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A New Horned Crocodile from the Plio- Pleistocene Hominid Sites at Olduvai Gorge, Tanzania

Article in PLoS ONE · February 2010 DOI: 10.1371/journal.pone.0009333 · Source: PubMed

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The user has requested enhancement of the downloaded file. A New Horned Crocodile from the Plio-Pleistocene Hominid Sites at Olduvai Gorge, Tanzania

Christopher A. Brochu1*, Jackson Njau2,3, Robert J. Blumenschine4, Llewellyn D. Densmore5 1 Department of Geoscience, University of Iowa, Iowa City, Iowa, United States of America, 2 Human Evolution Research Center, Department of Integrative Biology, University of California, Berkeley, California, United States of America, 3 National Natural History Museum, Arusha, Tanzania, 4 Center for Human Evolutionary Studies, Department of Anthropology, Rutgers University, New Brunswick, New Jersey, United States of America, 5 Department of Biological Sciences, Texas Tech University, Lubbock, Texas, United States of America

Abstract

Background: The fossil record reveals surprising crocodile diversity in the Neogene of Africa, but relationships with their living relatives and the biogeographic origins of the modern African crocodylian fauna are poorly understood. A Plio- Pleistocene crocodile from Olduvai Gorge, Tanzania, represents a new extinct species and shows that high crocodylian diversity in Africa persisted after the Miocene. It had prominent triangular ‘‘horns’’ over the ears and a relatively deep snout, these resemble those of the recently extinct Malagasy crocodile Voay robustus, but the new species lacks features found among osteolaemines and shares derived similarities with living species of Crocodylus.

Methodology/Principal Findings: The holotype consists of a partial skull and skeleton and was collected on the surface between two tuffs dated to approximately 1.84 million years (Ma), in the same interval near the type localities for the hominids Homo habilis and Australopithecus boisei. It was compared with previously-collected material from Olduvai Gorge referable to the same species. Phylogenetic analysis places the new form within or adjacent to crown Crocodylus.

Conclusions/Significance: The new crocodile species was the largest predator encountered by our ancestors at Olduvai Gorge, as indicated by hominid specimens preserving crocodile bite marks from these sites. The new species also reinforces the emerging view of high crocodylian diversity throughout the Neogene, and it represents one of the few extinct species referable to crown genus Crocodylus.

Citation: Brochu CA, Njau J, Blumenschine RJ, Densmore LD (2010) A New Horned Crocodile from the Plio-Pleistocene Hominid Sites at Olduvai Gorge, Tanzania. PLoS ONE 5(2): e9333. doi:10.1371/journal.pone.0009333 Editor: Carles Lalueza-Fox, Institute of Evolutionary Biology (CSIC-UPF), Spain Received December 9, 2009; Accepted January 27, 2010; Published February 24, 2010 Copyright: ß 2010 Brochu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: National Science Foundation (www.nsf.gov): NSF DEB 0444133, NSF DEB 0228648. Wenner-Gren Foundation for Anthropological Research (www. wennergren.org). Rutgers University Center for Human Evolutionary Studies (evolution.rutgers.edu). National Geographic Committee for Research and Exploration (www.nationalgeographic.com/field/grants-programs/cre.html). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected]

Introduction usually support a close relationship between the C. niloticus and a clade of Neotropical species [21,22,23,24,25], but relationships Until recently, it was thought that the ancestors of modern among other species of Crocodylus are largely unresolved, as is the African crocodiles would be found among Oligocene through placement of the African sharp-nosed crocodile (Mecistops Pliocene fossils found in Africa [1,2,3,4]. Many of these resembled cataphractus), which may be related to either Crocodylus or Osteolaemus the living Nile crocodile (Crocodylus niloticus), but recent phyloge- [23,25,26,27,28,29]. Thus, whether C. niloticus represents an netic analyses argue instead that many belong to an endemic clade African lineage separate from the osteolaemine radiation or a with only one unambiguous living representative – the African more recent immigrant is unclear [30]. A better understanding of dwarf crocodile Osteolaemus. Gross similarity with C. niloticus, along Neogene African crocodylids is needed to resolve these issues. with misconceptions of crocodiles as evolutionarily static ‘‘living One of these, Rimasuchus lloydi, was long thought to be close to fossils,’’ obscured the diversity of this group through the Neogene the ancestry of C. niloticus before phylogenetic analyses suggested of Africa, Madagascar, and possibly Aldabra Atoll and the an osteolaemine affinity [17,23]. But codings in these analyses are Arabian Peninsula [5,6,7,8,9,10,11,12,13,14,15,16,17]. Just as based on material from the Middle Miocene type locality in Egypt, living African crocodile species may represent cryptic species and fossils from all over Africa, ranging in age from the Early complexes [18,19,20], their fossil relatives were more diverse than Miocene through Quaternary, have been referred to R. lloydi previously supposed, with outwardly similar (though not always [2,13,15,16,31,32]. The phylogenetic relationships of these other related) species mistaken for geographically widespread species fossils remain untested. with long stratigraphic ranges. Some of these are from the Plio-Pleistocene deposits exposed in Several questions remain. Fossil and molecular data suggest a Beds I through IV at Olduvai Gorge, northern Tanzania. Bed I is Neogene divergence among living species of Crocodylus, and they the oldest level at Olduvai and is best known for key discoveries of

PLoS ONE | www.plosone.org 1 February 2010 | Volume 5 | Issue 2 | e9333 Extinct Horned Crocodile extinct human species, including the holotypes of Australopithecus obtainable (from the publication date noted on the first page of this boisei and Homo habilis, as well as evidence of the earliest stone tools article) for the purpose of providing a public and permanent [33,34,35]. Some of these hominids were bitten by crocodiles at or scientific record, in accordance with Article 8.1 of the Code. The near the time of death [36,37], and some objects thought to be separate print-only edition is available on request from PloS by early tools may be crocodile gastroliths [38]. The crocodiles were ending a request to PloS ONE, 185 Berry Street, Suite 3100, San referred first to C. niloticus [39] and later to Rimasuchus lloydi [2]. Francisco, CA 94107, USA along with a check for $10 (to cover A partial skull and skeleton collected in 2007 by the Olduvai printing and postage) payable to ‘‘Public Library of Science.’’ Landscape Paleoanthropology Project prompted a reevaluation of In addition, this published work and the nomenclatural acts it crocodile remains from Olduvai Gorge. It reveals a deep-snouted, contains have been registered in ZooBank, the proposed online horned animal outwardly similar to a recently-extinct osteolae- registration system for the ICZN. The ZooBank LSIDs (Life mine from Madagascar (Voay robustus) but referable to Crocodylus.It Science Identifiers) can be resolved and the associated information can be distinguished from other known species of Crocodylus, living viewed through any standard web browser by appending the LSID or extinct, and forms the basis for a new species. to the prefix ‘‘http://zoobank.org/’’. The LSID for this publication is urn:lsid:zoobank.org:pub:CB77D4ED-B0B6-4F16- Institutional Abbreviations AAE7-231CF9F4DEBE. AMNH, American Museum of Natural History, New York; Clade names follow currently-used phylogenetic definitions FMNH, Field Museum, Chicago; KNM, National Museums of [40]. Although the definition of Crocodylidae is context-depen- Kenya, Nairobi; NHM, Natural History Museum, London; dent based on the position of Gavialis, the new species would be a NNHM-OLD, National Natural History Museum, Arusha, crocodylid regardless of context. Tanzania (Olduvai Collections); PNCZ, Parque Nacional Cie´naga de Zapata, Playa Larga, Matanzas, Cuba; USNM, U.S. National Systematic Paleontology Museum of Natural History, Washington, DC. Eusuchia Huxley 1873 Crocodylia Gmelin 1789, sensu Benton and Clark 1988 Anatomical Abbreviations Crocodylidae Cuvier 1807 4t, 4th trochanter of femur; an, angular; art, articular; asf, Crocodylus anthropophagus, new species anterior sacral facet; bo, basioccipital; ccr, caviconchal recess; cor, urn:lsid:zoobank.org:act:052051B8-6503-42B3-8D7A- coronoid; cqc, cranioquadrate canal; cr, recesses on caviconchal 9E7E49578401 recess medial wall; d, dentary; dlc, deltoid crest; dp, diapophysis; Holotype specimen. NNHM-OLD-1001, partial skull and dpc, deltopectoral crest; ect, ectopterygoid; emf, external mandib- skeleton (Fig. 1, Fig. 2, Fig. 3). ular fenestra; en, external naris; eoa, external otic aperture; ex, Referred Material. NHM R.5891, cranial and postcranial exoccipital; f, frontal; faa, articular foramen aereum; faq, quadrate fragments; NHM R.5893, partial skull and skeleton (Fig. 4O–T; foramen aereum; fioc, foramen intermedius oralis caudalis; fm, Fig. 5D,E); NHM R.5894, postcranial elements; and several foramen magnum; gf, glenoid fossa of articular; gfs, scapular specimens in the KNM collections. Most do not have catalogue glenoid fossa; hyp, hypapophysis; ibc, constriction on psterior iliac numbers beyond their collection date and locality. Postcranial blade; if, incisive foramen; itf, infratemporal fenestra; j, jugal; k, elements cannot be associated with particular cranial material (or keel; l, lacrimal; lc, lacrimal crest; lcf, lateral carotid foramen; leu, with each other), but all available cranial evidence suggests a single lateral Eustachian foramen; lf, lingual foramen; lhc, lateral crocodylian species in these units. The following refer to particular hemicondyle; lp, lateral lamina of articular on surangular; specimens figured in this paper: m.pfp, medial process, prefrontal pillar; m5, fifth maxillary Crocodile Korongo (CROC K): OLD 62, partial skull (Fig. 4A– tooth/alveolus; mg, Meckelian groove; mhc, quadrate medial D); OLD 62 069/5866, right squamosal and quadrate ramus hemicondyle; mjf, medial jugal foramen; msc, muscle attachment (Fig. 4E). scar; mx, maxilla; n, nasal; o, orbit; oc, occipital condyle; op, Bell’s Korongo (BKII) channel: OLD 1960, right postdentary odontoid process; p.m5, protuberance on dorsal surface of maxilla elements of mandible (Fig. 5A–B). corresponding to 5th alveolus; pal, palatine; pf, prefrontal; pfp, Frida Leakey Korongo North I (FLKNI): cranial, mandibular, prefrontal pillar; pmx, premaxilla; pnr, prenarial rostrum; po, and postcranial material (Fig. 4F–N, Fig. 5C, Fig. 6, Fig. 7D). postorbital; pob, postorbital bar; poz, postzygapophysis; prz, These are derived from at least two (and probably more) prezygapophysis; psf, preotic siphonial foramen; psf, posterior individuals; the braincase (Fig. 6) is from a substantially smaller sacral facet; pt, pterygoid; q, quadrate; qj, quadratojugal; sa, animal than most other cranial fragments. surangular; soc, supraoccipital; sof, suborbital fenestra; sp, splenial; Douglas Korongo, trench 1B (DK IB): scapula and humerus sq, squamosal; stf, supratemporal fenestra; sym, symphysis; ta, (OLD 62 54). posteriormost (terminal) alveolus; tp, transition point between Etymology. anthropos, Greek, human and phagos, Greek, eater,in dorsal surface of skull table and squamosal horn; vf, vagus reference to the evidence that this animal included hominids in its foramen; xii, foramen for hypoglossal nerve (cranial nerve 12). diet. Articulation surfaces for adjacent bone denoted with ‘‘s.’’ (e.g. Locality and Age. Plio-Pleistocene, Olduvai Gorge, northern articulation surface for the maxilla = s.mx). Tanzania. The holotype was collected from the surface of Middle Bed I between Tuffs IB and IC, dated to 1.845+/20.002 and Nomenclatural Acts 1.839+/20.005 Ma, respectively [41]. FLKNI is near the type The electronic version of this document does not represent a localities of Australopithecus boisei and Homo habilis and is from Upper published work according to the International Code of Zoological Bed I. The DK locality also lies within Bed I. NHM R.5891 is Nomenclature (ICZN), and hence the nomenclatural acts from Bed I, and NHM R.5893 is from Bed II. Younger material contained in the electronic version are not available under that from BK II (upper Bed II) and CROC K (Bed III or IV) is also Code from the electronic edition. Therefore, a separate edition of referred to this species. Labels on KNM specimens from CROC K this document was produced by a method that assures numerous specify Bed IV, but published reports merely put crocodile remains identical and durable copies, and those copies were simultaneously from CROC K somewhere in Beds III or IV [35]. An additional

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preorbital crest typical of Indo-Pacific Crocodylus, and lacks the median rostral boss diagnostic for Neotropical Crocodylus. Description. The premaxillae (Figs. 1A–D and 4A,B) form the anterior and lateral margins of the narial aperture and are separated by the nasals medially behind the naris. Each bears an acute posterior process between the nasal and maxilla extending back to approximately the second maxillary alveolus. The naris opens anterodorsally, and the dorsal surface posterolateral to the narial rim and along the premaxillary-maxillary suture is inflated. The premaxillae surround a circular incisive foramen ventrally, and there is a deep occlusal pit anterolateral to the incisive foramen. The palatal lamina of each premaxilla has a convex posterior margin, causing the premaxilla-maxilla suture on the palate to form a shallow W. The right premaxilla of the holotype preserves three complete alveoli and the anterior margin of a fourth (Fig. 1B). There is a diastema between the first and second, and the second is smaller than both the first and third. The fourth is incomplete, but was larger than the third. The second alveolus is sometimes crowded away by the third during ontogeny in Crocodylus [42,43], but we do not believe this happened here; in crocodiles lacking the second alveolus, diastemata separate the three anteriormost alveoli, and the second remaining alveolus (originally the third) is similar in size to the first. Alveoli are imperfectly preserved on the KNM CROC K OLD 62 snout, but a small alveolus adjacent to the premaxilla-maxilla suture shows that C. anthropophagus had five premaxillary alveoli. None of the preserved maxillae are complete. One partial left element (Fig. 4G) preserves a complete series of 13 alveoli, of which the fifth behind the premaxilla is the largest. The maxillary palate is vaulted anteriorly, and the first six alveoli extend ventral to the palatal ramus. A small pit at the back of the toothrow might be the remnant of a fourteenth alveolus that no longer held teeth. Occlusal pits for the dentary teeth lie between the first ten alveoli. KNM FLKNI indicates that the suborbital fenestra extended anteriorly to the level of the ninth maxillary alveolus (Fig. 4J), and assuming the ectopterygoid was adjacent to four maxillary alveoli (see below), the maxillary ramus lateral to the fenestra bore five alveoli. An isolated right maxilla (KNM FLKNI, Fig. 4H–K) preserves the medial wall of the caviconchal recess, revealing a linear array of shallow pits. The circular posterior opening to the recess lateral to the nasopharyngeal duct is approximately medial to the eighth maxillary alveolus. The dorsal surface of the maxilla bears a prominent circular protuberance posterodorsal to the fifth Figure 1. Cranial remains of NNHM-OLD-1001, holotype, alveolus. The surface expands dorsally parallel to the sutural Crocodylus anthropophagus, preserving features diagnostic of contact with the nasal, forming a sharp linear crest. the species. Right premaxilla in medial (A), ventral (B), dorsal (C), and lateral (D) view; partial left squamosal in dorsal (F), posterior (G), and Each nasal bears a short conical process extending into the lateral (H) view; left lacrimal in dorsal view (J); frontal with adjoining narial aperture. The nasals flare posteriorly as they approach the parts of prefrontals in dorsal (K) and left lateral (L) view. Specimens are posterior tips of the premaxillae, but the point at which their compared with Crocodylus niloticus (KNM OR44, E; AMNH 7136, right lateral margins adopt a parasagittal orientation is not preserved. side reversed, I; KNM OR54, M). Scale = 1 cm. They taper posteriorly where they pass adjacent to the lacrimals doi:10.1371/journal.pone.0009333.g001 and prefrontals, forming short triangular processes separating the frontal from each prefrontal. specimen from Bed IV (NHM R.5892) may also pertain, but None is complete, but the preserved jugal fragments (Figs. 1B– diagnostic features were not preserved. All of these predate the E, 4S,T, 6A,B) collectively indicate the shape of the element. The Holocene. anterior ramus is flat and passes laterally over the maxilla. It forms Diagnosis. Crocodylus with a prominent triangular projection the ventral margin of the orbit and bears one or two large (‘‘horn’’) at the posterolateral corner of each squamosal dorsal to foramina between the medial surface and postorbital bar. The otic aperture at maturity; projection has discrete boundaries in posterior ramus is dorsoventrally shorter and mediolaterally lateral and posterior view. Pair of thin crests on rostrum thicker, tapering to a point posteriorly. It forms the ventral corresponding to the maxillary-nasal sutures. Maxillary ramus of margin and posteroventral corner of the infratemporal fenestra. ectopterygoid may not be forked, though expression of the cleft The jugal component of the postorbital bar is hemicylindrical, varies intraspecifically in most modern Crocodylus. External naris bearing a crescentic articulation facet for the ectopterygoid and opens anterodorsally rather than dorsally. Lacks the elongate postorbital medially.

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Figure 2. Craniomandibular remains of NNHM-OLD-1001, holotype, Crocodylus anthropophagus. A, partial left nasal, dorsal view; B, right quadratojugal, lateral view; C, right jugal, lateral view; D, left jugal, lateral view; E, left jugal, medial view; F, right otic region and quadrate ramus, lateral view; G, left quadrate ramus, dorsal view; H, left quadrate ramus, ventral view; I, left quadrate ramus and paroccipital process, posteromedial view; J, braincase, posterior view; K, right pterygoid wing, ventral view; L, left pterygoid wing, ventral view; M, right ectopterygoid, ventral view; N, left ectopterygoid, ventral view; O, right postdentary bones, lateral view; P, left quadrate, dorsal view; Q, left surangular, medial view; R, fragment of dentary; S, left surangular, lateral view. Scale = 5 cm. doi:10.1371/journal.pone.0009333.g002

The lacrimal forms the anterior margin of the orbit. The outline process that is constricted at its base and anteroposteriorly elongate is not completely preserved, but it extended further anteriorly than medially. the prefrontal. An oval aperture on its posterior surface, within the The dorsal surface of the frontal between the orbits is flat orbital margin, indicates the posterior opening of the lacrimal (Figs. 1K, 4C,F,O). Its anterior process is sharply demarcated from duct. It connected with the jugal laterally. the main frontal body, and the broad anterior process itself The partial left lacrimal associated with the holotype (Fig. 1J) terminates at an acute point approximately at the same level as the preserves a series of thin anteroposteriorly-oriented crests on its anterior margins of the prefrontal and the orbit. The frontopa- dorsal surface – a mediolaterally robust crest extending from the rietal suture is imperfectly preserved, but the posterior surface of lacrimal-prefrontal suture at the orbital margin and two thinner the frontal is convex, and the suture did not pass within the crests lateral to a shallow groove extending from the orbit. The supratemporal fenestra. medial crest and dorsal groove are generally present in most Those portions of the prefrontal and frontal bordering the orbit crocodyliforms (including most Crocodylus), but the lateral crests are are sharply upturned (Fig. 4D). On each side, they form a not. They are not apparent on the other specimens preserving continuous robust lamina extending from the prefrontal-lacrimal portions of the lacrimal (e.g. KNM FLKNI, Fig. 4F; NHM R5893, contact to the frontal-postorbital suture. The medial crest on the Fig. 4O), but this could be preservational – none of these preserves lacrimal can be seen as a rostral continuation of this structure. The much of the lacrimal lateral to the dorsal groove. Nevertheless, frontal-prefrontal suture changes orientation from mediolateral to pending better information on variation, these features are only anteroposterior at a right angle immediately medial to the lamina. provisionally considered diagnostic for the species. Two prominent knobs extend dorsally from each lamina, one The prefrontal forms the anteromedial margin of the orbit and entirely on the prefrontal and another at the frontal-prefrontal extends anteriorly to form an acute process between the nasal and contact. This is most apparent on the holotype (Fig. 1K). lacrimal. Based on NHM R5893 (Fig. 4O), the anterior process The postorbital includes a broadly crescentic dorsal corpus and extended approximately as far forward as the frontal. Its lateral columnar descending process comprising the dorsal and, ventrally, margin, where it contacts the lacrimal, is concave. The descending the medial portion of the postorbital bar. In at least one specimen processes forming the dorsal part of the prefrontal pillars are (e.g. NNHM-OLD-1001, Fig. 1H), it expands dorsally as it mediolaterally compressed structures, and the left descending approaches the squamosal posteriorly; but another isolated process of KNM CROC K OLD 62 (Fig. 4D) bears a medial squamosal (Fig. 4N) expands abruptly behind its sutural surface

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nasopharyngeal duct and the medial margins of the suborbital fenestrae. There are no discrete processes or expansions of the palatine into the fenestral space. Based on NHM R5893 (Fig. 4Q), the maxillary ramus of the ectopterygoid lies adjacent to four maxillary alveoli, possibly forming the medialmost wall of the posteriormost two alveoli. The anterior tip of the ramus appears to not be forked, although there is a modest concavity in its outline; the attachment scar for the ectopterygoid on the right maxilla of KNM FLKNI suggests the absence of an anterior cleft. The pterygoidal ramus (Fig. 2M,N) would have been fixed to the ventral surface of the pterygoid along the ventrolateral sides of the pterygoid wings. The pterygoids met the palatines along a linear sutural contact anterior to (and not intersecting) the internal choana (Fig. 4R). The pterygoid wings were broad and dorsoventrally thin, with flat articulation surfaces for the ectopterygoids ventrolaterally (Fig. 2K,L). The choana is partially preserved on a KNM specimen from FLKNI, and although the pterygoid surface was slightly elevated around the aperture, there was no choanal ‘‘neck.’’ Posteriorly, each pterygoid bears a small triangular process adjacent to the basioccipital, anterior to the lateral Figure 3. Postcranial remains of NNHM-OLD-1001, holotype, Eustachian foramen (Fig. 5C). Crocodylus anthropophagus. A, atlas intercentrum, anterior view. B, Anteriorly, the quadrate forms the margin of the otic aperture and axis centrum and odontoid process, right lateral view. C, cervical is pierced by a small circular preotic foramen (Figs. 2F, 4E, 5B). Its vertebra, right lateral view. D, dorsal osteoderm, posterior view. E, dorsolateral surface is smooth ventral to these openings, in marked dorsal osteoderm, dorsal view. F, proximal half of left humerus, ventral view. G, left ilium, medial view. H, metapodial, dorsal view. Scale = 5 cm. contrast to the heavily pitted quadratojugal and jugal. The quadrate doi:10.1371/journal.pone.0009333.g003 ramus bears a small foramen aereum on its dorsomedial surface, and the medial hemicondyle is dorsoventrally expanded relative to its for the postorbital, suggesting that the dorsal surface of the lateral counterpart (Figs. 2G, 5C). There is a large muscle attachment postorbital in that specimen would have been more planar. tubercle on the ventral surface of the ramus (Fig. 2H). The squamosal forms the posterolateral margin of the Details of the lateral braincase wall, including morphology of supratemporal fenestra. The lateral and posterior margins of the the laterosphenoid and prootic, are not preserved. Based on fenestra are almost linear, intersecting at a nearly right angle sutural contacts on the ventral surface of the frontal, the (Figs. 1F, 4M). The squamosal and postorbital together form the laterosphenoid capitate processes were oriented anterolaterally. roof of the external otic recess, and the cloverleaf-shaped otic The supraoccipital is likewise poorly known. Based on the aperture itself is bordered posterodorsally by the squamosal. The holotype (Fig. 2J), it is triangular in posterior view, bearing sagittal lateral squamosal groove for the ear flap musculature is crest that thickens dorsally. It would have been exposed on the dorsoventrally broad (Figs. 1F, 4N). The squamosal bears a flat skull table, but the shape of the dorsal exposure is not preserved. ventrolateral ramus that forms the anterior surface of the The exoccipital formed the posterior portion of the paroccipital paroccipital process. process, narrowing laterally from the post-temporal fenestra The dorsolateral margin of the squamosal forms a prominent (Fig. 2I,J). The cranioquadrate canal opens along the ventral dorsal hornlike projection. This takes the form of a mediolaterally margin of the exoccipital, passing anteromedially between the flattened lamina and is triangular in lateral view, with an apex exoccipital and quadrate. Medially, the exoccipitals meet at the dorsal to the otic aperture and posterolateral to the supratemporal midline dorsal to the foramen magnum and extend posteriorly fenestra. It arises abruptly from the dorsal surface of the skull table. dorsal to the occipital condyle, where each is pierced by one or two The apex is sharp in the holotype, and the lateral squamosal small foramina for the hypoglossal nerve. The descending process groove is continuous with a sulcus on the lateral surface of the of each exoccipital lateral to the main basioccipital body was horn (Fig. 1F–H). Other specimens suggest a more rounded apex pierced by a large common foramen for the ninth through and a broadly convex lateral surface (Fig. 4L–N). eleventh cranial nerves and the jugular vein (lateral to the foramen The parietal is incompletely known. Its articulation surface for magnum) and a carotid foramen lateral to the occipital condyle. the frontal is concave, and it did not contribute to the The basisphenoid is unknown, but based on sutural surfaces on supratemporal fenestra. Whether its dorsal surface was flat is the basioccipital of NNHM-OLD-1001and KNM FLKNI, it unknown, but it did not expand laterally as it approached the would have formed an anteroposteriorly thin sheet ventral to the squamosal and, hence, did not contribute to the squamosal horn. basioccipital. This sheet would have had a dorsoventrally short The quadratojugal lies between the jugal and quadrate. The exposure on the posterior occipital surface based on the minimal ascending ramus is not completely preserved, but based on sutural distance between the ventral margins of the basioccipital and surfaces on the quadrate and jugal, it formed nearly all of the pterygoid (Fig. 5C). posterior margin of the infratemporal fenestra, extending from just The basioccipital bears a robust spherical occipital condyle dorsal to the posteroventral corner to nearly to its dorsal apex; but projecting from a main body (Figs. 2J, 5C). The main body bears a whether it contacted the squamosal is unknown. sagittal crest, and the exoccipital descending processes did not The anterior process of the palatine was broad and formed a U- contribute to the modest basioccipital tubera. Notches for the shaped structure at its anteriormost extent at approximately the lateral Eustachian openings are nearly lateral to the circular level of the seventh maxillary alveolus (Fig. 4P). Posteriorly, the median Eustachian foramen. The main body is wedge-shaped in conjoined palatines (Fig. 4R) constitute the floor of the lateral view.

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Figure 4. Cranial remains referred to Crocodylus anthropophagus. KNM CROC K OLD 62: anterior end of rostrum, dorsal (A) and ventral (B) view; partial frontal with portions of prefrontals in dorsal (C) and anterior (D) view; right otic region and quadrate ramus, lateral view (E). KNM FLKNI: partial orbital region, dorsal view (F); left maxilla, ventral view (G); right maxilla, medial (H), lateral (I), ventral (J), and dorsal (K) view; right squamosal, posterior (L), dorsal (M), and lateral (N) view. NHM R.5893: orbital region, dorsal view (O); partial right maxilla, ventral view (P); partial right maxilla and ectopterygoid, ventral view (Q); partial palatines and pterygoids, ventral view ( R); partial right jugal, lateral (S) and medial (T) view. Scale = 5 cm. doi:10.1371/journal.pone.0009333.g004

No complete dentaries are preserved, but based on preserved One left (KNM BK II OLD 1960, Fig. 6A) and one right (KNM specimens (Fig. 6), there were at least fourteen alveoli on each FLKNI) coronoid are preserved. Each is mediolaterally flat and ramus. The fourth alveolus was enlarged, and the third was not communicates with the splenial anteriorly, angular ventrally, and confluent with it. Alveoli are circular, and a diastema separates the (to a minor extent) the surangular dorsally. The actual outline is eighth and ninth. The tenth and eleventh are enlarged relative to imperfectly preserved in both cases, but the KNM BK II mandible the anterior alveoli. The dentary symphysis extends to the level of reveals a small medial foramen intermandibularis oralis. The the fifth dentary alveolus, or to a level immediately behind it. dorsal ramus projects posteriorly for a short distance medial to the Lateral sulci between the seventh through ninth alveoli would have surangular, and its dorsal margin is oriented anteroposteriorly and received opposing maxillary teeth. does not slope anteriorly. The ventral ramus forms the The splenials do not meet at the midline. Its anteriormost extent ventromedial border of the adductor chamber. The coronoid is ventral to the slender Meckelian groove on the dentary at appears to contribute to the caudal formen intermandibularis approximately the level of the sixth dentary alveolus (Fig. 6E). The oralis, on the KNM specimen, but this most likely results from splenial expands posteriorly and contributes to the medial alveolar dorsoventral compression. borders beginning with the tenth dentary alveolus. It forms the The angular has a broadly convex ventral surface. Its medial anterodorsal border of the relatively large oval caudal foramen lamina forms the posteroventral and part of the dorsal margin of intermandibularis oralis, and there is no evidence for an anterior the caudal foramen intermandibularis oralis. Its lateral surface is perforation. smooth and unpitted where it forms the ventrolateral portion of

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the retroarticular process. Most preserved specimens (e.g. NNHM- OLD-1001, Fig. 2O) indicate a posterior ramus of the angular that extends roughly as far posteriorly as the surangular on the retroarticular process, but NHM R5893 suggests a truncated angular that terminates anterior to the surangular. Such a condition is highly unusual for any crocodylian, and in light of the consistently non-truncated angulars in other specimens, the NHM specimen is best viewed as aberrant. The surangular (Fig. 6) bears a pair of anterior processes. The dorsalmost process extends anteriorly to the dentary toothrow, and the ventral process is anteroposteriorly shorter and dorsoventrally wider. Its contact with the dentary in lateral view is linear and intersects the external mandibular fenestra along its anterodorsal margin. The surangular forms the entire posterior margin of the fenestra (Fig. 6B); the holotype (Fig. 3O) suggests intersection of the surangular-angular suture at the posteriormost end of the mandibular fenestra, but this is because the slender process of the surangular that would extend to the ventral margin is broken off. The smooth dorsal surface extends laterally between the mandibular fenestra and glenoid fossa, forming a robust lateral shelf (Fig. 2S). It passes along the dorsolateral surface of the retroarticular process and extends all the way to the posterior tip. Dorsally, the surangular contributes to the lateral glenoid subfossa. The descending ramus of the articular is triangular in cross- section, tapering to a rounded apex ventrally (Fig. 6). Its anterior surface is concave, and it bears a thin lamina on its lateral margin that passes along the medial surface of the surangular. A small foramen passes between the articular and surangular immediately ventral to this lamina. The glenoid fossa is comprised of two dorsal subfossae, and a sharply bowed angular-surangular suture passes through the lateral subfossa. The dorsal surface of the retro- articular process is also divided into two fossae separated by a low, broad anteroposterior ridge. A small foramen aereum pierces the articular at the anteromedial edge of the retroarticular process. All associated teeth are conical and bear unserrated mesiodistal Figure 5. Partial braincase and left quadrate ramus of KNM FLKNI, Crocodylus anthropophagus, in medial (A), dorsolateral carinae. (B), and posterior (C) view. Scale = 5 cm. Associated postcranial material is consistent with homologues in doi:10.1371/journal.pone.0009333.g005 living species of Crocodylus. The atlas intercentrum is a wedge-

Figure 6. Mandibular remains referred to Crocodylus anthropophagus. KNM BKII OLD 1960: left postdentary bones and posterior end of dentary, medial (A) and lateral (B) view; KNM FLKNI, dentaries and portion of right splenial, dorsal view (C); NHM R.5893, left dentary and splenial, medial (D) and lateral (E) view. Scale = 5 cm. doi:10.1371/journal.pone.0009333.g006

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sternbergii as the basalmost outgroup), Pristichampsus is closer to Crocodyloidea and trees are one step shorter. Character sampling in this analysis was focused on variation among crocodyloids. Most of the characters relevant to relationships among non-crocodyloid lineages were not included. Crocodylus is less resolved than in previous morphological analyses. This reflects incompleteness in two extinct species - Crocodylus anthropophagus and C. palaeindicus. Crocodylus anthropophagus assumes seven positions in the optimal trees – closely related to C. niloticus, C. rhombifer, C. palaeindicus, C. siamensis, the Neotropical clade, the Afro-Neotropical group, or the Indopacific group. Adams consensus trees (Fig. 8) restore the close relationship between the Neotropical species and C. niloticus supported by morphological [23] and molecular [24,25] evidence. Placements of C. anthropophagus within the Indopacific or Neotropical clades (other than as a close relative to C. rhombifer or C. siamensis) increase tree length by only one step. None of the most parsimonious placements has bootstrap support exceeding Figure 7. Postcranial material referred to Crocodylus anthro- 50%. Hence, although the data analyzed here support placement pophagus. A, KNM DK I B, left scapula, lateral view; B, NHM R.5894, of C. anthropophagus close to (if not within) Crocodylus, we are unable ?nuchal osteoderm; C, KNM DK I B OLD 62 54, right humerus, ventral to pinpoint its relationships more precisely. view; D, KNM FLKNI, right femur, ventral view. Scale = 5 cm. doi:10.1371/journal.pone.0009333.g007 Discussion shaped object with a dorsal concavity flooring the neural canal and Phylogenetic Relationships prominent diapophyses (Fig. 3C). The axis centrum bears a robust A close relationship between Crocodylus anthropophagus and extant hypapophysis behind the odontoid process, which in the holotype Crocodylus is supported by several unambiguous character states. In appears to have largely fused with the axial centrum (Fig. 3D), all crocodylians, the pharynx pneumatizes the braincase through even though the neural arch had popped off along its sutural three small openings (the Eustachian foramina) between the surface. Vertebrae are procoelous. The scapula has a relatively basioccipital and basisphenoid on the occipital plate [47,48]. slender dorsal blade, a narrow deltoid crest, and mediolaterally Osteolaemines (including Rimasuchus) and Mecistops share the wide body (Fig. 7A). The deltopectoral crest of the humerus was ancestral condition in which the lateral foramina are located concave proximally (Figs. 3E, 7A). The lateral surface of the ilium dorsal to the median foramen. In Crocodylus the lateral foramina is not visible on the holotype, but in posterior view it reveals a are located ventrally and almost in line with the median foramen wasp-waisted posterior blade (Fig. 3G). The femur is sigmoid in [23]. This coincides with a decrease in the dorsoventral depth of shape and had shallow depressions for the caudofemoralis the pterygoid ventral to the median Eustachian foramen, which in musculature on its ventral surface anterior and posterior to the turn limits the exposure of the basisphenoid ventral to the fourth trochanter (Fig. 7D). Most osteoderms (presumably from basioccipital on the posteroventral surface of the skull. This is the the dorsal shield) are square in dorsal view and, in most cases, bear condition found in C. anthropophagus (Fig. 5C). a robust dorsal keel (Fig. 3B); at least one (Fig. 7B) is oval in dorsal The medial wall of the caviconchal recess – a large pneumatic view, suggesting it is from the nuchal shield. feature in the maxilla dorsomedial to the toothrow – is perforated with a linear array of blind pits in C. anthropophagus (Fig. 4H). This Methods is a derived feature found only in Crocodylus [23,49]. The condition Crocodylus anthropophagus was added to a matrix of 98 morpho- in Rimasuchus is unknown, but they are absent from Osteolaemus, logical characters and 34 ingroup taxa (Appendix S1). A ‘‘Crocodylus’’ pigotti, and Voay [27] (pers. obs.). maximum parsimony analysis was conducted using TNT 1.1 An isolated ilium associated with the C. anthropophagus holotype [44]. 100 random-seed heuristic searches were performed. reveals a deeply concave dorsal and ventral margin to the posterior Borealosuchus sternbergii, Pristichampsus vorax, and Leidyosuchus canadensis blade, resulting in the ‘‘wasp-waisted’’ condition found in were used as sequential outgroups. Optimal trees were exported to Crocodylus but absent from other crocodyloids (Fig. 3G) [23]. The PAUP 4.10b [45] to construct Adams consensus trees. ilium of R. lloydi is unknown, but the posterior blade of Voay lacks substantial notching [27]. Results Derived states typically found in osteolaemines are absent from C. anthropophagus. The quadrate-squamosal suture follows the sulcus The heuristic searches recovered 426 equally optimal trees between the paroccipital process and anterior quadrate ramus, (length = 225, CI excluding uninformative characters = 0.493, and the squamosal does not lap over the dorsal surface of the RI = 0.717). Strict and Adams consensus trees of these results ramus. The surface of the fused pterygoids anterior to the internal (Fig. 8) are broadly congruent with previous morphological choana is elevated, but the elevation apparently does not surround analyses [23,27,46]. Mecistops is the closest relative of Crocodylus. the chaoanal aperture as it does in osteolaemines, and there is no Groups of Afro-Malagasy and Australasian forms – osteolaemines choanal neck. Trees supporting a close relationship between C. and mekosuchines, respectively – form subclades within Croco- anthropophagus and R. lloydi are minimally seven steps longer than dylinae. optimal. If the relationships among outgroup taxa are not constrained to Cranial ornamentation features that diagnose C. anthropophagus reflect more inclusive analyses of Crocodylia (i.e. forcing are elaborations of features found among most derived crocody- Leidyosuchus to be closest to Crocodyloidea and Borealosuchus loids. The orbital rim is upturned in all extant Crocodylus, but

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Figure 8. Phylogenetic relationships recovered by a maximum parsimony analysis of 98 morphological characters. Adams consensus of 426 equally optimal trees (length = 225, CI excluding uninformative characters = 0.493, RI = 0.717). Dashed lines indicate lost resolution in a strict consensus of the same trees. O = Osteolaeminae, M = Mekosuchinae, T = Tomistominae. Heavy branches indicate living lineages. doi:10.1371/journal.pone.0009333.g008 discrete knobs on the prefrontal are either absent or weakly Tanzania [53](pers. obs.), and Abu Dhabi [54] uniformly lack developed, and there is usually a discontinuity between the squamosal horns and discrete prefrontal knobs. The squamosals of upturned orbital margin and any dorsal reflection of the lateral large crocodiles from the Late Miocene and Pliocene Lothagam skull table margin. An anteroposterior crest is usually found on the and Koobi Fora localities referred in the past to Rimasuchus lloydi dorsal surface of the lacrimal in crocodylids, though it is especially [2,17], however, are dorsally inflated. Although not to the degree well-developed in most Indo-Pacific species of Crocodylus and some seen in C. anthropophagus, this contrasts the Kenyan skulls with R. extinct osteolaemines. But in these, the crest takes the form of a lloydi from the type locality [55] (pers. obs.), all of which have flat long continuous ridge, not the discrete knobs seen in C. skull tables. anthropophagus. Posterodorsal squamosal horns characterize the Cuban (Fig. 9B) These ornamental features are sufficient to distinguish C. and Siamese crocodiles [43,56]. Like C. anthropophagus, the horns of anthropophagus from most other Neogene crocodylines. Crocodylus these species are sharply demarcated in both posterior and lateral checchiai from the Miocene of Libya [7,11,50], Crocodylus gariepensis view, at least in larger individuals. It is because of these structures from the Miocene of Namibia [4], and Mio-Pliocene fossils that trees linking C. anthropophagus to C. rhombifer or C. siamensis are referred to Crocodylus from Italy [46,51,52], the Manonga Valley of among the optimal arrangements. Nevertheless, C. anthropophagus

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from the Quaternary of Madagascar (Fig. 9A)[59,60,61]. Indeed, squamosal horns of V. robustus and C. anthropophagus are similar enough that isolated elements may not be assignable to either species. Skeletal morphology strongly supports a close relationship between Voay and Osteolaemus, and squamosal horns are best viewed as independently derived features in Voay and C. anthropophagus. Another crocodylid with squamosal horns is Aldabrachampsus dilophus from the Quaternary of Aldabra Atoll [14]. Aldabrachampsus is incompletely known and its phylogenetic relationships are unclear, but its horns differ from those of both Voay and C. anthropophagus; they are broad and oblique in lateral view, with an apex anterodorsal rather than dorsal to the otic aperture. Moreover, known material of Aldabrachampsus suggests a very small animal (,2m) at maturity, and the holotype of C. anthropophagus is from a substantially larger animal. One character might suggest monophyly of extant Crocodylus to the exclusion of C. anthropophagus – a cleft in the maxillary ramus of the ectopterygoid. Preserved ectopterygoids and maxillae of C. anthropophagus suggest an unforked maxillary ramus that tapers anteriorly (Fig. 10A,B), the condition found in all other crocodylians. Cleft maxillary rami (Fig. 10C) are only seen in Crocodylus, and it was coded as present in all species in previous analyses [23]. If these codings are applied to the present analysis, C. anthropophagus is unambiguously outside (albeit close to) crown Crocodylus. But further examination of Crocodylus skulls indicates variability in living species – the cleft is not apparent in some individuals (Fig. 10E), and it lies right on the margin of the suborbital fenestra in others, making the medial tine of the fork difficult to see in ventral view (Fig. 10D). This character (63) was thus recoded as polymorphic in all living species, causing alternative placements of C. anthropophagus to become no less parsimonious. Variability was not observed in C. palaeindicus, and it remains coded as monomorphic for this trait, but fewer specimens are available and a larger sample may eventually reveal polymorphism. Even fewer specimens of C. anthropophagus preserve the relevant Figure 9. Squamosal horns of living and extinct crocodylines, parts of the skull, and our confidence that the species uniformly left lateral view. A, AMNH 3101, Voay robustus (right lateral view, lacked the cleft is less than robust. Moreover, the partial right photo inverted). B, PNCZ unnumbered, Crocodylus rhombifer. C, NHM ectopterygoid of NHM R5893 (Fig. 10A) bears a slight concavity 94.6.5.53, C. niloticus. Scale = 5 cm. on its anterior tip. We have interpreted this structure as unforked, doi:10.1371/journal.pone.0009333.g009 but one could argue for the forked condition. Recoding C. anthropophagus as polymorphic has no impact on the results of the can be readily distinguished from either living species; C. rhombifer, parsimony analysis. like other Neotropical species, has a prominent dorsal boss on the rostrum not present in C. anthropophagus, and C. anthropophagus lacks Crocodylus anthropophagus and Crocodylus niloticus the prominent long preorbital crest found in most Indopacific We have no complete skulls for C. anthropophagus and, thus, no species of Crocodylus (including C. siamensis) and the midline crest on solid grasp of the shape of the snout, but compared with C. niloticus, the frontal diagnostic of C. siamensis [23,57,58]. the premaxillae and maxillae indicate a comparatively deeper Although not as prominent, dorsally expanded squamosals are snout with a more highly vaulted palate; a relatively shorter sometimes found in very large specimens of most other living prenarial rostrum (Fig. 1A,E); a naris with more anterior species of Crocodylus, including C. niloticus (Fig. 9C). The horns of C. orientation; and more prominent crests along the margins of the anthropophagus are more prominent and have more acute dorsal tips orbit and skull table. Crocodylus niloticus lacks the prominent crest than these structures, and in lateral view, there is an abrupt along the maxillonasal suture seen in C. anthropophagus. Although transition from the dorsal surface of the postorbital (which is squamosal horns sometimes appear in C. niloticus, they are rarely (if parallel to the coronal plane) and the upturned squamosal horn. ever) as clearly demarcated from the dorsal surface of the skull This is most apparent on the KNM FLKNI right squamosal table as in C. anthropophagus, and they are neither as prominent nor (Fig. 4N), though this is case as well for the holotype (Fig. 1H). as sharply angled dorsally (Fig. 9C). Moreover, they appear in all Although true for Voay (Fig. 9A) and large C. rhombifer (Fig. 9B) and observed squamosals of C. anthropophagus, including some from C. siamensis, this is unlike the condition in other species of animals probably between 2 and 3 m in length, which suggests Crocodylus; when present, the dorsal expansion arises more regularity in expression absent from C. niloticus, in whom upturned gradually behind the postorbital bar (Fig. 9C). squamosals are only found in some very large individuals (.3 m). A few extinct crocodylians also bear squamosal horns similar to Nevertheless, differentiation of isolated fragments of C. those of C. anthropophagus, including the osteolaemine Voay robustus anthropophagus and C. niloticus may not always be possible, and this

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Figure 10. Variation in the morphology of the maxillary ramus of the ectopterygoid. All images from right side of skull in ventral view. A, NHM R.5893, Crocodylus anthropophagus, posterior end of right maxilla and partial maxillary ramus of ectopterygoid. B, KNM FLKNI, C. anthropophagus, partial right maxilla; articulation surface for ectopterygoid is preserved. C, USNM 194831, C. niloticus. D, USNM 248848, C. niloticus.E, FMNH 17157, C. niloticus. Arrow indicates cleft in maxillary ramus of ectopterygoid; questionably present in A, on medial margin of suborbital fenestra in D. Scale = 1 cm. doi:10.1371/journal.pone.0009333.g010 bears on interpretations of the Plio-Pleistocene crocodylian record consistently distinguished from C. niloticus, and we cannot at in Africa. Fossils as old as the Miocene have been referred to C. present conclude that one is phylogenetically closely related to the niloticus [2,17]; whether these are conspecific with C. niloticus (or other, even if biogeography strongly suggests such a relationship. even assignable to Crocodylus) is doubtful [62], but some geologically younger specimens (e.g. specimens forming the basis Paleoecology of C. niloticus kaisensis from the Pleistocene of Uganda [63]) are Fossil bones of at least two hominid individuals from Olduvai more consistent with the living species than with C. anthropophagus Gorge bear tooth marks characteristic of crocodile feeding [37]. (pers. obs.). At least two similar species of Crocodylus may have been These marks are similar to those produced by mammalian present in East Africa during the Late Pliocene and Pleistocene, and in the absence of diagnostic features permitting precise carnivores, except that they are bisected by the carinae of newly identification [64,65], referral of fragmentary remains to the erupted to moderately worn crocodile teeth [68]. Both tooth- species level may not be advisable. marked specimens are from the same Tuff IB-IC interval as Preliminary analyses of the phylogeny of Neogene African NNHM-OLD-1001, and were found by the Leakeys (L. Leakey, crocodiles suggested that Crocodylus might be a comparatively 1959; L. Leakey et al, 1964, M. Leakey, 1971) at two sites within recent immigrant into Africa and not a native lineage [30]. This 100 m of the collection site for NNHM-OLD-1001. Both hominid was based on incomplete taxonomic sampling, and more recent sites contain concentrations of vertebrate fossils and Oldowan stone work including a wider range of Mio-Pliocene forms suggests a artifacts. The FLK NN Level 3 site yielded the tooth-marked more complicated phylogenetic and biogeographic history for the Olduvai Hominid (OH) 8 foot, a paratype of H. habilis found in the group in the region [62], but assuming Crocodylus was absent from same assemblage as the species holotype. In situ elements of the C. Africa in the Early and Middle Miocene, the presence of two anthropohagus holotype are essentially contemporaneous with OH 8. species in at least the early Pleistocene, if not the Pliocene, suggests The FLK Level 22 site yielded the tooth-marked OH 35 tibia and either multiple dispersal events or dispersal early enough to have fibula, probably of H. habilis [69], from the same assemblage as the radiated by the Pleistocene. Further analysis of Late Miocene and holotype of A. boisei. Both OH 8 and OH 35 are from the left leg of a Pliocene fossils from the region is needed to test these scenarios, juvenile or adult [69], and have been argued to represent a single but regardless, crocodiles appear to have remained cryptically individual on the basis of their close articulation [70], despite speciose in Africa beyond their peak of diversity in the Miocene. deriving from different sites. Recent stratigraphic correlations of the That the features distinguishing C. anthropophagus from C. niloticus sites show that these formed on two allochronous land surfaces [71]. are dominated by gradational differences raises the general Curiously, the tooth mark patterning on both specimens indicates problem of how we recognize species in the fossil record. It is that each hominid individual lost its left foot to crocodiles during or possible that Olduvai Gorge crocodile is an extinct regional shortly after capture, or when being scavenged [37]. variant of the Nile crocodile and not a discrete species. Molecular The FLK 22 and FLK NN 3 sites formed in close proximity evidence reveals considerable genetic variation between popula- (,50 m) to wetland settings from which crocodile body and trace tions of C. niloticus [18,66]. However, biogeographic variation in C. fossils are documented [35,71]. FLK 22 formed on a topohigh niloticus morphology is expressed almost entirely in scalation [67]. adjacent to a freshwater marshland, and FLK NN 3 formed on the Different living populations of C. niloticus may ultimately be base of a shallow floodplain channel. NNHM-OLD-1001 likely distinguishable osteologically, but the differences will be subtle and derives from the floodplain deposits adjacent to this channel. The most apparent from morphometric rather than qualitative tooth-marked hominids died and were fed on by crocodiles at approaches. Qualitatively, the fossil Olduvai crocodile lies outside either the wetlands or the sites at which their remains were found. the range of osteological variation for C. niloticus, both within and Predation risk from crocodiles likely impacted the foraging and between populations. Cranially, the Olduvai form can be land use behavior of hominids at Olduvai and at other tropical and

PLoS ONE | www.plosone.org 11 February 2010 | Volume 5 | Issue 2 | e9333 Extinct Horned Crocodile sub-tropical near-wetland sites. Crocodiles were the largest Found at: doi:10.1371/journal.pone.0009333.s001 (0.06 MB predators encountered by hominids and are commonly found in DOC) the lake and river basins that also preserve fossil hominids in East Africa and elsewhere [2,72,73,74,75,76,77]. They inhabit settings Acknowledgments that afforded hominids potable water and rich food sources, in particular rootstock from marsh plants and scavengeable larger M. Norell, C. Raxworthy, M. Kearney, A. Milner, C. McCarthy, A. mammal carcasses [78]. Given the relatively small body sizes of Wynn, R. Sobero´n, R. Ramos, and E. Mbua permitted access to collections. Reviews by J. A. Alcover and M. Delfino prompted fossil hominids pre-dating H. erectus (e.g., H. habilis at ,1 m tall improvements to the paper, and we thank them. We are grateful to the and ,40 kg body weight; P. boisei at ,1.4 m tall, 80 kg body Tanzania Commission for Science and Technology, the Antiquities weight), crocodile feeding traces would likely have been inflicted Department of the Ministry of Natural Resources and Tourism, and the by younger small- to medium-sized crocodiles, as estimated from Ngorongoro Conservation Area Authority for permission to conduct the tooth mark size for OH 8 and 35 [37]. Larger crocodiles would be research that produced the new fossils reported here. We thank the capable of consuming hominids completely, leaving no trace. Olduvai Landscape Paleoanthropology Project for field support during our Crocodiles may have been common hominid predators, and as work at Olduvai Gorge, and the National Natural History Museum, Arusha, Tanzania, for cooperation during the curation and study of such should be considered in discussions of the ecological context NNHM-OLD-1001. Logistical support was provided by Joe’s Place I.C. of human origins. Author Contributions Supporting Information Conceived and designed the experiments: CB LD. Analyzed the data: CB. Appendix S1 List of characters and character matrix used in this Contributed reagents/materials/analysis tools: JN RB LD. Wrote the analysis. paper: CB JN RB.

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PLoS ONE | www.plosone.org 13 February 2010 | Volume 5 | Issue 2 | e9333 Appendix S1: List of characters and character matrix used in this analysis. Number in parentheses next to character number in the character list indicates corresponding character number in earlier versions of this matrix (e.g., Brochu, 1999, 2004, 2007).

1 (1). Ventral tubercle of proatlas more than one-half (0) or no more than one half (1) the width of the dorsal crest. 2 (2). Fused proatlas boomerang-shaped (0), strap-shaped (1), or massive and block-shaped (2). 3 (10). Proatlas with prominent anterior process (0) or lacks anterior process (1). 4 (14). Dorsal margin of atlantal rib generally smooth with modest dorsal process (0) or with prominent process (1). 5 (20). Axial rib tuberculum wide, with broad dorsal tip (0) or narrow, with acute dorsal tip (1). 6 (11). Anterior half of axis neural spine oriented horizontally (0) or slopes anteriorly (1). 7 (12). Axis neural spine crested (0) or not crested (1). 8 (3). Posterior half of axis neural spine wide (0) or narrow (1). 9 (7). Hypapophyseal keels present on eleventh vertebra behind atlas (0), twelfth vertebra behind atlas (1), or tenth vertebra behind atlas (2). 10 (8). Third cervical vertebra (first postaxial) with prominent hypapophysis (0) or lacks prominent hypapophysis (1). (Adapted from Norell, 1989, character 12; Norell and Clark, 1990, character 11; Clark, 1994, character 91.) 11 (9). Neural spine on third cervical long, dorsal tip at least half the length of the centrum without the cotyle (0) or short, dorsal tip acute and less than half the length of the centrum without the cotyle (1). 12 (13). Anterior sacral rib capitulum projects far anteriorly of tuberculum and is broadly visible in dorsal view (0), or anterior margins of tuberculum and capitulum nearly in same plane, and capitulum largely obscured dorsally (1). 13 (22). Scapular blade flares dorsally at maturity (0) or sides of scapular blade subparallel; minimal dorsal flare at maturity (1). (Adapted from Benton and Clark, 1988.) 14 (25). Scapulocoracoid facet anterior to glenoid fossa uniformly narrow (0) or broad immediately anterior to glenoid fossa, and tapering anteriorly (1). 15 (26). Proximal edge of deltopectoral crest emerges smoothly from proximal end of humerus and is not obviously concave (0) or emerges abruptly from proximal end of humerus and is obviously concave (1). 16 (27). Olecranon process of ulna narrow and subangular (0) or wide and rounded (1). 17 (30). Interclavicle flat along length, without dorsoventral flexure (0) or with moderate dorsoventral flexure (1) or with severe dorsoventral flexure (2). 18 (34). Iliac anterior process prominent (0) or virtually absent (1). (Adapted from Benton and Clark, 1988; Clark, 1994, character 84; although the transformation recorded here is different.) 19 (28). Dorsal margin of iliac blade rounded with smooth border (0) or rounded, with modest dorsal indentation (1) or rounded, with strong dorsal indentation (“wasp-waisted;” 2) or narrow, with dorsal indentation (3) or rounded with smooth border; posterior tip of blade very deep (4). 20 (32). Supraacetabular crest narrow (0) or broad (1). 21 (33). Limb bones relatively robust, and hindlimb much longer than forelimb at maturity (0) or limb bones very long and slender (1). 22 (35). Dorsal osteoderms not keeled (0) or keeled (1). (Adapted from Buscalioni et al., 1992, character 22.) 23 (36). Dorsal midline osteoderms rectangular (0) or nearly square (1). ) Adapted from Norell and Clark, 1990, character 16; Clark, 1994, character 95.) 24 (38). Nuchal shield grades continuously into dorsal shield (0) or differentiated from dorsal shield; four nuchal osteoderms (1) or differentiated from dorsal shield; six nuchal osteoderms with four central and two lateral (2) or differentiated from dorsal shield; eight nuchal osteoderms in two parallel rows (3). 25 (39). Ventral armor absent (0) or single ventral osteoderms (1) or paired ventral ossifications that suture together (2). (Adapted from Buscalioni et al., 1992, character 21.) 26 (40). Anterior margin of dorsal midline osteoderms with anterior process (0) or smooth, without process (1). (Adapted from Norell and Clark, 1990, character 13; Clark, 1994, character 96.) 27 (52). Alveoli for dentary teeth 3 and 4 nearly same size and confluent (0) or fourth alveolus larger than third, and alveoli are separated (1). 28 (166). Dentary symphysis extends to fourth or fifth alveolus (0) or sixth through eighth alveolus (1) or behind eighth alveolus (2.) 29 (68). Dentary gently curved (0), deeply curved (1), or linear (2) between fourth and tenth alveoli. 30 (167). Largest dentary alveolus immediately caudal to fourth is (0) 13 or 14, (1) 13 or 14 and a series behind it, (2) 11 or 12, or (3) no differentiation, or (4) behind 14. 31 (41). Splenial with anterior perforation for mandibular ramus of cranial nerve V (0) or lacks anterior perforation for mandibular ramus of cranial nerve V (1). (Adapted in part from from Norell, 1988, character 15 and 1989, character 8.) 32 (43). Splenial participates in mandibular symphysis; splenial symphysis adjacent to no more than five dentary alveoli (0) or splenial excluded from mandibular symphysis; anterior tip of splenial passes ventral to Meckelian groove (1) or splenial excluded from mandibular symphysis; anterior tip of splenial passes dorsal to Meckelian groove (2) or deep splenial symphysis, longer than five dentary alveoli; splenial forms wide “V” within symphysis (3) or deep splenial symphysis, longer than five dentary alveoli; splenial constricted within symphysis and forms narrow “V” (4). (Adapted from Clark, 1994, character 77.) 33 (54). Superior edge of coronoid slopes strongly anteriorly (0) or almost horizontal (1). 34 (47). Angular-surangular suture contacts external mandibular fenestra at posterior angle at maturity (0) or passes broadly along ventral margin of external mandibular fenestra late in ontogeny (1). (Adapted from Norell, 1988, character 40.) 35 (61). Surangular with spur bordering the dentary toothrow lingually for at least one alveolus length (0) or lacking such spur (1). 36 (106). Surangular continues to dorsal tip of lateral wall of glenoid fossa (0) or truncated and not continuing dorsally (1). 37 (44). Articular-surangular suture simple (0) or articular bears anterior lamina dorsal to lingual foramen (1) or articular bears anterior lamina ventral to lingual foramen (2) or bears laminae above and below foramen (3.) 38 (45). Lingual foramen for articular artery and alveolar nerve perforates surangular entirely (0) or perforates surangular/angular suture (1). 39 (49). Foramen aerum at extreme lingual margin of retroarticular process (0) or set in from margin of retroarticular process (1). (Adapted from Norell, 1988, character 16.) 40 (162). Surangular-articular suture oriented anteroposteriorly (0) or bowed strongly laterally (1) within glenoid fossa. 41 (60). Sulcus between articular and surangular (0) or articular flush against surangular (1). 42 (57). Dorsal projection of hyoid cornu flat (0) or rodlike (1). 43 (166). Teeth and alveoli of maxilla and/or dentary circular in cross-section (0), or posterior teeth laterally compressed (1), or all teeth compressed (2.) 44 (79). Naris projects anterodorsally (0) or dorsally (1). 45 (95). External naris bisected by nasals (0) or nasals contact external naris, but do not bisect it (1) or nasals excluded, at least externally, from naris; nasals and premaxillae still in contact (2) or nasals and premaxillae not in contact (3). (Adapted from Norell, 1988, character 3; Clark, 1994, characters 13 and 14.) 46 (97). Premaxilla has five teeth (0) or four teeth (1) early in posthatching ontogeny. (Norell, 1988, character 17.) 47 (153). Incisive foramen completely situated far from premaxillary toothrow, at the level of the second or third alveolus (0) or abuts premaxillary toothrow (1) or projects between first premaxillary teeth (2). 48 (145). Dorsal premaxillary processes short, not extending beyond third maxillary alveolus (0) or long, extending beyond third maxillary alveolus (1). 49 (78). All dentary teeth occlude lingual to maxillary teeth (0) or occlusion pit between 7th and 8th maxillary teeth; all other dentary teeth occlude lingally (1) or dentary teeth occlude in line with maxillary toothrow (2). (Adapted from Norell, 1988, character 5; Willis, 1993, character 1.) 50 (89). Largest maxillary alveolus is #3 (0), #5 (1), #4 (2), #4 and #5 are same size (3), #6 (4), or maxillary teeth homodont (5), or maxillary alveoli increase in diameter posteriorly toward penultimate alveolus (6). (Adapted from Norell, 1988, character 1.) 51 (135). Maxillary toothrow curved medially or linear (0) or curves laterally broadly (1) posterior to first six maxillary alveoli. (Adapted from Clark, 1994, character 79.) 52 (101). Dorsal surface of rostrum curves smoothly (0) or bears medial dorsal boss (1). 53 (144). Preorbital ridges absent or very modest (0) or very prominent (1) at maturity. 54 (126). Vomer entirely obscured by maxillae and palatines (0) or exposed on palate between palatines (1). 55 (148). Surface of maxilla within narial canal imperforate (0) or with a linear array of pits (1.) 56 (120). Medial jugal foramen small (0) or very large (1). 57 (111). Maxillary foramen for palatine ramus of cranial nerve V small or not present (0) or very large (1). 58 (91). Ectopterygoid abuts maxillary tooth row (0) or maxilla broadly separates ectopterygoid from maxillary tooth row (1). (Norell, 1988, character 19.) 59 (136). Medial process of prefrontal pillar expanded dorsoventrally (0) or anteroposteriorly (1). 60 (138). Medial process of prefrontal pillar wide (0) or constricted (1) at base. 61 (105). Maxilla has linear medial margin adjacent to suborbital fenestra (0) or bears broad shelf extending into fenestra, making lateral margin concave (1.) 62 (108). Anterior face of palatine process rounded or pointed anteriorly (0) or notched anteriorly (1). 63 (109). Anterior ectopterygoid process tapers to a point (0) or forked (1). 64 (110). Palatine process extends (0) or does not extend (1) significantly beyond anterior end of suborbital fenestra. (Adapted from Willis, 1993, character 2.) 65 (118). Palatine process generally broad anteriorly (0) or in form of thin wedge (1). 66 (94). Lateral edges of palatines smooth anteriorly (0) or with lateral process projecting from palatines into suborbital fenestrae (1). 67 (85). Palatine-pterygoid suture nearly at (0) or far from (1) posterior angle of suborbital fenestra. 68 (88). Pterygoid ramus of ectopterygoid straight, posterolateral margin of suborbital fenestra linear (0) or ramus bowed, posterolateral margin of fenestra concave (1.) 69 (73). Pterygoid surface lateral and anterior to internal choana flush with choanal margin (0) or pushed inward anterolateral to choanal aperture (1) or pushed inward around choana to form “neck” surrounding aperture (2) or everted from flat surface to form “neck” surrounding aperture (3). 70 (152). Internal choana not septate (0) or with septum that remains recessed within choana (1) or with septum that projects out of choana (2). 71 (93). Lacrimal makes broad contact with nasal; no posterior process of maxilla (0) or maxilla with posterior process within lacrimal (1) or maxilla with posterior process between lacrimal and prefrontal (2). 72 (70). Postorbital bar massive (0) or slender (1). (Norell, 1989, character 3.) 73 (103). Margin of orbit flush with skull surface (0) or dorsal edges of orbits upturned (1) or orbital margin telescoped (2). 74 (96). Palpebral forms from single ossification (0) or from multiple ossifications (1). (Adapted from Norell, 1988, character 8; Clark, 1994, character 65.) 75 (114). Quadratojugal spine low, near posterior angle of infratemporal fenestra (0) or high, between posterior and superior angles of infratemporal fenestra (1). 76 (75). Quadratojugal forms posterior angle of infratemporal fenestra (0) or jugal forms posterior angle of infratemporal fenestra (1) or quadratojugal-jugal suture lies at posterior angle of infratemporal fenestra (2). (Adapted from Norell, 1989, character 10.) 77 (76). Postorbital neither contacts quadrate nor quadratojugal medially (0) or contacts quadratojugal, but not quadrate, medially (1) or contacts quadrate and quadratojugal at dorsal angle of infratemporal fenestra (2) or contacts quadratojugal with significant descending process (3). 78 (83). Quadratojugal bears long anterior process along lower temporal bar (0) or bears modest process, or none at all, along lower temporal bar (1). 79 (80). Quadratojugal extends to superior angle of infratemporal fenestra (0) or does not extend to superior angle of infratemporal fenestra; quadrate participates in fenestra (1). (Adapted from Buscalioni et al., 1992, character 6.) 80 (84). Dorsal and ventral rims of squamosal groove for external ear valve musculature parallel (0) or squamosal groove flares anteriorly (1). 81 (132). Squamosal-quadrate suture extends dorsally along posterior margin of external auditory meatus (0) or extends only to posteroventral corner of external auditory meatus (1). 82 (102). Posterior margin of otic aperture smooth (0) or bowed (1). 83 (81). Frontoparietal suture deeply within supratemporal fenestra; frontal prevents broad contact between postorbital and parietal (0) or suture makes modest entry into supratemporal fenestra at maturity; postorbital and parietal in broad contact (1) or suture on skull table entirely (2). 84 (86). Frontoparietal suture concavoconvex (0) or linear (1) between supratemporal fenestrae. 85 (87). Supratemporal fenestra with fossa; dermal bones of skull roof do not overhang rim at maturity (0) or dermal bones of skull roof overhang rim of supratemporal fenestra near maturity (1) or supratemporal fenestra closes during ontogeny (2). (Adapted from Norell, 1988, character 9.) 86 . Posterolateral margin of squamosal horizontal or nearly so (0) or upturned to form a discrete “horn” (1.) 87 (150). Squamosal does not extend (0) or extends (1) ventrolaterally to lateral extent of paraoccipital process. 88 (82). Supraoccipital exposure on dorsal skull table small (0), absent (1), large (2), or large such that parietal is excluded from posterior edge of table (3). (Norell, 1988, character 11.) 89 (122). Sulcus on anterior braincase wall lateral to basisphenoid rostrum (0) or braincase wall lateral to basisphenoid rostrum smooth; no sulcus (1). 90 (129). Basisphenoid not exposed extensively (0) or exposed extensively (1) on braincase wall anterior to trigeminal foramen (Adapted from Norell, 1989, character 5.) 91 (74). Extensive exposure of prootic on external braincase wall (0) or prootic largely obscured by quadrate and laterosphenoid externally (1). (Adapted from Norell, 1989, character 5.) 92 (127). Significant ventral quadrate process on lateral braincase wall (0) or quadrate-pterygoid suture linear from basisphenoid exposure to trigeminal foramen (1). 93 (128). Lateral carotid foramen opens lateral (0) or dorsal (1) to basisphenoid at maturity. 94 (98). Posterior pterygoid processes tall and prominent (0) or small and project posteroventrally (1) or small and project posteriorly (2). 95 (119). Basisphenoid not broadly exposed ventral to basioccipital at maturity; pterygoid short ventral to median eustachian opening (0) or basisphenoid exposed as broad sheet ventral to basioccipital at maturity; pterygoid tall ventral to median eustachian opening (1). 96 (147). Lateral eustachian canals open dorsal (0) or lateral (1) to medial eustachian canal. (Adapted from Norell, 1988, character 46.) 97 . quadrate foramen aereum is small (0), comparatively large (1), or absent (2) at maturity. 98 (112). Quadrate with small, ventrally-reflected medial hemicondyle (0) or with small medial hemicondyle; dorsal notch for foramen aerum (1) or with prominent dorsal projection between hemicondyles (2) or with expanded medial hemicondyle (3).

Borealosuchus sternbergii 00000110?10000000000100??001020000000000000020001310000100??0000011101010?001000000000000000001000

Pristichampsus vorax ?????01001??0001?010010??1110?00?0?001?0??2010?0030010?000??0000001001011??0100010000000????101002

Leidyosuchus canadensis ???????????0001??10?011?11010?0000?000101?0010000300000001001000011101010?101000010000000000001001

Mecistops cataphractus 10?1100000011111212001110111041111011101?101201021000001001100001011010110010110012000001111110003

Crocodylus niloticus 10101101001111112120011201100211111111011101101021000011001100{01}00011011110010110012000001111110103

Crocodylus porosus 11101001101110112120011201100211111111011101101021001011001100{01}00011010110010110012000001111110103

Crocodylus rhombifer 00101101001111112110011201100211111111011101101021010011001100{01}00011011110010110012001001111110103

Crocodylus acutus 00101101001111112120011201100211111111011101101021010011001100{01}00011011110010110012000001111110103

Crocodylus palustris 10101001011111112121011201100211111111011101101021001011001100{01}00011010110010110012000001111110103

Crocodylus siamensis 11101111000111012120011201100211111111011101101021001011001100{01}00011010110010110012001001111110103

Crocodylus intermedius 00101101001111112120011201110211111111011101101021010011001100{01}00011010110010110012000001111110103

Crocodylus johnstoni 111010011011101121200112011?0211111111011101101021001011001100{01}01011010110010110012000001111110103

Crocodylus mindorensis 11101001101110112120011201100211111111011101101021001011001100{01}00011010110010110012000001111110103

Crocodylus novaeguineae 11101001101110112120011201100211111111011101101021001011001100{01}00011010110010100012000001101110103

Crocodylus moreletii 00101101001111112120011201100211111111011101101021010011001100{01}00011011110010110012000001111110103

Crocodylus palaeindicus ???????????1?????1????????10021111111?011?0110?0210000?100110010000101011?010110012000010111110103

Crocodylus anthropophagus ????????????111??120011??11?021111?111011?00101021000?1100110?0???1?0??11??1?100011001001?1?110103

Euthecodon arambourgii ???????????????????????????????0???????1??0020?1250010?10011000000???0?11?11011001210010????1??0?3

Osteolaemus tetraspis ??101001100111112111011111100211111011011111011021001001001110010111110111010100012110101111111003

Osteolaemus osborni ??101001100111112111011111100211101011011111111021001001001110010010110111010100012110101111111003

Voay robustus ???????????1???1?1110????1110211101111111?0110?02100100100110001011111011?01011001201111?111110003

Rimasuchus lloydi ???????????????????????????????1???????1??0110?0210010?1001100000????1111?01011001200010111?11?0?3

“Crocodylus” pigotti ?????00??001?111?????10??01102?1???111?1??0010?02100100100??0010101110?11??1?1?001210010??1?10?003

“Crocodylus” megarhinus ??????????0???????????????110211?010??011?0110?023000001?0??0000001101211?02?110012?000?110?110003

Australosuchus clarkae ?????????0????1?????010??1110?11?01011011?0110112100000100??000000???1011?0201101120000011??1?00?1

Kambara implexidens ??????????????1??110010??1110211?01011011?0110112100000100?10000001001011?020110012000001111110001

Trilophosuchus rackhami ??????????????????????????????????????????0?????2?0?00?100??1?000001???11?1201101121000211111??0?1

Tomistoma schlegelii 021010010011011111100103011?2?14010000010001201121000101001100010010011110001100012100001101110003

Gavialosuchus antiquus 0200?001?001011??11?000??11?2??41??031?1?0012011210000?100??0000101?01101??011?101200001??0?110023

Kentisuchus spenceri ???????????????????????????????4?0??11011?0110?1210000???0??0100101001111?????00??200000???11??003

Dollosuchoides densmorei 001??111?00?0011?1?00?????1?0??4?000??01??012??1210000??00??01?0101001101??????1??2000001????000?3

Brachyuranochampsa eversolei ??????????????????????????????????????????011??1210000??00??0?0??01101010??0?000?1210000????100003

“Crocodylus” depressifrons ?????11010010011?110010??1110211?01000011?0110?1110000?110??0001001?01?10?102000012000001101100003

“Crocodylus” acer ??????????????????????????????????????????0110?1210000??00??000100?101010?00?0100?2000001??1100003

“Crocodylus” affinis 00111100000100110110010??11102111010000110011010110000?010??0001001101010??010?0012000001???100003

Asiatosuchus germanicus 001?1001?01?0?11?1??0????1110200?010??01?00010?001000???10??00010???01010??0100001110000????10?003

Prodiplocynodon langi ??????????????????????????????????????????0110??030000??10?00001001101?10??0?0?0?11?00001??0101003

Benton, M. J. and J. M. Clark. 1988 Archosaur phylogeny and the relationships of the Crocodylia; pp. 295-338 in M. J. Benton (ed.), The Phylogeny and Classification of the Tetrapods. Clarendon Press, Oxford.

Brochu, C. A. 1999. Phylogeny, systematics, and historical biogeography of Alligatoroidea. Society of Vertebrate Paleontology Memoir 6:9-100.

Brochu, C. A. 2004. Alligatorine phylogeny and the status of Allognathosuchus Mook, 1921. Journal of Vertebrate Paleontology 24:856-872.

Brochu, C. A. 2007. Morphology, relationships and biogeographic significance of an extinct horned crocodile (Crocodylia, Crocodylidae) from the Quaternary of Madagascar. Zoological Journal of the Linnean Society 150:835-863.

Buscalioni, A. D., J. L. Sanz, and M. L. Casanovas. 1992. A new species of the eusuchian crocodile Diplocynodon from the Eocene of Spain. Neues Jahrbuch für Geologie und Paläontologie Abandlungen 187:1-29.

Clark, J. M. 1994. Patterns of evolution in Mesozoic Crocodyliformes; pp. 84-97 in N. C. Fraser and H. D. Sues (eds.), In the Shadow of Dinosaurs: Early Mesozoic Tetrapods. Cambridge University Press, New York.

Norell, M. A. 1988. Cladistic approaches to paleobiology as applied to the phylogeny of alligatorids. Ph.D., Yale University, New Haven.

Norell, M. A. 1989. The higher level relationships of the extant Crocodylia. Journal of Herpetology 23:325-335.

Norell, M. A., and J. M. Clark. 1990. A reanalysis of Bernissartia fagesii, with comments on its phylogenetic position and its bearing on the origin and diagnosis of the Eusuchia. Bulletin de l'Institut Royal des Sciences Naturelles de Belgique 60:115- 128.

Willis, P. M. A. 1993. Trilophosuchus rakhami gen et sp. nov., a new crocodilian from the Early Miocene limestones of Riversleigh, northwestern Queensland. Journal of Vertebrate Paleontology 13:90-98.

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