The anatomy, paleobiology, and evolutionary relationships of the largest extinct side-necked turtle
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Abstract
Despite being among the largest turtles that ever lived, the biology and systematics of Stupendemys geographicus remain largely unknown because of scant, fragmentary finds. We describe exceptional specimens and new localities of S. geographicus
from the Miocene of Venezuela and Colombia. We document the largest
shell reported for any extant or extinct turtle, with a carapace length
of 2.40 m and estimated mass of 1.145 kg, almost 100 times the size of
its closest living relative, the Amazon river turtle Peltocephalus dumerilianus, and twice that of the largest extant turtle, the marine leatherback Dermochelys coriacea.
The new specimens greatly increase knowledge of the biology and
evolution of this iconic species. Our findings suggest the existence of a
single giant turtle species across the northern Neotropics, but with
two shell morphotypes, suggestive of sexual dimorphism. Bite marks and
punctured bones indicate interactions with large caimans that also
inhabited the northern Neotropics.
INTRODUCTION
Since
the extinction of non-avian dinosaurs, the northern Neotropics have
harbored now-extinct vertebrates that have been at the extreme of large
size within their respective clades (1). Among them are the largest snake (2), caimanine crocodile (3), gharial (4), and some of the largest rodents (5). One of the most iconic of these species is the gigantic turtle Stupendemys geographicus, as it is the largest nonmarine turtle ever known from a complete shell (until now rivaled only by the extinct marine turtle Archelon ischyros from the Late Cretaceous). It was first described in 1976 from the Urumaco Formation in northwestern Venezuela (6),
but our knowledge of this animal has been based on partial specimens
that have resulted in a problematic taxonomy, especially due to a lack
of specimens with associated skull and shell elements. The species
diversity of the giant turtles inhabiting northern South America during
the Miocene is thus unclear (7, 8), with several forms having been proposed: the postcrania-based S. geographicus from the late Miocene, Urumaco region (6, 9–12); the skull-based Caninemys tridentata from the late Miocene, Acre region, Brazil (8); the controversial postcrania-based “S.” souzai, also from the late Miocene of Acre, Brazil (8, 13), currently attributed as Podocnemididae incertae sedis (14); and the skull-based Podocnemis bassleri from the late Miocene, Acre region (Loretto), Peru (15). The fossil record of large-sized littoral-freshwater Podocnemididae turtles of South America also includes the skull-based Carbonemys cofrinii, and the shell-based Pelomedusoides indet., from the middle to late Paleocene of Colombia (12).
We
here describe several new shells and the first lower jaw specimens from
discoveries made during regular fieldwork in the Urumaco region since
1994 (10, 16)
and recent finds from La Tatacoa Desert in Colombia. Together, these
fossils shed new light on the biology, past distribution, and
phylogenetic position of giant neotropical turtles. First, we report a
new size record for the largest known complete turtle shell. Second, our
findings support the existence of a sole giant erymnochelyin taxon, S. geographicus,
with an extensive geographical distribution in what were the Pebas and
Acre systems (pan-Amazonia during the middle Miocene to late Miocene in
northern South America). Third, we hypothesize that S. geographicus exhibited sexual dimorphism in shell morphology, with horns in males and hornless females.
RESULTS
Systematic paleontology
Testudines Batsch, 1788.
Pleurodira Cope, 1864 sensu Joyce et al., 2004.
Podocnemididae Cope, 1868.
Eymnochelyinae sensu Ferreira et al., 2018.
Stupendemys geographicus Wood, 1976.
Synonymy
Caninemys tridentata (8)
Stupendemys sp. (17)
Podocnemididae indet. (17)
Holotype. MCNC-244, medial portion of the carapace with associated left femur, fragments of scapulocoracoid and a cervical 8? (6).
Hypodigms. Specimens described in Wood (6):
MCZ(P)-4376, much of the carapace, fragments of plastron, cervical 7?,
both scapula-coracoids and a caudal vertebra; MCNC-245, a plastron
lacking the epiplastra and entoplastron, two nearly complete costals,
several peripherals, and one neural; MCZ(P)-4378, a right humerus.
Specimen described as C. tridentata (8): DNPM-MCT-1496-R, nearly complete skull (Fig. 4, A to D). Specimens referred to as S. souzai (13):
UFAC-1764, incomplete right humerus; UFAC-1163, cervical vertebra;
UFAC-1294, left peripheral 1; UFAC-1544, left costal 2; UFAC-1547, right
xiphiplastron; UFAC-1553, cervical vertebra; UFAC-1554, cervical
vertebra; UFAC-4370, pelvic girdle; UFAC-5275, cervical vertebra;
UFAC-5508, anterior margin of the carapace and left hypoplastron, and
LACM-131946, nuchal bone, originally attributed to Stupendemys sp. (17). Specimens referred to as Podocnemididae ind. (17): LACM-141498, left lower jaw ramus, and Stupendemys sp. (17): LACM-138028, right scapula. New specimens described here: CIAAP-2002-01 (allotype), nearly complete carapace (Fig. 1, A to E); AMU-CURS-85, nearly complete carapace, left humerus, and right scapula-coracoid (Figs. 2, B and C, and 3, A to D); AMU-CURS-1098, plastron and anterior portion of carapace (Fig. 2, D and E); MPV-0001, nearly complete carapace and complete plastron (Fig. 2, F to M); OL-1820, left humerus (Fig. 3, E to H); AMU-CURS-233, fragment of femur (Fig. 3, I to P); AMU-CURS-706, lower jaw (see fig. S6); VPPLT-979, lower jaw (Fig. 4, E to L).
(A and B) CIAAP-2002-01 carapace in dorsal view. (C) Close-up of the left horn in CIAAP-2002-01 [see red square in (B)]. (D) Medial-right view of the left horn showing its ventral projection. (E and F) Close-up of one of bone surface of the carapace showing the pitted sculpture [see red circle in (B)]. (G)
General reconstruction of CIAAP-2002-01 including the horns covered
with keratinous sheath (light gray). co, costal bone; M, marginal scute;
P, pleural scute; pe, peripheral bone; py, pygal bone; sp., suprapygal;
V, vertebral scute. Blue lines indicate sulci. Photo credit:
Edwin-Alberto Cadena, Universidad del Rosario.
(A) Reconstruction of S. geographicus male (front) and female (middle-left), together with the giant caimanine Purussaurus mirandai and the large catfish Phractocephalus nassi. (B and C) AMU-CURS-85 nearly complete carapace in ventral view. (D and E) AMU-CURS-1098 nearly complete plastron in ventral view. (F to N) Female shell anatomy of S. geographicus
MPV-0001 from Colombia. (F and G) Carapace in dorsal view. (H and I)
Plastron in ventral view. (J and K) Close-up of the right anterior
portion of the carapace in dorsoposterior view, showing bite marks and
punctured bone [(J) and rectangle in (G)]. (L and M) Nuchal-anterior
peripheral in dorsomedial view, showing thickened and moderately to
strongly upturned (arrows) [(L) and circle in (G)]. (N) Close-up of the
bone surface of one of the costal bones [(N) and circle in (G)],
exhibiting microvermiculation sculpturing pattern. Abd, abdominal scute;
Ana, anal scute; bm, bite mark; bp, bridge peripheral; co, costal bone;
ent, entoplastron; epi, epiplastron; Ext, extragular scute; Fem,
femoral scute; Hum, humeral scute; hyo, hyoplastron; hyp, hypoplastron;
Int, intergular scute; isc, ischium scar; Lpg, left pelvic girdle; M,
marginal scute; mes, mesoplastron; ne, neural bone; nu, nuchal bone; pe,
peripheral bone; Pec, pectoral scute; pub, pubis bone; py, pygal bone;
Rco, right coracoid; Rpg, right pelvic girdle; Rsc, right scapula; sp.,
suprapygal; tv, thoracic vertebra; V, vertebral scute; xip,
xiphiplastron. Blue lines indicate sulci. Art: Jaime Chirinos. Photo
credit: Edwin-Alberto Cadena, Universidad del Rosario.
(A to D) AMU-CURS-85 left humerus in ventral (A), medial (B), dorsal (C), and proximal (D) views. (E to H) OL-1820 left humerus in ventral (E), lateral (F), dorsal (G), and proximal (H) views. (I and J) AMU-CURS-233 partial femur in ventral (I) and dorsal (J) views. (K) Outline of the femur indicating the region where the thin section was elaborated. (L) Thin section of the partial femur, indicating the close-up presented in (M) to (P). (M) Close-up of the cortical region of the bone. (N) Close-up of the deeper part of the cortex. (O) Close-up of the central region of the bone. (P)
Close-up of the transitional region of the bone. Outlines of the
largest extant and extinct turtles ever, indicating their maximum
carapace length (see table S2): (Q) S. geographicus. (R) A. ischyros. (S) D. coriacea (extant). (T) M. cf. sivalensis. (U) R. swinhoei (extant). (V) C. niger
(extant). pco, primary cortex; SO, secondary osteon. Photo credit (A to
H): Edwin-Alberto Cadena, Universidad del Rosario; (I to P): Torsten
Scheyer, University of Zurich.
(A to D) DNPM-MCT-1496 skull described by Meylan et al. (8),
from Acre, Brazil in dorsal (A), ventral (B), and right lateral (C)
views. (D) Composite skull and lower jaw (not a scale) of S. geographicus using relief images of DNPM-MCT-1496 skull and VPPLT-979 lower jaw. (E to L)
VPPLT-979 lower jaw from La Tatacoa Desert, Colombia in dorsal (E and
F), ventral (G and H), and right-lateral (I and J) views. (K and L)
VPPLT-979 articular bone and facet in posterior view, exhibiting the
foramen posterius chorda tympani. (M to T) Right articular region of the lower jaw, Podocnemis expansa NHMW-137 (M and N), S. geographicus VPPLT-979 (O and P), S. geographicus AMU-CURS-706 (Q and R), P. dumerilianus AMNH-1886 (S and T). (U) Lower jaw of P. dumerilianus AMNH-1886 in dorsal view. (V) P. expansa
NHMW-137 lower jaw in dorsal view. ang, angular; arf, articular facet;
art, articular; cor, coronoid; den, dentary; fm, fossa Meckelii; fna,
foramen nervi auriculotemporalis; fos, fossa articularis mandibularis;
fpc, foramen posterius chorda tympani; pra, processus retroarticularis;
pre, prearticular; sr, symphisis ridge; sur, surangular. Photo credit (A
to C): Orangel Aguilera-Socorro, Universidade Federal Fluminense; (E to
V): Edwin-Alberto Cadena, Universidad del Rosario.
Range and distribution. Middle
to late Miocene, Tatacoa Desert, Villavieja, Departamento del Huila,
Colombia; late Miocene, Urumaco, Falcón State, Venezuela; late Miocene,
Acre region, Brazil; Loretto region, Peru (Fig. 5).
(A)
The phylogeny is based on the single MPT, resulting from the analysis
of 245 characters [L = 1180, consistency index (CI) = 0.319, and
retention index (RI) = 0.748]. Bremer support indices are indicated next
to the internodes. (B) A time-calibrated cladogram of
South American Erymnochelyinae; the bars indicate the stratigraphic
occurrence of taxa; internode length is hypothetical. (C)
Paleogeographic reconstruction of northern South America during the
late Miocene (10 Ma), including the localities with fossil record of S. geographicus and extension of the Pebas system, modified from Hoorn (44). (D) General stratigraphic column of Urumaco Formation, including the four localities where the new fossils of S. geographicus described here were found. (E)
Excavation of AMU-CURS-85 carapace from Tío Gregorio locality. H,
Holocene; L, tree length; Oligo, Oligocene; Paleo, Paleocene; Pleisto,
Pleistocene; Plio, Pliocene. Pr, present.
Diagnosis. S. geographicus
is recognized as a pleurodire based on (i) sutural articulation of
pelvis with shell, (ii) loss of medial contact of mesoplastra, (iii)
well-developed anal notch, (iv) fusion of gulars, (v) formed central
articulations of cervical vertebrae, (vi) a well-developed processus
trochlearis pterygoidei, and (vii) quadrate-basioccipital contact. It is
a podocnemidid based on (i) a fully developed, medially extensive cavum
pterygoidei with a completely developed pterygoid flange; (ii) an
incisura columellae auris enclosing stapes and eustachian tube; (iii) an
exoccipital-quadrate contact absent; and (iv) a cervical centra with
saddle-shaped posterior condyles. It shares with Peltocephalus dumerilianus and Erymnochelys madagascariensis
(i) a long parietal-quadratojugal contact; (iii) large postorbital
bones; (iii) cheek emargination potentially reduced or absent; (iv)
potentially advanced posterior roofing of the skull (reduced temporal
emargination); (v) an articular with a processus retroarticularis
posteroventromedially projected, differing from the ventrally projected Podocnemis spp. (Fig. 4, M to T, and fig. S6) acute tip of dentary at symphysis; and (vii) foramen chorda tympani enclosed in processus retroarticularis.
Further description and dimensions. Detailed anatomical descriptions, comparisons, and measurements of the fossilized bones and body mass estimation for S. geographicus and other fossil and extant giant turtles are presented in Fig. 3 (Q to V) and in the Supplementary Materials (text, figs. S1 to S6, tables S1 and S2, and data files S1 and S2).
Remarks. Skull:
Unique among podocnemidids (and all other pleurodires, the side-necked
turtles) in having greatly inflated maxillae, each with a ventral,
tooth-like process, which, together with a single process formed on the
midline of the premaxillae, form a tridentate condition in the upper
triturating surfaces. Lower jaw: Triturating surface deep, forming an
oval concavity, deeper than in any known living or extinct podocnemidid,
labial ridge curved anteriorly ending in acute tip; lingual ridge is a
blunt margin forming an accessory ridge that increases in height and
width anteriorly and runs as a narrow ridge at the medial symphysis;
high coronoid process; large dorsal opening of fossa Meckelii; the fossa
Meckelii fills the posterior end of the jaw to such an extent that the
area articularis mandibularis forms part of the posterior margin, and
the fossa opens posterolaterally next to the jaw articulation. Shell:
Carapace ≥2 m straight midline length, carapace low-arched, with
irregular nodular contours on external surface and deep median notch at
front; anterior border of nuchal-peripheral bones thickened and
moderately to strongly upturned; carapace with massive anterolateral
horns slightly projected ventrally in forms attributed as male; carapace
dorsal bone surface smooth to striated or slightly pitted; posterior
peripheral bones moderately scalloped along margins; thickness of
carapace relatively thin at the costals. Shell (plastron):
Pectoral-abdominal sulcus very anterior to mesoplastra, reaching almost
the hyoplastra lateral notch level. Neck: Cervical vertebrae (probably 7
and 8) with neural arches relatively high in relation to
anteroposterior lengths of centra, and articular facets of
postzygapophyses forming acute angle of less than 90°; cervical 8?
neural arch with large horizontal plane, prezygapophyses directed
perpendicularly, thin bladelike spine on anterior face of neural arch
and no ventral keel on centrum. Humerus: Humerus squat, massive; deep
bicipital fossa between lateral and medial articular facets on ventral
surface; prominent ridge traversing ventral surface of shaft from medial
process to distal end, terminating just above lateral condyle; medial
condyle broadest at anterior end; medial and lateral condyles facing
very ventrally; straight to slightly slender shaft and triangular in
cross section than circular. Femur: Femur squat, massive, greatly
flattened dorsoventrally; breadth of tibial condyle approximately
one-third total length of bone. Scapula: A dorsal strongly bowed
scapular process with a flattened flange projecting laterally from the
main axis.
Phylogenetic analysis
The
first analysis (all taxa separated) produced 156,070 most parsimonious
trees [MPTs; length = 1154, consistency index (CI) = 0.326, and
retention index (RI) = 0.749]. The strict consensus tree (fig. S7) shows
the lower jaws from Acre, Urumaco, and La Tatacoa in polytomy at the
base of the Stereogenyini clade, sensu Ferreira et al. (18), with the same position for C. tridentata and S. geographicus as presented in Ferreira et al. (18). The second analysis [C. tridentata + Acre jaw and S. geographicus
+ (Urumaco, La Tatacoa jaws)] produced 1157 MPT (length = 1157, CI =
0.325, and RI = 0.748). Here, the strict consensus tree (fig. S7) shows C. tridentata and S. geographicus forming a monophyletic clade inside the Erymnochelyinae clade sensu Ferreira et al. (18),
suggesting them to be closely related or potentially the same taxon. We
favor the latter monospecific scenario based on the following
considerations: (i) the three lower jaws from Urumaco, La Tatacoa, and
Acre resemble each other in all morphological aspects, varying only in
size and in preservation; (ii) the lower jaws from Urumaco, La Tatacoa,
and Acre were found in localities and/or formations where shell material
of S. geographicus was also found; and (iii) as Meylan et al. (8) stated, “there is a higher probability that the lower jaw, LACM-141498, does belong to Caninemys,
and they are sufficiently complementary to suggest that they are from
closely related taxa.” This scenario receives additional support from
the third phylogenetic analysis, which produced 36 MPTs (length = 1180,
CI = 0.319, and RI = 0.748). The strict consensus tree (Fig. 5A) and the time-calibrated cladogram pruned to the South American Erymnochelyinae clade (Fig. 5B) show S. geographicus
at the base, as sister taxon to all remaining erymnochelyin turtles.
This position is in agreement with the hypothesis presented by Meylan et al. (8) for C. tridentata (now S. geographicus),
based on a relatively different character-taxon matrix. Jointly
considering all these lines of evidence, we hypothesize that the skull
of C. tridentata and the lower jaws described here together correspond to the skull of S. geographicus.
It is thus both telling and fitting that turtle expert Eugene Gaffney,
when supervising the exhibit of the reconstructed skeleton of S. geographicus at the American Museum of Natural History in New York, provided the skull of Caninemys for that model.
Body size and body mass estimation
The measurements of the new specimens are given in fig. S2 and table S2. Of particular interest is the new S. geographicus
specimen CIAAP-2002-01 that we describe here. With its 286 cm
parasagittal straight carapace length, it is not only the largest known
specimen for this taxon but also the largest turtle shell found to date,
considering that the hitherto largest known specimen is the so-called
Vienna specimen of the turtle A. ischyros (NHMW-1977/1902/0001) with a shell length of 220 cm (19).
Among Asian trionychids, giant forms have been reported from the Eocene
of Pakistan, some reaching up to 2 m in shell length (20). Badam (21)
reported on giant tortoises from the Pliocene of India that, based on
reconstructed shell fragments, may have been larger than 3 m in carapace
length.
We estimated the body mass using the straight carapace length method (see data file S1) (22). For the largest specimen, CIAAP-2002-01, we obtained an estimate of 871 kg [compared to the 744 kg obtained by Iverson (22) for MCZ(P)-4376, previously the largest and most complete specimen]. However, in the case of S. geographicus,
to compensate for the effect of the large nuchal embayment, calculating
the body mass estimate as the average between estimations based on the
carapace midline and parasagittal lengths likely yields a more precise
body mass estimate. Doing this results in a body mass estimate of 1145
kg for the CIAAP-2002-01 specimen.
Bone histology
The thin section of AMU-CURS-233 (Fig. 3, L to P)
reveals an overall dense microanatomy with a central medullary region
completely filled by cancellous bone, surrounded by a transitional zone
with regular formed smaller spaces, which leads into a compact, external
cortex. Because of erosion of the femur surface, the external-most
layers of the bone are visible only in a few places.
The cortical tissue is increasingly dense toward the outer bone surface (Fig. 3M). The deeper parts of the cortex show a dense Haversian bone (Fig. 3N),
consisting mostly of longitudinally arranged or slightly angled
secondary osteons. In the more surficial parts of the cortex, remodeling
into dense Haversian bone is prominent, but remnants of primary
parallel-fibered bone matrix with numerous longitudinally arranged
primary osteons are still present. In these remnants, cell lacunae are
more irregular or of a roundish shape. The cortex also does not reveal
growth marks that could be counted, with the exception of a single spot
in the external-most cortical fragment that splits off from the main
section due to delamination processes and gypsum growth. In this
outermost-cortical layer, a few closely spaced lines (five lines?),
interpreted as lines of arrested growth (LAGs), form an outer
circumferential layer.
The cancellous bone in the center of the section (Fig. 3O)
consists of short bone trabeculae and few irregular larger
intertrabecular spaces. The trabeculae are secondarily remodeled and
consist of lamellar bone.
The transitional bone (Fig. 3P)
does not have distinct margins but is a zone of decreasing size of
individual extravascular spaces and increasing bone compactness.
Vascularization of the tissue is found in the form of longitudinally
arranged osteons and only few circumferentially oriented ones.
Remodeling by secondary osteons is extensive so that only interstitial
pockets of primary parallel-fibered bone tissue are discernible. The
overall bone compactness is 0.873, with modeled values at the center of
0.543 and at the periphery of 0.97 (see data file S2).
DISCUSSION
A pleurodiran turtle with a horned shell
In
vertebrates, different body parts have independently evolved into
protruding structures that are associated with a wide variety of
purposes, e.g., defense or attack, mating, display, communication, or
thermoregulation. Some of the most remarkable of these structures
include horns, antlers, spikes, spurs, plates, tail clubs, and tusks (23–25). In turtles, a notable example is the posterolateral horns of the skull of the extinct meiolaniids (26, 27).
Most examples, though, are connected to their shell, covering a
diversity of types. Knobby ridges can be found on the carapaces of the
extant matamata Chelus fimbriatus (28) and the alligator snapping turtle Macrochelys temminckii (29) and the extinct stem turtle Proganochelys quenstedti possessed serrations along the posterior shell margin (30). Among other examples, the extant spiny turtle Heosemys spinosa has peripherals with marginal spines (31)
that disappear ontogenetically, and many groups of testudinid tortoises
have highly lobulated and protruded anterior and posterior peripherals
or anterior plastron edges (32). Horn-like structures at the anterolateral margin of the carapace, such as those we report here for S. geographicus, have previously only been documented in the Cretaceous nanhsiungchelyid Anomalochelys angulata (see fig. S8) (33).
For this medium-sized (~65-cm straight parasagittal carapace length)
extinct terrestrial turtle, one interpretation of the horns’ purpose was
proposed as the protection of a large skull.
This hypothesis may also apply for S. geographicus, considering that we here interpret the massive skull DNPM-MCT-1496-R as its head. This specimen was previously described as C. tridentata,
and it had lower jaws, which in several morphological aspects resemble
the lower jaw of the extant South American big-headed turtle P. dumerilianus (Fig. 5
and the Supplementary Materials), including an acute symphyseal tip.
Another feature that supports the robustness of the head of S. geographicus
is the posterolateral opening of the fossa Meckelii in the newly
recovered lower jaws described here (AMU-CURS-706 and VPPLT-979),
implying a large main adductor tendon and associated musculature (17).
The occurrence of deep grooves in the massive horns of all three new specimens of S. geographicus from Urumaco described here (Fig. 1, C and D,
and the Supplementary Materials) indicates that they were true horns
with a bony core covered by a keratinous sheath that was strongly
attached via the grooves, similar to horns of extant artiodactyl bovid
mammals (34), and has been argued for meiolanid horns (26).
Sexual dimorphism
If the horns were for protection, then why do several S. geographicus
specimens lack horns? The anteroventrally facing orientation of the
horns is a distinct feature, suggesting that potentially they were
exclusively used not only for protection but also for combat. We
therefore hypothesize that the horned shells from Venezuela described
here represent males of S. geographicus and that the horns
served the main purpose of weapons in male-male combat behaviors. This
hypothesis is consistent with the occurrence of similar structures in
males of other groups of vertebrates, for example, in artiodactyl
mammals (23, 34).
In addition, in snapping turtles (Chelydridae), some of the largest
extant freshwater turtles, males that occupy overlapping areas often
establish dominance through fights (35).
The elongated and deep scar in the left horn of CIAAP-2002-01 (see the
Supplementary Materials) could be interpreted as a mark resulting from
combat between males. Many extant tortoises use their protruding
epiplastral horns for combat, often with the goal of flipping the
opponent (36–38).
The putative S. geographicus
males would also have been larger than females (see table S1), a
pattern similar to that documented in the closely related extant taxon P. dumerilianus, which exhibits a male-biased sexual size dimorphism (39).
Other sexually dimorphic traits of the turtle shell, such as a
xiphiplastral concavity in males, or a deeper anal notch in males than
in females (40, 41), are not distinct in S. geographicus, at least from a comparison between the specimens AMU-CURS-1098 (attributed to a male) and MPV-0001 (attributed to a female).
Paleoecology
The
climate and the productivity of the environment, habitat size, and
predation-competition interactions are some of the factors usually
considered as triggers or in favor of gigantism (42, 43). We hypothesize that in the case of S. geographicus, a combination of several factors favored the evolution of its large size.
Habitat
size, both in terms of individuals (home ranges large enough to sustain
giant body sizes) and in terms of populations (species distribution
ranges that can sustain long-term viable populations), was surely a
major determinant. During the Paleogene and until the late Miocene [~66
to 5 million years (Ma)], after the retreat of the dominant marine
conditions of the Cretaceous, northern South America harbored the most
extensive freshwater and littoral ecosystems in its geological history.
The coverage reached a particular peak during the Miocene, with the
development of a large wetland and lake system known as the Pebas system
(44),
which offered not only increased connectivity between habitats but also
the opportunity for the diversification and migration of faunas,
including turtles. It seems that the size of these wetland habitats in
northern South America during the Miocene facilitated the occurrence of
gigantism not only in turtles (this study) but also in several
vertebrate lineages such as crocodylians (Fig. 6 and table S3) and rodents (3–5).
Deep-sea benthic foraminifer oxygen isotope curve for 0 to 23 Ma, redraw from Zachos et al. (46),
showing major global climatic events (left). Major geological and
geographical events for northern South America (light brown bars).
Maximum skull or lower jaw (green values) and carapace (black values)
for turtles and crocodylians from northern South American fossil sites.
Formations are represented by yellow stars: 1, Barzalosa Fm., early
Miocene, Colombia; 2, Castillo Fm., early Miocene, Venezuela; 3,
Castilletes Fm., early-middle Miocene, Colombia; 4, La Victoria and
Villavieja Fms., middle-late Miocene, Colombia; 5, Pebas Fm., middle
Miocen, Peru; 6, Urumaco Fm., late Miocne, Venezuela; 7, Madre de Dios
and Ipururo Fms., late Miocene, Brazil; 8, Pisco Fm., late Miocene,
Peru; 9, Solimões Fm., late Miocene-Pliocene, Brazil; 10, San Gregorio
Fm., early Pliocene, Venezuela; 11, Ware Fm., Pliocene-Pleistocene,
Colombia; 12, Mesa Fm., Pleistocene, Venezuela. Carap, carapace; MMCO,
middle Miocene climatic optimum; MMCT, middle Miocene climatic
transition; Magda, Magdalena; Pleist; Pleistocene. Detailed information
on localities, specimens, and sources are in table S3.
Predation interactions could have also been involved in the evolution of large body size in S. geographicus, as it shared its habitat with gigantic crocodylians, including Purussaurus spp. and Gryposuchus spp., which could reach up to 10 m or more in body length. There is direct evidence of interactions between S. geographicus
and large South American crocodylians, in the form of bite marks in
Colombian and Venezuelan specimens, and an isolated tooth attached on
the ventral surface of the carapace in the CIAAP-2002-01 specimen (see
fig. S3).
Climate, particularly warmer temperatures,
could have been a potential factor favoring the evolution of large body
size in Miocene South American reptiles. For example, this causal link
has been inferred for the Paleocene fauna of Cerrejón, Colombia, which
includes the largest snake ever, Titanoboa cerrejonensis (2), and the largest Paleogene pelomedusoid turtles and crocodylians (12, 45).
Although less warm than the Paleocene and the Eocene, the Miocene was
also an epoch with notable climatic events that could have affected the
body size of neotropical animal species, for example, the warm middle
Miocene climatic optimum (MMCO) (46, 47),
the global cooling between ~15 and 13 Ma known as middle Miocene
climatic transition (MMCT), and continuous decreasing of global
temperature during the late Miocene (48). The time range so far known for S. geographicus
(middle Miocene to late Miocene) (this study) indicates that this taxon
overcame the MMCT event. It exhibited a gigantic (and potentially its
maximum) size during global cooling times (late Miocene) (Fig. 6).
The latter rules out a direct and rather unlikely simple effect of
climate on gigantism in neotropical Miocene reptiles. Thermally imposed
upper limits to body mass are more likely than a simple tracking of
changing temperature in body size evolution (49).
Unfortunately, the climatic conditions of terrestrial ecosystems during
the Miocene in tropical South America are still poorly known, and
better reconstructions of climatic conditions await information from
geochemical analyses of paleosols and carbonate isotopes. In addition,
for neotropical faunas in general and reptiles in particular, the
considerable gap in the South American Eocene and Oligocene fossil
record is a major obstacle to a clear understanding of the effect of
these climatic events on body size trends through time. It is therefore
currently impossible to track the evolutionary path of evolution of body
size that started during the Paleocene in detail or to establish
whether body sizes of late Eocene and Oligocene neotropical reptiles
remained large or decreased due, in part, to other cooling events such
as the late Eocene-Oligocene transition from “greenhouse” to “icehouse.”
To test the existence of a passive or driven trend in body size
evolution (50),
better sampling of the neotropical fossil record is needed. Both
internal or external factors could be associated with such trends (51),
and discoveries such as that reported here provide the primary evidence
with which to start to understand the range of possibilities in
morphospace occupation.
Turtles are a particularly
challenging group when it comes to the identification of potential
causal correlates in body size evolution, given the “atypical patterns”
in relation to latitude they show in body size and in geographic range (52), as opposed to major tendencies identified for other vertebrate groups.
Last,
the phylogenetic framework is likely an additional important factor,
given the association of biological attributes such as body size and
physiology to clades. Teasing out the relative importance of
physiological boundaries related to clades is currently equally limited
by the Eocene and Oligocene gap in neotropical faunas. For example, the
large body size of S. geographicus could be an inherited ancestral trait, rooted in the Paleocene forms from Cerrejón, Colombia [Carbonemys cofrinii and its potential shell, Pelomedusoides indet. (12)]. Our phylogenetic analysis (Fig. 5) supports the view that S. geographicus and Ca. cofrinii
both belong to the Erymnochelyinae clade but not as closely related
taxa. What is clear is that at least two separate clades inside
Podocnemididae exhibited large body size during the Miocene: one
including S. geographicus and another with P. bassleri (15) (15.7-cm skull length, potentially 2 m carapace length) in the line of Podocnemis group. In other turtle clades of the neotropics, this trend is represented by Chelonoidis sp. (1 m carapace length estimate) inside the terrestrial Testudinidae and Chelus colombianus (70 cm carapace length estimate) within the freshwater-inhabitant Chelidae (Fig. 6).
Paleogeography
Adding to the previously known records of S. geographicus from Urumaco and Acre (6–8, 13, 17),
we here report the first occurrence of this taxon in the well-known
fauna of La Venta, Tatacoa Desert. This notably expands the known
distribution of S. geographicus, highlighting that it likely
was a common taxon throughout the entire Pebas system, well adapted to
both fluvial conditions (La Venta and Acre) and fluvial-littoral
conditions (Urumaco) (Fig. 5C).
It is likely that the changes in the configuration of the Pebas and the
posterior Acre systems due to the uplifting of the Andes starting in
the middle Miocene (ca. 12.5 Ma) (53) (Fig. 6) had a deep impact on the populations of S. geographicus, considerably reducing their habitat size and leading to its final extinction, probably during the early Pliocene.
Paleodiet
Taking into account the morphology of the massive skull elements (skull and lower jaws, Fig. 4D) of S. geographicus, Meylan et al. (8)
interpreted this turtle as a pleurodiran snapping turtle, involving a
vacuum feeding system and capable of capturing and holding prey of very
large size, including fish, small caimanines, and snakes. In this
questionable interpretation, it was a carnivore much like the extant
cryptodires Macrochelys, Claudius, and Staurotypus, which also exhibit a depression in the upper triturating surface and have lower jaws with a well-developed symphyseal hook (8).
The very acute symphysial end and wider anteromedial triturating
surface of the well-preserved jaw (VPPLT 979 specimen) from La Tatacoa
described here indicate that S. geographicus may have had a
diet much broader than one consisting of the abovementioned vertebrate
preys. It could have had a more diverse diet. For example, it could have
had a generally durophagous diet, crushing hard-shelled prey such as
mollusks with the help of its large triturating surface and facilitated
by its large main adductor tendon and associated musculature. Increasing
the diet niche breadth would have favored maintaining a very large body
size in this turtle, resulting in a body size–environment productivity
correspondence (42).
Another
previously underestimated aspect of paleodiet is the potential of large
extinct turtles having acted as seed dispersers for many plant species.
A recent review of frugivory and seed dispersal in extant turtles (54)
highlighted that many species consume fruits, and thus potentially
disperse the seeds, even if fruits are not considered part of their
standard diet. Seasonally, high-energy fruits from, e.g., palms
(Araceae) can even form the major part of Amazonian turtles’ diets. This
is the case for the closest extant relative of S. geographicus, the big-headed Amazon river turtle, P. dumerilianus, where (55)
found that fruits and seeds formed the most diverse component of its
stomach contents and that palm seeds were the most common item (55).
Because of its huge gape size, S. geographicus
could have swallowed even the largest South American fruits and thus
qualify as a megafaunal frugivore and seed disperser [sensu (56)].
In general, larger turtles also include more fruits in their diet than
do smaller ones; for example, in the extant Asian big-headed turtle, Platysternon megacephalum, there is a positive relationship between body size and amount of fruit in their diet (57). Overall, S. geographicus could thus have been a highly efficient seed disperser [sensu (58)].
Paleohistology and life history considerations
As with the previously analyzed shell bones of S. geographicus (from CIAAP-2002-01) (59), our histological analysis of the femur did not reveal anything unusual about Stupendemys
growth, only that it is overall comparable to the microanatomical build
and the histology of smaller turtles. The high amount of Haversian bone
in the femur fragment might be related to the giant size as pointed out
by Foote (60)
or by advanced age of a skeletally mature specimen, as is tentatively
indicated by the tightly spaced LAGs in the outer circumferential layer.
The estimated compactness values of AMU-CURS-233 are comparable to
those of other aquatic, nonmarine turtles (61).
We
see the almost universal conserved arrangement of scutes of turtles in
the gigantic specimen described here, emphasizing how the developmental
program of turtles (62) results in early differentiation in which prolonged growth does not result in changes in epidermal structures. S. geographicus
probably lived for at least 110 years to be able to reach the largest
recorded size we report here, assuming a growth rate similar to that of
extant, large turtles (59).
MATERIALS AND METHODS
Institutional repositories
The
fossils referred here are in the collections of American Museum of
Natural History, New York, USA; Alcadía Bolivariana de Urumaco, Urumaco,
Falcón State, Venezuela (AMU-CURS); Centro de Investigaciones
Antropológicas, Arqueológicas y Palentológicas (CIAAP) of the
Universidad Nacional Experimental Francisco de Miranda, Coro, Falcón
State, Venezuela; Departmento Nacional de Produçaõ Mineral, Divisaõ de
Geologia e Mineralogia, Ciências da Terra, Rio de Janeiro, Brazil
(DNPM-MCT); The Geological Museum, Geology Survey Institute, Bandung,
Indonesia (K); Natural History Museum of Los Angeles, Los Angeles, USA
(LACM); Museo de Ciencias Naturales de Caracas, Caracas, Venezuela
(MCNC); Museum of Comparative Zoology-Harvard University, Cambridge, USA
[MCZ(P)]; Museo Paleontológico de Villavieja, Villavieja, Huila
Department, Colombia (MPV); Naturhistorisches Museum Wien, Vienna,
Austria (NHMW); Universidad Simón Bolívar, Caracas, Venezuela (OL;
specimens housed in the Museo Paleontógico de Urumaco); and Museo de
Historia Natural La Tatacoa, La Victoria, Huila Department, Colombia
(VPPLT).
Phylogenetic analyses
To explore the phylogenetic position of S. geographicus, three separate maximum parsimony analyses were run using PAUP 4.0 (63) and using the character-taxon matrix of Ferreira et al. (18) as the original template with some modifications (see the Supplementary Materials). For all the analyses, Pr. quenstedti, Notoemys laticentralis, and Platychelys oberndorferi
comprised the outgroup taxa; all the 245 characters were considered
equally weighted, and multistate states were treated as polymorphic.
Heuristic search, random search for 10,000 replicates, and
tree-bisection reconnection option were performed, seed 1000, holding
one tree per replicate and collapse branches if minimum length is zero.
Strict consensus trees and their decay index (Bremer support) were also
obtained. For the first analysis, we considered each of the three giant
lower jaws from Acre (17), Urumaco, and La Venta (described here) as separate taxa, as well as C. tridentata (8) and S. geographicus,
with the addition of information from previous and the new specimens
described here. A second analysis considering the lower jaw LACM-141498
from Acre as belonging to C. tridentata as considered originally by Meylan et al. (8) and the lower jaws AMU-CURS-706 from Urumaco and VPPLT-979 from La Tatacoa as belonging to S. geographicus was performed. For the third analysis, we considered a single taxon, S. geographicus, formed by the new and previously described S. geographicus shells and postcrania; the three lower jaws from Acre, Urumaco, and La Tatacoa; and the skull of C. tridentata
(see fig. S7). Twelve morphocline characters were treated as ordered
characters (14, 18, 19, 71, 95, 96, 99, 101, 119, 129, 174, and 175)
following Ferreira et al. (18). Results are also presented in a time-calibrated cladogram of South American Erymnochelyinae turtles (Fig. 5B) based on this and previous studies (12, 64).
Body mass estimation
Body mass estimation of S. geographicus
and some other taxa mentioned in table S1 was obtained using the
correspondence between carapace length and body mass reported by Iverson
(22) in extant representative of all lineages of turtles. Specifically, we used the general allometric equation y = axb, where y is the body mass (in grams), x is the carapace length (in centimeters), and a and b are the correlation coefficients established for each of the taxa (see the Supplementary Materials) (22).
Considering that none of the taxa included in this study were part of
Iverson’s study, we used the coefficients of the closest phylogenetic
and/or similar lifestyle representative, for example, in the case of S. geographicus as it was also used by Iverson (22), we used the coefficients established for Podocnemis unifilis; for A. ischyros and D. coriacea (both marine turtles), we used the coefficients of Chelonia mydas; for Megalochelys sivalensis and Chelonoidis niger (both tortoises), we used the coefficients of Geochelone elegans; and for Rafetus swinhoei (freshwater soft-shelled turtle), we used the coeficientes of Apalone (Trionyx) spinifera.
Bone histology
We sectioned a shaft fragment of a femur of S. geographicus
(AMU-CURS-233) recovered from a site next to the gas pipeline at El
Mamón locality, Urumaco, Falcón state, Venezuela (11°13′1.46″N;
70°16′51.2″W). The shaft section was roughly oval shaped, with the
longest axis of 8 cm and a perpendicular shorter axis of 6.2 cm. The
bone was cut with an iron hand saw and processed afterward, following
standard petrographic thin-sectioning procedures (65).
The thin section was studied and analyzed using a compound microscope
(DM 2500M, Leica) with a digital camera (DFC 420C, Leica). Comparative
material of S. geographicus included already published shell bone sections (59), and overall bone compactness was calculated using Bone Profiler software (66).
Maximum size versus climate and geological events
We
plotted the largest as-preserved or estimated length of skull, lower
jaw, and/or carapace of turtles and crocodylians from each of the
neotropical Neogene to Quaternary fossil sites, putting them in context
with the global climatic curve of Zachos et al. (46)
and the major geological and geographical events of northern South
America. We included the following lineages of turtles: Erymnochelyinae,
Podocnemidinae, Chelidae, and Testudinidae, and for the crocodylians:
Alligatoridae, Gavialidae, and Crocodylidae (Fig. 6,
fig. S9, and table S3), adding also the largest reported extant
representatives. We excluded from this plot very recently immigrant
lineages of turtles: Geoemydidae, Kinosternidae, Emydidae, and
Chelydridae, and turtles that occasionally reached South America, for
example, Trionychidae, as well as sea turtles and the extant Galápagos
tortoises (gigantism due to phylogenetic history and island isolation).
The extremely fragmentary Charactosuchus spp. were also excluded considering that they are still controversial if they are truly members of Crocodylidae (67).
SUPPLEMENTARY MATERIALS
Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/6/7/eaay4593/DC1
Supplementary Text
Fig. S1. S. geographicus CIAAP-2002-01 details.
Fig. S2. Outlines and indication of the measurements of the new specimens described here and reported in tables S1 and S2.
Fig. S3. S. geographicus CIAAP-2002-01 carapace.
Fig. S4. AMU-CURS-85 carapace of S. geographicus from Venezuela.
Fig. S5. Details of S. geographicus AMU-CURS-1098 from Venezuela.
Fig. S6. Lower jaws of S. geographicus from Venezuela, Colombia, and extant podocnemidids.
Fig. S7. Additional strict consensus trees.
Fig. S8. A. angulata from the Cretaceous of Japan.
Fig. S9. Phylogeny versus skull–lower jaw length for Miocene neotropical crocodylians.
Table S1. Measurements and body mass estimation for S. geographicus and other extant and extinct giant turtles as preserved in centimeters and kilograms.
Table S2. Specific measurements and thickness (see fig. S2) of new specimens of S. geographicus.
Table S3. Data on size for the Neogene to extant neotropical turtles and crocodylians.
Data file S1. Body mass estimation calculations.
Data file S2. Bone compactness calculations using Bone Profiler.
Data file S3. Character-taxon matrix Nexus file raw data.
Data file S4. Character-taxon matrix Nexus file final version.
Movie S1. Video of CIAAP-2002-01 specimen.
Movie S2. Video of the excavation of AMU-CURS-85 specimen.
This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
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Acknowledgments: We
are indebted to D. Gutiérrez and F. Parra for helping with the
preparation of fossil specimens and collaboration in fieldwork. We thank
R. Hirayama for color photos of Anomalochelys; M. Clauss for
discussion on the early stages of this work; and editors J. Jackson and
D. Erwin, reviewer W. Joyce, and an anonymous reviewer for input to
improve this paper. We thank the curators and museum staff of the
following institutions for permits and access to collections and
specimens: American Museum of Natural History; Alcadía Bolivariana de
Urumaco; Chelonian Research Institute; Instituto de Ciencias Naturales
Universidad Nacional de Colombia; Instituto del Patrimonio Cultural de
Venezuela; Museo Paleontológico de Urumaco; Centro de Investigaciones
Antropológicas, Arqueológicas y Paleontológicas de la Universidad
Experimental Francisco de Miranda; Museo de Ciencias Naturales de
Caracas; Museum of Comparative Zoology-Harvard University; Museo
Paleontológico de Villavieja; Museo de Historia Natural La Tatacoa;
Naturhistorisches Museum Wien; Servicio Geológico Colombiano; Divisaõ de
Geologia e Mineralogia Museu de Ciências da Terra do Rio de Janeiro;
Smithsonian Natural History Museum Collections; and University of
Florida Herpetology Collection. We thank H. Moreno, C. Morón, G. Ojeda,
A. Blanco, A. Reyes-Cespedes, J. Hernández, and the communities of
Urumaco and La Victoria for their valuable assistance. We thank the
Brazilian Council of Science and Technological Development (productivity
researches 305269/2017-8). We thank J. Moreno for information on some
fossil crocodylians. Funding: This research was funded
by grant 40215 from the National Geographic Society–Waitt Foundation
Grants Program and the Vicerrectoría Universidad del Rosario. Author contributions:
R.S., O.A.A.-S., M.P., A.V., M.R.S.-V., J.D.C.-B., and E.-A.C.
collected the fossils. E.-A.C. and T.M.S. designed the study. E.-A.C.,
T.M.S., M.R.S.-V., and J.D.C.-B., collected data, made comparisons, and
wrote the paper. All authors gave final approval for publication. Competing interests: The authors declare that they have no competing interests. Data and materials availability:
All data needed to evaluate the conclusions in the paper are present in
the paper and/or the Supplementary Materials. Additional data related
to this paper may be requested from the authors.
- Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).
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