EMBRYONIC SKIN FROM LATE CRETACEOUS SAUROPODS

(DINOSAURIA) OF AUCA MAHUEVO, PATAGONIA, ARGENTINA

Author(s): RODOLFO A. CORIA and LUIS M. CHIAPPE
Source: Journal of Paleontology, 81(6):1528-1532.
Published By: The Paleontological Society
https://doi.org/10.1666/05-150.1
URL: http://www.bioone.org/doi/full/10.1666/05-150.1

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J. Paleont., 81(6), 2007, pp. 1528–1532
Copyright 䉷 2007, The Paleontological Society
0022-3360/07/0081-1528$03.00

EMBRYONIC SKIN FROM LATE CRETACEOUS SAUROPODS (DINOSAURIA)

OF AUCA MAHUEVO, PATAGONIA, ARGENTINA
RODOLFO A. CORIA1 AND LUIS M. CHIAPPE2
CONICET—Museo Carmen Funes, Av. Córdoba 55, Plaza Huincul, 8318 Neuquén, Argentina, 具coriarod@copelnet.com.ar典 and 2The Dinosaur Institute,
1

Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles California 90007, United States of America, 具chiappe@nhm.org典

ABSTRACT—We describe the integumentary anatomy of titanosaur sauropod embryos from the Auca Mahuevo nesting site. Natural (calcitic)
casts of the skin show the non-imbricating, tuberculate scales (i.e., tubercles) typical of other non-avian dinosaurs. However, a variety of scale
patterns previously unknown for the skin of these animals is reported. The observed integumentary patterns include ground tubercles, large and
elongated tubercles, parallel rows of large tubercles, tubercles in rosette-like and flower-like arrangements, and in striate-like rows. Ground
tubercles and rosette-like patterns resemble the few examples of skin known for adult sauropods. The former pattern also resembles the
arrangement of osteoderms of the armored titanosaur Saltasaurus. Although the embryonic skin does not show definitive evidence of armor,
the posthatching development of osteoderms cannot be ruled out. This material, the only available evidence of the embryonic skin of non-avian
dinosaurs, contributes significantly to our knowledge of the integumentary morphology of these animals.

INTRODUCTION approximately 300 ␮m in diameter. They are densely ar-

I 1997, the exceptional sauropod nesting site of Auca Mahuevo
N
was discovered in the northern part of the Patagonian province
of Neuquén, Argentina (Chiappe et al., 1998). This unique fossil
locality has yielded a wealth of eggs containing the remains of
titanosaur embryos and information on the reproductive behavior
of these sauropods (Chiappe et al., 1998, 2001, 2005). In addition
to skeletal remains, embryonic material at Auca Mahuevo in-
cludes portions of integument (Chiappe et al., 1998; Coria et al.,
2001; Coria and Chiappe, 2004)—78 skin patches are catalogued
at the Vertebrate Paleontology collection of the Museo Carmen
Funes, in Plaza Huincul, Argentina. The highly cemented skin
patches contained within fragments of eggs provide the only ev-
idence to date of the epidermis of embryonic dinosaurs and sig-
nificantly augment our limited knowledge of sauropod integu-
mentary diversity.
Institutional abbreviations.⎯LACM, Natural History Museum
of Los Angeles County, Los Angeles, USA; MCF-PVPH, Museo
Carmen Funes, Paleontologı́a de Vertebrados, Plaza Huincul, Ne-
uquén, Argentina; MEF, Museo Egidio Feruglio, Trelew, Chubut,
Argentina; and PVL, Paleontologı́a de Vertebrados, Instituto Mi-
guel Lillo, Tucumán, Argentina.
DESCRIPTION
At Auca Mahuevo, in ovo skin patches are found on erosional
surfaces of egg-beds 2 and 3 (see Chiappe et al. [2005] for strati-
graphic information). Most of these are found in eggs lacking any
skeletal remains and only a few are associated with skeletal ele-
ments that are of problematic identification. However, the inclu-
sion of all these skin patches in eggs of morphology (e.g., surficial
texture, eggshell microstructure) identical to those containing the
remains of titanosaur embryos warrants the identification of these
specimens as those of titanosaurs. These eggs are subspherical,
13–15 cm in diameter, with a tuberculate surface texture and a
megaloolithid-type eggshell microstructure (Grellet-Tinner et al.,
2004).
The embryonic integument seems to be preserved as calcitic
casts (Chiappe et al., 1998), although occasional negative im-
pressions also occur. The skin is characterized by a pebbled sur-
face formed by non-overlapping tubercles. Tubercles greatly vary
in size (from less than 100 ␮m up to 800 ␮m)—they could double
in size within the span of a small-sized patch (MCF-PVPH-129,
Fig. 1.1). Six different patterns of integument are recognized on
the basis of the shape, size, and arrangement of individual tuber-
cles:
1. Ground tubercles: This is the prevailing pattern in all spec-
imens. These tubercles are subequal, pebblelike, smooth, and
1528
ranged (12–14 tubercles/mm2) and uniformly distributed (Fig.
2.
1.1).
Large, elongated tubercles: Large tubercles, almost 3 mm
long, surrounded by ground tubercles. In the only known ex-
ample (MCF-PVPH-135), more than 20 ground tubercles sur-
round a large tubercle. The surface of the latter is somewhat
inflated, with at least four slightly elevated areas. This con-
dition, and the presence of ground tubercles that partially co-
alesce with the edges of the large tubercle, suggests that the
latter consists of at least four fused tubercles, which are larger
than a typical ground tubercle (Fig. 1.2).
3. Parallel rows of large tubercles: These are stripelike arrange-
ments formed by a series of parallel rows of tubercles, with
the largest tubercles located in the central row (Fig. 1.3).
Some variation notwithstanding, this pattern is essentially
symmetrical along its main axis. Central tubercles are roughly
polygonal (pentagonal or hexagonal); their main axes are per-
pendicular to the row and the contact with the adjacent tu-
bercles is along their sides (Fig. 1.4). The adjacent rows of
tubercles on each side of the central row consist of tubercles
that are approximately half the size of the central ones. Each
of these smaller tubercles is wedged between every two large
central tubercles. In MCF-PVPH-126, the central row con-
tains tubercles that are approximately 800 ␮m across. On
each side of this row, there is a row of tubercles approxi-
mately 400 ␮m in diameter (Fig. 1.3 and 1.4). In MCF-
PVPH-686, one row of large tubercles is also flanked by par-
allel rows of smaller tubercles.
4. Rosettelike arrangement: A common pattern consisting of a
large, oval or slightly polygonal (pentagonal to hexagonal)
tubercle surrounded by smaller tubercles. These peripheral
tubercles are similar to, but slightly larger than, ground tu-
bercles. The number of peripheral tubercles varies from spec-
imen to specimen. In MCF-PVPH-130, the central tubercle
(⬃800 ␮m) is encircled by 11 tubercles (Fig. 1.5 and 1.6).
This central element is surrounded by seven tubercles in
MCF-PVPH-140 and MCF-PVPH-682, and 13 or 14 in MCF-
PVPH-135. In addition, the large tubercles of two rosettes in
MCF-PVPH-680 are encircled by 10 and 13 smaller tuber-
cles.
5. Flowerlike arrangement: Seven to eight tear-shaped tubercles
converging on a minute, central tubercle. While the central
tubercle is much smaller than the average ground tubercle,
the converging tear-shaped tubercles are 1.5–2 times the size
of typical ground tubercles. In MCF-PVPH-126, at least four
of these structures are observed associated with rosettelike
pattern (Fig. 2.1 and 2.2). Other specimens with flowerlike
arrangements include MCF-PVPH-147, 680, 681, and 686.
 PALEONTOLOGICAL NOTES 1529

FIGURE 1—Tubercle patterns in embryonic specimens from Auca Mahuevo. 1, Ground tubercles. MCF-PVPH-131; 2, large, elongated tubercles. MCF-
PVPH-135; 3, large tubercles forming parallel rows. MCF-PVPH-126; 4, close up of MCF-PVPH-126 as indicated in squared area of Fig. 1.3; 5, rosette
arrangement. MCF-PVPH-130; 6, close up of rosette arrangement shown in Fig. 1.5. Secondary electron images (1, 2, 4, 5, 6) were obtained with a SEM
Philips 515 operating at 2 kV.
1530 JOURNAL OF PALEONTOLOGY, V. 81, NO. 6, 2007

FIGURE 2—1, Flowerlike arrangements. MCF-PVPH-147, arrows point out two different Type E arrangements; 2, close up of one of the flowerlike
arrangements shown in Fig. 2.1; 3, striatelike rows. MCF-PVPH-142; 4, close up of striatedlike rows as indicated by squared sector of Fig. 2.3. All secondary
electron images were obtained with a SEM Philips 515 operating at 2 kV.

6. Striatelike rows: Parallel rows of minute, elongated tubercles
arranged in a tight formation. This pattern gives the skin a
conspicuous striated appearance. These tubercles are the
smallest observed among all available specimens. Rows are
separated by relatively deep and constricted grooves. The size
of the tubercles may vary along the same row and sometimes
tubercles appear to be fused to each other, forming long mul-
titubercle structures. Over 20 parallel rows of these tubercles
are preserved in MCF-PVPH-142 (Fig. 2.3 and 2.4).
DISCUSSION
Studies of non-avian dinosaur skin have been the focus of many
scientific contributions since the beginning of the Twentieth Cen-
tury (e.g., Osborn, 1909, 1911, 1912; Brown, 1916, 1917; Gil-
more, 1925, 1946; Sternberg, 1935; Lull and Wright, 1942) and
have continued in more recent years (e.g., Horner, 1984; Bona-
parte et al., 1990; Czerkas, 1992, 1994, 1997; Chiappe et al.,
1998; Anderson et al., 1998; Rich et al., 1999; Negro, 2001).
Skin remains of a Late Cretaceous embryonic dinosaur iden-
tified as a therizinosaurid theropod were reported by Manning et
al. (1997). This report, however, was based on small fragments
of in ovo spongy mineral materials with no resemblance to any
known dinosaur integument (e.g., they lack a tuberculate pattern)
and, as such, its identification as skin is problematic. Therefore,
Auca Mahuevo provides the only definitive evidence to date of
dinosaur embryonic skin.
As in other non-avian dinosaurs but in contrast to most non-
avian reptiles, the skin of the Auca Mahuevo embryos does not
exhibit overlapping scales. Reports of non-avian dinosaur skin
have invariably documented a tuberculate, non-imbricated pattern
 PALEONTOLOGICAL NOTES 1531

FIGURE 3—1, A skin patch with ground tubercles of a hadrosaur dinosaur from North America, LACM-17712; 2, portion of the lateral side skin of the
Gila Monster Heloderma horridum Allen, 1933, LACM 127327; 3, Rosettelike arrangement in the skin of the sauropod Tehuelchesaurus benitezii Rich,
Vichers-Rich, Giménez, Cuneo, Puerta, and Vacca, 1999 holotype MPEF-PV 1125; 4, ground tubercles in another skin patch of MPEF-PV 1125.

of scales (Fig. 3.1), which could be compared to portions of the
skin of helodermatids and chamaleontid squamates (Czerkas,
1997). For example, most of the skin of the Gila Monster (Helo-
derma horridus Allen, 1933) consists of a rather uniform pave-
ment of tubercles of different sizes without any discrete arrange-
ment (e.g., rosettes, flowerlike patterns) (Fig. 3.2)—limbs and the
ventral side of the body show a greater amount of imbricated
scales.
In the Auca Mahuevo embryos, ground tubercles cover most
of the surface of the preserved patches of skin. The remaining
patterns occur in different frequencies. The most common is the
rosettelike arrangement, a pattern found in 9% of a total of 78
studied samples. Ground tubercles notwithstanding, this pattern
was clearly more common than any other pattern. In MCF-PVPH-
131, rosettelike arrangements occur with a frequency of 2/cm2.
Other arrangements occur in a lower frequency. Among the 78
specimens collected, only two bear parallel rows of large tuber-
cles, and only one has striatelike tubercles.
Comparisons with the skin of adult sauropod dinosaurs are
hampered by the scarcity of specimens, which are limited to di-
plodocids from the Late Jurassic and Early Cretaceous of the
United States (Czerkas, 1994), an indeterminate sauropod from
the Early Cretaceous of England (Czerkas, 1994), and the basal
eusauropod Tehuelchesaurus benitezii Rich, Vickers-Rich, Gi-
ménez, Cuneo, Puerta, and Vacca, 1999 from the Late Jurassic of
Argentina (Giménez, 1996; Rich et al., 1999) (Fig. 3.3 and 3.4).
In general, the skin of these sauropods is formed by non-overlap-
ping tubercles of pentagonal, or more frequently, hexagonal out-
line. Just as in the Auca Mahuevo embryos, the patterns recorded
in these sauropods correspond to ground tubercles and rosettelike
arrangements, with the former covering most of the surface of the
preserved skin. However, several interesting differences between
the skin of these dinosaurs and that of the embryonic material
from Auca Mahuevo can be noted. One of these involves the
relative sizes of the tubercles forming rosettelike patterns. The
central tubercle of the embryonic skin (Fig. 1.6) is proportionally
much larger than those forming the rosettelike patterns of the
adult sauropod skin (Fig. 3.3). For example, in Tehuelchesaurus
Rich, Vichers-Rich, Giménez, Cuneo, Puerta, and Vacca, 1999 the
area of the rosettes central element is twice the area of the sur-
rounding tubercles (Fig. 3.3), while in the Auca Mahuevo embryo
this ratio is 3/1. Another significant difference between the skin
of Tehuelchesaurus and that of the Auca Mahuevo embryos is
the distinct graining surface of the tubercles of the former (Fig.
3.3). A similar morphology has been previously described for an
adult diplodocid from the Late Jurassic of Wyoming (Czerkas,
1532 JOURNAL OF PALEONTOLOGY, V. 81, NO. 6, 2007
1992). Whether these differences respond to ontogenic change,
integumentary diversity among sauropods—the basal eusauropod
Tehuelchesaurus is a probable remote outgroup of titanosaurs
(Wilson and Sereno, 1998)—or both, remains uncertain.
Consideration needs to be taken regarding the Late Cretaceous
titanosaur Saltasaurus loricatus Bonaparte and Powell, 1980 from
Argentina. Clusters of osteoderms found in association with skel-
etal remains of this titanosaur have been interpreted as intradermal
and compared with ossicles contained in the hide of extinct
ground sloths such as mylodontids (Powell, 2003). However, the
dermal armor of Saltasaurus Bonaparte and Powell, 1980 can be
better compared to the armor present in non-avian reptiles such
as cordylid lizards and crocodiles (Chiappe et al., 1998). In these
armored reptiles, osteoderms develop in a one-to-one correspon-
dence with scales (Romer, 1956). Thus, even if the skin of Sal-
tasaurus in not preserved, the pattern of osteoderms can be taken
as a proxy of the pattern of scales of this titanosaur. Saltasaurus
shows the typical sauropod pattern of uniform ground tubercles
(Powell, 2003). In one of the four preserved clusters (i.e., PVL-
4017-119), ground tubercles are interrupted by a much larger el-
ement, which in contrast to the rosettelike arrangements of other
sauropods, is surrounded by typical ground tubercles. Thus, Sal-
tasaurus’ osteoderms do not exhibit the diversity of patterns de-
scribed for the skin of the Auca Mahuevo embryos. Osteoderms
have been associated with only a few titanosaur remains (e.g.,
Bonaparte and Powell, 1980; Salgado and Coria, 1993; Curry-
Rogers and Forster, 2001) and the evolution of this condition—if
it evolved with the divergence of titanosaurs or multiple times
within this lineage—is as yet undocumented. Thin sections of the
Auca Mahuevo embryonic skin failed to show any indication of
bone development but this does not imply that the adults lacked
armor because extant armored reptiles develop their osteoderms
after they hatch (Chiappe et al., 1998).
The tuberculate arrangement seen in the skin of the Auca Ma-
huevo embryos displays a number of patterns previously un-
known for sauropods and suggests that the diversity of skin mor-
phologies of these dinosaurs was far greater than previously
thought.
ACKNOWLEDGMENTS
We are grateful to the many people who participated in the Auca Mahuevo
expeditions between 1997 and 2002. We also thank E. Ruigómez (MEF) and
R. Feeney (LACM) for access to specimens under their care, M. Alegria
(MCF) for microscope searching, and W. Evans (LACM) for editing the man-
uscript. To A. Caneiro and C. Cotaro from the Caracterización de Materiales
group of the Centro Atómico Bariloche for giving access to the scanning
electron microscope. D. M. Martill and L. Salgado reviewed the manuscript
and their comments are greatly appreciated. This research was funded by the
Fundación Antorchas, the Infoquest Foundation, the Municipalidad de Plaza
Huincul, and the National Geographic Society.
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