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: rodolfo.salas-gismondi@univ-montp2.fr

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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on March 5, 2015http://rspb.royalsocietypublishing.org/Downloaded from mentary 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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(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).

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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

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(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

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(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 ).

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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

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small caimanines with crushing dentitionnon-caimanine alligatoroids

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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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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

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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

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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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on March 5, 2015http://rspb.royalsocietypublishing.org/Downloaded from might 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

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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

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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

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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

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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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on March 5, 2015http://rspb.royalsocietypublishing.org/Downloaded from 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

12. Monsch KA. 1998 Miocene fish faunas from Gryposuchus, and the South American gavials. Inlogy ina Venta,

overview of potamotrygonid dental morphology.

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on March 5, 2015http://rspb.royalsocietypublishing.org/Downloaded from northwestern Amazonia basin (Colombia, Peru,Brazil) with evidence of marine incursions.

Vertebrate paleontoMiocene fauna of Lthe neotropicstheColombia (eds RF Kay,

Naturwissenschaften 101, 3345. (doi:10.1007/s00114-013-1127-1)marine molluscan faunas of the Pebasian and otherinland basins of north-western South America. Bull.Br. Mus. Nat. Hist. Geol. 45, 165371.

Paleontol. 34, 820834. (doi:10.1080/02724634.2014.838173)

23. Langston W, Gasparini Z. 1997 Crocodilians,

35. Adnet S, Salas-Gismondi R, Antoine PO. 2014 Riverstingrays (Chondrichthyes: Potamotrygonidae) fromthe middle Eocene of Peruvian Amazonia and anRecherche pour le Developpement. R.S.-G. bengrant of the Escuela Doctoral Franco-Peruana e

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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