949

Eggs of titanosaurid sauropods from the Upper

Cretaceous of Auca Mahuevo (Argentina)
Gerald Grellet-Tinner, Luis M. Chiappe, and R. Coria

Abstract: We provide a detailed description of the sauropod eggs from the Late Cretaceous nesting site of Auca
Mahuevo (Neuquén Province, Argentina), the only eggs that are unequivocally associated with titanosaurid dinosaurs.
These eggs are subspherical averaging 132 by 115 mm. Well-preserved specimens display a pronounced eggshell
ornamentation that consists mostly of single nodes averaging 0.58 mm in diameter and 0.28 mm in height (base to
apex) with internodular values of 0.52 to 0.87 mm. The pore canal network consists of vertical and horizontal canals
intersecting at the bases of eggshell units. Vertical canals may fork defining a “Y” pattern and their diameters vary
between 0.08 and 0.2 mm. Their surficial apertures of 0.15 to 0.29 mm are funnel like and located between the
surficial nodes. In pristine specimens, the eggshell thickness equals 1.31 mm, and radial sections exhibit a single structural
horizontal layer composed of juxtaposed shell units consisting of acicular calcite crystals radiating from an organic
core. Relying only on taxonomically identified oological material, we regard this character also shared in the innermost
layer (layer 1) of Deinonychus antirrhopus, oviraptorid theropods, and observed during an early oogenetic stage in
extant bird as primitive for saurischians. The eggshell morphology advocates that these eggs were likely incubated in
moist nesting environments, perhaps such as nests covered with vegetal matter. Examination of the South American
megaloolithid eggshells reveals that the titanosaurid eggs from Auca Mahuevo are mostly similar to those described as
Megaloolithus patagonicus and Megaloolithus pseudomamillare.

Résumé : Nous fournissons une description détaillée d’œufs de sauropodes du site de nidification (Crétacé tardif)
d’Auca Mahuevo (Province de Neuguén, Argentine), les seuls œufs qui sont sans équivoque associés aux dinosaures
Titanosauridés. Ces œufs sont sous-sphériques et mesurent en moyenne 132 mm sur 115 mm. Des spécimens bien
conservés montrent une ornementation prononcée sur la coquille qui consiste surtout en des nodes individuels ayant en
moyenne un diamètre de 0,58 mm et une hauteur de 0,28 mm (de la base au sommet) ainsi que des valeurs internodulaires
de 0,52 à 0,87 mm. Le réseau de canaux de pores comprend des canaux verticaux et horizontaux qui se recoupent aux
bases des unités de coquilles. Les canaux verticaux peuvent se ramifier, définissant un patron en Y, et leur diamètre
varie entre 0,08 et 0,2 mm. Les ouvertures de surface de 0,15 à 0,29 mm sont en forme d’entonnoir et elles sont situées
entre les nodes de surface. Dans les spécimens parfaits, l’épaisseur de la coquille est de 1,31 mm et des sections radiales
laissent voir une couche structurale horizontale unique composée d’unités de coquilles accolées comprenant des cristaux
de calcite aciculaires rayonnant d’un noyau organique. En se basant uniquement sur le matériel oologique identifié de
façon taxonomique, nous considérons que ce caractère se retrouve aussi dans la partie la plus intérieure (couche 1) de
Deinonychus antirrhopus, des théropodes oviraptoridés, et observé durant un stage ovarien précoce d’un oiseau historique
comme étant primitif chez les saurichiens. La morphologie de la coquille fait valoir le fait que ces œufs ont probablement
été incubés dans des environnements humides, peut-être dans des nids recouverts de matière végétale. L’examen des
coquilles de Mégaloolithidés sud-américains montrent que les œufs de Titanosauridés provenant d’Auca Mahuevo sont
surtout semblables à ceux décrits comme Megaloolithus patagonicus et Megaloolithus pseudomamillare.

[Traduit par la Rédaction] Grellet-Tinner et al. 960

Introduction Auca Mahuevo, in Argentina (Neuquén Province, northwestern

Patagonia), a site contained within the Late Cretaceous Anacleto
Formation (early Campanian; see Dingus et al. 2000), where
Dinosaur localities preserving embryonic remains inside skeletal remains and skin casts are abundant (Chiappe et al.
eggs are extremely rare (embryo in ovo). An exception is 1998, 1999, 2000, 2001a).

Received 6 February 2004. Accepted 2 June 2004. Published on the NRC Research Press Web site at http://cjes.nrc.ca on
11 August 2004.
Paper handled by Associate Editor H.-D. Sues.
G. Grellet-Tinner1,2 and L.M. Chiappe. Department of Vertebrate Paleontology, Natural History Museum of Los Angeles County,
900 Exposition Boulevard, Los Angeles, CA 90007, USA.
R. Coria. Dirección Provincial de Cultura, Museo Carmen Funes, Av. Cordoba 55, Plaza Huincul, Neuquén 8318, Argentina.
1
Present address: Department of Earth Sciences, University of Southern California, Los Angeles, CA 90089-0740, USA.
2
Corresponding author: (e-mail address: ggrellet@nhm.org).

Can. J. Earth Sci. 41: 949–960 (2004) doi: 10.1139/E04-049 © 2004 NRC Canada
950
The initial study of the Auca Mahuevo embryos in ovo
(Chiappe et al. 1998) documented several cranial characters
diagnostic of Neosauropoda, a cosmopolitan group of sauropod
dinosaurs comprising the common ancestor of Diplodocus
and Saltasaurus plus all its descendants (Wilson and Sereno
1998). This study provides only a brief description of the
eggshell structure, identifying it as Megaloolithidae, a diverse
parataxonomic group (Sahni et al. 1994; Vianey-Liaud et al.
1994; Bravo et al. 2000; Magalhães Ribeiro 2000; Mohabey
2000). Recently, Chiappe et al. (2001) reported on several
new eggs containing nearly complete embryonic skulls. The
cranial morphology of these embryos allowed fine-tuning of
the initial identification as those of titanosaurids, a subgroup
of neosauropod dinosaurs. Despite the fact that megaloolithid
eggs have been often identified as those of sauropods (Powell
1992; Faccio 1994; Sahni et al. 1994; Vianey-Liaud et al.
1994; Calvo et al. 1997; Bravo et al. 2000; Cousin and
Breton 2000; Magalhães Ribeiro 2000; Mohabey 2000; Peitz
2000), the Auca Mahuevo eggs are the only ones identified
on the basis of skeletal remains in ovo. In this paper, we pro-
vide a detail description of the shell structure and variation of
the titanosaurid eggs from Auca Mahuevo based on five eggs
that contain diagnostic embryonic skulls (Chiappe et al.
2001). Furthermore, we compare the morphology of these
eggs and eggshell with that of other South American Late
Cretaceous eggs alleged to be also of titanosaurid neo-
sauropods.
Abbreviations
Institutions
LACM, Natural History Museum of Los Angeles County,
USA; MCF-PVPH, Museo Carmen Funes, Plaza Huincul,
Argentina; MUCPV, Museo de Geología y Paleontología,
Universidad Nacional del Comahue, Neuquén, Argentina.
Technical terms
SEM, scanning electron microscope; MT, membrana testacea.
Material and methods
The studied eggs (MCF-PVPH 147, 250, 262, 263, 264)
and eggshells (MCF-PVPH 442, 445, 444) were recovered
from a quarry contained within Auca Mahueo’s egg-bed 3,
one of the four egg layers previously recognised within the
stratigraphic section of this locality (Chiappe et al. 2000).
These eggs were part of what were considered clutches during
the excavation process, and efforts were made to unearth and
preserve the entirety of these assemblages. The selected eggs
(MCF-PVPH 147, 250, 262, 263, 264) were further prepared
and their cranial skeletal content was recently described and
published (Chiappe et al. 2001). The studied eggshell fragments
(one or two samples) were removed during the preparation
of these embryos. Radial sections were examined to observe
the crystallographic arrangement of the eggshell units, the
shape of pore canals, presence and geometry of spherulites,
and the surficial ornamentation of the eggshell.
Eggshells used for SEM imaging were washed and dried,
then broken to obtain a fresh radial fracture, then glued
slightly tilted on an aluminum stub with its freshly broken
radial side upwards. This setting not only permits cross sectional
but also partial tangential observations. Adobe Photoshop
Can. J. Earth Sci. Vol. 41, 2004
software (version 5.5, R) was used to digitally capture, crop,
and enhance images and to measure designated features by
comparing the number of pixels between a digitally embedded
scale bar and the observed structure. Only mean values were
recorded when multiple measurements were taken.
Description
MCF-PVPH 147, 250, 262, 263, 264 displayed the same
spherical to subspherical general shape as other preserved
eggs from Auca Mahuevo egg-bed 3 (Fig. 1A). They show
signs of fractures and various degrees of compression (Fig. 1B),
interpreted as the result of sedimentary compaction. It is
worth mentioning that mini slickenslides are visible at the
quarry site vertically displacing some eggs. Eggs located at,
or close to a vertical displacement horizon are distorted in
the same direction as that of the displacement, thus demon-
strating a certain amount of plasticity. Two diameters of the
eggs were measured. The greatest diameter range between
125 and 140 mm, the smallest diameter is 10%–20% smaller.
However, these two diameters might be slightly underestimated
according to the degree of preservation and compaction.
Eggshell samples were taken from stacks of eggshell frag-
ments (arragement resulting from taphonomic processes)
randomly assorted in multiple layers surrounding the embryonic
skulls (Fig. 1C). These samples display a tremendous diagenetic
variation, manifesting itself by the calcite dissolution from
the internal structure of the eggshell, the pore canals and
apertures, as well as the outer eggshell surface. Calcium car-
bonate after being mobilized was re-deposited within the
pore canals in the form of two very distinct crystal shapes,
but both belonging to the rhombohedric form (Figs. 2A, 2B).
The outer eggshell surface displays nodes visible to the naked
eye, with some of them coalescing into a longer structure
(Fig. 1D). However, MCF-PVPH 250’s nodular surficial
ornamentation is totally flattened leaving only a rough and
pitted appearance (Fig. 2C). MCF-PVPH 262 displays a similar
chemical weathering to that of MCF-PVPH 250, but its eggshell
surface still displays an undulatory appearance, representing
remnants of preexisting nodes (Fig. 2D). MCF-PVPH 147
suffers from a similar alteration, although to a lesser degree.
In this specimen, only the apex of the nodes are affected,
displaying a concave appearance (Fig. 2E). The dissolution
of MCF-PVPH 263 is limited to a moderate pitting of the
surficial nodes (Fig. 2F). MCF-PVPH 264 is the best preserved
of all the samples and shows no surficial alteration (Fig. 3A).
In MCF-PVPH 264 and 263, the average diameter of the
nodes equals 0.58 mm and the average nodular height measured
from the base to the apex is 0.28 mm. Due to biases of
observation, nodes that coalesce were not observed in SEM
images, but only in light microscopy (Fig. 1D). It seems that
the width of these tubercles, however, does not exceed that
of a single node. The few internodular measurements
performed on MCF-PVPH 263 and 264 range from 0.52 to
0.87 mm.
The eggshell thickness of the studied specimens varies ac-
cording to the degree of diagenesis they have been submitted
to. MCF-PVPH 147’s thickness averages only 0.65 mm;
MCF-PVPH 250, 0.73mm; MCF-PVPH 262, 0.82 mm;
MCF-PVPH 263 and 264 have the same value of 1.31 mm.
© 2004 NRC Canada
Grellet-Tinner et al. 951

Fig. 1. (A). Egg clutch recovered from the quarry site in egg-bed 3 (LACM 149648). (B) Detail of Fig. 1. Note the subspheric aspect
of these eggs (LACM 149648). (C) Embryonic remais in ovo (MCF-PVPH 147). (D) Eggshell surface with single and coalescent nodes
(MCF-PVPH 442). Scale on the side (in mm).

© 2004 NRC Canada

952 Can. J. Earth Sci. Vol. 41, 2004

Fig. 2. (A) Diagenetic calcite infilling in and at the base of pore canals of MCF-PVPH 262. (B) Diagenetic rhombohedric calcite crystals
infilling in and at the base of pore canals of MCF-PVPH 147. (C) The eggshell outer surface of MCF-PVPH 250 displays an extreme
weathering (scaling) from purely chemical or, as suggested in another publication, of biochemical origin. (D) MCF-PVPH 262, same as
MCF-PVPH 250 but not as altered. Pore orifices can still be observed (arrow). (E) Eggshell outer surface of MCF-PVPH 147 with
moderate weathering. The nodular ornamentation although pitted (arrow) is clearly visible. (F). Pristine surficial ornamentation of
MCF-PVPH 263. However, note the infilling of the pore channel by secondary calcite deposits (arrow).

© 2004 NRC Canada

Grellet-Tinner et al. 953

Fig. 3. (A) Pristine surficial ornamentation of MCF-PVPH 264 and no secondary calcite deposits in pore canal. (B) Thin section of
MCF-PVPH 445. The membrana testacea (arrows) forms a fibrous mat underlaying the eggshell units. (C) Calcite crystals radiate from
a nucleation center (arrow), also called organic core, at the base of each egghsell unit (MCF-PVPH 263). (D) Detail view of a nucleation
center (MCF-PVPH 263). (E) Rhombohedric acicular calcite crystals in eggshell units (MCF-PVPH 263). (F) The fabric of each shell
unit only consists of fine acicular radiating acicular calcite crystals (MCF-PVPH 263).

In radial section, the eggshell is composed of a single structural membrana testacea (MT) (Fig. 3C). The core of MCF-PVPH
layer consisting of acicular calcitic crystals radiating from 263 measures 0.034 mm at its widest diameter (Fig. 3D),
nucleation centers (former organic cores) located above the and as observed in MCF-PVPH 444, the core is located

© 2004 NRC Canada

954
0.19 mm above the MT (Fig. 3B). The calcite crystals in
specimens MCF-PVPH 263 and 264 are particularly devoid
of pitting caused by acidification during the fossilization
process. Close observation of these specimens at high mag-
nification reveals that the crystals radiating from the core are
of rhombohedric form (Grellet-Tinner 2000). The diameter
of the rhombohedrons proximal to the core averages 0.004 mm
(Fig. 3E), and each crystal is subdivided in four long coales-
cent smaller crystals (Fig. 3F). The regular grouping of all
the acicular crystals radiating out of any given core and their
vertical extension define the eggshell unit and the thickness
of the eggshell. Unless they coalesce one another, each of
these eggshell units forms a round node at the outer eggshell
surface.
Eggshell units are best observable in MCF-PVPH 263 and
264 (Figs. 2F, 3A, 3B) and their geometry is best seen when
radial sections cut through their center. Beginning at the inner
surface, the units flare out at - 40° from both sides of the
vertical axis of the core. As they reach a third of the total
eggshell thickness (Figs. 2F, 3A, B), their lateral margins
still flare out but to a lesser degree, thus appearing nearly
parallel in some instances. The maximum width of any given
eggshell unit can only be obtained if the cut of a thin section
or the break of an SEM sample is centered at the sagital
plan. The measured width of MCF-PVPH 264 (Fig. 3A) is
close to 0.63 mm. This is congruent with the measurement
of one of the eggshell units in a thin section of a sample of
MCF-PVPH 444 (Fig. 3B). The apparent change of obliquicity
in the geometry of the eggshell units results from the pres-
ence of a network of horizontal pore canals, connected to the
vertical pores, that develops at the base of the eggshell units.
This network is particularly evident (Fig. 4A) when the MT
is preserved in situ. It is the development of such a network
that gives each eggshell unit the appearance of a massive pillar
separated by horizontal canals from that the adjacent units
(Fig. 4B).
Thin sections reveal that the eggshell units are trans-
versally crossed by thin and compact growth lines (Fig. 3B).
These lines are slightly convex at the base of the eggshell
unit following the primary radiation of the acicular crystals
from the core. They progressively flatten higher up in the
eggshell units and become horizontal. Once at the level of
the apex of the cavity created by the network of horizontal
canals, the growth lines more frequently cut through adjacent
eggshell units, thus becoming continuous across them. This
condition becomes the norm closer to the outer surface of
the eggshell.
The overall pore-canal network consists of vertical and
horizontal canals intersecting on a one-to-one basis at and
between the base of each eggshell unit (Fig. 4A). Mostly, the
vertical section of these pores is straight, although they some-
time diverge forming a Y pattern (Fig. 4A). The diameters of
the vertical canals are not precisely measurable in these speci-
mens because of the fracture orientation of the eggshells.
Nevertheless, it is possible to determine that their minimum
width is 0.08 mm — as previously observed by Chiappe et
al. (1998) — in MCF-PVPH 262 and that they do not exceed
the maximum diameter of 0.2 mm. As they reach the eggshell
surface, pore canals are funnel-shaped (Figs. 4C, 4D), creating
round depressions between the surficial nodes. In the studied
Can. J. Earth Sci. Vol. 41, 2004
specimens, the diameters of pore apertures vary from 0.15 to
0.29 mm.
The innertips of the eggshell units are particularly visible
in MCF-PVPH 263 (Fig. 4E). Contrary to expectations, they
do not display a typical concave appearance resulting from
the calcium absorption by a developing embryo, but rather
exhibit a perfect conic shape. In extant birds, calcium car-
bonate dissolution takes place on the innertips of the shell
units (mammillary cones) during embryogenesis by a process
where the carbonic acid results from the CO2 exhaled by the
breathing embryo. The lack of calcium resorption coupled
with the presence of a well-developed skull in MCF-PVPH- 263
suggests that calcium utilization from the eggshell by the
titanosaurid embryo must have happened at a later ontogenic
stage than that observed in modern birds.
Discussion
Taphonomic considerations
As noted in the precedingdescription, the recovered eggs
are mostly subspherical, a shape that could be either charac-
teristic of this oospecies or the result of post-burial com-
pression forces. Experimentation on recent eggs, however,
suggests that the latter is probably the case. Hayward et al.
(2000) documented that when chicken (Gallus gallus) eggs
are buried in sand under controlled environments and sub-
mitted to a compressive force of 700 kg, fresh and hollow
(blown) eggs were compressed to 85% and 82.1%, respec-
tively, of their original shape. It is possible that egg resis-
tance to high compressive pressures be correlated to the
number of structural layers in a given eggshell. Studies on
mollusk shells have documented an increased resistance to
pressure as the shell accumulates more structural layers, par-
ticularly when the internal crystallization varies in direction
from layer to layer (Kamat et al. 2000). The presence of
structural multilayered shells in birds, as well as in other
theropod dinosaurs (see Grellet-Tinner 2001; Grellet-Tinner
and Chiappe 2004; Grellet-Tinner and Norell 2002), suggests
that theropod eggshells may be more resistant to pressure
than the single structural layer of titanosaurid and other non-
theropod dinosaur eggs. If seemingly more resistant eggshells,
such as those of Gallus gallus, were significantly compressed
by sedimentary compaction, it is likely that the difference
between the two diameters observed in each of the studied
titanosaurid eggs, with only one eggshell structural layer,
also results from compressive burial forces.
Diagenetic variation greatly varies among the examined
eggshell fragments and is visible to the naked eye by the
amount of recrystallized calcite. At times, this secondary
calcite crystallization forms a white layer underlaying the
innerside of the eggshell. Examination with increasing mag-
nification of the samples reveals the degree of diagenesis to
which MCF-PVPH 147, 250, 262, 263, 264 were submitted.
The surface pitting of MCF-PVPH 147, 262, 263 can be
attributed to acid erosion, a process reported and described
particularly by Hirsch and Lopez-Jurado (1987) and Hayward
et al. (1991). As previously observed with other archosaur
eggshell (Kohring 1999) in Auca Mahuevo, the mobilized
calcium carbonate from the outermost part of the eggshells
was precipitated into the pore system (Figs. 3E, 3F) and on
© 2004 NRC Canada
Grellet-Tinner et al. 955

Fig. 4. (A) Total view of the radial section of a titanosaurid eggshell. Note the network of vertical and horizontal pore channels. Each
eggshell unit forms a massive pillar (upper arrows) at its base delineating horizontal pore canals. Note the node on the outer eggshell
surface surrounded by three pore apertures and the two branches (lower arrows) of a pore canal, one ending at the aperture
(MCF-PVPH 444). (B) View of the junction of the base of three eggshell units with a poorly preserved membrana testacea (arrow)
showing the horizontal network of pore canals infilled with secondary calcite (MCF-PVPH 444). (C) Detail of two pore apertures at
the base of a node on an outer eggshell surface (MCF-PVPH 444). (D) Detailed view of the circular, cup-like shape of a pore aperture
(MCF-PVPH 444). (E) View of the inner eggshell surface. Note the base of many eggshell units (MCF-PVPH 263).

© 2004 NRC Canada

956
the MT (Grellet-Tinner in press). Whether these weathering
and precipitation processes in Auca Mahuevo are the result
of chemical factors or from biotic mediation is still unclear
but experimental investigations (Hayward et al. 1997) and
previous reports advocate a biological activity (Kohring 1999;
Grellet-Tinner in press).
Paleoecologic and paleobiologic considerations
Pore canals assure the diffusion of gases and water vapor
through the eggshell (Paganelli 1980). Their size, geometry,
and number reflect a specialization to the habitat where nesting
occurs (Williams et al. 1984; Cousin and Breton 2000).
Williams et al. (1984) described 12 megaloothid eggs that
they labeled as “Type 31” from the Late Maastrichtian of
France, with a pore system matching in size, shape, and
geometry those of Auca Mahuevo eggs. According to these
authors, these French eggs would have a vapor conductance
equal to 24 times the calculated values for avian eggs.
Independent studies (Packard et al. 1979) have also shown
that hard-shelled eggs of extant non-avian reptiles deposited
in high moisture environments have vapor conductances from
2 to 5.5 times higher than those of avian eggs. In light of
this, Williams et al.’s (1984) conclusion that the French Late
Cretaceous megaloolithid eggs were incubated in high moisture
conditions seems reasonable, and such a conclusion could be
extended to the titanosaurid eggs from Auca Mahuevo, on
the basis of similarities of the pore system. This interpretation
would thus suggest the presence of high moisture content in
the Auca Mahuevo titanosaurid nests.
Other characteristics of eggshells that have been used to
infer the paleoenvironmental context of dinosaur eggs include
the surficial ornamentation. Cousin and Breton (2000) used
the characteristics of the nodular appearance of eggshell from
the Late Cretaceous of France as an indicator of the sub-
strate or nesting material surrounding the eggs. The nodular
surface of the titanosaurid eggs from Auca Mahuevo could
be interpreted as a specialization to facilitate gas and water
vapor conductance through the pores that are located around
and at the base of each node, by avoiding nesting debris
plugging their apertures (e.g., Sabath 1991). Following this
assumption, it is reasonable to hypothesize that to achieve
maximum efficiency in facilitating gas and water vapor con-
ductance, the internodular distance should be less than the
size of the nesting material, otherwise the pores would be
plugged. Multiple measurements taken from eggshell fragments
not suffering from diagenetic or taphonomic alterations show
that the internodular distance of the Auca Mahuevo eggs
varies from 0.6 to 1.6 mm. This observed variation seems
important, but each eggshell fragment has itself a nearly
constant internodular value. Notwithstanding these caveats,
these internodular values suggest that the nesting material
should optimally exceed 0.6 mm in size. The silicoclastic
sediments at the Auca Mahuevo site are smaller than the
minimal required internodal size for the pores to be func-
tional, and therefore it is feasible to speculate that the Auca
Mahuevo nests could have been lined and covered by vege-
tation. This interpretation seems to be supported by the
recent discovery of carbon remains, presumably of plants,
found inside some the nesting depression excavated by Auca
Mahuevo titanosaurids (Chiappe et al. 2004). This nesting
type has however already been suggested by Cousin (1997)
Can. J. Earth Sci. Vol. 41, 2004
for comparable eggs found at the nesting site of Rennes-
Le-Chateau (France) and Cousin and Breton (2000), Erben
(1970), and by Kérourio (1981) for the megaloolithid eggs
found at l’Arc (France).
Comparison with other South American putative
titanosaurid oospecies
Numerous South American isolated eggshell fragments and
complete eggs with various degrees of diagenetic alterations
have been referred to the megaloolithid parataxonomic group.
Among those, some have been alledged to be laid by titano-
saurid dinosaurs (e.g., Erben 1970; Powell 1992; Sahni et al.
1994; Faccio 1994; Moratalla and Powell 1994; Vianey-Liaud
et al. 1994, 1997; Calvo et al. 1997), although the lack of
diagnostic embryonic remains in ovo made each of these
taxonomic identifications unreliable. The Auca Mahuevo eggs
provide the opportunity of comparing the morphology of
unquestionable titanosaurid eggs with that of eggs alleged to
belong to this dinosaur group. A brief summary of these
comparisons is given in the following text.
Calvo et al. (1997) reported a partial egg (MUCPv-245)
and three crushed eggs (MUCPv-246) from rocks of the Late
Cretaceous (early Campanian; see Dingus et al. 2000)
Anacleto Formation in the vicinity of Neuquén, the same
stratigraphic unit that contains Auca Mahuevo although located
some 200 km towards the southeast. In most respects, the
Auca Mahuevo eggs are remarkably identical to those de-
scribed as Megaloolithus patagonicus by Calvo et al. (1997)
(Table 1). This similarity includes the surficial ornamentation,
pore diameter, pattern of growth lines within the eggshell
unit, and the apparent presence of a horizontal canal network.
The only noticeable differences involve the diameter of the
eggs, which is slightly larger in the Neuquén eggs (160 mm),
and a thicker eggshell 1.7–2.1 mm according to Calvo et al.
(1997). Differences in diameter, however, could be easily
explained by a greater degree of compaction of the Auca
Mahuevo eggs or as differences in value estimation since
none of the eggs reported by Calvo et al. (1997) is whole.
Faccio (1994) reported the presence of 27 spherical eggs
from the Mercedes Formation (Senonian) in Soriano
(Uruguay). The eggs were found with intact lower halves,
and upper halves reduced to fragments orientated concave
up at the bottom of the eggs, a taphanomy suggesting the
embryos hatched before burial, creating what is referred to
as a hatching window in the eggs (Breton et al. 1986; Faccio
1994). The diameter of these eggs range between 170 and
200 mm and their eggshell thickness varies from 2.5 to
5 mm, although in most samples, it is close to 5 mm (Table 1).
These values, much greater than those of the Auca Mahuevo
eggs, easily distinguish the eggs of the Mercedes Formation.
In addition, the Mercedes Formation eggs display a nodular
surficial ornamentation, in which nodes are 75% higher than
those from Auca Mahuevo. Pores in the Uruguayan eggs are
far more numerous and differ from those of the Auca Mahuevo
eggs by their shape and ramification pattern. Although Faccio
(1994) mentions the existence of two structural layers in the
eggshell of the Mercedes Formation eggs, close examination
of the published SEM images questions such a condition.
The eggs from the Mercedes Formation differ in many
characters from those of Auca Mahuevo and could hardly be
associated with the same dinosaur species.
© 2004 NRC Canada

Table 1. Comparison of eggs and eggshell characters among five sites in South America putatively associated with titanosaurid dinosaurs.
Location, authors:
Egg shape
Egg greater diameter
Egg smaller diameter
Eggshell thickness
Ornamentation (morphology)
Ornamentation (size)
Pore canal (morphology)
Pore canal (size)
Pore aperture (morphology)
Internodular space
Pore aperture size
Number of layers
Layer 1 (morphology)
Layer 1
(size)
Core location
Core size
Eggshell units (morphology)
Eggshell units (thin section)
Note: //, parallel.
© 2004 NRC Canada
Grellet-Tinner et al.
Neuquem, Calvo et al. Laguna Mayo, Sige
Auca Mahuevo, this paper 1997 Soriano, Faccio 1994 Salitral Moreno, Powel 1992 1968
Spherical to subspherical Spherical to subspherical Spherical Spherical ?
12.5–14 cm 16 cm 17–20 cm 15–23.5 cm ?
10%–20% smaller ? ? ? ?
0.6–1.31mm pristine 1.7–2.1 mm 2.5–5 mm, mostly 5 mm 5 mm and 1 mm 0.81–1.44 mm
1.31mm
Nodular: single nodes and Nodular: single nodes and Nodular: single nodes Nodular: single nodes and Nodular: single nodes
coalesecent nodes coalesecent nodes and coalesecent nodes coalesecent nodes smooth shell and coalesecent
nodes
Ø = 0.58 mm, H = Ø = 0.5–0.9 mm H = 0.8–1.3 mm ? ?
0.28mm
Straight or Y shape Straight Straight and ? Straight
multicanicular
Ø = 0.08–0.2 mm Ø = 0.07–0.110 mm ? ? ?
Round and funnel shape ? ? ? Round-elleptical and
funnel shape
0.52–0.87 mm ? ? ? ?
0.15–.029 mm ? 0.3–0.4 mm ? ?
1 1 2 ? 1
Acicular Acicular Microfibrous ? Acicular
1.31 mm 1.7–2.1 mm? ? ? 0.81–1.44 mm
0.19 mm above MT 0.19 mm above MT ? ? ?
0.034 mm 0.35 mm?? 0.39–0.64 mm ? ?
40° flare up to 30% of nearly // ? ? ?
height to nearly //
Convex growth lines to Convex growth lines to ? ? Convex growth lines
flat higher flat higher to flat higher
957
958
Powell (1992) briefly reported eggs found in two strati-
graphic layers of the Allen Formation in the locality of
Salitral Moreno, Río Negro Province (Argentina), that he
identified as those of titanosaurids. Published SEM images
and Powell’s (1992) succinct description indicates that two
types of eggshell structures are present among the studied
samples from this locality. Both egg types exhibit a nodular
surficial ornamentation and diameters ranging from 150 to
235 mm (Table 1). Yet, while one type has eggshell thickness
values of 5 mm and structural organization similar to the
eggs from the Mercedes Formation of Uruguay, the thickness
of the other type of eggshell measures only 1 mm. According
to Powell (1992), the latter type of eggshell can be subdivided
into three different morphotypes on the basis of their surficial
ornamentation, which varies from simple nodes to coalescent
nodes to a smooth eggshell. The limited information provided
by Powell (1992) hampers further comparisons with the Auca
Mahuevo eggs.
Sigé (1968) reported dinosaur eggshell material from the
Late Cretaceous Formation at Laguna Umayo, a site near the
Peruvian town of Puno. More material from that locality was
collected and described by Kérourio and Sigé (1984). Even
though no dinosaurian remains were directly associated with
the eggshell, Vianey-Liaud et al. (1997) re-evaluated 21 egg-
shell fragments (HEC 380–1, 381–1, 382–1, and 433) from
this site and assigned them to the oospecies Megaloolithus
pseudomamillare, an oologic species traditionally related to
titanosaurids. The thickness of these samples varies from
0.81 to 1.44 mm according to their degree of weathering
(Table 1). Surficial sculpting shows single nodes and other
nodes that coalesce into longer tubercles. The straight narrow
pores open at the surface creating a funnel-shape depression.
No other detailed description is supplied, but SEM and thin
section images provided in the 1997 publication coupled
with the brief structural description lead to the interpretation
that these Peruvian eggshells could be similar to those from
Auca Mahuevo and perhaps be associated with titanosaurs.
Conclusion
The abundance of eggs and eggshells in Auca Mahuevo
provide an unique opportunity to assess the variation of many
oological characters, whether these variations are the product
of taphonomic or diagenetic processes. The tremendous
variations observed in the eggshell thickness and surficial
ornamentation are sufficient to warrant against the erection
of new parataxonomic oological species without prior extensive
and thorough sampling of the material. Eggs and their egg-
shells are excellent indicators reflecting the paleobiological
conditions where they were laid and incubated. We can infer
from the internal and surficial eggshell structures of the
titanosaurid eggs that dinosaurs in Auca Mahuevo may have
laid and incubated their eggs in nests covered with vegetal
mounds creating an elevated moisture content nesting habitat
adapted to these eggs, a nesting habitat already proposed for
French eggs of similar structure and supported by recent
independent observations in one of the Auca Mahuevo nests
(N6).
Auca Mahuevo eggs and their eggshells, in association
with identifiable embryos in ovo, allow us to add to the skeletal
phylogenetic characters of titanosaurid dinosaurs the following
Can. J. Earth Sci. Vol. 41, 2004
oological synapomorphies: subspherical eggs with a greater
diameter of 12.5 to 14 cm; eggshell ornamentation, consisting
mostly of single but also coalescent hemispheric nodes of
0.58 by 0.28 mm; and funnel-shaped pore aperture, in between
nodes, that are connected to straight or Y-shaped vertical
pore canals transecting the entire eggshell thickness. Further-
more, each of these vertical canals coincide with a horizontal
conterpart of equivalent diameter. The eggshell thickness,
although varying according to the degree of diagenesis,
averages 1.31 mm for well-preserved eggs and is composed
of one single structural layer in contrast to two layers for
derived non-avian maniraptors and three to four layers for
extant bird taxa. The acicular calcitic crystallization observed
in the eggshell structure is also present in layer 1 of some
non-avian (well associated and identified) maniraptor eggs
but absent in this structural layer of extant bird eggshell.
However, developemental studies have shown that the primary
state of bladed-calcite crystals in modern birds has an acicular
state that transforms into the bladed morph during oogenesis.
These combined observation advocate that acicular calcite
crytals seen in the eggshell microstructure of titanosaurid
eggs is synapomorphic for Saurischia.
Considering the character list associated with the titanosaurid
eggs of Auca Mahuevo and comparing those with puplished
descriptions of unassociated oological material in South America
putatively assigned to this group of dinosaurs, leads to the
conclusion that presently only the oological material from
Neuquem (Megaloolithus patagonicus) and that from Peru
(M. pseudomamillare) are related to titanosaurid dinosaurs.
Acknowledgments
Fieldwork and laboratory work was supported by grants
from the Infoquest Foundation, Jurassic Foundation, the Geo-
logical Society of America, and the Department of Earth
Sciences of the University of Southern California to G. Grellet-
Tinner; the National Geographic Society and Antorchas
Foundation to L. Chiappe; and the Municipalidad de Plaza
Huincul to R. Coria. We are especially grateful to Frank
Corsetti for his insightful comments and the use of his car-
bonate laboratory (USC, Department of Earth Sciences,
Austin, Texas). SEM work was conducted at the Department
of Geological Sciences of the University of Texas. Finally,
this manuscript benefited from helpful reviews by E. Bray
and R. Kohring.
References
Bravo, A.M., Moratalla, J.J.,. Santafe, J.V., and De Santisteban, C.
2000. Faidella, a new Upper Cretaceous nesting site from the
Tremp basin (Lérida Province, Spain). In 1st International
symposium on dinosaur eggs and babies. Edited by A.M. Bravo
and T. Reyes. Isona I Conca Dellà Catalonia, Spain, pp. 15–22.
Breton, G., Fourniet, R., and Watté, J.-P. 1986. Le lieu de ponte de
dinosaures de Rennes-le-Chateau (Aude): Premiers résultats de
la campagne de fouilles 1984. Annales du Museum du Havre,
Vol. 32, pp. 1–13.
Calvo, J.O., Engelland, S., Heredia, S.E., and Salgado, L. 1997.
First record of dinosaur eggshells (? Sauropoda–Megaloolithidae)
from Neuquém, Patagonia, Argentina. GAIA, 14: 23–32.
Chiappe, L.M., and Dingus, L. 2001. Walking on Eggs: the Aston-
© 2004 NRC Canada
Grellet-Tinner et al.
ishing Discovery of Thousands of Dinosaur Eggs in the Bad-
lands of Patagonia, Scribner, New York.
Chiappe, L.M., Coria, R.A., Dingus, L., Jackson, F., Chinsamy, A.,
and Fox, M. 1998. Sauropod dinosaur embryos from the Late
Cretaceous of Patagonia. Nature (London), 396: 258–261.
Chiappe, L.M., Dingus, L., Jackson, F., Grellet-Tinner, G., and
Coria, R. 1999. Auca Mahuevo, an extraordinary dinosaur nesting
ground from the Late Cretaceous of Patagonia. Journal of Vertebrate
Paleontology, 19(3, Supplement): 37A.
Chiappe, L.M., Dingus, L. Jackson, F., Grellet-Tinner, G., Aspinal,
R., Clark, J., Coria, R., Garrido, A., and Loope, D. 2000. Sauropod
eggs and embryos from the Late Cretaceous of Patagonia. In 1st
International symposium on dinosaur eggs and babies. Edited by
A.M. Bravo and T. Reyes. Isona I Conca Dellà Catalonia, Spain,
pp. 23–29.
Chiappe, L.M., Salgado, L., and Coria, R.A. 2001. Embryonic
skulls of titanosaur sauropod dinosaurs. Science (Washington,
D.C.), 293: 2444–2446.
Chiappe, L.M., Schmitt, J.G., Jackson, F.D., Garrido, A., Dingus, L.,
and Grellet-Tinner, G. 2004. Sedimentary criteria for recognition
of dinosaur nesting traces. Palaios, 19: 89–95.
Cousin, R. 1997. Les gisements d’oeufs de dinosauriens des Hautes
Corbières et des Corbières Orientales (Aude): Ponte, nidification,
microstructre des coquilles. Bulletin de la Société d’Études
Scientifiques de l’Aude, XCVII: 29–46.
Cousin, R., and Breton, G. 2000. A precise and complete excavation
is necessary to demonstrate a dinosaur clutch structure. In 1st
International symposium on dinosaur eggs and babies. Edited by
A.M. Bravo and T. Reyes. Isona I Conca Dellà Catalonia, Spain,
pp. 31–42.
Dingus, L., Clark, J., Scott, G.R., Swisher, C.C., Chiappe, L.M.,
and Coria, R.A. 2000. Stratigraphy and magnetostratigraphic/
faunal constraints for the age of sauropod embryo-bearing rocks
in the Neuquen Group (Late Cretaceous, Neuquen Province,
Argentina). American Museum Novitates, 3290.
Erben, H. 1970. Ultrastrukturen und Mineralisation rezenter und
fossiler Eischalen bei Vögeln und Reptilien. Biomineralisation
Forschungsberichte, Vol. 1, pp. 1–66.
Faccio, G. 1994. Dinosaurian Eggs from the Upper Cretaceous of
Urugay. In Dinosaur eggs and babies. Edited by K. Carpenter,
K.F. Hirsch, and J.R. Horner. Cambridge University Press, New
York, pp. 47–55
Grellet-Tinner, G. 2000. A study of titanosaurid eggshell from
Auca Mahuevo. Journal of Vertebrate Paleontology, 20(3,
Supplement): 46A.
Grellet-Tinner, G. 2001. Phylogenetic interpretation of eggs and
eggshells and its implication for Paleognathae phylogeny.
Unpublished thesis, Department of Geological Sciences,Univer-
sity of Texas, Austin, Tex.
Grellet-Tinner, G. In press. The membrana testacea of titanosaurid
dinosaur eggs from Auca Mahuevo (Argentina). Journal of
Vertebrate Paleontology.
Grellet-Tinner, G., and Chiappe, L.M. 2004. Dinosaur Eggs and
Nesting: Implications for Understanding the Origin of Birds. In
Feathered dragons. Edited by P.J. Currie, E.B. Koppelhus, M.A.
Shugar, and J.L. Wright. Indiana University Press, Bloomington
and Indianapolis, pp. 185–214.
Grellet-Tinner, G., and Norell, M. 2002. An avian egg from the
Campanian of Bayn Dzak, Mongolia. Journal of Vertebrate
Paleontology, 22: 719–721.
Hayward, J.M., Hirsch, K.F., and Robertson, T.C. 1991. Rapid
dissolution of avian eggshells buried by Mount St. Helens ash.
Palaios, 6: 174–178.
Hayward, J.M., Folsom, S.D., Elmendorf, D.L., Tambrini, A.A.,
959
and Cowles, D.L. 1997. Experiments on the taphonomy of amnoite
eggs in marine environments. Palaios, 12: 482–488.
Hayward, J.M., Zelenitsky, D.K., Smith, D.L., Zaft, D.M., and.
Clayburn, J.K. 2000. Eggshell taphonomy at modern gull colonies
and a dinosaur clutch site. Palaios, 15: 343–355.
Hirsch, K.F., and Lopez-Jurado, L.F. 1987. Pliocene chelonian fossil
eggs from Gran Canaria, Canary Islands. Journal of Vertebrate
Paleontology, 7: 96–99.
Kamat, S., Su, X., Ballarini, R., and Heuer, A.H. 2000. Structural
basis for the fracture toughness of the shell of the conch Strombus
gigas. Nature (London), 405: 1036–1040.
Kérourio, P. 1981. Nouvelles observations sur le mode de nidification
et de ponte chez les dinosauriens du Crétacé terminal du Midi de
la France. Comptes Rendus Sommaires de la Société Geologique de
France, 1: 25–28.
Kérourio, P., and Sigé, B. 1984. L’apport des coquilles d’oeufs de
dinosaures de Laguna Umayo à l’âge de la Formation Vilquechico
et à la compréhension de Perutherium altiplanense. Newsletters
on Stratigraphy, 13: 133–142.
Kohring, R. 1999. Strukturen, Biostratinomie, systematische und
phylogenetische Relevanz von Eischalen amnioter Wirbeltiere.
Courier Forschunginstitut Senckenberg, Vol. 210, pp. 1–307.
Magalhães Ribeiro, C.M. 2000. Microstructural anlysis of dinosaur
eggshells from Bauru Basin (Late Cretaceous), Minas Gerais,
Brasil. In 1st International symposium on dinosaur eggs and
babies. Edited by A.M. Bravo and T. Reyes. Isona I Conca Dellà
Catalonia, Spain, pp. 117–122.
Mohabey, D.M. 2000. Indian Upper Cretaceous (Maastrichtian)
dinosaur eggs: their parataxonomy and implication in under-
standing the nesting behavior. In 1st International symposium on
dinosaur eggs and babies. Edited by A.M. Bravo and T. Reyes.
Isona I Conca Dellà Catalonia, Spain, pp. 139–154.
Moratalla, J.J., and Powell, J.E. 1994. Dinosaur Nesting Patterns.
In Dinosaur eggs and babies. Edited by K. Carpenter, K.F. Hirsch,
and J.R. Horner. Cambridge University Press, New York, pp. 317–
46.
Packard, G.C., Taigen, T.L., Packard, M.J., and Shuman, R.D. 1979.
Water-vapor conductance of testudinian and crocodilian eggs
(class Reptilia). Respiratory Physiology, 38: 1–10.
Paganelli, C.V. 1980. The physic of gas exchange across the avian
eggshell. American Zoologist, 20: 329–338.
Peitz, C. 2000. Megaloolithid dinosaur eggs from the Maastrichtian
of Catalunya (NE-Spain)-parataxonomic implications and strati-
graphic utility. In 1st International symposium on dinosaur eggs
and babies. Edited by A.M. Bravo and T. Reyes. Isona I Conca
Dellà Catalonia, Spain, pp. 155–160.
Powell, J.E. 1992. Hallazgo de huevos asignables a dinosaurios
titanosauridos (Saurischia, Sauropoda) de la Provincia de Río
Negro, Argentina. Acta Zoologica, Lilloana, 41: 381–389.
Sabath, K. 1991. Upper Cretaceous amniotic eggs from the Gobi
Desert. Acta Palaeontologica Polonica, 36: 151–192.
Sahni, A., Tandon, S.K., Jolly, A., Bajpai, S., Sood, A., and
Srinivasan, S. 1994. Upper Cretaceous dinosaurs eggs and nesting
sites from the Deccan Volcan Sedimentary of Peninsular India.
In Dinosaur Eggs and Babies. Edited by K. Carpenter, K.F.
Hirsch, and J.R. Horner. Cambridge University Press, New York,
pp. 204–226.
Sigé, B. 1968. Dents de micromammifères et fragments de coquilles
d’oeufs de dinosauriens dans la faune de vertébrés du Crétacé
supérieure de Laguna Umayo (Andes péruviennes). Comptes
rendus de l’Academie des Sciences, Paris (D) 267: 1495–1498.
Vianey-Liaud, M., Mallan, P., Buscail, O., and Montgelard, C.
1994. Review of French Dinosaur Eggshells: Morphology, Structure,
Mineral, and Organic Composition. In Dinosaur eggs and babies.
© 2004 NRC Canada
960
Edited by K. Carpenter, K.F. Hirsch, and J.R. Horner. Cambridge
University Press, New York, pp. 151–183.
Vianey-Liaud, M., Hirsch, K.F., Sahni, A., and Sigé, B. 1997. Late
Cretaceous Peruvian eggshells and their relationships with
Laurasian and Eastern Gondwanian material. Geobios, 30: 75–
90.
Can. J. Earth Sci. Vol. 41, 2004
Williams, D., Seymour, R., and Kerourio, P. 1984. Structure of fossil
Dinosaur eggshell from Aix Bassin, France. Palaeogeography,
Palaeoclimatology, Palaeoecology, 45: 23–37.
Wilson, J.A., and Sereno, P.C. 1998. Early evolution and higher-
level phylogeny of sauropod dinosaurs. Society of Vertebrate
Paleontology, Memoir 5, Vol. 18 supplement to No. 2, pp. 1–67.
© 2004 NRC Canada