related sauropodomorph taxa such as Antetonitrus and Lessemsaurus.

FIGURE 1.

FIGURE 1

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Photographs of NMQR 3314 (a) fibula and (b) tibia. Dashed red line show the area which was sectioned and described. Scale bar = 5 cm.

FIGURE 2.

FIGURE 2

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Photographs of NMQR 1551 (a) tibia and (b) femur. Dashed red lines show the area which was sectioned and described. Labels on the images correspond to the headings in Results. Scale bar = 5 cm.

1.1. Institutional abbreviations

NMQR—Bloemfontein National Museum, South Africa; SAM—Iziko South African Museum, South Africa.

2. MATERIALS AND METHODS

2.1. Phylogenetic analysis

SAM–PK–K382, due its unknown phylogenetic status, was scored and added to the Pol et al. (in press) data matrix, which already contains NMQR 1551 and NMQR 3314. It is a modified version of the data set originally published by Yates (2007a). Forty‐one characters were treated as ordered following Pol et al. (in press). The dataset includes some sauropodomorph outgroups, reaching a total of 90 taxa and 421 characters (Data S1,S2 for character list and character‐taxon matrix). The data matrix was created using Mesquite 3.51 (Maddison & Maddison, 2018) and analysed under equally weighted parsimony in TNT Version 1.5 (Goloboff et al., 2008), using a heuristic search of 1000 replicates of Wagner trees (with random addition sequence) followed by tree bisection and reconnection branch swapping. Node supports were calculated using decay indexes (Bremer support) and absolute GC bootstrap frequencies calculated after 10,000 pseudoreplicates. To evaluate the causes of the polytomy within the strict consensus tree and identify the taxa causing instability; we applied the iterative PCR procedure (Pol & Escapa, 2009) to the data matrix identifying and pruning (a posteriori) unstable taxa to obtain a more resolved reduced strict consensus (RSC) tree. The phylogenetic nomenclature follows the definitions proposed by Sereno (2007) for Sauropodomorpha and Sauropodiformes and Yates (2007b) for Sauropoda.

2.2. Histological analysis

Both indeterminate Sauropodiformes, NMQR 3314 and NMQR 1551, as well as sauropodomorph indet. (SAM–PK–K382) were excavated from the EF which ranges from the Late Triassic (Lower EF) to the Early Jurassic (Upper EF) and dates from approximately 220–140 million years ago. The selected elements of SAM–PK–K382 were 3D scanned, pre‐sectioning, using an Artec Space Spider light scanner (Artec3D) and 3D models were produced using the accompanying Artec Studio software. The sectioned material and 3D models are currently housed at the Iziko South African Museum, Cape Town, South Africa. The NMQR 1551 and 3314 material was provided post sectioning and casts are available from the Bloemfontein National Museum, Bloemfontein, South Africa. Long bones were sectioned in the midshaft area (Figures 1, 2, 3) (dashed red lines) as this portion of the bone best preserves a record of the complete bone growth (Chinsamy & Raath, 1992; Chinsamy‐Turan, 2005). The bone exterior showed clear breakages (Figures 1, 2, 3) but the deformation was minimal in the sectioned elements. One thin section was prepared from the fibula (Figure 1(a)) and tibia (Figure 1(b)) of NMQR 3314. Three thin sectioned marked A1 to A3 were prepared from the NMQR 1551 tibia (Figure 2(a)) and five marked B1 to B5 prepared made from the femur (Figure 2(b)). A partially complete femur (Figure 3(a)), a fragmented fibula (Figure 3(b)) and tibia (Figure 3(c)) from SAM–PK–K382 were sampled as shown. Thin sections were made using the procedure outlined in Chinsamy and Raath (1992).

FIGURE 3.

FIGURE 3

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Photographs of Sauropoda indet. SAM–PK–K382 (a) femur, (b) tibia and (c) fibula. Dashed red lines show the area which was sectioned and described. Scale bar = 5 cm.

Photomicrographs were taken using the Axiocam 208 Colour camera mounted on a Zeiss AX10 petrographic microscope. The photographs were processed in the Zeiss Blue software (V3.0) (Zeiss, Germany) and edited in Clip Studio Paint (Celsys, Japan). Composite photographs were obtained using AutoPanoGiga (Kolor, France). Histological descriptions were completed using terminology from Francillon‐Vieillot et al., (1990) and Chinsamy‐Turan (2005). Since the bone wall of the specimens were quite large, the bone wall was split into thirds for histological descriptions (i.e., outer, mid, and inner cortices). When specific portions are not preserved in the thin section, the same terminology is used as the regions are relative to the entire bone wall shown in the thin section schematics. The full histographs and high resolution images are available on Morphobank project 5620.

3. RESULTS

3.1. Phylogenetic analysis

The initial heuristic search resulted in 260 most parsimonious trees (MPTs) of 1750 steps found in 28 out of 1000 replicates. A further round of TBR branch swapping of these 260 trees resulted in 48,680 MPTs of the same tree length. The strict consensus has large polytomies in basal nodes of Sauropodomorpha. Applying the IterPCR procedure (Pol & Escapa, 2009) in TNT, we identified thirteen unstable taxa as the cause these polytomies: Arcusaurus, Pradhania, Nambalia, Xixipiosaurus, Seitaad, Yunnanosaurus youngi, Yizhousaurus, Blikanasaurus, Pulanesaura, Amygdalodon, Volkheimeri, Barapasaurus and Patagosaurus. Ignoring their positions in the MPTs results in a much more resolved RSC tree (Figure 4). Consistency index (CI) and retention index (RI) values for the RSC are 0.287 and 0.673, respectively. Bremer Support (decay index) values are low, rarely exceeding 2 indicating weak support for these relationships. Absolute (GC) Bootstrap values generally provide support for clades closer to terminal nodes above 50%.

FIGURE 4.

FIGURE 4

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Phylogenetic relationships of NMQR 1551, NMQR 3314 and SAM–PK–K382 within Sauropodomorpha sub‐tree of Reduced Strict Consensus Tree. 48,680 Most Parsimonious Trees (MPTs) with a best score of 1705 after 13 unstable taxa: Arcusaurus, Pradhania, Nambalia, Xixipiosaurus, Seitaad, Yunnanosaurus youngi, Yizhousaurus, Blikanasaurus, Pulanesaura, Amygdalodon, Volkheimeri, Barapasaurus and Patagosaurus were excluded from the consensus. Number above branches indicate bootstrap values (absolute) >50%, those below indicate Bremer supports. CI = 0.287, RI = 0.673.

NMQR 1551 (formerly considered to be Melanorosaurus) is recovered as the immediate outgroup to Sauropoda, with NMQR 3314 as one step more derived, falling within Sauropoda. This position is similar to that seen in Barret & Choiniere (2024) and identical to the topology in Pol et al. (in press). SAM–PK–K382 is recovered as a non‐Gravisaurian sauropod more derived than the Lessemsauridae.

3.2. Summary of the histology of NMQR 3314

NMQR 3314 is represented by a well‐preserved tibia displaying the full histological record and a poorly preserved fibula in which majority of the cortex is fragmented.

The tibia (Figure 1(a)) comprised of a consistent abundance of fibrolamellar bone tissue from inner cortex to the outer cortex except for the regions near the bone periphery where parallel‐fibred bone tissue has been deposited (Figure 5(a)). The inner cortex comprised of fibrolamellar and secondarily reconstructed bone tissue. A band of lamellar bone resembling at inner circumferential layer is located at the boundary of the medullary cavity (Figure 5(b)). The fibrolamellar and parallel‐fibred bone tissue generally showed a high degree of vascularisation and vascular canals were often in a reticular or plexiform arrangement. Secondarily reconstructed bone tissue is limited to the inner regions of the compacta. These regions often consist of small secondary osteons and resorptive canals dispersed within the fibrolamellar bone dominated compacta. While the bone tissue is well preserved, LAGs are poorly preserved and only two are located in the outer regions of the cortex.

FIGURE 5.

FIGURE 5

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Histological thin section of NMQR 3314 tibia (a & b) and fibula (c, d & e). (a) Composite micrograph of the general histology of the femur from the inner cortex of the femur to the peripheral bone tissue. White arrows indicate the growth marks. Yellow arrow indicates the ICL‐like bone tissue. (b) Lamellar bone tissue lining the medullary cavity shown by the yellow arrow. This band of lamellar bone tissue is not present in other regions of the compacta. (c) Intensively reconstruction bone tissue in the inner regions of the mid cortex. Large secondary osteons are formed around several large resorptive cavities. (d) Low magnification view of the fibrolamellar bone tissue with vascular canals in a plexiform arrangement. White arrows indicate the growth marks. (e) High magnification view of a growth mark embedded in fibrolamellar bone tissue.

Although, the cortex of the NMQR 3314 fibula (Figure 1(b)) is fragmented, it still provides information about the general bone histology. The inner regions of the cortex comprised mostly of fibrolamellar and cancellous bone tissue (Figure 5(c)). Well vascularised fibrolamellar and parallel‐fibred bone tissue is common throughout the mid and outer cortex (Figure 5(d)). The vascular canal arrangement varies between a reticular and plexiform arrangements and tends to be more organised in the outer regions of the compacta. Secondary osteons and resorptive canals are present in the innermost regions of the cortex but due to the fragmentation, the extent of secondary reconstruction cannot be determined. The locations of LAGs are limited by the fragmentary state as three are located within the mid portion of the compacta embedded within the fibrolamellar bone tissue (Figure 5(e)).

3.3. Summary of the histology of NMQR 1551

The histology of the tibia (Figure 2(a)) of NMQR 1551 is described from three thin sections. The inner cortex comprises of primarily fibrolamellar and secondarily reconstructed bone tissue (Figure 6(a)). Moderately sized secondary osteons and resorptive canals are common within the inner cortex and is often surrounded by the primary fibrolamellar bone tissue. The mid cortex shows a decrease in secondary bone tissue, that is, the number of secondary osteons and resorptive cavities (Figure 6(b)) and well vascularised fibrolamellar bone is abundant throughout this region. Vascular canals are arranged in a reticular pattern through the inner and mid regions and transition to a plexiform arrangement in the outer cortex. The outer cortex comprises of predominantly fibrolamellar bone tissue (Figure 6(c)) but the abundance of parallel‐fibred tissue increases near the outermost margin of the bone wall. The vascularity decreases within the region near the bone periphery where six to seven LAGs are located (Figure 6(d)).

FIGURE 6.

FIGURE 6

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Histological sections A1—A3 of NMQR 1551 tibia. (a) Composite micrograph of the tibia from the perimedullary to the periphery region. White arrows indicate the growth marks. (b) High magnification view of fully formed and small secondary osteons in the fragmented mid cortex. (c) High magnification view of framed area in (a) showing fibrolamellar tissue with long radially branching vascular canals. (d) High magnification view of a LAG surrounded by a low density of osteocytes.

The histology of the femur midshaft (Figure 2(b)) of NMQR 1551 comprises of a transition from fibrolamellar and secondarily reconstructed bone to fibrolamellar and parallel‐fibred bone (Figure 7(a)). The inner cortex consists of well vascularised fibrolamellar and secondarily remodelled bone tissue (Figure 7(b)). Secondary osteons and resorption canals are common in this region and range in size from moderate to large. Vascular canals are in a haphazard, reticular arrangement and this continues into the mid cortex. The mid cortex is similar to the inner cortex but the amount of secondary reconstruction is considerably lower. The fibrolamellar bone tissue is still dominant continuing from the inner to mid cortex and vascular canals tend to be in a plexiform arrangement. This trend continues (Figure 7(c)) in the outer cortex, but there are some areas of parallel‐fibred bone. Vascular canals tend to have a plexiform arrangement. Additionally, a band of radially fibrolamellar bone occurs near the peripheral margin of the cortex. Similar yet thinner bands of radially deposited fibrolamellar bone are observed to a lower degree in outer third of the cortex.

FIGURE 7.

FIGURE 7

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Histological sections B1–B5 of the NMQR 1551 femur. (a) Composite micrograph showing the histology of the femur from the medullary region to bone periphery. White arrows indicate the growth marks. (b) Low magnification view of large resorptive cavities near the medullary cavity. (c) Low magnification view of two LAGS between loosely arranged fibrolamellar bone. (d) High magnification view of the well vascularised, radially organised fibrolamellar bone tissue (green arrow) located between two LAGs shown by the white arrows. The radial fibrolamellar bone tissue is only present in this half of the cross section of the femur.

3.4. Summary of the histology of Sauropoda indet (SAM‐PK‐K328)

The femoral histology of SAM‐PK‐K382 is described from five different thin sections. In all the sections, fibrolamellar bone was the predominant bone tissue throughout the compacta (Figure 8(a)). The inner cortex comprised fibrolamellar bone and secondarily reconstructed bone tissue consisting of numerous large, resorptive canals and secondary osteons that are visible within the fibrolamellar matrix. Clumps of dense Haversian bone are dispersed throughout the inner regions of the compacta (Figure 8(b)). The mid cortex comprised of predominantly fibrolamellar bone tissue which show intense birefringence (Figure 8(c)). LAGs are located in the middle portion of the compacta (Figure 8(a)) and become more abundant in the outer third. Lamellar tissue becomes common as these LAGs are embedded in a thin layer of lamellar bone tissue resembling an annulus (Figure 8(d)). Three to four LAGs are seen in the outer part of the mid cortex whereas five to seven LAGs are located in the outer cortex. The fibrolamellar bone tissue is well vascularised throughout the cortex but a drastic decrease in vascularisation is seen in the lamellar bone surrounding the LAGs.

FIGURE 8.

FIGURE 8

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Histological section of the Sauropoda indet. (SAM–PK–K382) femur. (a) Composite micrograph showing the general histology of the femur from the medullary cavity to the bone periphery. White arrows indicate the growth marks. (b) Fully formed secondary osteons in the inner cortex. Some secondary osteons start to overlap forming incipient Haversian bone. (c) High magnification view of the typical loose intrinsic fibre organisation in the well vascularised fibrolamellar tissue. (d) High magnification view of plexiform fibrolamellar bone tissue between two growth marks (white arrows) in relatively close succession.

The tibial histology (Figure 3(b)) is comprised predominantly of fibrolamellar bone tissue in the mid and outer cortex whereas the inner cortex is primarily secondarily reconstructed tissue (Figure 9(a)). The inner cortex consists of numerous large resorptive canals giving the area a cancellous texture. Secondary osteons are found embedded in the fibrolamellar bone tissue. Dense Haversian bone tissue is common on the outer regions of the inner cortex (Figure 9(b)). The secondary reconstruction continues into the mid cortex albeit the size of resorptive cavities and secondary osteons decreases. Well vascularised fibrolamellar bone tissue in a plexiform arrangement is the most abundant bone tissue in the mid cortex (Figure 9(c)) and continues towards the bone periphery. The outer cortex is primarily fibrolamellar bone tissue with more parallel‐fibred bone at the bone periphery. LAGs are located throughout the mid and outer cortex interrupting the fibrolamellar bone tissue. Lamellar bone tissue can be seen surrounding LAGs forming annuli. Three to four LAGs are located in mid cortex and four to five are located in outer cortex.

FIGURE 9.

FIGURE 9

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Histological section of the Sauropoda indet. (SAM–PK–K382) tibia. (a) Composite micrograph showing the general histology of the tibia from in medullary cavity to the bone periphery. White arrows indicate the growth marks. (b) Concentration of secondary osteons forming dense Haversian bone tissue in the inner compacta. (c) Fibrolamellar bone tissue with vascular canals in a laminar to plexiform arrangement. One growth mark in visible within a narrow band of lamellar bone tissue.

The fibular histology (Figure 3(c)) was poorly preserved but the general bone tissue can be discerned (Figure 10(a)). The inner cortex comprised fibrolamellar, cancellous and secondarily remodelled bone tissue. The remodelled tissue consists of large resorptive cavities (Figure 10(b)), numerous secondary osteons and dense Haversian bone tissue (Figure 10(c)) is found in isolated patches in the inner parts of the compacta. The mid cortex is primarily fibrolamellar bone tissue with vascularisation in either a plexiform or laminar arrangement. Small resorptive cavities and secondary osteons are dispersed throughout the middle regions of the cortex. The outer cortex is comprised of mostly moderately vascularised fibrolamellar bone with more parallel‐fibred bone tissue present nearing the outer bone wall. Secondary osteons are sparse but present in the outer regions. LAGs are only located within the region nearing the bone periphery and there is a thin band of lamellar bone surrounding the LAGs (Figure 10(a)).

FIGURE 10.

FIGURE 10

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Histological section of the Sauropoda indet. fibula. (a) Composite micrograph of the anterior end of the fibula. Osteocytes are poorly preserved and bone texture resembles a fibrolamellar‐parallel‐fibred complex. White arrows indicate the growth marks. (b) Low magnification view of the cancellous bone which surrounds the fragmented medullary cavity. (c) High magnification view of dense Haversian bone in the middle cortex.

4. DISCUSSION

The growth dynamics of Sauropodiformes and Sauropoda are quite variable and is supported by the findings of this study. All three dinosaurs show a trend of rapid growth through the deposition of fibrolamellar bone tissue but the location and duration of the interruptions in growth are highly variable. NMQR 3314 shows a rapid growth throughout ontogeny with lesser amounts of parallel‐fibred bone at the periphery. There are only three LAGs observed in NMQR 3314 which are located in the outer half of the cortex. NMQR 1551 presents with more ‘typical’ sauropod growth (Sander et al., 2004; Sander, Christian, et al., 2011) of the three dinosaurs, in that its cortex is primarily composed of rapidly deposited fibrolamellar bone tissue with parallel‐fibred bone occurring late in ontogeny. All seven LAGs are located within the outer third of the cortex and the density of the LAGs increases towards the outer bone wall. Sauropoda indet. is the most phylogenetically derived of the three taxa studied. Rapidly deposited fibrolamellar was the most common bone tissue within its cortex but there were regular interruptions in growth shown by the ten LAGs throughout the compacta. The abundance of fibrolamellar bone tissue and significant azonal growth suggests that the typical derived sauropod‐like growth (Sander et al., 2004, Sander, Klein, et al., 2011) was already evident within the Sauropodiformes clade (Botha et al., 2022; Cerda et al., 2017; Cerda et al., 2022; Krupandan et al., 2018).

4.1. Intraskeletal variation and general histology

4.1.1. NMQR 3314

The well‐preserved tibia of NMQR 3314 shows the complete histological record of growth, which contrasts with the poor preservation evident in the highly fragmented fibula. Despite these differences, it is evident that the tibia and fibula have similar bone histology, although they vary slightly in terms of the extent of secondary remodelling.

The abundance of fibrolamellar tissue in the compacta suggests that this sauropodiform dinosaur had experienced rapid early growth (Chinsamy‐Turan, 2005; Erickson et al., 2007) and had sustained this rapid growth for much of its life. It is apparent that the animal experienced a decrease in growth rate only during later stages of ontogeny as parallel‐fibred tissue is evident in the outer parts of the compacta. The fragmented fibula shows similar growth patterns as the compacta is primarily fibrolamellar bone tissue with parallel‐fibred bone occurring late in ontogeny. In both elements growth marks only form late in ontogeny. The dominance of fibrolamellar bone tissue in the compacta, and the delayed deposition of LAGs is similar to Antetonitrus (Krupandan et al., 2018) and some Mussaurus specimens (Cerda et al., 2017, 2022; Chinsamy, 2023). The delays in LAG deposition would also suggest that sexual maturity was achieved later in ontogeny but extrapolating from the current state of its histology, it is likely that this individual would have grown much larger, and for a longer period.

Secondary reconstruction

Secondary reconstruction occurs in response to a number of factors, such as the repair of microcracks caused by biomechanical stress (Chinsamy, 2023; Chinsamy et al., 2020; Enlow, 1962a; McFarlin et al., 2016) or as a result of the phosphocalcic metabolism (Chinsamy, 1994; Huttenlocker et al., 2013). The associated secondary reconstruction associated with muscle attachment would change over time as the animal get older and larger (McFarlin et al., 2016). However, it appears that this specimen was relatively young as shown by the three to four LAGs in the compacta which would suggest a small amount of secondary reconstruction within the compacta. Generally, older individuals tend to show more secondary reconstruction (Klein & Sander, 2008). The moderate amount of secondary reconstruction is likely a combination of factors such as resorption for the repair of damage caused by biomechanical or environmental stressors leadings to nutritional deficiencies (Chinsamy et al., 2021; Enlow, 1962a; McFarlin et al., 2016) which would in turn impact the amount of calcium for phosphocalcic metabolism (Chinsamy, 1994; Huttenlocker et al., 2013).

4.1.2. NMQR 1551

The histology of the femur and tibia of NMQR 1551 present similar bone tissue types suggesting similar growth dynamics. Both elements show rapid deposition of fibrolamellar bone tissue during initial stages of ontogeny‐ a trait shared among the Sauropodomorpha, which later transitions to a moderate rate of deposition leading to the deposition of parallel‐fibred tissue in late ontogeny. The growth during early and mid‐stages of ontogeny in NMQR 1551 primarily comprised of azonal growth and only much later is there the deposition of growth marks in the outer cortex. Although, the number of growth marks observed are variable because of diagenesis and secondary reconstruction, most of the sections show six or seven LAGs. It is generally held that the termination of early rapid rates of growth (indicated by fibrolamellar bone tissue) and the onset of growth marks (or change in bone texture to a more parallel‐fibred or lamellar‐like bone tissue) likely indicates the attainment of sexual maturity (Chinsamy‐Turan, 2005; Griebeler et al., 2013; Sander, 2000). There are no LAGs located within the NMQR—1551 inner cortex thus the late deposition of the LAGs suggests that sexual maturity was obtained much later in its ontogeny. In terms of skeletal maturity, there is a notable accumulation of LAGs towards the bone periphery but there is no observable outer circumferential layer (OCL) (Enlow, 1962b) suggesting that this individual was still growing albeit slowly and that an OCL would likely have formed soon.

Secondary reconstruction

Secondary remodelling was far more abundant in the femur than in the tibia (Figures 6 and 7). This would suggest that the NMQR 1551 femur would have likely experienced more biomechanical stress than the tibia (McPhee et al., 2018) which in turn would experience more secondary reconstruction to repair fatigued bone (Schaffler & Burr, 1984). When comparing the amount of secondary reconstruction, the femur of Mussaurus was observed to undergo more secondary reconstruction than all its other long bones that were studied (Cerda et al., 2022). Since Mussaurus is known to be an obligate quadruped; it is likely that NMQR 1551 which shows similar secondary reconstruction levels may have had a similar loading of its femur, and hence a similar locomotion towards a gravisaurian body plan (McPhee et al., 2018).

Radial fibrolamellar bone

The most significant difference between the histology of the femur and the tibia of NMQR 1551 is the development of radially oriented fibrolamellar bone tissue in the peripheral region of the femur. The radial spiculate, sunburst pattern or hair‐on‐end fibrolamellar tissue has been identified as a pathology in several vertebrates, including modern birds and nonavian dinosaurs (Chinsamy, 2023; Chinsamy & Tumarkin‐Deratzian, 2009; Lehrer et al., 1970; Lorigan et al., 1989). Thus, the resemblance of this unusual radially organised fibrolamellar bone tissue in NMQR—1551, to that observed as pathological in other dinosaurs (Chinsamy & Tumarkin‐Deratzian, 2009; Jentgen‐Ceschino et al., 2020) suggests that this tissue is pathological in NMQR 1551 as well. The pathological tissue tends to be localised in only one half of the outer cortex of the femoral thin sections. Similar distribution of pathological bone tissue has been observed in other Sauropodomorpha (Krupandan et al., 2018; Jentgen‐Ceschino et al., 2020; de Cerff et al., 2021). The actual cause of the pathology in the femur of NMQR 1551 is uncertain but could have been the result of infection or disease.

4.1.3. Sauropoda indet (SAM–PK–K382)

The Sauropoda indet. specimen is represented by a large partial femur, a fragmented tibia and a fibula, The long bones are relatively homogenous in their histology with only slight differences. Among all the long bones, the early stages of bone deposition are characterised by the uninterrupted deposition of fibrolamellar bone tissue. These rapid rates of bones deposition continue throughout most of the compacta but becomes interrupted by deposits of growth marks during late ontogeny. Such rapid rates of early growth to mid‐ontogeny observed in Sauropoda indet., is shared by both the sauripodiformes in this study, as well as numerous other later branching Sauropodomorpha such as Antetonitrus (Krupandan et al., 2018), Ingentia (Apaledetti, et al., 2018), Lessemsaurus (Cerda et al., 2017) and Volkheimeria (Cerda et al., 2017).

The number of growth marks visible in the compacta is somewhat variable among the long bones. The femora had at most ten LAGs starting from approximately halfway into the compacta, the tibia had about seven, whereas the fragmented compacta of the fibula only had four. The late deposition of growth marks shows that this indeterminate sauropod underwent a large amount of uninterrupted growth prior to the deposition of its first LAG. It may be that the onset of LAGs in the cortex marked the onset of sexual maturity (Erickson et al., 2007; Griebeler et al., 2013; Sander, 2000). The delayed deposition of the growth marks and early azonal growth are traits concomitant with those commonly observed in the osteohistology of Sauropoda (Cerda et al., 2017; González et al., 2020; Sander, Christian, et al., 2011). However, the overall characteristics of the osteohistology of the indeterminate sauropod studied here is more like the sauropodiform dinosaurs, such as Antetonitrus (Krupandan et al., 2018) and some Mussaurus specimens (Cerda et al., 2022). During times of slowed growth, thin bands of lamellar tissue are deposited and suggest that the animal might have experienced some environmental pressure (such as temperature, nutrient availability etc.) (Chinsamy, 1990, 2023; Horner et al., 2009; Köhler et al., 2012). Once the unfavourable period is over, the deposition of fibrolamellar tissue resumes. The distance between growth marks decreases towards the bone periphery suggesting that growth slowed down, and that the individual was approaching skeletal maturity.

Secondary reconstruction

Secondary reconstruction is common among all the elements studied in this indeterminate sauropod. The amount of reconstruction within the outer half of these elements is minimal as most secondary bone is found in the inner third. Portions of Haversian bone are in the inner cortex of the tibia and fully developed dense Haversian bone is seen in the inner cortex of the fibula. Given the larger size of this individual, and the number of LAGs in the cortex, it is likely that most of the secondary reconstruction would be attributed to biomechanical stress over extended periods of time (McFarlin et al., 2016). The intensive secondary reconstruction in the tibia when compared to femur is unexpected as the femur usually undergoes more biomechanical stress throughout life (McPhee et al., 2018; McFarlin et al., 2016). It is possible that other life history and environmental factors—such need for calcium for the phosphocalcic metabolism or other life history events such as egg laying (Chinsamy, 1994; Cubo & Huttenlocker, 2020; Montoya‐Sanhueza & Chinsamy, 2018)—are the likely reasons for the osteohistological variation.

4.1.4. The growth dynamics of Sauropodiformes and early diverging Sauropoda

Our understanding of sauropodomorph growth dynamics has greatly improved as more recent, studies have been conducted on various members of the clade (Apaldetti et al., 2018, 2021; Botha et al., 2022; Chapelle et al., 2021; Cerda et al., 2022; Cerda et al., 2017; de Cerff et al., 2021; Krupandan et al., 2018; Chinsamy, 2023). Prior to the research of Cerda et al. (2017), the existing paradigm suggested a binary distinction of zonal versus azonal growth when comparing early to late diverging Sauropodomorpha. However, today it is well recognised that there was greater variability in the growth dynamics of sauropodomorph dinosaurs (Botha et al., 2022; Cerda et al., 2017; Cerda et al., 2022; Chinsamy, 2023).

In the current study, the phylogenetic placement of NMQR 3314 places it in a position slightly more derived than NMQR 1551 (Figure 4). Its bone histology and inferred growth dynamics appears to resemble the derived sauropodomorphs such as Antetonitrus (Krupandan et al., 2018), Volkheimeria (Cerda et al., 2017), some specimens of Mussaurus (Cerda et al., 2022) as well as NMQR 1551 studied here. s. The NMQR 3314 resembles the derived sauropodiform dinosaurs due to the abundance of fibrolamellar bone prior to the first growth mark deposition and the late onset of LAG deposition. These specific features of its growth are much like sauropod dinosaurs such as Isanosaurus (Jentgen‐Ceschino et al., 2020) and Patagosaurus (Cerda et al., 2017). The osteohistology of NMQR 3314 shows that the evolution of rapid sauropod‐like growth was present prior to the evolution of Sauropoda as observed in other Sauropodiformes and basal Sauropoda.

Sauropodiformes NMQR 1551 together with NMQR 1551, provide valuable insight into the transition from the early to late Sauropodomorpha (Figure 1). In both of these dinosaurs, the compacta predominantly comprises of fibrolamellar bone prior to the transition to parallel‐fibred bone in the late stages of ontogeny. LAGs are seen in both the fibrolamellar and parallel‐fibred tissue but only in the outer third of the cortex. Similar in femur size to our Sauropoda indet. specimen. NMQR 1551 shows the most sauropod‐like growth dynamics in terms of its uninterrupted growth until the very late stage of ontogeny where LAGs are visible in the outer cortex (Curry Rogers & Kulik, 2018; González et al., 2020; Sander, 2000; Sander, Christian, et al., 2011). NMQR 1551 clearly shows that rapid growth and large body sizes (Apaldetti et al., 2018) was present before the evolution of the Sauropoda (Figure 14: Cerda et al., 2017). The trait of rapid and extended uninterrupted growth (i.e., deposition of azonal fibrolamellar bone) becomes increasing evident in the Sauropodiformes and early diverging Sauropoda. This growth strategy which was typically associated with Eusauropoda (Sander, Klein, et al., 2011) is observed in Antetonitrus (Krupandan et al., 2018) and some specimens of Mussaurus (Cerda et al., 2022), however it is notable that this trend towards sustained uninterrupted growth until late stages of ontogeny is absent in the medium sized sauropodiforms Sefapanosaurus (Botha et al., 2022) and Aardonyx (Botha et al., 2022; Yates et al., 2010). It is noteworthy that the woven‐parallel complex observed in these two sauropodiforms do show an increase in growth rates when compared to the ‘typical’ sauropodomorph growth dynamics.

Of all three dinosaurs in our study, Sauropoda indet. (SAM–PK–K382) was the most comprehensively sampled. LAGs are visible throughout the later portions of the outer half of its long bones. The initial uninterrupted deposition of fibrolamellar tissue through most of ontogeny is like that of the derived Sauropoda (e.g. González et al., 2020; Sander, 2000). More specifically, the entire compacta of Sauropoda indet. consists of mostly fibrolamellar bone except when the growth rate slows down during the deposition of thin bands of lamellar bone and the very late‐stage deposition of parallel‐fibred bone. The presence of the annuli formed by thin bands of lamellar tissue is likely formed due to environmental pressures causing growth to slow down prior to LAG deposition (see Section 4.1.4). The absence of these thin lamellar bands (surrounding the actual LAG) in other later branched Sauropodomorpha suggest that they experienced more abrupt interruptions in growth. An earlier onset of zonal growth, like SAM–PK–K382, is observed in Lessemsaurus (Cerda et al., 2017), which is less derived than our Sauropoda indet., but shows a similar pattern in growth in that it reached large body size without exclusive uninterrupted growth to late ontogeny. However, the zonal growth observed in the mid ontogenetic stages of Sauropoda indet. is different to the primarily zonal growth of Lessemsaurus in that there is periods of slow growth prior to arrested growth. However, it is clear that they both show mostly rapidly deposited fibrolamellar bone tissue throughout their cortices. Thus, it seems that Sauropoda indet., like Lessemsaurus (Cerda et al., 2017), was also able to reach a large body size without exclusive uninterrupted growth. The differences observed in terms of bone deposition between these two dinosaurs could be explained in terms of the variation and plasticity in growth such as those observed in Mussaurus (Cerda et al., 2022).

Some sauropodomorph taxa also show varying bone depositional rates (i.e., how quickly bone is deposited and how this can result in mixtures of typical bone types) as seen in Aardonyx (Botha et al., 2022; Yates et al., 2010) and Sefapanosaurus (Botha et al., 2022) as well as in the plasticity in growth seen in Mussaurus specimens (Cerda et al., 2017). Both rapid and moderate growth (in late ontogeny) are observed in these three sauropodomorph dinosaurs and in the three dinosaurs in our study. However, it is apparent that the dominance of fibrolamellar in our study taxa is similar to the later diverging sauropods than the early sauropodomorph dinosaurs. It is also worth emphasising that in our study, we found both interrupted (primarily in the indet. sauropod SAM–PK–K382), as well as largely uninterrupted growth patterns (in both NMQR 1551 and 3314 but more evident in NMQR 1551). Cerda et al. (2017) suggested that the growth patterns of Sauropodomorpha was variable and that there were less likely constraints on how sauropodomorph dinosaurs were able to grow.

Our understanding of the growth dynamics of the Sauropodiformes, is greatly enhanced with the addition of our study on NMQR 3314 and NMQR 1551 (and Sauropoda indet. (SAM–PK–K382) towards the growth of basal Sauropoda). Our sauropodiform dinosaurs sampled are closely related to sauropodiformes Mussaurus (Cerda et al., 2017; Cerda et al., 2022), Aardonyx (Botha et al., 2022; Yates et al., 2010), Leonerasaurus (Cerda et al., 2017), Antetonitrus (Krupandan et al., 2018 ), and Sefapanosaurus (Botha et al., 2022) but only share similarities with some Mussaurus specimens that show sauropod‐like growth dynamics and Antetonitrus. Zonal growth is observed in Aardonyx, Leonerasaurus, and Sefapanosaurus but these three sauropodiform dinosaurs also show a compacta dominated by a moderate rate of deposition leading to mostly parallel‐fibred bone. It is worth noting that Botha et al. (2022) suggested an intermediate growth rate through the deposition of a woven parallel‐fibred bone matrix in Sefapanosaurus and Aardonyx. This mixture of rapidly deposited woven bone and moderately deposited parallel‐fibred bone would suggest increases from the typical parallel‐fibred bone observed in basally branched Sauropodomorpha (Chinsamy, 1994, 2023; Klein & Sander, 2007). Interestingly, the sauropodiform, Mussaurus shares the latter growth pattern in some specimens. However, Cerda et al. (2022) have demonstrated that Mussaurus, the most comprehensively sampled sauropodomorph dinosaur, shows a significant amount of plasticity and has traits of both derived and basal growth patterns.

Thus, it seems that the changes in the growth dynamics from early to late diverging Sauropodomorpha does not follow a straightforward progression from slow, zonal growth to fast, azonal growth. The dichotomy suggested by early researchers (Klein, 2005; Klein & Sander, 2007; Sander et al., 2004; Sander, Klein, et al., 2011) has been refuted by several recent studies (Apaledetti et al., 2018; Krupandan et al., 2018; Chapelle et al., 2021, 2022; Botha et al., 2022; Cerda et al., 2017, 2022; Cerda et al., 2022) which is further supported by the rapid growth evident in all three of our sampled dinosaurs. The general trend in the basal Sauropodomorpha clade show the majority growing zonally with some variation in the growth rates, while among the Sauropodiformes clade, the prevalence of extended uninterrupted (azonal) growth increases (Cerda et al., 2017, 2022; Krupandan et al., 2018). Notable exceptions are seen in the derived taxa Lessemsaurus and Ingentia which showed fast yet zonal growth throughout the cortex, which permitted them to attain large body size. On the whole among the Sauropodomorpha, there appears to be general shifts in the deposition of growth marks from being present in the entire cortex (i.e., throughout ontogeny) to primarily occurring in the outer portion of the compacta (i.e., the late stages of ontogeny). NMQR 1551, Antetonitrus, Volkheimeria and some Mussaurus specimens show the most sauropod‐like growth via the deposition of uninterrupted fibrolamellar bone growth from early to late stages of ontogeny and only forming LAGs exclusively in the outermost portions of the cortex. The presence of the partially ‘derived’ growth dynamics in the early sauropodomorph taxa suggest that traits of sauropod‐like growth had already started to evolve early on in Sauropodomorpha (Cerda et al., 2017).

The overall changes in the growth dynamics of Sauropodomorpha to Sauropodiformes to Sauropoda shows the substantial variation and the mosaic nature of the occurrence of zonal and azonal growth in the whole clade (Cerda et al., 2017). Generally, the rates of bone growth increase from mostly moderate (i.e., parallel‐fibred bone) to rapid deposition (i.e., fibrolamellar bone) as the taxa become more derived but it evident that presumably derived traits can be observed in basal taxa. With the addition of two sauropodiforms dinosaurs, NMQR 1551 and NMQR 3314, and basal sauropod SAM–PK–K382, we see a clear increase in the abundance of rapid azonal growth in the Sauropodiformes compared to early diverging sauropodomorph dinosaurs (Cerda et al., 2017; Chinsamy, 2023). The evolution of rapid growth trajectories are key factors in the evolution of gigantism in the Sauropoda. However, among the Sauropodomorpha it is evident that giant sizes can be obtained with zonal growth (i.e., periodic periods of rapid growth) although azonal growth appears to dominate among the larger Sauropodiformes, but Mussaurus demonstrates a polymorphic condition in having both zonal and azonal growth dynamics (Cerda et al., 2022) emphasising the importance of studying a large number of individuals.

5. CONCLUDING REMARKS

Our findings support that the evolution of gigantism and growth dynamics of Sauropodomorpha is far more variable than initially thought. Here we report on the osteohistology and growth patterns of three Sauropodomorpha, (two Sauropodiformes and a basally branching Sauropoda). We demonstrate that although they all experienced rapid growth, the duration of uninterrupted growth varied between the three dinosaurs. The growth of these dinosaurs and other Sauropodiformes present a mix of both plesiomorphic and derived traits, with Mussaurus being the only sauropodomorph showing presenting with both cyclical and continuous growth dynamics. Thus, it is apparent that the growth dynamics of Sauropodiformes and early diverging Sauropoda is highly variable, and that although fast rates of growth are important to reach gigantic proportions, the latter is independent of whether the animal experiences such growth rates periodically or uninterruptedly.

AUTHOR CONTRIBUTIONS

F. T., E. K. and A. C. provided the concept and methodology of the study. F.T. and E. K. produced the thin sections. F.T. did the histological descriptions and wrote the first draft of the paper. E.K. provided phylogenetic support for the classification of the taxa under study, and A.C. supervised the study, edited and improved the manuscript.

Supporting information

Data S1.

JOA-247-712-s002.docx (105.6KB, docx)

Data S2.

JOA-247-712-s003.docx (64.5KB, docx)

Data S3.

JOA-247-712-s001.docx (27.9MB, docx)

ACKNOWLEDGEMENTS

We thank Claire Browning and Zaituna Skosan of the Iziko South African Museum, as well as Jennifer Botha of Bloemfontein National Museum for access to their collections and permission for histological sampling. SAHRIS for the permits for destructive analysis. Victoria Gibbon of the Department of Human Biology, UCT, for access to the Artec Space Spider and associated software. Thank you to the reviewers and editors for their comments and suggestions. The NRF (National Research Foundation of South Africa) (Grant no. 136510) is thanked for their funding to A. Chinsamy. This research was supported by GENUS: DSI‐NRF Centre of Excellence in Palaeosciences under Grant No. 86073 to F. Toefy.

Toefy, F.‐y. , Krupandan, E. & Chinsamy, A. (2025) Palaeobiology and osteohistology of South African sauropodomorph dinosaurs. Journal of Anatomy, 247, 712–727. Available from: 10.1111/joa.14229

DATA AVAILABILITY STATEMENT

Please contact the corresponding author as all data in this research is available.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Data S1.

JOA-247-712-s002.docx (105.6KB, docx)

Data S2.

JOA-247-712-s003.docx (64.5KB, docx)

Data S3.

JOA-247-712-s001.docx (27.9MB, docx)

Data Availability Statement

Please contact the corresponding author as all data in this research is available.

Articles from Journal of Anatomy are provided here courtesy of Anatomical Society of Great Britain and Ireland

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