-
ResearchCite this article: Salas-Gismondi R, Flynn JJ,Baby P,
Tejada-Lara JV, Wesselingh FP, Antoine
P-O. 2015 A Miocene hyperdiverse crocodylian
community reveals peculiar trophic dynamics
in proto-Amazonian mega-wetlands.
Accepted: 22 January 2015
proto-Amazonia, Pebas System, molluscs,
durophagy
Rodolfo Salas-Gismondi
e-mail: [email protected]
Electronic supplementary material is available
A Miocene hyperdiverse crocodylian
Marcos, Avenida Arenales 1256, Lima 14, Peru3Division of
Paleontology, American Museum of Natural History, New York, NY
10024-5192, USA4Geosciences-Environnements Toulouse, Universite de
Toulouse, UPS (SVT-OMP), CNRS, IRD,
on March 5,
2015http://rspb.royalsocietypublishing.org/Downloaded from at
http://dx.doi.org/10.1098/rspb.2014.2490 or
via http://rspb.royalsocietypublishing.org.Author for
correspondence:Subject Areas:palaeontology, evolution, taxonomy
and systematics
Keywords:Miocene, caimanine crocodylians,Proc. R. Soc. B 282:
20142490.http://dx.doi.org/10.1098/rspb.2014.2490
Received: 10 October 2014rspb.royalsocietypublishing.org14
Avenue Edouard Belin, Toulouse 31400, France5Convenio
IRD-PeruPetro, Avenida Luis Aldana 320, San Borja, Lima,
Peru6Florida Museum of Natural History and Department of Biology,
University of Florida, PO BOX 117800,Gainesville, FL 32611,
USA7Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA, Leiden,
The Netherlands
Amazonia contains one of the worlds richest biotas, but origins
of this diver-sity remain obscure. Onset of the Amazon River
drainage at approximately10.5 Ma represented a major shift in
Neotropical ecosystems, and proto-Ama-zonian biotas just prior to
this pivotal episode are integral to understandingorigins of
Amazonian biodiversity, yet vertebrate fossil evidence is
extra-ordinarily rare. Two new species-rich bonebeds from late
Middle Mioceneproto-Amazonian deposits of northeastern Peru
document the same hyper-diverse assemblage of seven co-occurring
crocodylian species. Besides thelarge-bodied Purussaurus and
Mourasuchus, all other crocodylians are newtaxa, including a stem
caimanGnatusuchus pebasensisbearing a massiveshovel-shaped
mandible, procumbent anterior and globular posterior teeth,and a
mammal-like diastema. This unusual species is an extreme exemplarof
a radiation of small caimans with crushing dentitions recording
peculiarfeeding strategies correlated with a peak in
proto-Amazonian molluscandiversity and abundance. These faunas
evolved within dysoxic marshes andswamps of the long-lived Pebas
Mega-Wetland System and declined withinception of the
transcontinental Amazon drainage, favouring diversificationof
longirostrine crocodylians and more modern generalist-feeding
caimans.The rise and demise of distinctive, highly productive
aquatic ecosystems sub-stantially influenced evolution of Amazonian
biodiversity hotspots ofcrocodylians and other organisms throughout
the Neogene.
1. IntroductionIn Western Amazonia, the beginning of the Neogene
(at approx. 23 Ma) wasmarked by a peak in Andean uplift that
favoured onset and development ofthe Pebas Mega-Wetland System [1].
Ten million years later, just prior to estab-lishment of the
transcontinental Amazon River drainage, this inland
ecosystemattained huge size (more than 1 million km2) and extreme
complexity with mul-tiple environments, such as lakes, embayments,
swamps and rivers that drainedtowards the Caribbean [2,3]. The
exceptional depositional and fossil record ofthe Pebas/Solimoes
Formations around the PeruvianColombianBrazilianjunction permits
detailed reconstructions of these Miocene palaeoenvironmentsand
their distinctive biotas [2,48]. Aquatic invertebrates (ostracods
and mol-luscs) are extremely abundant and diverse within those
deposits [2,4,911],
& 2015 The Author(s) Published by the Royal Society. All
rights reserved.community reveals peculiar trophicdynamics in
proto-Amazonianmega-wetlands
Rodolfo Salas-Gismondi1,2, John J. Flynn3, Patrice Baby4,5,
JuliaV. Tejada-Lara2,6, Frank P. Wesselingh7 and Pierre-Olivier
Antoine1
1Institut des Sciences de lEvolution, Universite de Montpellier,
CNRS, IRD EPHE, Montpellier 34095, France2Departamento de
Paleontologa de Vertebrados, Museo de Historia Natural, Universidad
Nacional Mayor de San
-
Locality and horizon: Locality IQ114 (electronic supple-
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material, figure S1 and text S1), Iquitos area, Peru;Pebas
Formation, late Middle Miocene, ca 13 Ma; MolluscZone 8 (MZ8)
[4].
Referred specimens: MUSM 1979, right mandible (figure1c,d),
Locality IQ114 (electronic supplementary material, tableS2); MUSM
662, partial left mandible (figure 3ac), LocalityIQ116 (electronic
supplementary material, table S2); MUSM2040, partial left mandible
(figure 3d), Locality IQ114 (see elec-tronic supplementary
material, text S1).
Diagnosis: Gnatusuchus is a blunt-snouted caimaninealligatoroid
diagnosed by the following combination ofcharacters (autopomorphies
within Crocodyliformes aredemarcated with an asterisk): skull short
and broad, parallel-sided with a reduced rostrum and a wide rounded
snout;upturned orbital rims absent; rostral canthi or
spectacleabsent; thick laterosphenoid; attachment scars on ventral
sur-face of quadrate forming a prominent knob; anterior teeth
peg-shaped with blunt crowns and posterior teeth globular, bothwith
no carinae*; dentary with an extensive diastema that sep-arates
seven anterior alveoli from four close-packed posteriorcheek teeth
alveoli*; anterior dentary teeth strongly procum-bent; posterior
mandibular teeth completely surrounded bythe dentary; shovel-like
mandible with a long symphysisdenoting an extensive radiation of
endemic lacustrine taxa byabout 13 Ma [2]. The biostratigraphic
framework for thePebas/Solimoes Formation is based on molluscs and
pollen[4,5]. Although fishes [12] had been reported prior to
ourexploration of this region, other fossil vertebrates wereunknown
other than a teiid lizard later discovered [13]. Since2002,
systematic survey of Peruvian localities of the Iquitosarea in
northwestern Amazonia has yielded well preservedremains of mammals,
turtles, fishes and crocodylians, thelatter in great abundance. Two
nearby, correlative and contem-poraneous lignitic bonebeds in
outcrops of approximately 20and approximately 200 m2 each document
at least sevenco-occurring crocodylian species, contrasting with
the threespecies that rarely occur sympatrically within the
Amazonbiodiversity hotspot today. Here, we report discovery of
thisnew highly diverse and endemic crocodylian community,dominated
by small blunt-snouted taxa with crushing denti-tions that
inhabited the Pebas Mega-Wetland System at itsclimax, just after
the Middle Miocene Climate Optimum(MMCO). We describe three new,
sympatric, blunt-snoutedcaimans to assess distinctive trophic
dynamics of proto-Amazonian wetlands and identify a key interval of
ecologicalturnover at the dawn of the Amazon River drainage.
2. Results(a) Systematic palaeontologyCrocodyliformes Hay, 1930;
Alligatoroidea Gray, 1844;Globidonta Brochu, 1999; Caimaninae
Brochu, 1999.
Gnatusuchus pebasensis, gen. et sp. nov.Etymology: Gnatusuchus
from Quechua Natu for small
nose, and Greek souchos, crocodile; pebasensis from Pebas,after
the old Amazonian village of Pebas, Peru, for whichthe source
geological formation was named.
Holotype: Vertebrate Palaeontology Collection of theNatural
History Museum of San Marcos University(MUSM) 990, nearly complete
skull (figures 1a,b and 2a;electronic supplementary material,
figure S2 and table S1).reaching the level of the eleventh dentary
tooth alveolus (ofrelated taxa); large participation of splenial in
symphysis;posterior half of the mandibular ramus tilted
lateroventrally*.
General description: The snout of G. pebasensis is
substan-tially wider than long, with a lengthbreadth index [15]
of1.55a slightly higher value than the 1.45 index of the
bizarrepug-nosed Malagasy Cretaceous crocodyliform Simosuchusclarki
[16]. As in Acynodon iberoccitanus [17], the skull is soshort that
the orbits are situated midway between the anteriortip and
posterior margin of the skull. The index of rostral-skulllength is
0.49. Skull bone sculpturing is generally moderate,but a little
stronger in the jugal bones and skull table. The exter-nal naris is
apple-shaped. Orbits are large and nearly circular,but with long
axis oriented mediolaterally. The suborbitalfenestrae are short,
lacking a posterior notch and appearingto be widely separate from
each other. The anterior and lateralrims of the choana lie flush
with the surrounding pterygoidbones; the posterior rim is deeply
incised.Mandibular articula-tion of the quadrates is proportionally
larger than usuallyobserved in caimans. Tooth loci count probably
consisted ofa total of five and nine in each premaxilla and
maxilla, respect-ively. The mandible is short and wide. Symphyseal
region isdorsoventrally compressed, with dentary and splenial
forminga continuous concave dorsal surface. The surangular
reachesthe tip of the short, massive retroarticular
process.Gnatusuchusshares with other caimanines small supratemporal
fenestraewith overhanging rims (character 1521), trapezoid
supraocci-pital on skull table (character 160-4) and slender
process ofexoccipital ventrally to basioccipital tubera (character
176-2).Total body length estimate is 148.9167.7 cm
(electronicsupplementary material, table S7 and text S1).
Specialized dentition: Compared with other blunt-snoutedor
generalized caimans, which possess around 1820 toothalveoli, the
mandibular dentition of G. pebasensis is extremelyreduced in
number. Mandibular teeth include 11 tooth alveoligrouped into seven
anterior teeth and four posterior cheekteeth, with these groups
separated by a long diastema. Toothpositions, dentary shape and
vestigial dental alveoli indicatethat the diastema results from the
evolutionary loss of at leastthree tooth alveolus loci (the eighth,
ninth and tenth loci ofrelated taxa). Significant evolutionary loss
of several alveoliposterior to the 14th tooth locus also occurred
within the rearmandibular dentition, as the ancestral caimanine
conditionmay have included four to six more tooth loci posterior
tothe 14th locus [18,19]. Additional alveolar closure withintooth
loci posterior to the fourth is observed among most indi-viduals,
but itmight be a consequence of secondary bone filling(i.e. bone
resorption) after tooth loss that probably occurredduring in vivo
feeding activity on hard food (e.g. durophagy).
Teeth are distinctly modified in shape from the
generalizedcrocodylian pattern. Anterior teeth are thin and
peg-like inshape, bearing blunt crownswith no carinae ridges or
striae. Pre-served teeth show apical wear. Anterior teeth are
notablyprocumbent. In MUSM 2040, one posterior tooth is preservedin
the eleventh dentary position (figure 3d). This tooth is globu-lar
in shapewith a distinct neck at the base of the crown.
Similarmorphology is expected for adjoining teeth fromedentulous
loci.
Kuttanacaiman iquitosensis, gen. et sp. nov.Etymology: Kuttana
from Quechua for grinding or crush-
ing machine, and caiman, referring to tropical
Americanalligatoroids; iquitosensis from the Iquitos native
ethnicgroup inhabiting the Maynas province close to the
PeruvianAmazonian city of Iquitos near the specimen locality.
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pt
m9?m8?m7?m6m5m4m3
m21
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mx
m3
j
ec
m
pm5pm4pm3
pm2pm1
lpf
f
n
(a) (b)Holotype: MUSM 1490, nearly complete skull and mand-ibles
in anatomical connection (figures 1e,f,i and 2b;
electronicsupplementary material, table S3).
Locality and horizon: Locality IQ26 (electronic supplemen-tary
material, figure S1 and text S1), Iquitos area, Peru;
PebasFormation, late Middle Miocene, ca 13 Ma; MZ8 [4].
Referred specimens: MUSM 1942, associated left mandible,maxilla
and skull table (figures 3e and S3a; electronic sup-plementary
material, table S4), Locality IQ114 (see electronicsupplementary
material, text S1).
j
qj q
QKppo
q
sq so
pm
d1 d4 na mx ec
m4d
emf an
f sq
ar
pm
mx
n
lpf
f
p
d1
d4
na
mx
pm
qj
j
d
s
pa
pt
bo
ar
eo
m4
ec
ec
po
an
qjq
sq
ar
jsa
(e)
(i) ( j
(g( f )
Figure 1. Pebasian crushing-dentition caimans. Gnatusuchus
pebasensis gen. et sp. nov.mandible (MUSM 1979) in dorsal view. (d
) Comparison among coloured bone photographand cross sections at
the level of the adductor fossa. Values of 708 and 908 indicate
theplane. Kuttanacaiman iquitosensis gen. et sp. nov. (e,f,i).
Skull and mandibles (holotypelangstoni sp. nov. (g,h, j ). Skull
(holotype, MUSM 2377) in dorsal (g), ventral (h) and ricanthi
rostralii; d, dentary; d17, d1114, dentary tooth positions; ec,
ectopterygoid;adductor fossa; j, jugal; j.mx, maxilla surface for
jugal; l, lacrimal; m19, m12, maxillarypf, prefrontal; pm,
premaxilla; pm15, premaxillary tooth positions; po, postorbital;
pt, pQK, knob of quadrate crest A; s, splenial; sa, surangular; so,
supraoccipital; sq, squamod1
sa
sa
sa
arar
d d
s
san an
co
co
sa
an
an
90 70
FADFAD
d2 d3d4
d5d6d7
d11d12d13d14
(d )Diagnosis: Kuttanacaiman is a small caimanine diagnosedby
the following combination of characters: robust, bluntand short
snout; interorbital bridge flat and slender; posteriormaxillary and
dentary teeth closely packed, globular, lowand laterally
compressed. Symphysis reaching level of thesixth dentary alveolus,
splenial excluded from mandibularsymphysis, anterior dorsal process
of splenials turned medi-ally; abrupt elevation of surangular
dorsal margin posteriorto dentary series; first and fourth dentary
teeth piercingpremaxilla; angularsurangular suture contacting
external
arar
q qj.qj.mx
ec
pt
m12
m9 m4 mx
pm
na
cr
mx
pa
j
qjpt
mx
pf
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po f pfl
nna
sq
sq
l
ec
n
f
p
q
m4
m9
m12
pmpm
)
) (h)
(ad ). Skull (holotype, MUSM 990) in dorsal (a) and ventral (b)
view. (c) Rights of mandible of G. pebasensis (right) and Caiman
crocodilus (left) in dorsal viewscorresponding lateral vertical
angle of the mandibular ramus with the horizontal, MUSM 1490) in
dorsal (e), ventral ( f ) and left lateral (i) view. Caiman
wann-ght lateral ( j) view. an, angular; ar, articular; bo,
basioccipital; co, coronoid; cr,emf, external mandibular fenestra;
eo, exoccipital; f, frontal; FAD, mandibular
tooth positions; mx, maxilla; n, nasal; na, narial opening; p,
parietal; pa, palatine;terygoid; q, quadrate; qj, quadratojugal;
qj.q, quadrate surface for quadratojugal;sal. Scale bars, 5 cm.
Slightly smaller scale bar for (c) and (d ).
Proc.R.Soc.B282:20142490
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the sixentary
490), skright duadrant, rostra
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(a)
Globidentosuchus0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.3 0.4 0.5 0.6RL/SL
RW/P
OW
0.7 0.80.2
1.0
(c)
(g)
( f )
(b)(d ) (e)
(b) (c)
Figure 2. Pebasian crocodylian diversity and snout morphotypes.
Positions ofplot of relative snout width and length within the
Eusuchia (electronic supplem(MUSM 990), skull. (b) Kuttanacaiman
iquitosensis gen. et sp. nov. (MUSM 1neivensis (MUSM 1392), right
dentary. (e) Mourasuchus atopus (MUSM 2379),(g) Pebas gavialoid
(MUSM 1981), skull. Bivariate plot modified from [14]. Qshaped
morphospace. RW/POW, rostral widthpostorbital width index;
RL/SLmandibular fenestra at posterior angle; maxillary bearinga
broad shelf extending into suborbital fenestra; palatinelateral
margins extending into suborbital fenestra anteriorlyand
posteriorly; parietal excluded from posterior margin ofskull
table.
General description: The snout is blunt and rounded.
Lateralrostral margins are slightly convex, without significant
trans-verse expansion posteriorly. The index of rostral-skull
length is0.52 (figure 2). The narial opening projects dorsally and
appearslonger than wide. The nasal bones form the posterior rim
ofnarial opening. Nasals and lacrimals are not in contact.
Theorbits are large, long and subtriangular in shape, with
anteriorangle displaced laterally as in Globidentosuchus
brachyrostrisand Eocaiman cavernensis. The skull table is
parallel-sided, pro-portionally small and flat. The supratemporal
fenestrae arecircular and small owing to overlap of squamosal,
parietal andpostorbital bones. The incisive foramen is
teardrop-shaped.Suborbital fenestrae are relatively small and
roughly triangular.The choana is transversely wide. Skull bones are
heavilysculpted with subcircular pits, particularly on rostrum
andskull table. The skull bears five and 13 alveoli in
premaxillaandmaxilla, respectively, and 18 alveoli in dentary.
Mandibularsymphysis is relatively flat as in G. brachyrostris and
E. cavernen-sis. Kuttanacaiman differs from E. cavernensis in
having palatineprocesses projecting anteriorly into suborbital
fenestrae (charac-ter 119-1), ectopterygoidpterygoid flexure
present throughoutontogeny (character 126-1), enlarged 12th dentary
alveolus(character 51-1) andposterior teeth laterally compressed
(charac-ter 79-1) and globular (character 198-2). It differs fromG.
pebasensis and G. brachyrostris in lacking splenial symphysis.9
5 cm
2 cm
gavialoidscaimanines
crocodyloidsbasal eusuchians
small caimanines with crushing dentitionnon-caimanine
alligatoroids
) (e)
(g)( f )
caimanines (af ) and the sole gavialoid (g) from Iquitos are
indicated in amaterial, figure S3 and text S1). (a) Gnatusuchus
pebasensis gen. et sp. nov.,ull. (c) Caiman wannlangstoni sp. nov.
(MUSM 2377), skull. (d ) Purussaurusentary. ( f ) Pebas Paleosuchus
sp. (MUSM 1985), right maxilla in lateral view.s correspond to the
four potential combinations of the bidimensional snout-l
lengthskull length index.(character 54-2). Total body length
estimate is 171.2189.1 cm(see electronic supplementary material,
table S7).
Caiman wannlangstoni, sp. nov.Etymology: wannlangstoni after
Wann Langston Jr, for
his invaluable contributions to the knowledge of SouthAmerican
fossil crocodylians.
Holotype: MUSM 2377, partial skull (figures 1g,h,j,
2c;electronic supplementary material, figure S3b and table S5).
Locality and horizon: Locality IQ26 (electronic supplemen-tary
material, figure S1 and text S1), Iquitos area, Peru;
PebasFormation, late Middle Miocene, ca 13 Ma; MZ8 [4].
Referred specimens: MUSM 1983, associated cranial andmandibular
elements (figure 3f ), locality IQ114 (see electro-nic
supplementary material). Also AMU-CURS-49, a rightpremaxilla and
maxilla, from the Urumaco Formation [20].
Diagnosis: Small- to medium-sized Caiman species diag-nosed by
the following combination of characters: high andblunt snoutwith
lateralmargins strongly sinuous anddivergingposteriorly; canthi
rostralii very prominent; maxilla bearingbroad shelf extending into
suborbital fenestra, prefrontalscontacting medially; edges of
orbits upturned; narial openingoriented anterodorsally; crown teeth
smooth to ribbed withincrown upper half; dentary and maxillary
posterior teeth large,globular, tightly packed and rounded in
section; pterygoid sur-face pushed inward anterolateral to choana;
dentary symphysisextended to level of sixth alveolus.
General description: The skull is roughly triangular in
dorsalview. It bears a markedly high and robust rostrum. The
nasalbones project into a fairly large narial opening. The orbits
areoval and large. The jugal barely reaches the anterior margin
-
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d7
d s
d1113
d4d3
d2d1of the orbits, thus its medial contact with lacrimal is
reduced.The supratemporal fenestrae are constricted, as is typical
in cai-manines. Posterior margin of skull table is semicircular
andoverhangs the occipital plate. Configuration of the skull
tablebones resembles that of Caiman latirostris and
Melanosuchusniger. Caiman wannlangstoni differs from K.
iquitosensis in
(b)
(c)
(e)
Pachother
(g)
(h)
(k)( j)
7.5% 72.9% 42.1%
swamp
( f )br(6) m10m5
DI
d2d1
d1
d12d10d17
d4
d4 d7
Figure 3. Crushing-dentition caimanines and co-occurring
pachydontine molluscs. (dorsal (a), anterodorsal (b) and lateral
view (c). (d ) MUSM 2040, posterior mandibposterior dentition. ( f
) Caiman wannlangstoni, MUSM 1983, posterior dentition. (g)
Ienvironments of the Pebas System [2]. Percentage values correspond
to the estimateshelled Pachydon obliquus (h,i,k,l) and Pachydon
cuneatus ( j) with convex outline mpredation scars in specimens
that survived and then resumed growth. (k) Sharp edgewithout
(right) crushing damage. See electronic supplementary material, and
[2] andtooth wear. d, dentary; d14, d7, d914, d17, dentary tooth
positions; DI, diastemapositions; s, splenial. Scale bars: 5 cm for
(a), 2 cm for (b f ) and 1 cm for (h l).having upturned orbital
edges (character 137-1), canthi rostralii(character 96-1), alveoli
circular in cross section (character 79-0),pterygoid surface
lateral and anterior to internal choanapushedinward (character
123-1) and surangularangular sutureintersecting external mandibular
fenestra along its ventralmargin (character 60-1). Here, we refer
AMU-CURS-49, a
ydon obliquus assemblage molluscan assemblages
(l)
(i)
38.7% 88.8%
lake
dysoxicbottom
d14d9
m10m13
(d )
DI
d12
ad) Gnatusuchus pebasensis. MUSM 662, anterior mandibular
anatomy inular dentition in lateral view. (e) Kuttanacaiman
iquitosensis, MUSM 1942,nferred distribution of molluscan
assemblages within the typical depositionald average abundance of
the Pachydon group within each assemblage. Thick-aking them well
capable to withstand external pressure. (h,i) Crushing types
typical of this type of predation. (l ) Detail of cardinal tooth
with (left) and[4] for molluscan data and localities. Arrows in
(b,c,e,f ) indicate severe crown; br(6), bone resorption in
alveolar position 6; m5, m10, m13, maxillary tooth
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tris [21]. It shares several features with C. wannlangstoni
and
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belong to this new species as well. However, La VentaCaiman lacks
the distinctive high rostrum and anterodorsallynarial opening
observed in C. wannlangstoni. Although pre-served teeth are blunt,
there is no conclusive evidence thatLa Venta Caiman had enlarged
and globular posterior teeth.Consequently, we propose to treat it
as a distinct entity ofuncertain taxonomic affinities until more
anatomical dataare available. Caiman brevirostris from Acre
(Brazil) and proba-bly Urumaco (Venezuela) [22] can be
distinguished fromC. wannlangstoni in having a proportionally
shorter andparallel-sided rostrum as well as long dorsal
premaxillaryprocesses (character 90-1), prefrontals separated by
frontalbone (character 129-1), and pterygoid surface lateral
andanterior to internal choana flush with choanal margin
(character123-1). The estimated total body length of C.
wannlangstoni is210.5226.7 cm (see electronic
supplementarymaterial, table S7).
(b) Other crocodylians of the Pebas SystemBesides the
blunt-snouted caimanines with crushing dentitionand stout jaws, we
also recovered the first unambiguousfossil of the extant
smooth-fronted caiman Paleosuchus, whichpossesses a relatively more
generalist snout shape (figure 2f ).It bears a lightly built
maxilla with vertically orientedwalls, and distinctive sharply
pointed teeth. As in other speciesof Paleosuchus, it has four
premaxillary teeth (character 87-1)and a notched palatine anterior
process (character 113-1).Although still poorly known, this fossil
taxon (Paleosuchussp.) differs from its extant relatives in having
fewer maxillaryteeth and a proportionally longer anterior process
of the ectop-terygoid running medially to posterior alveoli
(electronicsupplementary material, figure S4). Large caimanines are
rep-resented by Purussaurus neivensis and Mourasuchus atopus,
theonly two Pebasian taxa previously known from Miocenelocalities
in the region [15]. Purussaurus possessed a hulkingskull and
amandiblewith large robust anterior teeth and smal-ler blunt
posterior teeth (figure 2d). Among a set ofPurussaurusteeth from
IQ125 (electronic supplementary material, figureS1), we recognized
teeth with bulb-shaped crowns that areindistinguishable from those
of coeval Balanerodus longimus[15], suggesting that material of
this latter species [23,24]pertains instead to specific regions of
Purussaurus jaws, under-mining recognition of it as a distinct
taxon. The duck-facedtaxon Mourasuchus occupies one extreme of
crocodyliansnout morphotypes, with an exceptionally long and wide
ros-trum (figure 2e). Its feeding habits are controversial,
although itwas considered to eat small organisms (e.g. fishes) by
somekind of filtering strategy [15]. A new, unnamed gavialoid
docu-ments the only crocodylian with a longirostral morphotype
inthis community (figure 2g), a fact that contrasts with the
highdiversity of longirostrine crocodylians characteristic of
LateMiocene Neotropical assemblages [20,25].
3. DiscussionThe crocodylian assemblage of the Iquitos bonebeds
is extra-ordinary in representing both the highest taxonomic
diversityright premaxilla andmaxilla, from the Urumaco Formation
[20]toC. wannlangstoni based on the presence of strong sinuous
ros-tral margins and robust globular posterior teeth. UCMP 39978,a
partial skull from La Venta (Colombia), was originallyreferred to
Caiman lutescens [15] and more recently to C. latiros-and the
widest range of snout morphotypes ever recorded inany crocodyliform
community, recent or extinct. Other pre-viously proposed peaks in
sympatric diversity (e.g. in LateMiocene faunas of Venezuela and
Brazil) are based onmaterialfrom correlated strata of various
localities and multiplehorizons within basins rather than from a
single site [18,25].The hyperdiverse Iquitos assemblage (six
caimanines andone gavialoid; figure 2) includes five new taxa that
form theendemic Pebasian crocodylian fauna of the long-lived
proto-Amazonian lakes that occupied most of western Amazoniaduring
the Middle Miocene. Taxonomic distinctions fromcoeval assemblages
within the same Neotropical realm, suchas La Venta, Colombia [15]
and Fitzcarrald, Peru [24], probablyrepresent more
fluvial-dominated palaeoenvironments. Theextraordinary
heterogeneity of snout shapes at Iquitos coversmost of the
morphospace range known for the entire Cro-codylia clade (figure
2), reflecting the combined influences oflong-term evolution,
resource abundance and variety, andniche partitioning in a complex
ecosystem.
Small caimanines with posterior globular teeth wereconspicuous
components of the Pebasian crocodylian assem-blage (figure 3).
These posterior teeth resemble those of theextant teiid lizard
Dracaena, which has a strictly malacopha-gous diet [26]. In
addition to the globular dentition, thesetaxa share several other
distinctive traits (i.e. massive jaws,long symphysis, blunt snouts)
of particular ecologicalrelevance in the context of the peculiar
Pebas palaeoenviron-ment as they together strongly suggest
durophagy [27,28].We propose that this array of crushing-toothed
caimans predo-minantly fed on endemic molluscs that were copious in
thistime interval (MZ8; figure 4). Within the diverse fauna
ofapproximately 85 co-occurring endemic species [4,9],
corbulidpachydontine bivalves were especially abundant [2].
Thesebivalves display high morphological disparity and
distinctanti-predatory adaptations, including thick shells,
profuseornamentation, overlapping valves, globose shape and a
ros-trum projecting siphons [10]. Successful and unsuccessful(i.e.
healed) crushing predation scars are common and the pro-portion of
shell fragments with sharp edges typical of this kindof damage
reach up to 93% in valves of some molluscansamples (figure 3h l;
see electronic supplementary material).This extremely intense
predation had been attributed tofishes and decapod crustaceans
[10], but the Pebasian ichthyo-fauna does not differ significantly
from itsmodern Amazoniancounterpart [12], which lacks large-shell
crushing fishes and ispoor in molluscan species [33]. Instead, an
array of crushing-dentition Pebasian caimans co-evolved with and
exploitedthis trophically distinct, long-lasting, proto-Amazonian
epi-sode of increasing molluscan diversity and abundance,resulting
in the high mollusc predation intensity observed.Consistent with
these predatorprey interactions, the crocody-lian crusher
morphotype exhibits anterior and posterior teethwith severe wear
(figure 3e,f). The Iquitos bonebeds are alsorich in isolated
globular caiman teeth that were worn flat,suggesting active
crushing or grinding during normal feedingactivity. Small
globidontan crocodylians from the Cretaceousand Palaeogene of the
Great Plains of United States were inter-preted as shell crushers
owing to similar feeding-related traitsand heavy surface wear
pattern [27,28]. At least during thePalaeocene epoch, the huge
freshwater systems of the GreatPlains hosted three genera of
corbulid bivalves that alsooccurred in the Pebasian Mega-Wetland
System (Pachydon,Ostomya and Anticorbula), possibly indicating a
much longer
-
Kutta
naca
iman
iqui
tose
nsis
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MZ
Plt.
Plio
cene
Mio
cene
Pala
eo-O
rinoco Am
azonia
n R
iver
s Sys
tem
cust
rine-
tidal
fluvi
al-tid
al
Acr
e ph
ase
Ages/events Molluscan diversity Palaeomaps
Palaeo-Orinoco
Acre
Pebas
(a)Amazon drainage onset
(b)
0 30 60 spp.
4
6
8
10
12121110987
m
65432
14
16 Gna
tusu
chus
peb
asen
sisG
lobi
dent
osuc
hus b
rach
yrost
riscorbulidglobidontan interaction [34]. Similar interactions
arehypothesized for molluscs and durophagous freshwater sting-rays,
co-occurring in early Palaeogene deposits of both theGreat Plains
(Palaeocene) and Western Amazonia (MiddleEocene-onward) [35].
Even though correlations betweenmorphotype and ecologycannot be
stated with certainty in extinct taxa, the singularG. pebasensis
anatomy not only further supports durophagybut also reveals other
distinctive aspects of its feeding strategy.Unique among
crocodyliforms, Gnatusuchus possesses a den-tary bearing a large
edentulous gap between the sevenprocumbent anterior and four
globular posterior teeth. Thismammal-like diastema of about 30 mm
results from the evol-utionary loss of most of the alveoli lying
between the dual(anterior and posterior) regions of maximum
alveolar diameter
PALA
EOG
ENE
Cret
aceo
us
prot
o-A
maz
on
iaPe
ba la
1
18
20
22
GlobidontaC
Alligatorinae
Globidontan crocodylianswith crushing dentition
ASEUNA
NA
Al
logn
atho
such
us-lik
e
Albe
rtoch
amps
aBr
ach
ycha
mps
aSt
ange
roch
amps
a
Eoca
iman
cav
erne
nsis
oth
er a
lliga
torin
es
NA
Figure 4. Phylogenetic position of the Pebasian caimanines
within the Alligatoroide(see electronic supplementary material,
figure S6 and test S1). Gnatusuchus pebasensoutgroup to all
remaining caimanines; these two taxa reveal unknown character
statesglobular teeth) and their inclusion influenced the topology
of relationships within thebetween the South American caimans and
the North American Cretaceous globidonwhereas prior analyses showed
either the monophyly of Alligatoridae (Caimaninae polytomy within
the globidontan alligatoroids (Caimaninae [alligatorines and
Cretwhen the alligatorine Allognathosuchus wartheni is excluded
from the analysis. Resultdating back to the end of the Cretaceous
or Palaeocene interval. (a) The Acre Phase (cRiver System. (b) The
Pebas Mega-Wetland System in northwestern South America
durdentition caimanines, black lines for other taxa) relative to
major Neogene stages and evetriangles) and marine incursions (m)
are from Hoorn et al. [1]. Molluscan Zones and dsuitable, internal
nodes were time-calibrated with molecular data from Oaks [32].
Darker(CA), Europe (EU) or North America (NA).rei
Pale
osuc
hus t
rigon
atus
Pale
osuc
hus p
alpe
brosu
s
Caim
an la
tirost
ris
C. c
roco
dilu
s
Mel
anos
uchu
s nig
er
Mel
anos
uchu
s fis
heri
P. m
iranda
iP.
br
asi
liens
is
M. n
ativ
usM
. are
nds
iM
. am
azon
ensi
s
C. b
revi
rost
ris
Caim
an w
annl
angs
toni
Puru
ssau
rus n
eive
nsis
Mou
rasu
chus
ato
pus
La Ve
nta
Ca
iman
C. ja
care
Peba
s Pale
osuc
hus s
p.
CAof most crocodylians [36]. Mandibular rami are firmly
sutured,yielding the longest symphysis observed within
globidontanalligatoroids, and a stable shovel-like structure for
the lowerjaws (figure 3ac). Posteriorly, the mandibular ramus is
highand robust. In this region, the entire ramus is tilted
latero-ventrally and houses a wider and more capacious
adductorfossa (figure 1d). In Gnatusuchus, strong adductor
musclesand robust mandibular joints might have facilitated any
feed-ing activity involving powerful dislocating jaw forces.
Thisdistinctive dental and craniomandibular anatomy is
consistentwith a durophagous diet, as well as with head
burrowingactivity in search of prey. Infaunal pachydontine
bivalves(length approx. 725 mm) were diverse and abundant
inunconsolidated bottoms of dysoxic lakes of the Pebas
System(figure 3h l ) [2,10]. Gnatusuchus probably fed on them
by
aimaninae
JacareaNe
crosu
chus
ione
sis
Cent
enar
iosu
chus
gilm
o
C. tr
emem
bens
is
Tsoa
bich
i gre
enri
vere
nsi
s
NA
a. Time-calibrated, strict consensus cladogram of 70 most
parsimonious treesis is the most basal caimanine and
Globidentosuchus brachyrostris is the nextancestrally present
within the caimans (i.e. long splenial symphysis, posterior
caimanine clade. Character support provides a novel
sister-grouped relationshiptan alligatoroids (i.e. Brachychampsa,
Albertochampsa and Stangerochampsa),Alligatorinae) exclusive of
Cretaceous globidontans [29,30] or, more recently, aaceous
globidontans]) [18,31]. Here, this polytomy (dotted lines) is
obtaineds also suggest an early diversification of major groups
within the Caimaninaea 9 Ma) after intense Andean uplift and onset
of the transcontinental Amazoning MZ8 (ca 13 Ma). Stratigraphic
distribution of taxa (yellow bars for crushing-nts in Amazonia.
Palaeogeographical reconstructions, Andean uplift peaks
(blackiversity for the Pebas System (MZ112) are from Wesselingh et
al. [4]. Whengrey marks MZ8. Alligatoroids are from South America,
Asia (AS), Central America
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shoveling with the jaw and the procumbent anterior teeth,then
crushing shells with the globular, tightly packed posteriorteeth.
During durophagy, traumatic tooth avulsion and severedamage
involving tooth replacement might provide expla-nations for cases
of bone resorption of posterior tooth loci inGnatusuchus mandibles.
Alveolar remodelling is also observedin one specimen of K.
iquitosensis (figure 3e). Although this con-dition is common among
crushing-dentition Pebasian caimans,it is unusual among extinct or
extant reptiles [37]. Oxygen-stressed environments might be adverse
for many potentialpredators feeding on mud bottoms (e.g. benthic
fishes orcrustaceans) but not for air-breathing caimans.
This new fauna highlights co-occurrence at approximately13 Ma of
every phylogenetic lineage currently recognizedwithin the
Caimaninae, emphasizing the role these proto-Amazonian
mega-wetlands played in fostering the persistenceof basal lineages
simultaneously with the initial diversificationof their modern
relatives (figure 4; electronic supplementalmaterial, figure S6).
Phylogenetic analysis of a morphologi-cal dataset (see electronic
supplemental material) positionsGnatusuchus as the most basal
caiman, suggesting that a blunt-snouted rostrum with crushing
dentition could have been theancestral condition for the entire
clade, while the more general-ized morphology of the caiman
crown-group is derived (figure4). A long mandibular splenial
symphysis also might be associ-ated with early stages of caimanine
evolution [18]. Anevolutionary pattern in which generalist taxa,
such as theextant species of Caiman, originated from
blunt-snoutedcrushers was similarly proposed for a different
crocodylianclade: the alligatorines [38]. This distinctive
caimanine morpho-type, closer to that of Cretaceous alligatoroids,
was unknownprior to the discovery of the Miocene taxa Gnatusuchus
and Glo-bidentosuchus, probably owing to the scarce Palaeogene
fossilrecord in tropical South America. Similarly, Palaeocene
oreven Cretaceous origins and diversification of some
caimaninegroups consequently are expressed as long ghost
lineageswithin the time-calibrated phylogenetic tree (figure 4),
predict-ing currently unrecovered high morphotypic and
taxonomicdiversity continuously along caimanine evolutionary
historyuntil the LateMiocene. Regarding the evolution of globular
den-titions, results of this analysis also suggest that a
reversaloccurred later within jacarean caimanines. Posterior
globularteeth of the new crushing-dentition taxon C.
wannlangstoniwould have evolved from a generalized dental pattern
as anopportunistic adaptation to the increasing abundance
anddiversity of molluscs throughout theMiddle Miocene (figure
4).
The Pebas fossil record further underlines the occurrence ofa
key ecological turnover in western Amazonia around theMiddleLate
Miocene transition, providing new insights onestablishment of
modern ecosystems. The Iquitos bonebedsimmediately underlie strata
documenting episodes of marineincursions and the first decline in
endemic mollusc diversity[3,4]. This stage (MZ9, ca 12 Ma)
represents the initial demiseof dysoxic lacustrine Pebas
environments [4] and coincideswith events of intense Andean uplift
that dissected proto-Ama-zonia into the modern Magdalena, Orinoco
and Amazonianriver basins. Major reorganization of drainage
patterns atapproximately 10.5 Ma included initiation of the
transcontinen-tal Amazon River drainage (figure 4) [1,39,40].
Lignite-pooroutcrops just above MZ9 [41] in the Nueva Union area
southof Iquitos yield the youngest record of Gnatusuchus, but donot
contain other crushing-dentition caimanines. Giant cai-mans like
Purussaurus and Mourasuchus are common atNueva Union, as is also
characteristic in the Late Miocene Soli-moes Formation of Acre that
represents the fluvio-tidal AcrePhase, when a transcontinental
river system first became estab-lished [3]. Contrary to the Pebas
System, small- to medium-sized caimanines in Acre are represented
by two Caimanspecies, including only one short-snouted species
(i.e. C. brevir-ostris) with blunt posterior teeth considered
ecologically similarto the extant C. latirostris [22,25].
Relatively depauperate fluvialmollusc assemblages dominate the Acre
Phase [42], resemblingmodern Amazonian faunas. In northern South
America, theUrumaco Formation (coeval with the Late Miocene
SolimoesFormation) documents life in the palaeo-Orinoco basin,
includ-ing at least three crushers among both basal (i.e.
G.brachyrostris) and advanced caimanines, such as the PebasianC.
wannlangstoni [18,20]. Freshwater molluscs have not beendescribed
there yet, but shells are abundant throughout theUrumaco Formation
[43]. As a whole, Acre and Urumaco cro-codylian faunas are highly
similar (i.e. several longirostrinecrocodylians, giant taxa among
gavialoids and caimanines)[25], although evidence suggests that an
equivalent array ofthe Pebas crushing-dentition caimanines
persisted during theLate Miocene within the palaeo-Orinoco [18],
whereas theydecayed in the Amazonian Acre Phase, suggesting faunal
pro-vincialism and persistence of Pebas-like ecosystems
throughoutthe Late Miocene only in the northernmost Neotropics.
Morphological diversification of crusher crocodyliansduring the
Pebas System, including the singular anatomy ofthe shoveling
caimanG. pebasensis, appears to have been largelydriven by
adaptation to the abundance of molluscan foodsources in dysoxic
lake bottom habitats. Crocodylian peakdiversity was reached near
the end of theMMCO, prior to frag-mentation of these
proto-Amazonian wetlands. Central andnorthern Andean uplift at
approximately 12 Ma (MiddleLateMiocene transition) not only
contributed to retreat of the Peba-sian system to northernmost
South America but also fosteredthe origin of the transcontinental
flow of the modern AmazonRiver [1,44]. This transition ultimately
led to the developmentof earlyAmazonian-type trophic dynamics that
favoured fluvialfaunas, including the initial replacement of more
archaic, dieta-rily specialized crocodylians by the more
generalist-feedingcaimans that dominate modern Amazonian
ecosystems.
Acknowledgements. We thank A. Balcarcel, A. Goswami, B.
Shockey,R. Varas, A. Wyss and everybody who helped us during
fieldwork;A. Balcarcel and W. Aguirre for the fossil preparation;
M. Ellison andA. Benites for specimen photographs; C. de Muizon
(MNHN) andR. Hulbert (UF) for access to comparative collections; J.
Clarke,A. Valdes-Velasquez, G. Billet, S. Jouve and J. Martin for
valuable dis-cussions; K. Montalban-Rivera for modelling the life
reconstruction ofGnatusuchus pebasensis and O. Delgado for painting
it. We are muchindebted to G. Vermeij and an anonymous reviewer for
their construc-tive critical reviews. Iquitos specimens are
permanently deposited atthe Museo de Historia Natural, UNMSM
(MUSM), Lima, Peru. This isISEM publication 2015-006 SUD.
Author contributions. J.J.F., P.-O.A. and R.S.-G. designed the
research;R.S.-G., J.J.F., P.-O.A., P.B. and J.V.T.-L. contributed
to the survey andcollecting the crocodylian fossil material. F.P.W.
provided data onPebasianmolluscan fossil record and ecology. P.B.
provided geologicaldata. R.S.-G. wrote the manuscript and performed
anatomical descrip-tions and the systematic research,with
additionalwriting contributionsfrom all authors. All authors
contributed to the discussions andinterpretation of the
results.Funding statement. The study was financially supported by
the NationalAeronautics and Space Administration, Field Museum
(Chicago),Frick Fund (Vertebrate Paleontology, AMNH),
Environnements etCLImats du Passe: hiStoire et Evolution (ECLIPSE)
Program of
-
France, Centre National de la Recherche Scientifique and
Institut deefn C
and from financial support of the Frick Fund (AMNH) for
visitingme a
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A Miocene hyperdiverse crocodylian community reveals peculiar
trophic dynamics in proto-Amazonian
mega-wetlandsIntroductionResultsSystematic palaeontologyOther
crocodylians of the Pebas System
DiscussionAcknowledgementsAuthor contributionsFunding
statementCompeting interestsReferences