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Soft-Tissue Vessels and Cellular Preservation in Tyrannosaurus rex

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 Soft-Tissue Vessels and Cellular Preservation in
Tyrannosaurus rex
Mary H. Schweitzer, et al.
Science 307, 1952 (2005);
DOI: 10.1126/science.1108397

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 REPORTS
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century global warming has also resulted in a material on Science Online. NOAA National Environmental and Satellite Data
stronger east-west SST gradient (34) on a 13. At the critical site for our new interpretation, site 847, and Information Service, U.S. Department of Com-
contrastingly rapid time scale. Both of these carbonate accumulation rates were higher prior to merce, Washington, DC (1994).
4 Ma, which implies that preservation was improved 42. D. W. Lea, D. K. Pak, H. J. Spero, Science 289, 1719 (2000).
scenarios, reflecting mean and transient Pacif- during the Pliocene relative to today (17). The chem- 43. E. C. Farmer, Thesis, Columbia University (2000).
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Bjerknes feedback inhibiting an El NiDo posi- to chemical homogeneity throughout the test (38). change of ideas, two anonymous reviewers who greatly
Planktonic Sr/Ca is a potential indicator of dissolution. improved this manuscript, J. Arden for technical sup-
tive feedback to global warming. Interestingly, port, and D. Sansom for art support. Further thanks
Further evidence of the minimal influence of disso-
during the Pliocene the increase in east-west lution on these records is the covariation of Sr/Ca of to the Ocean Drilling Program for providing samples
SST gradient is due to eastern cooling, whereas G. sacculifer and G. tumida from both sites (Fig. 1E), and to the Natural Environment Research Council for
during the 20th century it is due to WEP warm- which also parallels oceanic Sr/Ca evolution (39). providing financial support.
14. S. G. Philander, A. V. Federov, Paleoceanography 18,
ing. In the near future, if the warming of the 837 (2003); 10.1029/2002PA000837. Supporting Online Material
WEP warm pool reaches a limit without a 15. T. Izumo, J. Picaut, B. Blanke, Geophys. Res. Lett. 29, www.sciencemag.org/cgi/content/full/307/5717/1948/
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by the EUC during the Pliocene), could the 17. T. King, Mar. Micropaleontol. 27, 63 (1996). References
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References and Notes

1. W. J. Cai, P. H. Whetton, Geophys. Res. Lett. 27, 2577
(2000).
2. K. E. Trenberth, D. P. Stepaniak, J. M. Caron, J. Geophys.
Soft-Tissue Vessels and Cellular
Res. 107, 4066 (2002); 10.1029/2000JD000297.
3. Here, we use ‘‘hothouse’’ to denote the warm early-mid
Pliocene climate regime when the Northern Hemi-
Preservation in Tyrannosaurus rex
sphere lacked substantial ice sheets, and ‘‘icehouse’’
for the Middle to Late Pleistocene regime charac- Mary H. Schweitzer,1,2,3* Jennifer L. Wittmeyer,1 John R. Horner,3
terized by the waxing and waning of major Northern Jan K. Toporski4.
Hemisphere ice sheets.
4. M. Budyko, Y. A. Izrael, Eds., Anthropogenic Climate
Changes (L. Gidrometeoizdat, Leningrad, 1987). Soft tissues are preserved within hindlimb elements of Tyrannosaurus rex
5. T. C. Crowley, Quat. Sci. Rev. 10, 275 (1991). (Museum of the Rockies specimen 1125). Removal of the mineral phase reveals
6. M. E. Raymo, B. Grant, M. Horowitz, G. H. Rau, Mar. transparent, flexible, hollow blood vessels containing small round micro-
Micropaleontol. 27, 313 (1996).
7. Global climate is influenced by the seesaw of the structures that can be expressed from the vessels into solution. Some regions
tropical Pacific thermocline tilt, or ENSO. This con- of the demineralized bone matrix are highly fibrous, and the matrix possesses
nection underpins the proposal of persistent El Niño elasticity and resilience. Three populations of microstructures have cell-like
conditions during geological ‘‘hothouse periods.’’ The
natural mode of oscillation is attributable to ocean- morphology. Thus, some dinosaurian soft tissues may retain some of their
atmosphere interactions in which the trade winds original flexibility, elasticity, and resilience.
create SST gradients that in turn reinforce the winds.
In the Pacific, the prevailing easterly trade winds blow A newly discovered specimen of Tyranno- Hell Creek Formation, 8 m above the Fox
warm surface waters along the equator, creating a
deep warm pool toward the western Pacific margin saurus rex EMuseum of the Rockies (MOR) Hills Sandstone, as an association of disartic-
(35). This causes the tropical Pacific thermocline to specimen 1125^ was found at the base of the ulated elements. The specimen was incorpo-

1952 25 MARCH 2005 VOL 307 SCIENCE www.sciencemag.org

 REPORTS
rated within a soft, well-sorted sandstone that crushed, preservation is excellent. MOR compared to the Field Museum (Chicago)
was interpreted as estuarine in origin. Al- 1125 represents a relatively small individual specimen (FMNH PR2081) that has a fem-
though some bones are slightly deformed or of T. rex, with a femoral length of 107 cm, as 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
1
Department of Marine, Earth, Atmospheric Sciences,
Fig. 1. Demineralized fragments of end- North Carolina State University, Raleigh, NC 27695,
osteally derived tissues lining the mar- USA. 2North Carolina State Museum of Natural
row cavity of the T. rex femur. (A) The Sciences, Raleigh, NC 27601, USA. 3Museum of the
demineralized fragment is flexible and Rockies, Montana State University, Bozeman, MT
resilient and, when stretched (arrow), 59717, USA. 4Carnegie Institution of Washington,

Downloaded from www.sciencemag.org on April 19, 2007

returns to its original shape. (B) De- Geophysical Laboratory, 5251 Broad Branch Road
mineralized bone in (A) after air dry- N.W., Washington, DC 20018, USA.
ing. The overall structural and functional *To whom correspondence should be addressed.
characteristics remain after dehydration. E-mail: schweitzer@ncsu.edu
(C) Regions of demineralized bone show .Present address: Department of Geosciences, Christian-
fibrous character (arrows). Scale bars, Albrechts University Kiel, Olshausenstrasse 40, 24098
0.5 mm. Kiel, Germany.

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.

www.sciencemag.org SCIENCE VOL 307 25 MARCH 2005 1953

 REPORTS
after 7 days, several fragments of the lining the mineral phase left a flexible vascular tissue peated stretching was possible (Fig. 1A, arrow),
tissue exhibited unusual characteristics not that demonstrated great elasticity and resil- and small pieces of this demineralized bone
normally observed in fossil bone. Removal of ience upon manipulation. In some cases, re- tissue could undergo repeated dehydration-
rehydration cycles (Fig. 1B) and still retain
Fig. 3. SEM images of this elastic character. Demineralization also
aldehyde-fixed vessels. revealed that some regions of the bone were
(A) Isolated vessel from highly fibrous (Fig. 1C, arrows).
T. rex. (B) Vessel isolated Partial demineralization of the cortical bone
from extant ostrich af- revealed parallel-oriented vascular canals that
ter demineralization
and collagenase diges-
were seen to bifurcate in some areas (Fig. 2A,
tion (3). (C) Vessel from arrows). Occasional fenestrae (marked F)
T. rex, showing internal were observed on the surface of the vascular
contents and hollow canals, possibly correlating with communicat-
character. (D) Exploded ing Volkmann_s canals. Complete demin-
T. rex vessel showing eralization of the cortical bone released thin
small round microstruc-
tures partially embed-
and transparent soft-tissue vessels from some
ded in internal vessel regions of the matrix (Fig. 2, B and C), which
walls. (E) Higher magnifi- floated freely in the demineralizing solution.
cation of a portion of T. Vessels similar in diameter and texture were
rex vessel wall, showing recovered from extant ostrich bone, when de-

Downloaded from www.sciencemag.org on April 19, 2007

hypothesized endotheli- mineralization was followed by digestion with
al nuclei (EN). (F) Sim-
ilar structures visible on
collagenase enzyme (3) to remove densely fi-
fixed ostrich vessel. Stri- brous collagen matrix (Fig. 2D). In both dino-
ations are seen in both saur (Fig. 2C) and ostrich (Fig. 2D), remnants
(E) and (F) that may rep- of the original organic matrix in which the
resent endothelial cell vessels were embedded can still be visualized
junctions or alternatively under transmitted light microscopy. These
may be artifacts of the
fixation/dehydration
vessels are flexible, pliable, and translucent
process. Scale bars in (A) (Fig. 2E). The vessels branch in a pattern
and (B), 40 mm; in (C) consistent with extant vessels, and many bi-
and (D), 10 mm; in (E) furcation points are visible (Fig. 2E, arrows).
and (F), 1 mm. Many of the dinosaur vessels contain small
round microstructures that vary from deep red
Fig. 4. Cellular features to dark brown (Fig. 2, F and G). The vessels
associated with T. rex and contents are similar in all respects to
and ostrich tissues. (A) blood vessels recovered from extant ostrich
Fragment of demin- bone (Fig. 2H). Aldehyde-fixed (3) dinosaur
eralized cortical bone
from T. rex, showing
vessels (Fig. 2I) are virtually identical in over-
parallel-oriented fibers all morphology to similarly prepared ostrich
and cell-like microstruc- vessels (Fig. 2J), and structures consistent with
tures among the fibers. remnants of nuclei from the original endothe-
The inset is a higher lial cells are visible on the exterior of both
magnification of one of dinosaur and ostrich specimens (Fig. 2, I and
the microstructures seen
embedded in the fibrous
J, arrows).
material. (B) Demin- Under scanning electron microscopy (SEM)
eralized and stained (3) (Fig. 3), features seen on the external surface of
ostrich cortical bone, dinosaurian vessels are virtually indistinguish-
showing fibrillar, parallel- able from those seen in similarly prepared
oriented collagen matrix extant ostrich vessels (Fig. 3, B and F), sug-
with osteocytes embed-
ded among the fibers.
gesting a common origin. These features
The inset shows a high- include surface striations that may be consistent
er magnification of one with endothelial cell junctions, or alternatively
of the osteocytes. Both may be artifacts of fixation and/or dehydration.
inset views show elon- In addition, small round to oval features dot the
gate bodies with multi- surface of both dinosaur and ostrich vessels,
ple projections arising
from the external sur-
which may be consistent with endothelial cell
face consistent with nuclei (Fig. 3, E and F, arrows).
filipodia. (C) Isolated Finally, in those regions of the bone where
microstructure from T. fibrillar matrix predominated in the deminer-
rex after fixation. In alized tissues, elongate microstructures could
addition to the multiple filipodial-like projections, internal contents can be seen. The inset shows a be visualized among the fibers (Fig. 4A,
second structure with long filipodia and an internal transparent nucleus-like structure. (D) Fixed ostrich
osteocyte; inset, ostrich osteocyte fixed and stained for better visualization. Internal contents are
inset). These microstructures contain multiple
discernible, and filipodia can be seen extending in multiple planes from the cell surface. (E and F) SEM projections on the external surface and are
images of aldehyde-fixed (3) microstructures isolated from T. rex cortical bone tissues. Scale bars in (A) virtually identical in size, location, and overall
and (B), 50 mm; in (C) and (D), 20 mm; in (E), 10 mm; in (F), 1 mm. morphology to osteocytes seen among colla-

1954 25 MARCH 2005 VOL 307 SCIENCE www.sciencemag.org

 REPORTS
gen fibers of demineralized ostrich bone (Fig. structures consistent with osteocytes in at least 3. Materials and methods are available as supporting
material on Science Online.
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sils, are known to be extremely well preserved lar and analytical methods to well-preserved Harmon, E. Lamm, N. Myrhvold, A. de Ricqles, and A.
histologically and occasionally retain molecu- dinosaur specimens has important implica- Steele for funding, preparation, insight, consultation,
and valued feedback; and J. Fountain and K. Padian
lar information (6, 17, 18), the presence of tions for elucidating preservational mi- for editorial advice. Research was funded by North
which is closely linked to morphological croenvironments and will contribute to our Carolina State University as well as by grants from
preservation (19). Vascular microstructures understanding of biogeochemical interac- N. Myhrvold (J.R.H.) and NSF (M.H.S.).
that may be derived from original blood ma- tions at the microscopic and molecular Supporting Online Material
terials of Cretaceous organisms have also been levels that lead to fossilization. www.sciencemag.org/cgi/content/full/307/5717/1952/
DC1
reported (14–16). Materials and Methods
Pawlicki was able to demonstrate osteo- Figs. S1 to S5
cytes and vessels obtained from dinosaur References and Notes References
1. J. R. Horner, K. Padian, Proc. R. Soc. London Ser. B
bone using an etching and replication tech- 271, 1875 (2004). 7 December 2004; accepted 26 January 2005
nique (14, 15). However, we demonstrate the 2. M. Schweitzer, J. L. Wittmeyer, J. R. Horner, in preparation. 10.1126/science.1108397
retention of pliable soft-tissue blood vessels
with contents that are capable of being liber-
ated from the bone matrix, while still retain- Glycan Foraging in Vivo
ing their flexibility, resilience, original hollow
nature, and three-dimensionality. Additionally,
we can isolate three-dimensional osteocytes
by an Intestine-Adapted
with internal cellular contents and intact, sup-
ple filipodia that float freely in solution. This Bacterial Symbiont
T. rex also contains flexible and fibrillar bone Justin L. Sonnenburg,1,2 Jian Xu,1,2 Douglas D. Leip,1,2
matrices that retain elasticity. The unusual
Chien-Huan Chen,1,2 Benjamin P. Westover,1,3
preservation of the originally organic matrix
may be due in part to the dense mineralization Jeremy Weatherford,3 Jeremy D. Buhler,1,3 Jeffrey I. Gordon1,2*
of dinosaur bone, because a certain portion of Germ-free mice were maintained on polysaccharide-rich or simple-sugar diets
the organic matrix within extant bone is intra- and colonized for 10 days with an organism also found in human guts,
crystalline and therefore extremely resistant to Bacteroides thetaiotaomicron, followed by whole-genome transcriptional
degradation (20, 21). These factors, combined profiling of bacteria and mass spectrometry of cecal glycans. We found that
with as yet undetermined geochemical and these bacteria assembled on food particles and mucus, selectively induced
environmental factors, presumably also outer-membrane polysaccharide-binding proteins and glycoside hydrolases,
contribute to the preservation of soft-tissue prioritized the consumption of liberated hexose sugars, and revealed a
vessels. Because they have not been embed- capacity to turn to host mucus glycans when polysaccharides were absent
ded or subjected to other chemical treatments, from the diet. This flexible foraging behavior should contribute to ecosystem
the cells and vessels are capable of being stability and functional diversity.
analyzed further for the persistence of molec-
ular or other chemical information (3). The adult human body is a composite of many genome, including the ability to harvest other-
Using the methodologies described here, species. Each of us harbors È10 times as many wise inaccessible nutrients from our diet (2). The
we isolated translucent vessels from two other microbial cells as human cells (1). Our resident intestine contains an estimated 10 trillion to 100
exceptionally well-preserved tyrannosaurs microbial communities provide us with a variety trillion microorganisms that are largely members
(figs. S1 and S2) (3), and we isolated micro- of metabolic capabilities not encoded in our of Bacteria but include representatives from

www.sciencemag.org SCIENCE VOL 307 25 MARCH 2005 1955

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