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DOI: 10.1126/science.1108397
, 1952 (2005); 307Science
et al.Mary H. Schweitzer,
Tyrannosaurus rex
Soft-Tissue Vessels and Cellular Preservation in
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Anomalies in the strength of the Hadley cells
are inversely correlated with anomalies in the
strength of the Walker oscillation (18, 31):
Weakened Hadley cells correlate with epi-
sodes of La NiDa and strong Walker circula-
tion. Second, the stronger oceanic heat flux to
the high latitudes is consistent with enhanced
Ekman flow of warm water poleward as a re-
sult of increased Walker circulation. The con-
straint of a balanced heat budget during the
Pliocene implies that this increased heat loss
at high latitudes through vigorous deep-ocean
thermohaline circulation is accompanied by a
shoaling of the tropical thermocline (32). Most
oceanic heat gain occurs in low and mid-
latitude upwelling zones and is large (small)
when the thermocline is shallow (deep). Dur-
ing the Pliocene, the deeper thermocline in the
WEP argues that thermocline tilt must be great-
er to allow shoaling of the EEP thermocline.
Our data rebut the hypothesis that Bhothouse[
climates collapse onto an El NiDo–like state,
in agreement with Eocene hothouse studies
(33), and indicate that the tropical upper-ocean
structure during the warm Pliocene was indic-
ative of a La NiDa–like state consistent with
the dynamical Bocean thermostat.[ Twentieth-
century global warming has also resulted in a
stronger east-west SST gradient (34)ona
contrastingly rapid time scale. Both of these
scenarios, reflecting mean and transient Pacif-
ic states, respectively, support the role of the
Bjerknes feedback inhibiting an El NiDo posi-
tive feedback to global warming. Interestingly,
during the Pliocene the increase in east-west
SST gradient is due to eastern cooling, whereas
during the 20th century it is due to WEP warm-
ing. In the near future, if the warming of the
WEP warm pool reaches a limit without a
compensating cooling in the east (afforded
by the EUC during the Pliocene), could the
Bjerknes feedback be reversed to incite accel-
erated warmth of an El NiDo–like state?
References and Notes
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to the Ocean Drilling Program for providing samples
and to the Natural Environment Research Council for
providing financial support.
Supporting Online Material
www.sciencemag.org/cgi/content/full/307/5717/1948/
DC1
Materials and Methods
References
30 August 2004; accepted 24 January 2005
10.1126/science.1104666
Soft-Tissue Vessels and Cellular
Preservation in Tyrannosaurus rex
Mary H. Schweitzer,
1,2,3
*
Jennifer L. Wittmeyer,
1
John R. Horner,
3
Jan K. Toporski
4
.
Soft tissues are preserved within hindlimb elements of Tyrannosaurus rex
(Museum of the Rockies specimen 1125). Removal of the mineral phase reveals
transparent, flexible, hollow blood vessels containing small round micro-
structures that can be expressed from the vessels into solution. Some regions
of the demineralized bone matrix are highly fibrous, and the matrix possesses
elasticity and resilience. Three populations of microstructures have cell-like
morphology. Thus, some dinosaurian soft tissues may retain some of their
original flexibility, elasticity, and resilience.
A newly discovered specimen of Tyranno-
saurus rex EMuseum of the Rockies (MOR)
specimen 1125^ was found at the base of the
Hell Creek Formation, 8 m above the Fox
Hills Sandstone, as an association of disartic-
ulated elements. The specimen was incorpo-
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rated within a soft, well-sorted sandstone that
was interpreted as estuarine in origin. Al-
though some bones are slightly deformed or
crushed, preservation is excellent. MOR
1125 represents a relatively small individual
of T. rex, with a femoral length of 107 cm, as
compared to the Field Museum (Chicago)
specimen (FMNH PR2081) that has a fem-
oral length of approximately 131 cm. On the
basis of calculated lines of arrested growth
(LAG), we estimated that this animal was 18 T
2 years old at death (1).
No preservatives were applied to interior
fragments of the femur of MOR 1125 during
preparation, and these fragments were reserved
for chemical analyses. In addition to the dense
compact bone typical of theropods, this spec-
imen contained regions of unusual bone tissue
on the endosteal surface (2). Cortical and end-
osteal bone tissues were demineralized (3), and
Fig. 1. Demineralized fragments of end-
osteally derived tissues lining the mar-
row cavity of the T. rex femur. (A) The
demineralized fragment is flexible and
resilient and, when stretched (arrow),
returns to its original shape. (B)De-
mineralized bone in (A) after air dry-
ing. The overall structural and functional
characteristics remain after dehydration.
(C) Regions of demineralized bone show
fibrous character (arrows). Scale bars,
0.5 mm.
Fig. 2. Demineralization of cortical bone reveals the presence of soft-
tissue structures. (A) Partial demineralization of a fragment of T. rex
cortical bone shows an emerging network of vascular canals, some of
which are bifurcated (arrows). All are aligned in parallel, consistent
with Haversian canals in cortical bone. Small fenestrae (marked F)
may indicate invaginations for communicating Volkmann’s canals. (B)
A second fragment of T. rex cortical bone illustrates transparent
vessels (arrows) arising from bone matrix in solution. (C) Complete
demineralization reveals transparent flexible vessels in what remains
of the cortical bone matrix, represented by a brown amorphous sub-
stance (marked M). (D) Ostrich vessel after demineralization of cortical bone and subsequent digestion of fibrous collagenous matrix. Transparent
vessels branch and remain associated with small regions of undigested bone matrix, seen here as amorphous, white fibrous material (marked M). Scale
bars in (A) to (D), 0.5 mm. (E) Higher magnification of dinosaur vessels shows branching pattern (arrows) and internal contents. Vascular structure is
not consistent with fungal hyphae (no septae, and branching pattern is not consistent with fungal morphology) or plant (no cell walls visible, and
again branching pattern is not consistent). Round red microstructures within the vessels are clearly visible. (F) T. rex vessel fragment, containing
microstructures consistent in size and shape with those seen in the ostrich vessel in (H). (G) Second fragment of dinosaur vessel. Air/fluid interfaces,
represented by dark menisci, illustrate the hollow nature of vessels. Microstructure is visible within the vessel. (H) Ostrich vessel digested from
demineralized cortical bone. Red blood cells can be seen inside the branching vessel. (I) T. rex vessel fragment showing detail of branching pattern and
structures morphologically consistent with endothelial cell nuclei (arrows) in vessel wall. (J) Ostrich blood vessel liberated from demineralized bone
after treatment with collagenase shows branching pattern and clearly visible endothelial nuclei. Scale bars in (E) to (J), 50 mm. (F), (I), and (J) were
subjected to aldehyde fixation (3). The remaining vessels are unfixed.
1
Department of Marine, Earth, Atmospheric Sciences,
North Carolina State University, Raleigh, NC 27695,
USA.
2
North Carolina State Museum of Natural
Sciences, Raleigh, NC 27601, USA.
3
Museum of the
Rockies, Montana State University, Bozeman, MT
59717, USA.
4
Carnegie Institution of Washington,
Geophysical Laboratory, 5251 Broad Branch Road
N.W., Washington, DC 20018, USA.
*To whom correspondence should be addressed.
E-mail: schweitzer@ncsu.edu
.Present address: Department of Geosciences, Christian-
Albrechts University Kiel, Olshausenstrasse 40, 24098
Kiel, Germany.
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after 7 days, several fragments of the lining
tissue exhibited unusual characteristics not
normally observed in fossil bone. Removal of
the mineral phase left a flexible vascular tissue
that demonstrated great elasticity and resil-
ience upon manipulation. In some cases, re-
peated stretching was possible (Fig. 1A, arrow),
and small pieces of this demineralized bone
tissue could undergo repeated dehydration-
rehydration cycles (Fig. 1B) and still retain
this elastic character. Demineralization also
revealed that some regions of the bone were
highly fibrous (Fig. 1C, arrows).
Partial demineralization of the cortical bone
revealed parallel-oriented vascular canals that
were seen to bifurcate in some areas (Fig. 2A,
arrows). Occasional fenestrae (marked F)
were observed on the surface of the vascular
canals, possibly correlating with communicat-
ing Volkmann_s canals. Complete demin-
eralization of the cortical bone released thin
and transparent soft-tissue vessels from some
regions of the matrix (Fig. 2, B and C), which
floated freely in the demineralizing solution.
Vessels similar in diameter and texture were
recovered from extant ostrich bone, when de-
mineralization was followed by digestion with
collagenase enzyme (3) to remove densely fi-
brous collagen matrix (Fig. 2D). In both dino-
saur (Fig. 2C) and ostrich (Fig. 2D), remnants
of the original organic matrix in which the
vessels were embedded can still be visualized
under transmitted light microscopy. These
vessels are flexible, pliable, and translucent
(Fig. 2E). The vessels branch in a pattern
consistent with extant vessels, and many bi-
furcation points are visible (Fig. 2E, arrows).
Many of the dinosaur vessels contain small
round microstructures that vary from deep red
to dark brown (Fig. 2, F and G). The vessels
and contents are similar in all respects to
blood vessels recovered from extant ostrich
bone (Fig. 2H). Aldehyde-fixed (3) dinosaur
vessels (Fig. 2I) are virtually identical in over-
all morphology to similarly prepared ostrich
vessels (Fig. 2J), and structures consistent with
remnants of nuclei from the original endothe-
lial cells are visible on the exterior of both
dinosaur and ostrich specimens (Fig. 2, I and
J, arrows).
Under scanning electron microscopy (SEM)
(Fig. 3), features seen on the external surface of
dinosaurian vessels are virtually indistinguish-
able from those seen in similarly prepared
extant ostrich vessels (Fig. 3, B and F), sug-
gesting a common origin. These features
include surface striations that may be consistent
with endothelial cell junctions, or alternatively
may be artifacts of fixation and/or dehydration.
In addition, small round to oval features dot the
surface of both dinosaur and ostrich vessels,
which may be consistent with endothelial cell
nuclei (Fig. 3, E and F, arrows).
Finally, in those regions of the bone where
fibrillar matrix predominated in the deminer-
alized tissues, elongate microstructures could
be visualized among the fibers (Fig. 4A,
inset). These microstructures contain multiple
projections on the external surface and are
virtually identical in size, location, and overall
morphology to osteocytes seen among colla-
Fig. 3. SEM images of
aldehyde-fixed vessels.
(A) Isolated vessel from
T. rex.(B)Vesselisolated
from extant ostrich af-
ter demineralization
and collagenase diges-
tion (3). (C)Vesselfrom
T. rex,showinginternal
contents and hollow
character. (D)Exploded
T. rex vessel showing
small round microstruc-
tures partially embed-
ded in internal vessel
walls. (E)Highermagnifi-
cation of a portion of T.
rex vessel wall, showing
hypothesized endotheli-
al nuclei (EN). (F)Sim-
ilar structures visible on
fixed ostrich vessel. Stri-
ations are seen in both
(E) and (F) that may rep-
resent endothelial cell
junctions or alternatively
may be artifacts of the
fixation/dehydration
process. Scale bars in (A)
and (B), 40 mm; in (C)
and (D), 10 mm; in (E)
and (F), 1 mm.
Fig. 4. Cellular features
associated with T. rex
and ostrich tissues. (A)
Fragment of demin-
eralized cortical bone
from T. rex, showing
parallel-oriented fibers
and cell-like microstruc-
tures among the fibers.
The inset is a higher
magnification of one of
the microstructures seen
embedded in the fibrous
material. (B)Demin-
eralized and stained (3)
ostrich cortical bone,
showing fibrillar, parallel-
oriented collagen matrix
with osteocytes embed-
ded among the fibers.
The inset shows a high-
er magnification of one
of the osteocytes. Both
inset views show elon-
gate bodies with multi-
ple projections arising
from the external sur-
face consistent with
filipodia. (C) Isolated
microstructure from T.
rex after fixation. In
addition to the multiple filipodial-like projections, internal contents can be seen. The inset shows a
second structure with long filipodia and an internal transparent nucleus-like structure. (D)Fixedostrich
osteocyte; inset, ostrich osteocyte fixed and stained for better visualization. Internal contents are
discernible, and filipodia can be seen extending in multiple planes from the cell surface. (E and F)SEM
images of aldehyde-fixed (3) microstructures isolated from T. rex cortical bone tissues. Scale bars in (A)
and (B), 50 mm; in (C) and (D), 20 mm; in (E), 10 mm; in (F), 1 mm.
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gen fibers of demineralized ostrich bone (Fig.
4B, inset). These cell-like microstructures
could be isolated and, when subjected to al-
dehyde fixation (3), appeared to possess in-
ternal contents (Fig. 4C), including possible
nuclei (Fig. 4C, inset). These microstructures
are similar in morphology to fixed ostrich
osteocytes, both unstained (Fig. 4D) and
stained (3) for better visualization (Fig. 4D,
inset). SEM verifies the presence of the fea-
tures seen in transmitted light microscopy,
and again, projections extending from the
surface of the microstructures are clearly vis-
ible(Fig.4,EandF).
The fossil record is capable of exceptional
preservation, including feathers (4–6), hair (7),
color or color patterns (7, 8), embryonic soft
tissues (9), muscle tissue and/or internal organs
(10–13), and cellular structure (7, 14–16).
These soft tissues are preserved as carbon
films (4, 5, 10) or as permineralized three-
dimensional replications (9, 11, 13), but in
none of these cases are they described as still-
soft, pliable tissues.
Mesozoic fossils, particularly dinosaur fos-
sils, are known to be extremely well preserved
histologically and occasionally retain molecu-
lar information (6, 17, 18), the presence of
which is closely linked to morphological
preservation (19). Vascular microstructures
that may be derived from original blood ma-
terials of Cretaceous organisms have also been
reported (14–16).
Pawlicki was able to demonstrate osteo-
cytes and vessels obtained from dinosaur
bone using an etching and replication tech-
nique (14, 15). However, we demonstrate the
retention of pliable soft-tissue blood vessels
with contents that are capable of being liber-
ated from the bone matrix, while still retain-
ing their flexibility, resilience, original hollow
nature, and three-dimensionality. Additionally,
we can isolate three-dimensional osteocytes
with internal cellular contents and intact, sup-
ple filipodia that float freely in solution. This
T. rex also contains flexible and fibrillar bone
matrices that retain elasticity. The unusual
preservation of the originally organic matrix
may be due in part to the dense mineralization
of dinosaur bone, because a certain portion of
the organic matrix within extant bone is intra-
crystalline and therefore extremely resistant to
degradation (20, 21). These factors, combined
with as yet undetermined geochemical and
environmental factors, presumably also
contribute to the preservation of soft-tissue
vessels. Because they have not been embed-
ded or subjected to other chemical treatments,
the cells and vessels are capable of being
analyzed further for the persistence of molec-
ular or other chemical information (3).
Using the methodologies described here,
we isolated translucent vessels from two other
exceptionally well-preserved tyrannosaurs
(figs. S1 and S2) (3), and we isolated micro-
structures consistent with osteocytes in at least
three other dinosaurs: two tyrannosaurs and
one hadrosaur (fig. S3). Vessels in these spec-
imens exhibit highly variable preservation,
from crystalline morphs to transparent and
pliable soft tissues.
The elucidation and modeling of processes
resulting in soft-tissue preservation may form
the basis for an avenue of research into the
recovery and characterization of similar struc-
tures in other specimens, paving the way for
micro- and molecular taphonomic investiga-
tions. Whether preservation is strictly morpho-
logical and the result of some kind of unknown
geochemical replacement process or whether
it extends to the subcellular and molecular
levels is uncertain. However, we have identi-
fied protein fragments in extracted bone sam-
ples, some of which retain slight antigenicity
(3). These data indicate that exceptional mor-
phological preservation in some dinosaurian
specimens may extend to the cellular level or
beyond. If so, in addition to providing in-
dependent means of testing phylogenetic
hypotheses about dinosaurs, applying molecu-
lar and analytical methods to well-preserved
dinosaur specimens has important implica-
tions for elucidating preservational mi-
croenvironments and will contribute to our
understanding of biogeochemical interac-
tions at the microscopic and molecular
levels that lead to fossilization.
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Steele for funding, preparation, insight, consultation,
and valued feedback; and J. Fountain and K. Padian
for editorial advice. Research was funded by North
Carolina State University as well as by grants from
N. Myhrvold (J.R.H.) and NSF (M.H.S.).
Supporting Online Material
www.sciencemag.org/cgi/content/full/307/5717/1952/
DC1
Materials and Methods
Figs. S1 to S5
References
7 December 2004; accepted 26 January 2005
10.1126/science.1108397
Glycan Foraging in Vivo
by an Intestine-Adapted
Bacterial Symbiont
Justin L. Sonnenburg,
1,2
Jian Xu,
1,2
Douglas D. Leip,
1,2
Chien-Huan Chen,
1,2
Benjamin P. Westover,
1,3
Jeremy Weatherford,
3
Jeremy D. Buhler,
1,3
Jeffrey I. Gordon
1,2
*
Germ-free mice were maintained on polysaccharide-rich or simple-sugar diets
and colonized for 10 days with an organism also found in human guts,
Bacteroides thetaiotaomicron, followed by whole-genome transcriptional
profiling of bacteria and mass spectrometry of cecal glycans. We found that
these bacteria assembled on food particles and mucus, selectively induced
outer-membrane polysaccharide-binding proteins and glycoside hydrolases,
prioritized the consumption of liberated hexose sugars, and revealed a
capacity to turn to host mucus glycans when polysaccharides were absent
from the diet. This flexible foraging behavior should contribute to ecosystem
stability and functional diversity.
The adult human body is a composite of many
species. Each of us harbors È10timesasmany
microbial cells as human cells (1). Our resident
microbial communities provide us with a variety
of metabolic capabilities not encoded in our
genome, including the ability to harvest other-
wise inaccessible nutrients from our diet (2). The
intestine contains an estimated 10 trillion to 100
trillion microorganisms that are largely members
of Bacteria but include representatives from
R EPORTS
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