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ONTOGENETIC HISTOLOGY OF STEGOSAURUS
PLATES AND SPIKES
by SHOJI HAYASHI1 , KENNETH CARPENTER2 , MAHITO WATABE3 and
LORRIE A. MCWHINNEY4
1Steinmann Institute Division of Paleontology, University of Bonn, 53115 Bonn, Germany; e-mail: [email protected] Museum, 155 East Main Street, Price, UT 84501, USA; e-mail: [email protected] for Paleobiological Research, Hayashibara Biochemical Laboratories, Inc., Okayama 700-0907, Japan; e-mail: [email protected] of Earth Science, Denver Museum Nature and Science, 2001 Colorado Boulevard, Denver, CO 80205, USA; e-mail: [email protected]
Typescript received 17 November 2010; accepted in revised form 17 June 2011
Abstract: The dinosaur Stegosaurus is characterized by
osteoderms of alternating plates and terminal paired spikes.
Previous studies have described the histological features
and possible functions of these osteoderms. However,
ontogenetic changes are poorly documented. In this study,
the ontogenetic changes of the osteoderms are examined
using eight different ontogenetic skeletons (a juvenile, a
subadult, a young adult, and five old adults based on the
cortical histology of their body skeletons). The juvenile
plate and subadult spike show thin cortex and thick can-
cellous bone. The young adult plates have an extensive
vascular network, which is also seen in old adults. Old
adult spikes are different from old adult plates in having a
thick cortex and a large axial channel. The cortical histol-
ogy, in both plates and spikes, show well-vascularized bone
tissue consisting of dense mineralized fibres in young adult
forms. In old adult forms, the bone tissues in the spikes
become more compact and are extensively remodelled. This
might contribute to the structural reinforcement of the
spikes. The plates in old adult forms also show extensive
remodelling and lines of arrested growth, but only limited
signs of compaction. The timing for acquisition of features
seen in old adults is different between plates (an extensive
vascular network in the young adult) and spikes (a thick
cortex with a large axial channel in old adults). The result
suggests that the timing for plate and spike functions is
different. The extensive vascular networks seen in large
plates suggest their function is for display and ⁄ or thermo-
regulation. The thick cortical bone of spikes of old adults
suggests that spikes acquire a weapon function for defence
ontogenetically late.
Key words: Stegosaurus, osteoderms, bone histology,
growth, function, Upper Jurassic, western USA.
T he possible function of plate and spike-shaped osteo-
derms in Stegosaurus has had a long and colourful his-
tory. Based on the position on the body and external
morphology, the plates have been assumed to play a pas-
sive role in defence, whereas the spikes have long been
assumed to be offensive weapons (e.g. Marsh 1877; Lull
1910; Gilmore 1914; Carpenter 1998; McWhinney et al.
2001; Carpenter et al. 2005).
More recently, external and internal morphology have
been used to infer the function of plates for thermal regu-
lation or display (Farlow et al. 1976; de Buffrenil et al.
1986; Main et al. 2005; Hayashi et al. 2009; Farlow et al.
2010). The use of plates in species recognition has been
proposed based on the absence of any phylogenetic trends
in the shape of plates and spikes within Stegosauria
(Main et al. 2005). Plate function has focused mainly on
the presence of large pipe-like vascular canals on both
internal and external surfaces (Farlow et al. 1976; de Buff-
renil et al. 1986; Main et al. 2005; Farlow et al. 2010). In
contrast, it has been assumed that the spikes were used as
a weapon based on the conical morphology and thick
cortical bone (e.g. McWhinney et al. 2001; Carpenter
et al. 2005). A damaged Allosaurus vertebra supported
this hypothesis (Carpenter et al. 2005). Previously, how-
ever, de Buffrenil et al. (1986) argued against a weapon
function because the spike they examined had a cancel-
lous internal structure. All of these studies have been
based on small sample sizes and have not focused on the
ontogenetic changes of plates and spikes. Therefore, the
conflicting interpretations may be due to individual
and ⁄ or ontogenetic variations.
This study approaches the argument on the function of
plates and spikes of Stegosaurus by examining multiple
individuals at different ontogenetic stages. Additionally,
to elucidate the function of the large pipe-like vascular
grooves on the plates, developmental patterns of the vas-
culature are examined in detail. These comparisons will
allow this study to test the cause of the conflicting
[Palaeontology, 2011, pp. 1–17]
ª The Palaeontological Association doi: 10.1111/j.1475-4983.2011.01122.x 1
differences in the previous studies and should lead us to a
better understanding of the functions of the Stegosaurus
osteoderms.
Institutional abbreviations. DMNH, Denver Museum of Nature
and Science, Denver, CO, USA; NSM-PV, National Science
Museum, Tokyo, Japan; HMNS, Hayashibara Museum of Natu-
ral Sciences, Okayama, Japan; UMNH, Utah Museum of Natural
History, Salt Lake City, UT, USA; YPM, Yale Peabody Museum,
Yale University, New Haven, CT, USA.
Other abbreviation. CT, Computed tomography; EFS, external
fundamental system; LAG, line of arrested growth.
MATERIALS AND METHODS
Materials. This study used eight ontogenetically different
Stegosaurus individuals from the Upper Jurassic Morrison
Formation (Table 1). Seven plates and eight spikes from
six skeletons (DMNH 33359, 1483, 2818, YPM 4634,
NSM-PV 20380 and HMNS 14) were examined using CT
scans. Eight plates and five spikes from eight individuals
(DMNH 33359, 1483, 2818, HMNS 14, NSM-PV 20380,
YPM 1853, 4634 and UMNH-VP 13688) were studied
using thin sections and ⁄ or polished sections. The position
of sampled plates and spikes was summarized in Table 1.
The taxonomy of these specimens followed Carpenter
et al. (2001) and Maidment et al. (2008). Most specimens
were previously identified as S.armatus (DMNH 1483,
2818 and YPM 1856; Maidment et al. 2008) or Hespero-
saurus (or Stegosaurus) mjosi (HMNS 14 (HMNH 001 in
previous studies); Carpenter et al. 2001; Maidment et al.
2008). A skeleton of NSM-PV 20380 was identified as
S. armatus because this specimen possesses all diagnostic
characters of S. armatus proposed in Maidment et al.
(2008). The characters are as follows: edentulous portion
of the dentary, anterior to the tooth row and posterior to
the predentary; dorsally elevated postzygapophyses of cer-
vical vertebrae; bifurcated summits of neural spines of the
anterior and middle caudal vertebrae; unexpanded poster-
ior end of the pubis; and the presence of dermal ossicles
embedded in the skin on the underside of the cervical
region (Maidment et al. 2008). Some specimens could
not be identified beyond the level of genus (DMNH
33359, YPM 4634 and UMNH-VP 13688) because they
bear no characters that allow referral to either Stegosaurus
species. Given present uncertainty about the specific and
even generic taxonomy of some of these specimens (Car-
penter et al. 2001; Maidment et al. 2008; Carpenter 2010),
we report the current names without expressing an opin-
ion about their validity.
Five Stegosaurus individuals (DMNH 33359, 1483,
NSM-PV 20380, YPM 4634 and 1856) are from the Salt
Wash Member of the Upper Jurassic Morrison Forma-
tion, Wyoming, USA, while two individuals (DMNH
2818 and UMNH-VP 13688) were collected from the
Brushy Basin Member of the Upper Jurassic Morrison
Formation, Colorado and Utah, USA (see also Carpenter
1998 for DMNH 2818). An individual of Hesperosaurus
(Stegosaurus) mjosi (HMNS 14) was from the Windy Hill
Member of the Upper Jurassic Morrison Formation,
Wyoming, USA (see Carpenter et al. 2001). Localities and
stratigraphic position of the Morrison Formation for
these materials were also noted in Table 1. More strati-
TABLE 1 . Sampled bones and the femur length (mm) of Stegosaurus.
Specimen Taxa Femur
length
(mm)
Observed element Ontogenetic
stage
Locality Stratigraphic
units in
Morrison Fm.
DMNH 33359 Stegosaurus sp. 233* Dorsal plate (1) Juvenile BQ SW
YPM 4634 S. sp. 487 Fore spike (2) Subadult Q13W SW
NSM-PV 20380 S. armatus 734 Dorsal plate (1), caudal plate (1),
fore spike (1), hind spike (1)
Young adult BQ SW
DMNH 1483 S. armatus 950 Caudal plate (1), hind spike (1) Old adult Q13W SW
DMNH 2818 S. armatus 1048 Caudal plate (1), hind spike (1) Old adult GP BM
HMNS 14 S. (Hesperosaurus)
mjosi
NA Plate (position unknown) (1),
cervical plate(1), dorsal plate (1)
Old adult SR WH
YPM 1856 S. armatus NA Fore spike (1), hind spike (1)
dorsal plate (1)
Old adult Q13W SW
UMNH-VP13688 S. sp. NA Plate (position unknown) (1) Old adult CLQ BM
Sample number of scanned and ⁄ or sectioned materials was shown in parentheses. The determination of ontogenetic stages was based
on histological features of body elements (see Hayashi et al. 2009). NA, not applicable; BM, Brushy Basin Member; BQ, Bone Cabin
Quarry; CLQ, Cleveland-Lloyd Quarry; GP, Garden Park; SR, S. B. Smith Ranch, Johnson Country; SW, Salt Wash Member; Q13W,
Reed’s Quarry 13; WH, Windy Hill Member (see Turner and Peterson 1999 and Carpenter et al. 2001 for all of these localities).
*Inferred limb measurements from the length of fibula.
2 P A L A E O N T O L O G Y
graphic data are summarized by Turner and Peterson
(1999) and Carpenter et al. (2001).
Preparations for CT scans and sections. The Stegosaurus
plates and spikes were scanned using a medical helical CT
scanner (CT-W2000; Hitachi Medical Corporation, 1 mm
slice thickness, 120 kV, 175 mA) at the National Institute
of Advanced Industrial Science and Technology, Tsukuba,
Japan. These data revealed that some specimens (a plate
and a spike of NSM-PV 20380) necessitated the use of a
high-resolution helical CT scanner to obtain optimal data
for the vasculature. The CT scanning was performed at
TESCO Corporation, Tokyo, Japan (BIR ACTIS + 3; TE-
SCO Corporation, 200 lm slice thickness, 180 kV,
0.11 mA). The raw scanned data of all specimens were
reconstructed using a bone algorithm. Data were output
from the scanners in DICOM format and then imported
into VG-Studio Max (Volume Graphics) for viewing,
analysis and visualization of vascular networks in plates
and spikes. All CT data, regardless of source, were analy-
sed on 64-bit PC workstations with 4 GB of RAM and
Intel HD Graphics video card and running Microsoft
Windows 7.
To directly examine the internal structures of plates
and spikes, thin sections and ⁄ or sections were made
based on the methodology outlined in Chinsamy and
Raath (1992) and Sander (2000). Because this is a
destructive method, all specimens were first photo-
graphed, had their morphological variations recorded,
and standard measurements taken before sectioning. In
addition, the juvenile plate was moulded and cast before
sectioning. Thin sections, except for a juvenile plate
(DMNH 33359) and fragmentary plates (HMNS 14 and
UMNH-VP 13688), were taken at standardized locations
for each element. The thin sections were taken at the
base, middle and apex because the histology of the plate
varies from the base to the apex (de Buffrenil et al.
1986). This study uses the terms ‘base’ for the most
proximal region of an osteoderm and ‘apex’ for the most
distal part (or apical region) of an osteoderm. ‘Middle’ is
used for the mid-region between the base and apex. After
cutting, both sides of the slice were impregnated with a
synthetic epoxy resin (Petropoxy 154; Maruto Co, Japan),
finely ground and polished to a high gloss. Entire images
of the thin sections were photographed with a digital
film scanner (Canon Pixus Mp 800). Furthermore, the
thin sections were observed by two standard light micro-
scopes (normal transmitted light and transmitted polar-
ized light) with a Leica DMLP and Nikon Optiphot2-pol
microscopes. Microscopic photographs were taken with a
Nikon Coolpix 5000 and Olympus C-5050 Zoom.
Nomenclature and definitions of bone microstructures
are based on Francillon-Vieillot et al. (1990) and Casta-
net et al. (1993).
Determination of ontogenetic stages. The determination of
ontogenetic stages was based on the cortical histology of
body elements as previously discussed by Hayashi et al.
(2009) and Redelstorff and Sander (2009). The results of
Hayashi et al. (2009) and Redelstorff and Sander (2009)
are mostly consistent. Each ontogenetic stage in Hayashi
et al. (2009) is characterized by the following features:
(1) juvenile – a fibro-lamellar tissue with a radial and ⁄ or
reticular vascular network; (2) subadult – fibro-lamellar
tissue with a longitudinal vascular network; (3) young
adult – with lines of arrested growth (LAGs), and (4)
old adult – with an external fundamental system (EFS),
which is tightly packed growth lines that develop
throughout the skeleton as full adult size is attained (Er-
ickson 2005; Erickson et al. 2007). Ontogenetic stages of
most specimens in this study were previously identified
by Hayashi et al. (2009), who classified them into a
juvenile (DMNH 33359), a young adult (NSM-PV
20380) and old adults (DMNH 1483, 2818, UMNH-VP
13693 and YPM 1856). In addition, thin sections were
taken from the femur mid-shaft of YPM 4634 and a rib
mid-shaft for HMNS 14 to determine their ontogenetic
stage. Based on Hayashi et al. (2009), these were deter-
mined to be a subadult (YPM 4634) and an old adult
(HMNS 14).
RESULTS
We start our discussion of the osteoderm histology of
Stegosaurus armatus and Stegosaurus sp. with the descrip-
tion of samples of DMNH 33359, 1483, 2818, NSM-PV
20380, YPM 1853, 4634 and UMNH-VP 13688. Hespero-
saurus (or Stegosaurus) mjosi (HMNS 14) will be dis-
cussed later because it is possibly a different genus (see
Carpenter et al. 2001; Carpenter 2010).
Stegosaurus armatus and Stegosaurus sp.
Plate. Seven plates from a juvenile (DMNH 33359), a
young adult (NSM-PV 20380) and four old adult individ-
uals (DMNH 1483, 2818, UMNH-VP 13688 and YPM
1853) were examined. Each ontogenetic character in his-
tology is described here.
Juvenile. A plate was examined from a juvenile individual
(DMNH 33359), which is the smallest dorsal plate known
to us. The specimen was examined using the medical CT
scanner and thin section. The plate shows the general
plate morphology of Stegosaurus (e.g. Gilmore 1914),
which is transversely flat (Fig. 1A). The surface is uni-
formly flat with some large vascular grooves and pits. The
base is covered in rugosities and pits.
H A Y A S H I E T A L . : P L A T E A N D S P I K E G R O W T H O F S T E G O S A U R U S 3
The CT images and thin section show that the internal
structure consists of only thin cortex and thick cancellous
bone (Fig. 1B–C). The plate lacks ‘pipe-like extensive
large canals’ previously reported in the basal regions of
other plates (de Buffrenil et al. 1986; Main et al. 2005;
Farlow et al. 2010). However, the basal region shows a
more cancellous structure than those of other regions
(Fig. 1B–C). In particularly, the trabeculae are thin and
the cavities between the thin trabeculae are relatively large
in the region where one would expect to find pipe-like
canals in older individuals. The pits on the external sur-
face invade the inside of the plate through nutrient
foramina and connect pores between trabeculae.
The cortical bone consists of well-vascularized tissue
composed of dense ossified collagen fibres (Fig. 1D–G).
Previously, many studies of extant and fossil tetrapods
have suggested that many osteoderms form through
metaplastic ossification, a process in which a pre-existing
fully developed tissue is transformed into bone (Haines
and Mohuiddin 1968). Metaplastic tissue in fossils has
been identified in osteoderms by the presence of interwo-
ven bundles of mineralized collagen fibres (Scheyer and
Sander 2004, 2007; Main et al. 2005; Witzmann and
Soler-Gijon 2008; Scheyer 2009; Cerda and Desojo 2010;
Cerda and Powell 2010). Therefore, we refer to the pri-
mary cortical bone of the juvenile plate as metaplastic
bone. Radial and ⁄ or reticular vascular canals are present
in the cortex (Fig. 1D–G). Many simple primary vascular
canals without surrounding bone lamellae are seen, but
primary osteons are rare in the cortex. There are numer-
ous large osteocyte lacunae, and the outermost vascular
canals open to the surface. Secondary bone tissue is very
rare in the cortex. There are no lines of arrested growth
(LAGs). The cancellous bone comprises mostly primary
bone tissue with many large resorption cavities (Fig. 1E–
G). The resorption cavities exhibit scalloped surfaces and
many Howship’s lacunae, indicating osteoclast activity in
this region (see also Fig. 2L). The primary bone tissue
shows simple primary vascular canals and some primary
osteons embedded in a bone tissue consisting of mineral-
ized collagen fibres. Secondary reconstructions are present
in the cancellous region, but are still not extensively
developed. There is no histological variation from the
base to the apex of the plate except for the orientation
and size of the mineralized collagen fibres. While they are
short and mainly perpendicular to the bone surface in
A
C
B D
E
F
G
F IG . 1 . A plate of a juvenile Stegosaurus (DMNH 33359). A, photograph in lateral view. A plane of sectioning is marked by a dashed
line. B, vertical thin section. C, detail of the basal bone tissue. Note absence of pipe-like large vascular canals in this plate. D–G,
cortical bone tissue of the plate. D–E, detail of the cortex and inner trabecular bone at the apical regions of the plate in normal (D)
and polarized (E) light. F–G, detail of the cortex and inner trabecular bone at the basal regions of the plate in normal (F) and
polarized (G) light. The bone tissues, both in cortical and in cancellous bone, consist of well-vascularized tissue composed of dense
ossified collagen fibres with radial and ⁄ or reticular vascularity. Notably, there are many large resorption cavities in the cancellous
bone. There are no LAGs. Bone surface is to the left and right in D–E and is to the right in F–G.
4 P A L A E O N T O L O G Y
most places, in the middle and basal regions, there are
large fibre bundles (Sharpey’s fibre in de Buffrenil et al.
1986). These are also directed at high angles to the bone
surface and apparently act as an anchor on the plate in
the skin (de Buffrenil et al. 1986; Scheyer and Sander
2004).
A
F I
G J L
H K
B
C
D
E
F IG . 2 . Young adult plate (NSM-PV 20380). A, photograph of a plate in lateral view. B–E, transverse thin sections of the plate. The
internal structure is composed of thin cortex and thick cancellous bone. Note presence of pipe-like large vascular canals in the base
(E). The sectioning is marked by dashed lines in A. F–L, Cortical bone tissue of the plate. F–G, detail of the cortex and inner
trabecular bone at the apical regions of the plate in normal (F) and polarized (G) light. H, detailed view of the matrix of cortical bone
in figure G in polarized light. Notably, the matrix consists of many ossified fibres. I–J, detailed view of the cortex and inner trabecular
bone at the basal regions of the plate in normal (I) and polarized (J) light. Cortical histology of young adult plates still retains many
primary bone tissues without secondary reconstructions. Many large resorption cavities are present in the cancellous bone. K, detailed
view of the cortical bone at the basal side in normal light. There are many large fibre bundles that apparently served to anchor the
plate in the skin. L, detailed view of the resorption cavities of K in polarized light. There are many Howship’s lacunae, indicating
osteoclast activity. Bone surface is to the left in F–G and is to the top in H–L.
H A Y A S H I E T A L . : P L A T E A N D S P I K E G R O W T H O F S T E G O S A U R U S 5
Young adult. Two different-sized plates (a large dorsal
plate situated above the pelvis and a small plate from the
distal caudal region) were sectioned from a skeleton
(NSM-PV 20380). The external surfaces are characterized
by large vascular grooves, pits, frayed texture at the apex
and rugose roughing bone with multiple pits at the base
(Fig. 2A).
Despite their gross size differences, the CT images and
thin sections show no obvious variations in internal
structure between plates. The plates show typical plate
structures, which were previously reported (de Buffrenil
et al. 1986; Main et al. 2005; Farlow et al. 2010). These
are composed of thin cortex and thick cancellous bone,
but significantly differ from a juvenile plate (DMNH
33359) in the presence of large, extensive, pipe-like canals
in the cancellous bone (Figs 2E, 5). These large canals
have previously been interpreted as vascular canals based
on the similarity of vascular canals in living alligator os-
teoderms (Seidel 1979; Farlow et al. 2010). Most of the
thin sections show that these canals outlined by trabecu-
lae pinch out in the middle region as previously reported
in Main et al. (2005). However, a thin section and 3D
analyses using a high-resolution CT scanner show that
the vascular canals connect to the vascular grooves of the
external surface, making extensive vascular networks
(Fig. 3A, B; see also Farlow et al. 2010). The large vascu-
lar canals invade the inside of the plate through pits of
the basal region and connect with the external vascular
grooves through a small number of pits of the middle
region (Fig. 3A).
These cortical bone tissues show well-vascularized bone
that consists almost entirely of coarse fibres oriented in
many directions, suggesting metaplastic bone (Fig. 2F–K).
Histological variations are present in the vascular canal’s
shape and in the degree of remodelling between a large
dorsal plate and small caudal plate. The large dorsal plate
exhibits more reticular vascular canals and less remodel-
ling than those of the small caudal plate. The simple
vascular canals and ⁄ or primary osteons grade into large
resorption cavities from the cortex to cancellous bone.
LAGs are absent. Many osteocyte lacunae are present in
the matrix and are aligned with fibre bundles. Most of
the vascular canals are simple canals, but some primary
osteons are present. The outermost vascular canals are
still open to the surface. Notably, their cortical bone tis-
sues differ from a juvenile plate (DMNH 33359) in show-
ing variations in the vascular canal shape in a single plate
(Fig. 2F, I). In the basal region of plates, vascular canals
A B
F IG . 3 . A, Pattern of inferred pipe-like extensive vascular network in a plate from NSM-PV 20380, a young adult individual of
Stegosaurus armatus. The digital images were created by microfocus CT scanning, with the pipe-like vascular canals, and spaces within
cancellous bone, indicated in black. The sequence of images begins near the sagittal interior, and successive images are progressively
closer to the plate surface, ending with a view of the surface itself. The arrangement of isolated black spaces in the cancellous bone
with respect to the pipes suggests that at least some of the isolated black spaces represent sections through small tributary blood
vessels. The box contains an enlarged image of a portion of the plate surface, showing that some of the internal vascular canals
connect with vascular grooves and foramina on the plate surface. Such connections between interior and surface features of the
inferred vascular system occur on both sides of this plate. B, Portion of Stegosaurus armatus dorsal plate of YPM 1856, showing an
internal pipe-like large vascular canal connecting with a superficial vascular groove.
6 P A L A E O N T O L O G Y
show a reticular configuration at the inner cortex, but
they change to the longitudinal arrangement at the outer-
most cortex (Fig. 2I–J). In apical regions, most of the vas-
cular canals exhibit a longitudinal arrangement (Fig. 2F–
G). Remodelling occurs at the deepest part of the cortical
bone, although not extensively. Also, the degree of
remodelling in the cancellous bone is different in the sin-
gle plates. While secondary reconstructions are extensively
developed at the middle and upper regions, they are seen
in only a few regions at the basal region. Particularly,
there are many large resorption cavities in the cancellous
bone. Howship’s lacunae are seen in many resorption cav-
ities (Fig. 2L). Numerous osteocyte cell lacunae, which
are aligned with fibre bundles, are present in the cancel-
lous bone matrix. Remodelling is not extensive in the
cancellous bone. Large fibre bundles, known as Sharpey’s
fibres, act as anchors between the plate and skin (de Buff-
renil et al. 1986); these are extensively developed in the
basal to middle region of the plates (Fig. 2J–K). The large
fibre bundles are present in cortical regions, but are lack-
ing in the inner cancellous bone.
Old adult. Four plates were sampled from four individu-
als (DMNH 1483, 2818, YPM 1853 and UMNH-VP
13688). Two isolated plates (YPM 1853 and UMNH-VP
13688) show the multiple growth marks and extensive
remodelling seen in the old adult specimens of this study
and were therefore classified as potentially old adult indi-
viduals. All specimens were examined using thin sections.
One plate (DMNH 1483) was examined using the helical
medical CT scanner as well.
The external surfaces of all plates exhibit similar fea-
tures with other ontogenetic plates, which are large vascu-
lar grooves, pits, a frayed texture at the tip, and rough,
rugose bone with multiple pits at the base. The CT
images and thin sections show that all plates consist of
thin cortex and thick cancellous bone with large pipe-like
vascular canals (Fig. 4B–D). Large vascular canals are
connected to grooves on the external surface and make
extensive vascular networks (Fig. 3B, 5). Cortical thick-
nesses increase from those of young adult (NSM-PV
20380) and juvenile plates (DMNH 33359), but are dis-
tinctly thinner than those of spikes. Cortical bone tissue,
from all plates, consists of almost entirely, coarsely ossi-
fied, collagen fibres, except where it has been replaced in
the cortex by secondary osteons (Fig. 4F). The cancellous
bone in all plates shows extensive remodelling. Notably,
some histological variations in cortical bones are present
among old adult plates.
The cortical bone tissue of a caudal plate from the larg-
est adult individual (DMNH 2818) comprises dense min-
eralized fibres with longitudinal simple vascular canals,
few LAGs and well-developed large collagen fibre bundles
in the basal region. Some primary osteons are seen in the
cortex, but simple vascular canals dominate in this sam-
ple. Secondary reconstructions occur in the inner cortex
and cancellous region (Fig. 4E–F).
A thin section from a large plate fragment from the
middle or apical region (UMNH VP13688) was previ-
ously described as UDSH C-LQ 085 by Reid (1990). The
cortex consists of dense ossified collagen fibres. Multiple
LAGs with decreasing spacing towards the outer surface
are also seen. Notably, the peripheral bone tissue com-
prises a zone of mostly avascular tissue with tightly
packed LAGs, which is known as an external fundamental
system (EFS) in the ossified tendons and long bones of
dinosaurs (e.g. Adams and Organs 2005; Sander et al.
2006). The simple longitudinal vascular canals dominate
in the cortex (Fig. 4G). Remodelling is moderately devel-
oped at the perimedullary to the middle cortex.
The histology of another isolated plate (YPM 1856)
was described by de Buffrenil et al. (1986). The cortex
histology varies from the base to apex of the plate. In the
basal region, the histology consists of dense ossified colla-
gen fibres with strong remodelling towards the interior of
the plate, whereas in the middle region, remodelling is
more extensive towards the basal and apical parts. The
apical region has a similar histology to UMNH VP13688,
that is, bone tissue consisting of dense mineralized colla-
gen fibre bundles with many LAGs.
The cortical bone tissue of a caudal plate (DMNH
1483) is characterized by strong remodelling (Fig. 4H, I).
The tissues are completely or almost completely replaced
by secondary osteons, sometimes by three or fourth gen-
erations from the basal and apical parts of the plate. Sec-
ondary osteons can be seen crosscutting each other. Some
Sharpey’s fibres are present in the outermost cortex, but
most of the fibres are eliminated by secondary reconstruc-
tions. Due to the strong remodelling, it was impossible to
detect the original tissue.
Spike
Six spikes from a subadult (YPM 4634), a young adult
(NSM-PV 20380), and two old adult individuals (DMNH
1483 and 2818) were examined. Each ontogenetic charac-
ter in histology was described here.
Subadult. Two fore spikes were examined from a suba-
dult individual (YPM 4634). All specimens were exam-
ined using the medical CT scanner and sections.
Unfortunately, the cortical bone tissues could not be
observed in this study because thin sections could not be
taken from YPM 4634. The spikes from a subadult indi-
vidual (YPM 4634), previously described by Galton
(1982), were examined for this study. These spikes have
sharp, compressed, anterior and posterior margins with
H A Y A S H I E T A L . : P L A T E A N D S P I K E G R O W T H O F S T E G O S A U R U S 7
A
B
C
D
E G H
F I
B
C
D
F IG . 4 . Sections of old adult Stegosaurs plates (YPM 1856, DMNH 2818, UMNH-VP 13688 and DMNH 1483). A, sketch of YPM
1856 plate in lateral view (modified from de Buffrenil et al. 1986). B–D, sections of A. B, section of the apical part. C, section of the
middle part. D, section of the basal part. Pipe-like large vascular canals are seen from the basal to middle part (C, D). The sectioning
is marked by dashed lines in A. E–I, cortical bone tissue of plates (DMNH 2818, UMNH-VP 13688 and DMNH 1483). E, detail of the
cortex of a plate from Stegosaurus armatus (DMNH 2818) in normal light. F, detail of the matrix of cortical bone in figure E in
polarized light. Notably, the bone tissue consists of many ossified fibres. G, detail of the cortex of a plate from Stegosaurus sp.
(UMNH-VP 13688) in polarized light. H–I, detail of the cortex of a plate from Stegosaurus armatus (DMNH 1483) at the middle part
(H) and the basal part (I) in polarized light. The cortical bone tissue of a caudal plate (DMNH 1483) is characterized by strong
remodelling. Bone histologies of old adult plates are characterized by extensive remodelling, multiple LAGs, and EFS. Bone surface is
to the top in E–G and is to the right in H–I.
8 P A L A E O N T O L O G Y
asymmetrical bases (Fig. 6A). Vascular grooves are present
on the external surface of the distal part but are absent
elsewhere. The base is pierced by large pits and lacks the
rugose roughening structure seen in old adult spikes.
The CT images and sections of the spikes show cancel-
lous internal structures similar to a spike examined in a
previous study (de Buffrenil et al. 1986) and are com-
posed of thin cortex with thick cancellous bone (Fig. 6B,
C). Spikes show small canals at the middle of the shaft,
but lack a large axial channel within the core of the can-
cellous bone (sensu Acharjyo and Bubenik 1983; a large
medullary cavity in McWhinney et al. 2001), and also lack
the thick cortical bone previously reported in other spikes
(McWhinney et al. 2001). The small canals of the mid-
shaft change into cancellous bone at the proximal and
distal regions. They connect pits and apical grooves on
the external surface, although these do not make extensive
networks such as those of adult plates.
Young adult. A fore spike and a hind spike were sampled
from a young adult individual (NSM-PV 20380). The
external morphology of young adult spikes is similar to
that of subadult spikes (YPM 4634): oblique bases with
large pits; few vascular grooves; and sharp, compressed,
anterior and posterior margins (Fig. 7A). The basal mor-
phology of the fore spikes shows a blunter angle than that
of the hind spikes. The young adult spikes show cancel-
lous internal structures like those of the subadult spikes
(YPM 4634). These are composed of a thin cortical bone
and a thick cancellous bone (Fig. 7B–E). The small canals
occur in a hind spike, but are absent in a fore spike.
Histologically, spike cortical bone tissues are similar to
those of a small caudal plate. They exhibit metaplastic bone
composed of dense ossified collagen fibres with a combina-
tion of both radial and reticular vascularity at the basal side
(Fig. 7J–M) and longitudinal vascularity at the apical side
(Fig. 7H–I). The fibres are distributed throughout the
whole spike (Fig. 7F–G). Large fibre bundles (Sharpey’s
fibre in de Buffrenil et al. 1986) are present in the mid- to
basal regions (Fig. 7M). These are directed at high angles to
the bone surface and apparently served to anchor the spikes
in the skin. LAGs do not occur in the cortex. Secondary
reconstruction is not extensive throughout the cortex, but
is extensive in cancellous bone. Osteocytes are aligned with
fibre bundles, which are abundant in the cortex.
Old adult. Two hind spikes were observed from two adult
individuals (DMNH 1483 and DMNH 2818). The exter-
nal morphology of old adult spikes is characterized by
having a more conical shape than those of younger indi-
viduals (Fig. 8A–E). A few pits, and large, longitudinal,
vascular grooves mark the external surfaces.
A
A B A B
A B
A B
A BA B
B
F IG . 5 . Comparison of internal structures of Stegosaurs plates in different ontogenetic stages (DMNH 33359, NSM-PV 20380 and
DMNH 1483). Pipe-like extensive large vascular networks are present from the young adult (NSM-PV 20380) to the old adult
(DMNH 1483). A, vertical cross sections. B, parasagittal cross sections. Black dashed lines indicate cutting planes. Upper row of the
figure, CT images. Lower row of the table, interpretative drawing of large vascular canals in plates. Vascular canals, which connect
with foramina and ⁄ or grooves on the plate surface, indicated by black in the drawings. Indeterminate features, either vascular canals
or cracks, indicated by dashed lines. Broken parts in plates indicated by diagonal lines. Subadult plate was not examined in this study.
H A Y A S H I E T A L . : P L A T E A N D S P I K E G R O W T H O F S T E G O S A U R U S 9
All sampled spikes are similar in having thick cortical
bone with a large axial channel (Fig. 8C–E), but distinctly
differ from those of subadult and young adult spikes
(YPM 4634 and NSM-PV 20380) in the absence of thick
cancellous bone. The cancellous bone is more compact
than that of younger spikes because trabeculae are thicker
and the resorption cavities are smaller than those of suba-
dult and young adult spikes (Fig. 8C–E). CT analysis of
spikes detected the presence of some large vascular canals
in the basal region. These canals invade through pits on
the basal surface and then connect with a large axial
channel and some external grooves. However, there are
no indications of pipe-like extensive vascular canals in the
spikes.
The histology of these spikes is identical to that of old
adult plates and is characterized by bone tissue consisting
of dense ossified collagen fibres with longitudinal simple
vascular canals, multiple LAGs and extensive remodelling
(Fig. 8F–I). Extensively developed large collagen fibre
bundles are seen in the basal region. Some primary ost-
eons are observed in the cortex, but simple vascular
canals dominate in these spikes. The cancellous bone is
completely remodelled.
Hesperosaurus (or Stegosaurus in Maidment et al. 2008)
mjosi
Three plates and two spikes were examined using a CT
scanner and a thin section from a holotype of Hespero-
saurus mjosi (HMNS 14; Fig. 9).
Plate. A small plate from the proximal cervical region, a
large plate situated above the dorsal region and a frag-
mentary sample from an apical region of a possible dor-
sal plate were examined. All plates were examined using
a CT scan, but only a fragmentary plate was observed
using thin sections. Plate morphologies differ between
Hesperosaurus (or Stegosaurus) mjosi (HMNS 14) and
Stegosaurus armatus (DMNH 1483, 2818 and YPM
1856). The plate length of Hesperosaurus (or S.) mjosi is
greater than the height, whereas the length of S. armatus
is less than the height (see more descriptions in Carpen-
ter et al. 2001). The external surfaces of these plates
show large vascular grooves, pits, a frayed texture at the
tip, and rough, rugose bone with multiple pits at the
base.
A
B
C
F IG . 6 . Spike section of a subadult
Stegosaurus (YPM 4634). The plane of
sectioning marked by a dashed line. A,
photograph of the fore spike in dorsal
view. B, the transverse section of spike
showing the cancellous internal
structure. C, interpretative drawing of B.
The cortex in the sections is very thin.
Dark grey indicates the regions covered
with resin.
10 P A L A E O N T O L O G Y
There are no obvious histological variations between
Hesperosaurus mjosi (HMNS 14) and Stegosaurus armatus
(DMNH 1483 and 2818), nor between the different sizes
of plates in a single specimen of Hesperosaurus (HMNS
14). All plates consist of thin compact bone and thick
cancellous bone. Extensive pipe-like large vascular canals
are present in all plates (Fig. 9D). The cortical bone his-
tology in a fragmentary plate shows metaplastic bone
A
B
C
D
E
B D
F
C
H
I
J M
F
G
K
L
E
F IG . 7 . Young adult Stegosaurs spike (NSM-PV 20380). A, photograph of a spike in dorsal view. B–E, transverse thin sections of the
spike. The internal structure is composed of thin cortex and thick cancellous bone without large vascular canals. The sectioning is
marked by dashed lines in A. F–M, cortical bone tissue of the spike. F, the cortex at the middle region (D) of the spike in polarized
light. G, detailed view of the matrix of cortical bone in figure F in polarized light. Notably, the matrix consists of many ossified fibres.
H, detail of the cortex at the apical regions of the spike in normal (H) and polarized (I) light. J–M, detailed view of the cortex at the
basal regions of the spike in normal (J, L) and polarized (K, M) light. Cortical histology of young adult spikes is similar with that of
the plate. Spike shows well-vascularized bone tissue consisting almost entirely of coarse fibres. Large fibre bundles are present at the
basal side (M). Bone surface is to the left in F and is the top in G–M. NA in E indicates reconstructed regions.
H A Y A S H I E T A L . : P L A T E A N D S P I K E G R O W T H O F S T E G O S A U R U S 11
consisting of dense ossified collagen fibres, with multiple
growth marks. EFS and few simple vascular canals are
present in the bone tissue (Fig. 9I–J). Remodelling is
extensively developed from the inner to mid-cortex. The
cancellous bone is completely remodelled. Sharpey’s fibres
are not seen in this section. This is possible because the
sample was taken from the apex region of a plate.
Spike. A fore spike and a hind spike were examined using
a CT scanner. Unfortunately, the histological features in
the cortical bones could not be observed because thin sec-
tions could not be taken from these specimens. The CT
images show that all spikes from Hesperosaurus mjosi
consists of a thick cortical bone with a large axial channel
(Fig. 9F–H). The cancellous bone has small cavities
between the trabeculae. These are proportionally small and
are seen in the basal and apex side. These results are con-
sistent with the old adult spikes of Stegosaurus armatus.
Summary of ontogenetic trends in the structure and
histology
Examination of osteoderms from different aged individu-
als of Stegosaurus shows ontogenetic trends in the struc-
ture and the histology through life history. The cortical
A
F H
G I
B C
D
D
E
C
E
F IG . 8 . Sections of old adult Stegosaurs
spikes (DMNH 1483 and 2818). A,
photograph of DMNH 1483 spike in
dorsal view. B, photograph of DMNH
2818 spike in dorsal view. C, E, sections
of A. D, a section of B. The sectioning is
marked by dashed lines in A and B. The
internal structure of the spikes of
DMNH 1483 and 2818 is distinctly
compact and shows a large axial channel
(D). F–I, cortical bone tissue of the
spikes. F–G, detailed view of the cortex
of a spike (DMNH 2818) in normal (F)
and polarized (G) light. H–I, detailed
view of the cortex of a spike (DMNH
1483) in normal (H) and polarized (I)
light. The cortical bone histology shows
multiple LAGs (F–G) and extensive
secondary reconstruction (H–I). Bone
surface is to the top in F–I.
12 P A L A E O N T O L O G Y
bone histology in both plates and spikes, throughout the
ontogeny, is comprised of dense ossified collagen fibres,
suggesting metaplastic bone. Histological features in each
ontogenetic stage are summarized in Table 2.
In the plate, the ontogenetic change from juvenile
(DMNH 33359) to young adult (NSM-PV 20380) is the
acquisition of the extensive pipe-like large vascular net-
works (Fig. 5). The cortical bone histology in the plate
shows a progressive increase in remodelling, a number of
LAGs, the eventual presence of an EFS and the type of
vascular canals through ontogeny. The juvenile plate
shows reticular vascular canals and only a little remodel-
ling in that cancellous bone. LAGs are absent. In the
young adult plates, vascularity is less extensive than in a
juvenile plate, and longitudinal vascularization dominates
the external cortex. LAGs are still absent. The old adult
plates show the development of LAGs throughout the
cortex, which consists of the metaplastic bone having lon-
gitudinal vascular canals. Spacing between LAGs dimin-
ishes towards the outer surface of the bone. Notably, old
plates are characterized by an EFS in the outermost cortex
and the extensive development of dense secondary tissue.
These tissues have tightly packed LAGs in a lamellar
and ⁄ or parallel fibre bone matrix, indicating attainment
of maximum size of the plate (e.g. Sander 2000; Adams
and Organ 2005; Erickson 2005).
The ontogenetic change of the spikes occurs in the
increasing thickness of cortical bone and trabeculae in the
cancellous bone, and acquisition of a large axial channel
from the young adult (NSM-PV 20380; Fig. 7) to old
A B
C
D
F
G
H
E
I J
F IG . 9 . A plate and spike from old
adult Hesperosaurus mjosi (HMNS 14).
A, photograph of a dorsal plate in lateral
view. B–D, transverse CT images of the
plate. Note presence of pipe-like large
vascular canals in the base (D). The
sectioning is marked by dashed lines in
A. E, photograph of an anterior spike in
dorsal view. F–H, transverse CT images
of the spike. The internal structure of
the spike shows a large axial channel (G,
H). The sectioning is marked by dashed
lines in E. I–J, cortical bone tissue of the
dorsal plate in normal (I) and polarized
(J) light. The cortical bone histology is
characterized by extensive remodelling
and EFS. Bone surface is to the top in
I–J.
H A Y A S H I E T A L . : P L A T E A N D S P I K E G R O W T H O F S T E G O S A U R U S 13
adult forms (DMNH 1483 and 2818; Fig. 8). The bone
tissue lacks LAGs in the young adult stage. In old adults,
the bone tissues exhibit multiple LAGs with extensive
remodelling, indicating a decrease in growth rate (e.g.
Sander 2000; Erickson et al. 2007). The vasculature
changes from reticular to longitudinal shape, and vascu-
larization decreases in old adult spikes.
Surprisingly, there are no histological differences in
plates and spikes between Stegosaurus armatus and
Hesperosaurus mjosi, despite differences in the external
morphology of the plates. Histological features of Hesp-
erosaurus osteoderms are identical with those of old adult
Stegosaurus armatus.
DISCUSSION AND CONCLUSIONS
We could not mention whether our growth series of
Stegosaurus represents a single species because three speci-
mens (DMNH 33359, YPM 4634 and UMNH-VP 13688)
could not be identified beyond the level of genus. Addi-
tionally, Hesperosaurus (Stegosaurus) mjosi specimens are
found at the same locality as specimens indentified as
Stegosaurus armatus (Maidment et al. 2008; Siber and
Mockli 2009). However, at least at the stage that is obser-
vable for Hesperosaurus, their histology of plates and
spikes are very similar with those of Stegosaurus armatus.
This might suggest that growth patterns do not vary very
much between these taxa. Therefore, our growth series
would capture important growth changes of Stegosaurus
osteoderms even if it consists of different species.
Development implication of Stegosaurus osteoderms
Previously, Main et al. (2005) suggested that the develop-
ment of Stegosaurus osteoderms may be mainly a meta-
plastic bone process because of the fibrous nature in
Stegosaurus plates. Our observations of the plates and
spikes we studied are largely concordant with their
results. All ontogenetic stages of Stegosaurus osteoderms
show a cortical bone tissue consisting of dense ossified
collagen fibres. Also, plates and spikes from juvenile and
young adult individuals show the bone tissue of dense
ossified fibres both in the cortical and in the cancellous
bone. These results suggest that the main developmental
formation of Stegosaurus osteoderms is metaplastic bone
process, and plates and spikes are mostly formed from
the direct mineralization of an existing dense connective
fibre network in their skin. Additionally, the cancellous
bone in plates and spikes from a juvenile and young adult
comprises many large resorption cavities. This suggests
that osteoclasts produce many resorption cavities in the
inner region of the plates and spikes and then finally
make the cancellous region.
Furthermore, de Buffrenil et al. (1986) proposed a
growth model of a Stegosaurus plate in which growth rate
differs in different regions of a single plate. The base of
the plate was where the highest rates of growth took
place, and because more secondary reworking took place
in the apical regions, the uppermost regions were progres-
sively older ontogenetically than the basal regions. How-
ever, bone continued to be deposited periosteally both on
the outer surfaces of the plate and at its base (de Buffrenil
et al. 1986). In cortical histology, plates and spikes from
our young adult and old adults show growth rate differ-
ences in different regions of a single plate, as in the plate
described by de Buffrenil et al. (1986). While the bases
are well vascularized and have less remodelled bone tissue
with radial or reticular vascular canals, the upper regions
have a more remodelled cortex with longitudinal vascular
canals. On the other hand, our juvenile specimen, which is
possibly less than 1 year old, based on the long bone histol-
TABLE 2 . Histological features of the Stegosaurus osteoderms through ontogeny.
Ontogenetic
stage
Specimen Structure
features of plate
Structure
features of spike
Cortical bone tissue
(plate and spike)
Remodelling
(plate and spike)
Juvenile DMNH 33359 Thin CO and
thick CB
NA Metaplastic bone
and reticular VC
Only a little remodelling
at cancellous bone
Subadult YPM 4634 NA Thin CO and thick CB NA NA
Young adult NSM-PV 20380 Thin CO, thick
CB and Pipes
Thin CO and thick CB Metaplastic bone
Longitudinal and
reticular VC
Remodelling only in
perimedullary region.
Old adult DMNH 1483, 2818,
HMNS 14, YPM
1856 and
UMNH-VP 13688
Thin CO, thick
CB and Pipes
Thick CO, thin CB
and an large axial
channel
Metaplastic bone
LAGs, EFS and
longitudinal VC
Remodelling from
perimedullary region
to mid-cortex or
throughout cortex
The histological features of Stegosaurus osteoderms sampled include structures, cortical bone tissue type, shape of vascularization and
degree of secondary reconstruction. CB, cancellous bone; CO, compact bone; NA, not available; Pipes, pipe-like large vascular canals;
VC, vascular canal.
14 P A L A E O N T O L O G Y
ogy (see Hayashi et al. 2009), shows no indication of
growth rate difference in the plate. Therefore, our results
suggest that Stegosaurus plates and spikes grew constantly
in all regions of a single plate and spike during an early
ontogenetic stage, after which the basal region continued to
show a fast growth rate, accompanied by a decline in the
growth rate in the upper region. This differential growth
may reflect positive allometric growth of the plates.
Histological variations are present among a single indi-
vidual’s dorsal large plate, caudal small plate and spikes
(NSM-PV 20380). The large dorsal plate exhibits more
reticular vascular canals and less remodelling than those of
the small caudal plate and spikes. Generally, the growth
rate of reticular vascular canals is relatively higher than that
of longitudinal vascular canals in living animals and other
dinosaurs (e.g. Castanet et al. 2000; Sander 2000). There-
fore, this result probably suggests that the relative growth
rate of dorsal large plates is higher than small plates and
spikes. This differential growth may reflect the size differ-
ences of plates in a single individual of Stegosaurus.
Functional implication for Stegosaurus plates and spikes
The plates and spikes we examined show different timing
of development of structural features seen in old adults.
While plates acquire pipe-like large canals in the young
adult, spikes acquire a thick cortex with a large axial
channel in old adults. These results may suggest that the
acquisition timing for the respective functions of the
plates and spikes might be different.
The extensive pipe-like large canals in plates are likely
large vascular canals because of the connectivity with
nutrient foramina and vascular grooves on the plate sur-
face and the structural similarity of large vascular canals
of living alligator osteoderms (detailed discussion in Far-
low et al. 2010). Main et al. (2005) reported that the
pipe-like large vascular canals are not connected with the
outside of the plate. However, our observations on the
pipe-like vascular canals using a high-resolution CT scan
and thin sections revealed that these vascular canals are
apparently connected with the outside of the plate and
make extensive vascular networks (see also Farlow et al.
2010). Because of the complexity in the network of pipe-
like vascular canals, the networks might not have been
detected in the previous study. The large pipe-like vascu-
lar canals of plates might facilitate the creation of large
plates because a large amount of nourishment from these
vascular canals makes a high growth rate possible. Similar
vascularization is seen in antlers of extant deer, permit-
ting high growth rates (Goss 1983). Having large plates
would be useful for enhancing the size of the animal
towards rivals and ⁄ or mates as suggested by Carpenter
(1998). This hypothesis is also supported by the cortical
histologies of plates, which show that relatively fast
growth rates continue long after sexual maturity is
reached (Hayashi et al. 2009). The extensive pipe-like vas-
cular networks are acquired when the large body size of
Stegosaurus is attained (see also Farlow et al. 2010).
Therefore, in addition, the acquisition of the extensive
vascular networks in the young adult might allow plates
to have a secondary thermoregulatory function like that
of the extant Toucan bill (Tattersall et al. 2009), elephant
ears (Phillips and Heath 1992) and possibly alligator os-
teoderms (Farlow et al. 2010). Hence, it is probable that
plates may acquire a display and ⁄ or possible thermo-
regulation function in the young adult form.
The acquisition of thick cortical bone in old adult
spikes probably strengthens the osteoderms. This suggests
that spikes might be used as weapons for defence, but not
until late in ontogeny. Ontogeny may also explain the
apparent contradiction between previous studies (de Buff-
renil et al. 1986 vs. McWhinney et al. 2001 and Carpenter
et al. 2005). Spikes retain small canals in the mid-shaft in
the subadult form, which become a large axial channel.
This developmental process is also seen in some living
tropical deer antlers (Acharjyo and Bubenik 1983). The
enlarged axial channel might provide more nutrients for
spikes enabling them to become larger, similar to the
function of the pipe-like extensive vascular networks in
plates. Bone tissue in both plates and spikes show well-
vascularized bone tissue consisting of dense mineralized
fibres in a young adult. In old adult forms, the bone tis-
sues in the spikes become more compact and are exten-
sively remodelled. Also, they are less vascularized. This
might contribute to structural reinforcement of the
spikes. On the other hand, the plates in old adults also
show extensive remodelling and LAGs, but only limited
signs of compaction.
Soft tissue implication of Stegosaurus osteoderms
Plates and spikes of Stegosaurus and Hesperosaurus show
prominent vascular grooves and obliquely oriented vascu-
lar foramina on bone surfaces (e.g. Fig. 3). Most of speci-
mens also show basal sulcus that describes a saddle-
shaped curve at the base (e.g. Figs 1, 9; see also Main
et al. 2005, fig. 3). Their cortical bone tissues are charac-
terized by dense concentrations of metaplastically ossified
fibres. These features are similar with those of ceratopsian
horns (Hieronymus et al. 2009) and, based on an integu-
ment study of living animals (Hieronymus et al. 2009),
may suggest that plates and spikes were covered by a ker-
atinous sheath. Main et al. (2005) and Christansen and
Tschopp (2010) have also suggested that plates were cov-
ered in keratin. Particularly, Christansen and Tschopp
(2010) noted that they found what was possibly keratin
H A Y A S H I E T A L . : P L A T E A N D S P I K E G R O W T H O F S T E G O S A U R U S 15
on a plate. The external and internal vascular canals in
plates and spikes probably contribute to the production
of the keratin sheath.
Acknowledgements. This paper is a portion of the PhD disserta-
tion of the first author (S. Hayashi), who would like to acknowl-
edge his supervisors, namely Y. Kobayashi (Hokkaido University
Museum, Sapporo, Japan), M. Manabe (National Science
Museum, Tokyo, Japan), P. M. Sander (Institut fur Palaontogie,
Universitat Bonn, Bonn, Germany), K. Endo (Nihon University,
Tokyo, Japan) and D. Suzuki (Sapporo Medical University, Hok-
kaido, Japan) for their guidance during this research. We are
grateful to D. Brinkman, W. Joyce and M. Fox (Yale Peabody
Museum, Yale University, New Haven, CT, USA), S. Suzuki and
S. Ishigaki (Hayashibara Natural History Museum, Okayama,
Japan), K. Siber and his staff (Sauriermuseum Aathal, Switzer-
land), M. Getty and S. Sampson (Utah Museum of Natural
History, Salt Lake City, UT, USA), M. Carrano and M. Brett-
Surman (United States National Museum, Washington, DC,
USA) for access to materials in their care and for information
regarding many of the specimens. B. Small, A. Ryan (Denver
Museum of Nature and Science) and B. Ryan (Comcast Com-
pany, Denver, CO, USA) for support in this study. We also wish
to thank M. Okumura (Hokkaido University, Sapporo, Japan)
and T. Takemura (Nihon University, Tokyo, Japan) for permis-
sion to CT-scan the Stegosaurus plates and spikes. The manu-
script benefited greatly from the comments and suggestions of P.
Galton (University of Bridgeport, Bridgeport, CT, USA), K. Stein
and J. Mitchell (Institut fur Palaontogie, Universitat Bonn,
Bonn, Germany) who kindly reviewed earlier versions of the
manuscript. We acknowledge the helpful reviewers by K. Angi-
elczyk (Field Museum of Chicago, Chicago, IL, USA), J. O. Far-
low (Indian-Purde University, Fort Wayne, IN, USA) and S.
Werning (University of California, Berkeley, CA, USA). This
research was funded by JSPS (the Japan Society for the Promo-
tion of Science) the DAAD (German Academic Exchange Ser-
vice) and the Jurassic Foundation.
Editor. Kenneth Angielczyk
REFERENCES
A C H A R J Y O , N. L. and B UB E N I K, B. A. 1983. The struc-
tural peculiarities of antler bone in genera Axis, Rusa and
Rucervus. 195–209. In B R O W N , D. R. (ed.). The antler devel-
opment in cervidae. Caesar Kleberg Wildlife Research Institute,
Kingsville, Texas, 480 pp.
A D A M S , J. and O R G A N , C. L. 2005. Histologic determination
of ontogenetic patterns and processes in hadrosaurian ossified
tendons. Journal of Vertebrate Paleontology, 25, 614–622.
B U F F R E N I L , V. de., F A R L O W , J. O. and R I C Q L E S , A.
de. 1986. Growth and function of Stegosaurus plates: evidence
from bone histology. Paleobiology, 12, 459–473.
C A R PE N TE R , K. 1998. Armor of Stegosaurus stenops, and the
taphonomic history of a new specimen from Garden Park,
Colorado. Modern Geology, 23, 127–144.
—— 2010. Species concept in North American stegosaurs. Swiss
Journal of Geosciences, 103, 155–162.
—— M I L E S , A. C. and C L OW A R D, K. 2001. New primitive
stegosaur from the Morrison Formation, Wyoming. 55–75. In
CA R P E N T E R , K. (ed.). The armored dinosaurs. Indiana
University Press, Bloomington, 526 pp.
—— S A N DE R S , F., M C W H I N N E Y , L. A. and W OO D , L.
2005. Evidence for predatory-prey relationships. Examples for
Allosaurus and Stegosaurus. 325–350. In C A R P E N T E R , K.
(ed.). The carnivorous dinosaurs. Indiana University Press,
Bloomington, 371 pp.
C A S T A N E T , J., F R A N C I L L O N - V I E I L L O T , H., M E U -
N I E R , F. J. and R I CQ L E S , A. de. 1993. Bone and individ-
ual aging. 245–283. In HA L L , B. K. (ed.). Bone, Vol. 7. Bone
growth – B. CRC Press, Boca Raton, 368 pp.
—— R O G E R S , K. C., C UB O , J. and B OI S A R D, J. J. 2000.
Periosteal bone growth rates in extant ratites (ostriche and
emu). Implications for assessing growth in dinosaurs. Comptes
Rendus de l’Academie des Sciences – Series III, 323, 543–550.
C E R DA , I. A. and D E S O J O , J. B. 2010. Dermal armour his-
tology of aetosaurs (Archosauria: Pseudosuchia), from the
Upper Triassic of Argentina and Brazil. Lethaia, 44, 416–428.
—— and P OW E L L , J. E. 2010. Dermal armor histology of
Saltasaurus loricatus, an Upper Cretaceous sauropod dinosaur
from Northwest Argentina. Acta Palaeontologica Polonica, 55,
389–398.
C HI N S A M Y , A. and R A A T H , M. A. 1992. Preparation of
fossil bone for histological examination. Palaeontologia Afri-
cana, 29, 39–44.
C HR I S T A N S E N , A. N. and T S C H OP P , E. 2010. Excep-
tional stegosaur integument impressions from the Upper
Jurassic Morrison Formation of Wyoming. Swiss Journal of
Geosciences, 103, 163–171.
E R I C K S ON , G. M. 2005. Assessing dinosaur growth patterns:
a microscopic revolution. Trends in Ecology and Evolution, 20,
677–684.
—— CU R R Y , K. A., V A R R I CH I O , D. J., N OR E L L , M. A.
and X U , X. 2007. Growth patterns in brooding dinosaurs
reveal the timing of sexual maturity in non-avian dinosaurs
and genesis of the avian condition. Biology Letters, 3, 558–561.
F A R L O W , J. O., T H OM PS O N , C. V. and R OS N E R , D. E.
1976. Plates of Stegosaurus: forced convection heat loss fins?
Science, 192, 1123–1125.
—— H A Y A S H I , S. and T A TT E R S A LL , G. 2010. Internal
vascularity of the dermal plates of Stegosaurus (Ornithischia:
Thyreophora). Swiss Journal of Geosciences, 103, 173–185.
F R A N C I L L O N - V I E I L LO T , H., D E BU F F RE N I L , V.,
CA S TA N E T, J., G E R A UD I E , J. F., M E U N I E R , J., S I R E ,
J. Y., Z Y L B E R BE RG , L. and R I C QL E S , A. de. 1990.
Microstructure and mineralization of vertebrate skeletal tis-
sues. 471–530. In C A R T E R , J. G. (ed.). Skeletal biomineral-
ization: patterns, processes and evolutionary trends, Vol. 1. Van
Nostrand Reinhold, New York, 832 pp.
G A L T ON , P. M. 1982. Juveniles of the stegosaurian dinosaur
Stegosaurus from the Upper Jurassic of North America. Journal
of Vertebrate Paleontology, 2, 47–62.
G I L M OR E , C. W. 1914. Osteology of the armored Dinosauria
in the United States National Museum, with special reference
16 P A L A E O N T O L O G Y
to the genus Stegosaurus. United States National Museum Bul-
letin, 89, 1–143.
G O S S , R. J. 1983. Developmental anatomy of antlers. 133–171.
In G OS S , R. J. (ed.). Deer antlers: regeneration, function, and
evolution. Academic Press, New York, 316 pp.
H A I N E S , R. W. and M O HU I D DI N , A. 1968. Metaplastic
bone. Journal of Anatomy, 103, 527–538.
H A Y A S HI , S., C A R PE N T E R , K. and S UZ U KI , D. 2009.
Different growth patterns between the skeleton and osteoderm
of Stegosaurus (Ornithischia: Thyreophora). Journal of Verte-
brate Paleontology, 29, 123–131.
H I E R O N Y M US , L. T., W I T M E R, M. L., T A N K E , H. D.
and C UR R I E , J. P. 2009. The facial integument of centrosau-
rine ceratopsids: morphological and histological correlates
of novel skin structures. The Anatomical Record, 292, 1370–
1396.
L U L L , R. S. 1910. The armor of Stegosaurus. American Journal
of Science, 29, 201–210.
M A I D M E N T , S. C. R., N O R M A N , D. B., B A R R E T T , P.
M. and U P CH UR C H , P. 2008. Systematics and phylogeny
of Stegosauria (Dinosauria: Ornithischia). Journal of Systematic
Palaeontology, 6, 367–407.
M A I N , R. P., R I CQ L E S , A. de., H OR N E R , J. R. and PA -
DI A N , K. 2005. The evolution and function of thyreophoran
dinosaur scutes: implications for plate function in stegosaurs.
Paleobiology, 31, 291–314.
M A R S H , O. C. 1877. A new order of extinct Reptilia (Stegosa-
uria) from the Jurassic of the Rockey Mountains. American
Journal of Science Series 3, 14, 13–514.
M CW H I N N E Y , L. A., RO T H S CH I LD , B. M. and CA R -
PE N TE R , K. 2001. Posttraumatic chronic osteomyelitis in
Stegosaurus spikes. 141–155. In C A R P E N T E R , K. (ed.). The
armored dinosaurs. Indiana University Press, Bloomington, 526
pp.
P H I L L I P S , P. and H E A T H , J. 1992. Heat exchange by the
pinna of the African elephant (Loxodonta africana). Compara-
tive Biochemistry and Physiology, 101A, 693–699.
R E D E L S T OR F F , R. and S A N DE R , P. M. 2009. Long and gir-
dle bone histology of Stegosaurus: implications for growth and
life history. Journal of Vertebrate Paleontology, 29, 1087–1099.
R E I D, R. 1990. Zonal ‘‘growth rings’’ in dinosaurs. Modern
Geology, 15, 19–48.
S A N D E R , P. M. 2000. Long bone histology of the Tendaguru
sauropods: implications for growth and biology. Paleobiology,
26, 466–488.
—— M A T E US , O., L A V E N , T. and K N O T S CH K E , N.
2006. Bone histology indicates insular dwarfism in a new Late
Jurassic sauropod dinosaur. Nature, 441, 739–741.
S C H E Y E R , T. 2009. Conserved bone microstructure in the
shells of long-necked and short-necked chelid turtles (Testudi-
nata, Pleurodira). Fossil Record, 12, 47–57.
—— and S A N D E R , P. M. 2004. Histology of ankylosaur
osteoderms: implications for systematics and function. Journal
of Vertebrate Paleontology, 24, 874–893.
—— —— 2007. Shell bone histology indicates terrestrial palaeoe-
cology of basal turtles. Proceedings of the Royal Society of Lon-
don, Series B, 274, 1885–1893.
S E I DE L , R. M. 1979. The osteoderms of the American alliga-
tor and their functional significance. Herpetologica, 35, 375–
380.
S I BE R, J. H. and M O CK L I , U. 2009. The stegosaurs of the Sauri-
ermuseum Aathal. Sauriermuseum Aathal, Switzerland, 55 pp.
T A T T E R S A L L , G., A N DR A D E , D. and A B E , A. 2009. Heat
exchange from the toucan bill reveals a controllable vascular
thermal radiator. Science, 325, 468–470.
T U R N E R , C. E. and P E T E R S ON , F. 1999. Biostratigraphy of
dinosaurs in the Upper Jurassic Morrison Formation of the
western interior. 77–114. In G I L E TT E , D. (ed.). Vertebrate
paleontology in Utah. Utah Geological Survey, Miscellaneous
Publication 99-1, Utah, 568 pp.
W I T ZM A N N , F. and S O L E R - GI J O N , R. 2008. The bone
histology of osteoderms in temnospondyl amphibians and in
the chroniosuchian Bystrowiella. Acta Zoologica (Stockholm),
89, 1–19.
H A Y A S H I E T A L . : P L A T E A N D S P I K E G R O W T H O F S T E G O S A U R U S 17