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Vertebral Anomaly in Fossil Sea Cows (Mammalia Sirenia).

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THE ANATOMICAL RECORD 294:980–986 (2011)
Vertebral Anomaly in Fossil Sea Cows
(Mammalia, Sirenia)
Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung,
Berlin, Germany
Institut für Radiologie, Charité – Universitätsmedizin Berlin, Campus Mitte, Berlin,
Helmholtz-Zentrum Berlin für Materialien und Energie GmbH, Institut für Angewandte
Materialforschung, Berlin, Germany
Four incompletely preserved caudal vertebrae lacking the neural
arches of two fossil sirenian individuals of Halitherium schinzii (Oligocene) from the Rhine area in Germany and northern Belgium reveal
osteological alterations. The caudal vertebrae possess a transverse process with growth retardation. This asymmetry indicates that the affected
transverse processes are less developed than their counterparts and, consequently, deviate from the norm. Computed tomography (CT) scans
reveal osteosclerotic patterns, a morphological feature that characterizes
sea cows and supports the nonpathological state of the vertebrae. Additionally, no indications of vertebral fractures or any other occurrences
due to external factors are present. This is the oldest documentation of
such an anomaly in any sirenian and is interpreted here as hypoplasia,
the underdevelopment of an organ or parts of it that might cause a funcC 2011 Wiley-Liss, Inc.
tional deficiency. Anat Rec, 294:980–986, 2011. V
Key words: Oligocene; Germany; Belgium; caudal vertebrae;
transverse process; asymmetry; hypoplasia
Sirenia, or sea cows, are a group of aquatic mammals
that have a fossil record extending from the early
Eocene (50 Ma) to the present. Sirenians possess relatively large, stout but streamlined bodies, paddlelike
flippers, no hind legs, and a powerful horizontal tail
fluke. They are unique among living marine mammals
in having an herbivorous diet and several morphological
features distinguishing them from all other mammals,
such as pachyostosis and osteosclerosis (Domning and de
Buffrenil, 1991; Domning, 1994). The development of
pachyostosis and osteosclerosis, or pachyosteosclerosis, is
indicated by greatly thickened bones and the partial or
complete loss of the marrow cavity and the spongiosa in
the bones of the sirenian skeleton (Kaiser, 1974).
Pachyosteosclerosis, in connection with the achievement
of equilibrium in the aqueous medium, produces a
weight increase corresponding to the environmental
requirements for Sirenia (Kaiser, 1974; Kleinschmidt,
According to Sickenberg (1934, p. 243), pachyosteosclerosis reaches a high degree in the vertebral column,
especially in the spinous and transverse processes. The
vertebral bone histology is dense in the vertebral arches
and processes; greater parts of cancellous bone are rare
and restricted to the centra. Sickenberg (1934) already
noted the occurrence of left–right asymmetries in vertebrae of the fossil sea cow Halitherium schinzii from the
Oligocene (30 Ma) of Belgium, but only referred to alterations of the spinous process and the centrum. Those
observations of vertebral asymmetries are supplemented
in this study by presenting four caudal vertebrae of
two fossil sirenian individuals from the Oligocene of
Germany and Belgium. These vertebrae possess an
*Correspondence to: Manja Voss, Museum für Naturkunde,
Leibniz-Institut für Evolutions- und Biodiversitätsforschung,
Invalidenstraße 43, 10115, Berlin, Germany. Fax: þ49-30-20938868. E-mail:
Received 7 November 2010; Accepted 18 March 2011
DOI 10.1002/ar.21397
Published online 28 April 2011 in Wiley Online Library
underdeveloped transverse process causing a left–right
The normally developed transverse processes are important as attachment areas for ligaments and muscles
of the back (Nickel et al., 1984). They thus contribute to
static and dynamic stability during the extension and
flexion of the vertebral column. Therefore, abnormalities
of the development of the transverse processes have clinical relevance. One of the most important diseases that
affect the attachment modes is enthesitis, a common
finding in spondyloarthritis, which indicates an inflammatory disease of the musculoskeletal system (Rothschild and Martin, 1993, 2006; Hermann et al., 2005).
Pathologic rotation of the transverse processes on the
basis of blockage (blocking) of the spine can result in
irritation or even compression of the spinal nerves, causing various neurologic symptoms (Biedermann and
Sacher, 2002). Congenital defects (malformations) of the
transverse processes are also known and can affect these
either directly or indirectly (Wolfers and Hoeffken,
1974). Direct effects on the transverse processes include
hypoplasia, the retarded development of an organ or
parts of it caused by either a genetic defect or an ontogenetic alteration, and aplasia, which is the total absence
of an organ. Assimilation malformations, for example
the lumbosacral junction, which can be associated with
pseudoarticulation of the transverse process and the sacrum, induce indirect effects.
The observation of asymmetrical transverse processes
in the fossil sea cow specimens presented here is interpreted as hypoplasia and documented for the first time
in this group of animals. In this study, we aim at clarifying and elucidating the development of this vertebral
anomaly. For this purpose, we externally describe the
affected vertebrae and provide Computed tomography
(CT) scans for the internal investigations of the bones.
This study may contribute to the knowledge of skeletal
alterations in sea cows.
Four caudal vertebrae of the extinct sirenian Halitherium schinzii were analyzed. H. schinzii was a dugongid
sea cow of up to 3 m in body length living in the coastal
areas of the early Oligocene (30 Ma) Sea of Europe,
especially of Germany (e.g. Lepsius, 1882; Böhme, 2001;
Voss, 2008) and Belgium (Sickenberg, 1934).
One specimen is represented by a single vertebra (P
2068/5) of H. schinzii, which is deposited in the National
Museum of Victoria (MV) in Melbourne, Australia. Vertebra P 2068/5 is assumed to be from the lower Miocene
(20 Ma) of the Rhine area in western Germany, but may
be most probably from the sandy facies of the Ratingen
Formation (Rupelian, lower Oligocene), because no lower
Miocene deposit is known in this area of the Rhine
The other three vertebrae (Plt.M.137.1–3) belong to an
individual of H. schinzii (Plt.M.137) from the Rupelian
(lower Oligocene, 30 Ma) of Steendorp, southwest of Antwerp (Belgium), which is stored in the Institut Royal des
Sciences Naturelles de Belgique (IRSNB) in Brussels.
The specimen Plt.M.137 is a partial skeleton consisting
of fragmentarily preserved cranial and postcranial elements including the frontal, maxilla, scapula, humerus,
radius, and ulna of the right side; the humerus and ulna
of the left side; the second cervical vertebra; 10 thoracics; 13 caudals; and 5 ribs and 4 chevron bones.
CT was applied to investigate the internal structure of
the H. schinzii vertebrae. Two objects of about 10 cm in
diameter were scanned, the vertebrae Plt.M.137.2 and 3
of the Belgian specimen (Fig. 4). The CT scans were performed at the tomography station CONRAD (Cold Neutron Radiography) in the Helmholtz-Zentrum Berlin für
Materialien und Energie (Hilger et al., 2006). At the end
of a curved neutron guide, a pinhole aperture of 2 cm
was installed. The sample position and the detector system were located 5 m behind the aperture. A combination of a 200-lm-thick lithium(6)fluoride scintillator and
a CCD-camera (Andor DW436N-BV) with a 50 mm lens
system was used as a detector. For each scan, 400 projections were measured with an exposure time of 20 sec.
The software Octopus was used for the reconstruction of
the datasets. Subsequently, multiplanar visualization
was obtained in the transverse, sagittal, and frontal
planes with the VGStudioMax1.2 software (Volume
Graphics GmbH, Heidelberg, Germany).
The vertebrae reported in this study are incompletely
preserved, all missing the neural arches. Vertebrae
Plt.M.137.1 and 2 also lack their right transverse processes (Fig. 1A and B). The vertebrae are identified as
caudal vertebrae based on the presence of the characteristic and more or less prominent and paired anterior and
posterior demifacets for the chevrons on the ventral side
of each centrum. The centra are wider than high, having
a slightly hexagonal outline. The cranial and caudal epiphyses are flat to slightly concave. Even though the centra Plt.M.137.1–3 are disarticulated, their size might
indicate their arrangement in a craniocaudal series (Fig.
1). The centra have a maximum width of 72 mm in
Plt.M.137.1 and 73 mm in Plt.M.137.2 and 3, and a
dorsoventral height of 44 mm in Plt.M.137.1 and about
52 mm in Plt.M.137.2 and 3. Vertebrae Plt.M.137.1–3
are from the middle part of the caudal vertebral column,
as indicated by the single almost completely preserved
right transverse process in Plt.M.137.3 (Fig. 2), which is
more or less horizontally directed and only slightly caudally inclined. Vertebra P 2068/5 is one of the more posterior caudals within the vertebral column; because of
its strongly caudally inclined left transverse process
(Fig. 3), it is evidently from the peduncular region of the
tail. Its centrum measures only 40 mm in width and
about 33 mm in dorsoventral height. The transverse
processes form lateral extensions of the centrum as is
typical for caudal vertebrae. However, the left ones of
caudal Plt.M.137.1–3 (Fig. 1) and the right one of P
2068/5 (Fig. 3) are exceptional. These transverse processes are present, but vestigial. This is best observable
in the dorsal view of Plt.M.137.3 (Fig. 2A) and P 2068/5
(Fig. 3A), because these are the only vertebrae having a
completely preserved counterpart and, therefore, provide
the best contrast. The affected transverse processes have
the form of a stump and, in contrast to their normal
counterparts, do not extend to their full length laterally,
but end in a slight caudal tip. They are miniature editions of transverse processes in normal condition without
any indication of a pathological pattern or an association
with other malformations and, therefore, reveal a
Fig. 1. Caudal vertebrae Plt.M.137.1–3 of Halitherium schinzii with vestigially developed left transverse
processes in dorsal views. c, vertebral centrum; fs, fracture surface of broken neural arch; tp, transverse
process; and vtp, vestigial transverse process.
hypoplasia, an anomaly or alteration of the vertebrae for
which the reason is unknown. However, the diagnosis of
associated malformations is limited because of the lack
of preservation in the specimens of H. schinzii. Even
though the right transverse processes of Plt.M.137.1 and
2 are broken (Fig. 1A and B), it can be assumed that
they reached their normal extent during life, because
their bases are distinctly longer in anteroposterior direction than their vestigial counterparts.
Fractures or abrasion that could have caused the asymmetry of the transverse processes can be excluded,
because the surfaces of the vertebrae are smooth. Generally, fractures can be easily identified by a sharply defined
area, which is missing at the hypoplastic transverse processes. The uniform shape of the affected transverse processes is another argument against external factors that
may have caused the anomaly reported here. Their shape
is similar not only among Plt.M.137.1–3 from one individual (Fig. 1), but also corresponds to P 2068/5 from another
specimen (Fig. 3).
Fractures along the bases of the neural arches of each
vertebra (Figs. 1, 2A, and 3A) and along the right transverse processes of Plt.M.137.1 and 2 reveal the dense,
osteosclerotic histology peculiar to sirenian bones. Neutron scans of Plt.M.137.2 and 3 (Fig. 4) confirm the typical compact bone histology, therefore, supporting a
nonpathological condition of the vertebrae. A distinction
between compact and cancellous parts of the bone cannot be inferred from the CT scans.
It is assumed that the dense bone situation prevents
the vertebrae to be completely penetrated by the neutron
scans, which indicates that the cancellous bone has been
almost completely displaced (compare Sickenberg, 1934).
Consequently, possible alterations in detail remain
The left transverse processes of the caudals
Plt.M.137.1–3 (Figs. 1 and 2) and the right one of P
2068/5 (Fig. 3) deviate from the norm in showing less development than their counterparts. In contrast to aplasia (resulting in the total absence of an organ), the
transverse processes are still present and cause an
observable left–right asymmetry of the vertebrae, indicating a hypoplastic pattern.
As stated above, hypoplasia of the transverse processes
is a congenital defect (Wolfers and Hoeffken, 1974), which
might be developmental and/or genetically induced. This
is supported by Rathke (1952), who states that a constant
type of alteration and its restriction to a certain vertebral
region argue for a congenital defect. In the studies of
Tanaka and Uhthoff (1981a,b) and Erol et al. (2002), congenital malformations of the vertebral body were classified
into two categories. Type 1 includes failure of formation
and Type 2 is a developmental failure of segmentation.
Failure of formation implies total or partial defects of the
vertebral body, and also specific abnormalities in the shape
of the vertebral body. Failure of segmentation signifies
unsegmented vertebrae due to abnormalities of the intervertebral disc. Tanaka and Uhthoff (1981b) emphasize
that this concept is accepted for all congenital vertebral
malformations and, additionally, suggest a subdivision
into defect and error. ‘‘Defect of formation’’ implies absence
Fig. 2. Caudal vertebra Plt.M.137.3 of Halitherium schinzii. A: Dorsal view; B: posterior view; and C:
ventral view. c, vertebral centrum; d, demifacet for chevron bones; fs, fracture surface of broken neural
arch; tp, transverse process; and vtp, vestigial transverse process.
of the vertebral body or part of it and ‘‘defect of segmentation’’, total or partial absence of the intervertebral disc.
‘‘Error’’ signifies some other malformation. A third category refers to a mixed type and can be any combination of
the above anomalies. Ghebranious et al. (2007) enumerate
failures of formation as butterfly vertebrae, hypoplasia,
and hemivertebrae.
According to the classifications of Tanaka and Uhthoff
(1981a,b) and Ghebranious et al. (2007), the less developed transverse processes in this study can be explained
by error of formation leading to hypoplastic transverse
processes. The left–right asymmetry in the vertebrae
caused by this failure of formation is confirmed by Erol
et al. (2002) stating that this may occur on the right or the
left side of the body. Even though congenital malforma-
tions are mostly referred to in the literature as affecting
the vertebral body alone, Tanaka and Uhthoff (1981b)
point out that the extent of the defect can involve different
parts of the centrum to different degrees, as is observable
in the specimens presented here.
The vestigial transverse processes support their cartilaginous anlagen and even that of their bony cores.
However, according to the comments of Rathke (1952)
and Matsuura et al. (1998) on incompletely developed
organs, the growth impulse of the transverse processes
must have been disturbed during ontogeny, causing the
development of only one normal transverse process. Following Tanaka and Uhthoff (1981a,b) and Erol et al.
(2002), all types of congenital malformations result from
disruption of normal vertebral development.
Fig. 3. Caudal vertebra P 2068/5 of Halitherium schinzii with right vestigially developed transverse
process. A: Dorsal view and B: ventral view. c, vertebral centrum; d, demifacet for chevron bones; fs,
fracture surface of broken neural arch; tp, transverse process; and vtp, vestigial transverse process.
The vertebrae of the spine are formed during somitogenesis and even a slight disruption of this process, as
has been done in animal models, results in congenital
vertebral defects (Erol et al., 2002). Erol et al. (2002)
hypothesized that the close interaction of genes and
environment produces the normal spine and the environmental factors affect the delivery of the genetic instructions during development. According to Erol et al. (2002)
and Maisenbacher et al. (2005), the interaction of genes
and environment is disrupted in embryonic somite formation leading to deformities. Tanaka and Uhthoff
(1981b) even state that vertebral malformations may
have greater environmental than genetic components to
their origin.
Concerning the genetic cause of vertebral malformations, developmental studies in animal models have
identified many genes regulating somite formation and
segmentation (Erol et al., 2002). One family of these
somite genes is that in the ‘‘notch’’ pathway. The cycling
of these genes regulates the periodic activation of the
notch signaling pathway, which would be required for
the somite segmentation process. A possible candidate
gene for the congenital vertebral malformations is the
protein-coding WNT3A gene, which has recently been
identified as a negative regulator of notch signaling and
somitogenesis (Ghebranious et al., 2007). Mutations in
this gene are known to cause caudal vertebrae malfor-
mations in mice. Some abnormalities of genes involved
in mouse somitogenesis have been found to cause spinal
deformities even in humans (Erol et al., 2002).
Following Maisenbacher et al. (2005), genetic disruption is supposed to produce multiple severe defects.
However, this is not the case in the vertebrae of this
study. Environmental influences are more probably
expected to induce single or localized axial defects (Maisenbacher et al., 2005). In this study, hypoplasia is only
observed in the transverse processes, resulting in a
localized defect of the vertebrae, which is most probably
related to environmental factors. However, hypoplastic
transverse processes are reported from neither extant
nor fossil sea cows to date. Therefore, the environmental
factors in the animal’s lifetime cannot be completely
established. However, the developmental toxicity of the
environmental factors, such as increased body temperature, carbon monoxide, and chemical reactions, and their
undesirable effects on the development of the organism
during the prenatal and postnatal period have been
investigated experimentally in animal models (Edwards,
1986; Erol et al., 2002). Transient exposure to toxic substances such as carbon monoxide during the fetal period
has been shown to induce hypoxia, causing congenital
vertebral anomalies in mice (Erol et al., 2002).
A possible environmental setting that could be associated with the development of hypoplastic transverse
Fig. 4. Neutron scans of vertebrae Plt.M.137.2 (A–C) and 3 (D–E) showing osteosclerosis characteristic
of Sirenia (not to scale). A: Oblique anterodorsal view; B: oblique posterodorsal view; C: posterior view;
and D and E: dorsal view.
processes in the sea cow specimens of this study is naturally occurring harmful algal or red tide blooms. Recent
studies point out that marine mammals including manatees are commonly susceptible during moderate and
severe red tides and that they are affected by toxins produced by red tide dinoflagellates (Kimm-Brinson and
Ramsdell, 2001; Flewelling et al., 2005; Walsh et al.,
2005). However, skeletal malformations in manatees
that might have resulted from red tides are not reported
to date. This might be because toxication of sea cows
resulting from intense algae blooms is a fast process
indicating a short-term effect not leading to skeletal
alterations, but to the animal’s death. This is supported
by Flewelling et al. (2005), who showed that sea grass,
the main food of Florida manatees (Trichechus manatus
latirostris), has acted as the primary source of toxin during recent deaths of manatees, because of its ability to
accumulate high concentrations of red tide toxins. The
possibility of long-term effects such as skeletal malformations was apparently not investigated here.
However, algal blooms are natural events in the habitat of manatees. Therefore, it cannot be excluded that
extant sea cows are morphologically affected by algal
blooms if they encounter low concentrations of red tide
toxins over a long time. This hypothesis is supported by
Kimm-Brinson and Ramsdell (2001), who describe
adverse developmental effects of red tide toxins in
embryos of Medaka fish (Oryzias latipes) in the form of
morphologic abnormalities, such as lateral curvature of
the spinal column. In view of the similar developmental
processes found in higher and lower vertebrates, KimmBrinson and Ramsdell (2001) confirm that developmen-
tal toxicity and abnormalities potentially occur among
different phylogenetic classes as a result of cumulative
exposure to red tide events.
The form of hypoplastic anomaly reported here is
occasionally noted on X-rays of the human vertebral
column (P. Asbach, pers. obser.) and the German shepherd dog (Julier-Franz, 2006). However, both observations are supposed to have probably no predisposition
for clinical significance. In humans, for example, asymmetries that refer to the transverse processes are used
as landmarks during radiographical investigations (P.
Asbach, pers. obser.). According to Rathke (1952), congenital anomalies especially in the centra cause
changes in the stasis of the vertebral column. Junghans
(1933, 1937) stated that congenital defects of the vertebral column may result in a compensatory growth of
other vertebrae, particularly of the adjacent ones,
maintaining an equilibrium. However, this cannot be
confirmed in this study because of the disarticulated
preservation of the specimens. Although an impairment
of caudal mobility during the lifetime of these specimens of H. schinzii cannot be excluded, because of the
direct relationship of the transverse processes with the
muscular system, it is assumed that the impact of the
anomaly was to a minor degree. According to Biedermann and Sacher (2002), only an association of hypoplastic transverse processes with other malformations
of the spine implies a relative clinical importance of
such findings, which, however, is not the case in the
specimens described here.
In conclusion, this is the first record of hypoplasia in
vertebrae of extinct as well as extant sea cows. The
hypoplastic transverse processes of H. schinzii reflect an
anomaly caused by a deformity of one lateral anlage.
Their development can potentially be explained by red
tide toxin exposure affecting the delivery of the genetic
instructions during ontogeny. However, further investigations on extant sea cows are required to verify this
The authors thank Etienne Steurbaut, IRSNB, Brussels, for permission to borrow the vertebrae of H. schinzii, and Aneliese Folie for facilitating this loan. Eric
Fitzgerald provided access to the specimen housed in the
Museum Victoria Melbourne. We thank Jan MüllerEdzards for preparing the line drawings of the vertebrae. Daryl Domning and an anonymous referee provided helpful comments to improve this article. This
research was funded by the German Research Foundation (DFG).
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