Late Cretaceous sauropod tooth morphotypes may …Femke M. Holwerda1,2 3, Verónica Díez Díaz4 5, Alejandro Blanco2,6, Roel Montie1,2 3 and Jelle W.F. Reumer1 1 Faculty of Geosciences,

Submitted 14 March 2018Accepted 13 October 2018Published 12 November 2018

Corresponding authorFemke M Holwerdafholwerdalrzuni-muenchendefmholwerdagmailcom

Academic editorKenneth De Baets

Additional Information andDeclarations can be found onpage 32

DOI 107717peerj5925

Copyright2018 Holwerda et al

Distributed underCreative Commons CC-BY 40

OPEN ACCESS

Late Cretaceous sauropod toothmorphotypes may provide supportingevidence for faunal connections betweenNorth Africa and Southern EuropeFemke M Holwerda123 Veroacutenica Diacuteez Diacuteaz45 Alejandro Blanco26Roel Montie123 and Jelle WF Reumer1

1 Faculty of Geosciences Utrecht University Utrecht Netherlands2 SNSB-Bayerische Staatssammlung fuumlr Palaumlontologie und Geologie Munich Bavaria Germany3Department of Earth and Environmental Sciences and GeoBioCenter Ludwig-Maximilians-UniversitaumltMuumlnchen Munich Bavaria Germany

4Museum fuumlr Naturkunde Leibniz-Institut fuumlr Evolutions-und Biodiversitaumltsforschung Berlin Germany5Humboldt Universitaumlt Berlin Berlin Germany6Centro de Investigacioacutens Cientiacuteficas Avanzadas (CICA) Facultade de Ciencias Universidade da CoruntildeaA Coruntildea Spain

ABSTRACTThe Cretaceous Kem Kem beds of Morocco and equivalent beds in Algeria haveproduced a rich fossil assemblage yielding amongst others isolated sauropod teethwhich can be used in species diversity studies These Albian-Cenomanian (sim113ndash939Ma) strata rarely yield sauropod body fossils therefore isolated teeth can help toelucidate the faunal assemblages from North Africa and their relations with thoseof contemporaneous beds and geographically close assemblages Eighteen isolatedsauropod teeth from three localities (Erfoud and Taouz Morocco and Algeria) arestudied here to assess whether the teeth can be ascribed to a specific clade andwhether different tooth morphotypes can be found in the samples Two generalmorphotypes are found based on enamel wrinkling and general tooth morphologyMorphotype I with mainly rugose enamel wrinkling pronounced carinae lemon-shaped to (sub)cylindrical cross-section and mesiodistal tapering towards an apicaltip shows affinities to titanosauriforms and titanosaurs Morphotype II characterizedby more smooth enamel cylindrical cross-section rectangular teeth with no apicaltapering and both labial and lingual wear facets shows similarities to rebbachisauridsMoreover similarities are found between these northwest African tooth morphotypesand tooth morphotypes from titanosaurs and rebbachisaurids from both contempo-raneous finds from north and central Africa as well as from the latest Cretaceous(CampanianndashMaastrichtian 836 Mandash660 Ma) of the Ibero-Armorican Island Theseresults support previous hypotheses from earlier studies on faunal exchange andcontinental connections between North Africa and Southern Europe in the Cretaceous

Subjects Biodiversity Biogeography Paleontology TaxonomyKeywords Titanosauria Late Cretaceous Europe Africa Teeth Diversity

How to cite this article Holwerda et al (2018) Late Cretaceous sauropod tooth morphotypes may provide supporting evidence for fau-nal connections between North Africa and Southern Europe PeerJ 6e5925 DOI 107717peerj5925

INTRODUCTIONThe early Late Cretaceous of northwestern Africa is well-known for its rich vertebratefauna many taxa having been described in particular from the AlbianndashCenomanian(sim113ndash939 Ma) Kem Kem beds of Morocco and the AlbianndashCenomanian equivalentcontinental intercalaire of Algeria The Moroccan Kem Kem beds include aquatic faunasuch as sharks lungfish coelacanths bony fish amphibians turtles crocodylomorphs aswell as terrestrial vertebrates such as squamates pterosaurs sauropods and an abundanceof theropods (Lavocat 1954 Russell 1996 Sereno et al 1996Wellnhofer amp Buffetaut 1999Cavin et al 2010 Richter Mudroch amp Buckley 2013 Laumlng et al 2013 Mannion amp Barrett2013) Despite this large diversity most fossil material consists of isolated elements fromtheropods and chondrichthyans (eg Spinosaurus Carcharodontosaurus OnchopristisLaumlng et al 2013 C Underwood pers comm 2018) Laumlng et al (2013) attributed thisto the deltaic palaeoenvironment being unsuitable for the setting of stable terrestrialvegetation Because of this the herbivorous fauna has not received much attention thusfar and sauropod material is rare (C Underwood pers comm 2018 but seeMcGowan ampDyke 2009) Studies of sauropod material from this region thus far found Rebbachisaurusgarasbae and other rebbachisaurids (Lavocat 1954 De Lapparent amp Gorce 1960 Russell1996 Mannion amp Barrett 2013 Wilson amp Allain 2015) as well as several titanosauriformremains and also a possible titanosaurian (De Broin Grenot amp Vernet 1971 Kellner ampMader 1997 Mannion amp Barrett 2013 Lamanna amp Hasegawa 2014 Ibrahim et al 2016)De Lapparent amp Gorce (1960) also mentioned brachiosaurid finds however these remainsare now considered to be rebacchisaurid or titanosauriform (Mannion 2009 Mannion ampBarrett 2013)

Sauropod body fossils are restricted to mostly isolated elements or if associatedmaterial is not as numerous as with theropod material (see egMahler 2005 Novas DallaVecchia amp Pais 2005 Cau amp Maganuco 2009) Sauropod teeth however are preservedin relative abundance One isolated sauropod tooth had already been reported on byKellner amp Mader (1997) Sauropod teeth are commonly preserved in the fossil record dueto their hardness resilience against weathering and due to their high tooth replacementrates (see eg Calvo 1994 Erickson 1996 Garciacutea amp Cerda 2010 Garciacutea amp Cerda 2010b)Studying isolated teeth has previously been applied to assessing theropod species diversity inNorth Africa (Richter Mudroch amp Buckley 2013) Sauropod teeth can be used for a similarpurpose as well as morphological classifications based on shape size and position of wearfacets (Calvo 1994 Salgado amp Calvo 1997 Chure et al 2010Mocho et al 2016 Carballidoet al 2017) and enamel wrinkling patterns (Carballido amp Pol 2010 Diacuteez Diacuteaz PeredaSuberbiola amp Sanz 2012Diacuteez Diacuteaz Tortosa amp Loeuff 2013Holwerda Pol amp Rauhut 2015)have classified tooth assemblages into morphotypes or even down to family or genus level(eg Amygdalodon Patagosaurus)

Mannion amp Barrett (2013) suggested that the Cretaceous North African titanosauriformsmay not be closely related to southern African forms as the lineages were cut off fromeach other by the trans-Saharan seaway Moreover close relations are suggested betweenCretaceous North African sauropods and Italian sauropods (Zarcone et al 2010 Dal

Holwerda et al (2018) PeerJ DOI 107717peerj5925 243

Sasso et al 2016) and Iberian sauropods (Sallam et al 2018 Diacuteez Diacuteaz et al 2018) Morespecifically close relations between Egyptian and European sauropods (Sallam et al 2018)and between Tunisian and European sauropods (Fanti et al 2015) have been found Thesestudies proposed faunal exchanges during the Late Cretaceous between northern Africaand southern Europe Several migratory routes have been suggested such as the lsquoApulianroutersquo during the Early Cretaceous (Dalla Vecchia 2002 Canudo et al 2009) Continentalconnections would have been made possible by peri-Adriatic carbonate platforms in theMediterranean connecting North Africa with Adria throughout the Cretaceous makingmigration possible between the northern African and southern European islands andpeninsulas (Zarcone et al 2010) Indeed these carbonate platforms contain numeroustetrapod footprints including those of sauropods (Zarcone et al 2010) The hypothesis ofa faunal exchange during the Cretaceous is not new Late Cretaceous abelisaurid theropodsand titanosaurian sauropods from France are found to have Gondwanan affinitiesindicating migration from Gondwana to Europe an event which could already have takenplace in the Early Cretaceous (Buffetaut Mechin amp Mechin-Salessy 1988 Buffetaut 1989)Next to sauropods Early Cretaceous abelisaurid and carcharodontosaurid theropods werefound with Gondwanan affinities as well as other terrestrial fauna such as amphibianssnakes and ziphodont crocodyliforms (Le Loeuff 1991 Vullo et al 2005 Vullo Neraudeauamp Lenglet 2007 Pereda-Suberbiola 2009) Oumlsi Apesteguiacutea amp Kowalewski (2010) foundSantonian theropods from the Mediterranean region to have both Gondwanan andNorth American affinities Dalla Vecchia amp Cau (2011) added a notosuchian from the LateCretaceous of Italy andRabi amp Seboumlk (2015) a sebecosuchian to this faunal assemblage withGondwanan affinities Reviewing undescribedNorth African Cretaceous sauropodmaterialcould add information on both the biogeographical patterns of the Euro-Gondwanan areaas well as on sauropod species diversity in northwestern Africa

Here we present a morphological and quantitative analysis of a sauropod toothassemblage from the Cenomanian of Morocco and Algeria Teeth are categorized intotwo morphotypes which are then compared to contemporaneous Cretaceous sauropodtooth morphotypes including sauropod teeth from Africa and southern Europe

GEOLOGICAL SETTINGFourteen of the teeth studied here are from the Kem Kem beds of Morocco and fourwere supposedly found in the Late Cretaceous Continental Intercalaire of Algeria Fourof the Moroccan sample are labeled as originating from lsquoTaouz Algeriarsquo and four arelabeled lsquoKem KemMoroccorsquo Taouz Algeria might actually mean Taouz Morocco whichis the southern part of the Kem Kem beds and ten samples are labeled as originating fromErfoud Morocco which is the more northern part of the Kem Kem beds (Fig 1) TheKem Kem area is located in the south-east of Morocco (Fig 1) Here the Kem Kem bedsform an escarpment around the eastern end of the Anti-Atlas from near Goulmima inthe northwest (C Underwood pers comm 2018 see Fig 1) past Erfoud in the north(Wellnhofer amp Buffetaut 1999 Cavin amp Forey 2004) and along the east parallelling theAlgerian border (C Underwood pers comm 2018) The Kem Kem ends to the west south


carbonate

marls and sandstones

cross bedded sandstones

sandstones

Cenomanian-

Turonian

Upper m

arly unitLow

er sandstone unit

Cenomanian-(A

lbian-Aptian)

D

Morocco

Algeria

Spain

Kem Kem

Continental Intercalaire

Lo Hueco

Fox-Amphoux-Meacutetisson

France

A

Erfoud

Taouz

ferruginous sandstones


Cenomanian

and teeth

C

A B

Figure 1 Geological setting of KemKem beds Morocco and Continental Intercalaire Algeria Taouzand Erfoud are indicated localities of Lo Hueco Spain and France (FAM AIX Massecaps) are also por-trayed (A) Map of Europe and Africa (B) Close-up of North Africa and Southern Europe (C) strati-graphical column of Kem Kem beds (after Belvedere et al 2013 Ibrahim et al 2014) (D) stratigraphicalcolumn of Continental Intercalaire Algeria (after Forey Loacutepez-Arbarello amp MacLeod 2011)

Full-size DOI 107717peerj5925fig-1

of Taouz thereby in total stretching to about 300 km of outcrop (C Underwood perscomm 2018 see Fig 1) The Kem Kem is usually mentioned to be Cenomanian in ageas it has been found to match ammonites from the Lower Cenomanian of Bahariya Egypt(Le Loeuff et al 2012) However the age range could span over the AlbianndashCenomanian(C Underwood pers comm 2018) which is closer to the age given to the Algerian


Cretaceous Continental Intercalaire (Lefranc amp Guiraud 1990 Le Loeuff et al 2012) andto the fossil-rich Cretaceous lsquoContinental Intercalairersquo beds of Tunisia (Fanti et al 2016)as well as sauropod bonebeds from Niger (Sereno amp Wilson 2005) The Kem Kem beds areconsidered to be made up of two formations (see Fig 1) the fossil-rich lower IfezouaneFormation and the upper Aoufous Formation rich in ichnofossils (Cavin et al 2010Belvedere et al 2013) also named the lower sandy unit (a braided fluvial system) and theupper marly unit (a coastal lagoon) respectively (Cavin et al 2010 Belvedere et al 2013Mannion amp Barrett 2013 Ibrahim et al 2014) Practically all fossil vertebrates originatefrom the lower Ifezouane Formation (Cavin et al 2010 C Underwood pers comm2018) The Continental Intercalaire of Algeria is less studied than the Kem Kem and theage ranges from Barremian to Turonian However most authors set the age of the bedsclose to the Moroccan border (where our Algerian specimens are supposedly from) toAlbian-Cenomanian-Turonian with the Cenomanian layers being the most fossil-rich(Laumlng et al 2013 Benyoucef et al 2015 Meister et al 2017) As said before the labelinghowever of lsquoTaouz Algeriarsquo is most likely not correct as Taouz is situated in Moroccosouth of Erfoud close to the border with Algeria where many fossils from the southernKem Kem exposures towards Ouzina are collected over a broad expanse usually inmines around Bagaa (M Dale C Underwood pers comm 2018 Fig 1) Indeed TaouzMorocco is indicated as fossil locality in other Kem Kem fossil vertebrate studies (egWellnhofer amp Buffetaut 1999 Cavin et al 2010 Forey Loacutepez-Arbarello amp MacLeod 2011Richter Mudroch amp Buckley 2013) As the Kem Kem outcrops at present run parallel to theborder the labelling of lsquoAlgeriarsquo is probably still be correct as the lsquoKem Kemrsquo beds extendout across the border (Alloul et al 2018) however the specific provenance of these teethis unclear

Next to the labelling the colour of the fossils likely confirms the provenance on thelabels as fossils from Bagaa (Taouz) are chocolate brown in colour and fossils from northof Erfoud show a range of colours usually shades of beige and black (C Underwood perscomm 2018) matching the provenance on the collection reference (see lsquoDescriptionrsquo)

As most of the fossils retrieved from the Kem Kem and equivalent beds from Algeriaare found via mining the provenance is unfortunately usually unclear and only traceableto a regional provenance (Forey amp Cavin 2007 Rodrigues et al 2011 C Underwood perscomm 2018)

MATERIALS AND METHODSIn this study eighteen isolated sauropod teeth from the Kem Kem beds and ContinentalIntercalaire are studied for shape size position of wear facets (where applicable) andenamel wrinkling The four teeth from around Taouz (Morocco) are BSPG 1993 IX 331ABSPG 1993 IX 331B BSPG 1993 IX 331C and BSPG 1993 IX 313A see Figs 2Andash2DThe ten teeth from Erfoud (Morocco) are labeled PIMUZ AIII 0823 and are given theadditional labeling of a b c etc for convenience see Figs 3Andash3J The four Algerianspecimens are BSPG 1993 IX 2A BSPG 1993 IX 2B BSPG 1993 IX 2C and BSPG 1993 IX2D see Figs 2Endash2HMeasurements were taken with a caliper to mm scale For imaging the


1cm

A B

C D

E F

G H

Figure 2 Images of BSPG 1993 IX 331A (A) BSPG 1993 IX 331B (B) BSPG 1993 IX 331C (C) BSPG1993 IX 313A (D) BSPG 1993 IX 2A (E) BSPG 1993 IX 2B (F) BSPG 1993 IX 2C (G) and BSPG 1993IX 2D (H) In basal view apical view labial view lingual view distal view and mesial view The scale barequals 1 cm Images taken by RM


teeth were photographed using normal andmacro settings Scanning ElectronMiscroscopy(SEM) pictures were taken of the Munich sample at the Zoologisches Institut in Munichto obtain a detailed view of the enamel wrinkling patterns SEM images were not possibleto obtain for the Zuumlrich sample The specimens were examined using a LEO 1430VP SEMIn this study the proposed dental orientations of Smith amp Dodson (2003) are followedThe Slenderness Index (SI sensu Upchurch 1998) was measured for each crown tooth


Figure 3 Images of PIMUZ AIII 0823a (A) PIMUZ AIII 0823b (B) PIMUZ AIII 0823c (C) PIMUZAIII 0823d (D) PIMUZ AIII 0823e (E) PIMUZ AIII 0823f (F) PIMUZ AIII 0823g(G) PIMUZ AIII0823 h (H) PIMUZ AIII 0823i (I) PIMUZ AIII 0823j (J) In apical view basal view labial view lingualview distal view and mesial view The scale bar equals 1 cm Images taken by FH



by dividing the apicobasal length by the mesiodistal width in the middle of the crownThe Compression Index (CI sensu Diacuteez Diacuteaz Tortosa amp Loeuff 2013) was measured foreach tooth by dividing the labiolingual width by the mesiodistal width in the middle ofthe crown The abrasion stages of the functional dentition proposed by Saegusa amp Tomida(2011) and Wiersma amp Sander (2016) will be assessed for each tooth in order to assesspossible tooth position in the toothrow The angles of the wear facets were measured withrespect to the labiolingual axes of the teeth See Table 1 for all tooth measurements

The studied sample was compared with teeth from other sauropod taxa in a quantitativeapproach by multivariate analysis The comparative tooth sample is measured by firsthand observations (i e the Lo Hueco Massecaps Fox-Amphoux-Meacutetisson samplesAmpelosaurus Atsinganosaurus Lirainosaurus Patagosaurus Lapparentosaurus) as wellas from literature where SI and CI were reported or could be confidently measured orestimated and a minimum sample size of three tooth specimens was reached (Upchurchamp Barrett 2000 Barrett et al 2002 Carpenter amp Tidwell 2005 Apesteguiacutea 2007 FreireMedeiros amp Lindoso 2007 Diacuteez Diacuteaz et al 2012a Diacuteez Diacuteaz Pereda Suberbiola amp Sanz2012 Diacuteez Diacuteaz Tortosa amp Le Loeuff 2013 Diacuteez Diacuteaz Ortega amp Sanz 2014 Holwerda Polamp Rauhut 2015 Franca et al 2016 Averianov amp Sues 2017) Taxa from different periodsand palaeobiogeographic origins were included where possible A total of 102 teeth weregrouped by taxon if possible or sorted by morphotype finally creating 17 different groupsBoth damagedworn as well as unworn teeth were used due to paucity of sample size SeeTable S1 for this data Differences in SI and CI ratios were tested amongst groups throughstatistical analyses The shape of the cross section and the number angle and size of thewear facets were not considered for this purpose because these features may be morerelated to other functional factors (ie tooth position stage of tooth wear) rather thana taxonomic factor Due to the small sample size the non-normal distribution and thenon-homoscedastic variances amongst sample groups the non-parametric multivariateone-way PERMANOVA test was performed followed by post-hoc tests assessing differencesfor each pair of groups (Hammer amp Harper 2006) The analysis was implemented usingPAST v320 (Hammer Harper amp Ryan 2001) Finally the tooth groups were depicted ina dispersion plot together with additional taxa for which sample size was too small to beincluded in the statistical analyses (see lsquoDiscussionrsquo)

RESULTSMorphological descriptionMoroccan sample TaouzBSPG 1993 IX 331A (Fig 2A) The crown of this chocolate-to reddish-brown colouredapicobasally elongated tooth is more or less cylindrical It tapers towards the apex bothmesiodistally and labiolingually The labial side is strongly convex the lingual side isstraight to concave The convexity increases towards the apex as the distal 13rd bendsmore strongly towards the lingual side The tooth has an almost circular cross section at thebase of the crown becoming slightly more flattened in the labiolingual direction apicallyIt has a SI of 431 and a CI of 085 (see Table 1) Two distinct wear facets are present on


Table 1 Measurements wear stage (after Saegusa amp Tomida 2011) and enamel morphology of each tooth Measurements in mm

Specimennr

Apico-basallength

Abrasionstage

Mesio-distalbase

Mesio-distalmiddle

Mesio-distalapex

Labio-lingualbase

Labio-lingualmiddle

Labio-lingualapex

SI CI Abrasionstage

Numberand locationofwearfacets

Hypotheticalplacementin the snout

Apicalthirdcross-section

Enamelornamentation

BSPG 1993 IX 331A 60 53 12 123 62 10 105 4 43089 08536 F2 2 (ap ln) Premaxilla Elliptical Anastomosed

BSPG 1993 IX 331B 48 24 108 111 45 85 85 3 21621 07657 F1 0 ndash Elliptical Anastomosed

BSPG 1993 IX 331C 37 37 10 9 55 75 75 2 41111 08333 F4-F5 4 (lb ln m d) Maxilla Elliptical (worn)scratches andapical pits

BSPG 1993 IX 313A 275 275 82 82 45 6 62 1 33536 07560 F2 1 (ln) Premaxilla Elliptical Longitudinal ridges(but worn)

BSPG 1993 IX 2A 51 50 105 115 55 85 9 2 43478 07826 F2 1 (ln) Maxilla Lemonshaped

Longitudinal ridges(but worn)

BSPG 1993 IX 2B 475 475 13 13 115 9 92 3 36538 07076 F2ndashF3 2 (lb ln) Anteriordentary

Lemonshaped

Longitudinal ridges

BSPG 1993 IX 2C 47 47 10 115 5 8 10 2 40869 08695 F2 1 (lb) Anteriordentary

Lemonshaped

No(because ofpreservation)

BSPG 1993 IX 2D 38 38 95 105 15 65 75 15 36190 07142 F1 0 Anterior () Lemonshaped

(worn)wpits and scratches

PIMUZ AIII 0823 a 66 59 15 12 7 8 7 4 49166 05833 F2 1 (ln) Premaxilla Elliptical Anastomosed(but worn)

PIMUZ AIII 0823 b 39 31 145 13 7 8 9 7 23846 06923 F2 1 (ln) Premaxilla D-shaped Anastomosed

PIMUZ AIII 0823 c 57 34 11 9 5 6 6 3 37777 06666 F1 0 ndash Lemonshaped

Anastomosedwprotrusions

PIMUZ AIII 0823 d 24 21 7 9 6 6 6 4 23333 06666 F2ndashF3 2 (lb ln) Anterior Elliptical(worn)


PIMUZ AIII 0823 e 43 37 10 9 8 9 7 4 41111 07777 F2 2 (lb ln) Premaxilla Lemonshaped

Reticulatew protrusions

PIMUZ AIII 0823 f 42 38 9 8 4 6 7 3 475 0875 F1 0 ndash Elliptical Smooth

PIMUZ AIII 0823 g 31 29 7 6 3 6 5 3 48333 08333 F4 3 (ln m d) Maxilla Lemonshaped(faint)

Smooth(w apicobasalstriations)

PIMUZ AIII 0823 h 26 26 5 6 5 4 45 3 43333 075 F1ndashF2 1 (ap) ndash Elliptical Smooth

PIMUZ AIII 0823 i 21 21 5 55 3 3 4 2 38181 07272 F2ndashF3 2 (lb ln) Anteriordentary

Lemonshaped

Smooth

PIMUZ AIII 0823 j 34 34 11 9 8 9 10 4 37777 11111 F4 3 (ln m d) Maxilla Elliptical(worn)

Chevron-like

Holw

erdaetal(2018)PeerJD

OI107717peerj5925

943

the lingual and the apical side of the tooth (F2 abrasion stage) The lingual wear facethas an angle of almost 90 degrees with respect to the labiolingual axis As no mesial anddistal wear facets are present this tooth was probably located anteriorly in the upper jaw(premaxilla) A polished surface is found on the labial side of the crown Either damage orwear is present on the mesial and distal edges on the carinae exposing the dentine Theenamel wrinkling pattern is more pronounced on the labial side than on the lingual sideof the tooth (see Figs 4Andash4B) On the labial as well as the lingual side the pattern is morepronounced in the middle of the tooth and fades out slightly toward the apex and the baseThe labial enamel wrinkling pattern consists of frequently anastomosing sinuous groovesand crests of varying width with a general apicobasal orientation Grooves and crests arediscontinuous crests are often interrupted by pits and islets The crests are rounded totriangular in shape The distribution of crests and grooves is roughly equal Compared tothe other teeth excepting BSPG 1993 IX 331B the crests protrude sharply and the groovesare relatively deep On the lingual side more pits are present and the grooves and crestsappear slightly less rounded in shape but retain their apicobasal orientation The groovesappear more shallow on the lingual side

BSPG 1993 IX 331B (Fig 2B) This unworn tooth has the same colour and enamel textureas BSPG 1993 IX 331A It curves towards the lingual side with the labial side slightly moreconvex on the upper half resulting in a labiolingually tapering apex The tooth crownis convex toward the distal side tapering to a mesiodistally narrow apex The tooth isgenerally distally inclined however the apex curves slightly towards the mesial side It hasan oval cross section at the base which becomes lsquolsquolemon-likersquorsquo (sensu Diacuteez Diacuteaz Tortosaamp Loeuff 2013) at the apex due to the presence of pronounced carinae on the mesial anddistal edges Its SI is 261 and the CI 077 see Table 1 The carina on the distal side is slightlymore pronounced and continues further basally than the one on the mesial side The apexcontains a polished surface on the mesial side

The wrinkling is similar to BSPG 1993 IX 331A however due to the unworn state ofBSPG 1993 IX 331B it is more pronounced The enamel wrinkling pattern consists ofsharply protruding angular narrow and discontinuous grooves (see Figs 4Cndash4D) Thewrinkling on the lingual side is more pronounced than the labial side and also appearsslightly more rounded Although it is fully developed the crown lacks wear facets andthe root does not seem to have any resorption as in the F1 abrasion stage proposed byWiersma amp Sander (2016) This together with the coarse enamel pattern of the crown (Figs4Cndash4D) with no signs of abrasion by occlusion indicates that this was probably a recentlyerupted (unused) tooth Due to this we cannot hypothesize the placement of this tooth inthe jaw This specimen differs from the other teeth in this study by the strong curvature ofthe crown and its low SI ratio This can be attributed to a distal (posterior) placement ofthe tooth in the jaw as for example is seen in the nearly complete tooth row of Giraffatitan(MBR218121) Sarmientosaurus (Martiacutenez et al 2016) and Abydosaurus (Chure et al2010) In addition and because of its size it probably belonged to a juvenile individual


Figure 4 SEM pictures of enamel wrinkling BSPG 1993 IX 331A in labial (A) and lingual (B) viewBSPG 1993 IX 331B in labial (C) and lingual (D) view BSPG 1993 IX 313A in labial (E) and lingual (F)view BSPG 1993 IX 2A in labial (G) and lingual (H) view BSPG 1993 IX 2B in labial (I) and lingual (J)view and BSPG 1993 IX 2D in labial (K) and lingual (L) view The scale bar equals 500 microm Images takenby FH and RM



BSPG 1993 IX 331C (Fig 2C) This chocolate to reddish-brown coloured tooth differsfrom the first two Kem Kem teeth in that it is rather straight both labially and linguallyshows little tapering and has a distinctive enamel wrinkling pattern The apex showstapering due to labial and lingual wear facets and only a slight apical mesiodistal taperingis present A slight curvature towards the lingual side is present The base and middle ofthe tooth is oval in cross section the apex shows a slightly more elliptical shape It has a SIof 411 and a CI of 083 see Table 1

Four wear facets are present on the tooth one on each of the labial lingual mesialand distal surfaces respectively The lingual wear facet is angled at around 60 degrees withrespect to the labiolingual axis The labial wear facet is angled at almost 90 degrees withrespect to the labiolingual axis Both the mesial and distal wear facets are more pronouncedon the lingual side and are positioned basal to the lingual wear facet They appear almostparallel to the toothrsquos main axis The number and development of the wear facets indicatethat this tooth is between the F4 and F5 abrasion stages with an important tooth-to-toothcontact The food-to-tooth contact seems to not be as important as the crown enamel isnot as worn as in other specimens of this sample (see eg BSPG 1993 IX 313A) Due to thehigher development of the lingual wear facet and the placement of the mesial and distalones this tooth was probably located in the maxilla

The enamel of BSPG 1993 IX 331C is ornamented with thick mesiodistally orientedsharply protruding ridges and relatively wide grooves At about two thirds of the apicobasalheight the grooves slope towards the base from the mesial and distal edges at an angleof about 45 degrees and meet in the midpoint Towards the base the ridges becomemore horizontally positioned Some grooves seem to be connected forming a chevron-likemorphology This wrinkling pattern is also seen in PIMUZAIII 0823j Some pits are visiblein the apex probably due to a diet with some grit content

The four wear facets of BSPG 1993 IX 331C are not seen in similar shapes in any of theother teeth Moreover the deep grooves of the enamel wrinkling on the labial and lingualsides of the tooth do not resemble any taphonomic patterns as described by King Andrewsamp Boz (1999) but this does not rule out taphonomic processes completely However thepeculiar pattern is also seen in PIMUZ AIII 0832j therefore it is probably natural

BSPG 1993 IX 313A (Fig 2D) The upper half of this chocolate-brown coloured worntooth crown is inclined towards the lingual side with the labial side curving convexlyand the lingual side curving concavely The apex tapers mesiodistally and the mesial sideof the tooth inclines distally creating a convex mesial apical end The tooth has an ovalcross-section at the base becoming more lsquolsquolemon-likersquorsquo (sensu Diacuteez Diacuteaz Tortosa amp Loeuff2013) towards the apex due to the presence of protruding carinae on the mesial and distaledges The carina on the distal edge continues further towards the base than the carina onthe mesial edge Its SI and CI are 335 and 076 respectively see Table 1

The apex contains one wear facet on the lingual side angled at around 75 degrees withrespect to the labiolingual axis of the tooth The presence of only one wear facet theocclusal one groups this tooth within the F2 abrasion stage Due to this this tooth wasprobably placed anteriorly in the upper jaw (premaxilla)


The enamel appears smooth except for thin apicobasally-oriented discontinuousgrooves (see Figs 4Endash4F)

Moroccan sample ErfoudPIMUZ AIII 0823a (Fig 3A) This reddish-brown worn tooth crown is apicobasallystraight in lingual and labial view Only at the apex in labial view does the tip taper veryslightly to the distal side In both mesial and distal views the tooth is seen to curve towardsthe lingual side showing a moderate convexity on the labial side and an equally moderateconcavity on the lingual side also seen in BSPG 1993 IX 331A The width at the base is onlyslightly higher than at the middle of the crown showing a moderate mesiodistal taperingtowards the apex The cross-section of the tooth is oval to elliptical at the base to oval topossibly lemon-shaped at the apex The carinae are not pronounced on this tooth thereforethe apical lemon-shaped cross-section is not clear The carinae on both sides of the toothappear worn This tooth has a SI value of 492 and a CI value of 058 see Table 1

Labiolingual tapering towards the apex is caused by the presence of a round to ovallingual wear facet (meaning a F2 abrasion stage) This could mean that this tooth couldhave been a premaxillary one

The enamel wrinkling pattern is not well-preserved possibly due to abrasion of thetooth Only faintly reticulate wrinkling is seen on mostly the labial side of the tooth Thispattern could be a worn enamel wrinkling type similar to that of the more unworn BSPG1993 IX 331A and BSPG 1993 IX 331B No protruding ridges or deep prominent groovesare present in the enamel wrinkling pattern of this tooth

PIMUZ AIII 0823b (Fig 3B) This worn grey to beige coloured tooth displays a uniquemorphology amongst the tooth sample as it is a relatively apicobasally short mesiodistallywide tooth with a D-shaped cross-section representing more a general non-neosauropodeusauropod tooth shape (though this feature also exists in basal titanosaurs Barrett ampUpchurch 2005 Holwerda Pol amp Rauhut 2015) In labial and lingual view the tooth isapicobasally straight at its lower half showing a similar mesiodistal width at the base as atthe middle The tooth then tapers mesiodistally at its upper half and also tapers slightlytowards the distal side Moreover in lingual view the upper half of the crown towards theapex is slightly mesiodistally constricted giving the tooth a pear-shaped appearance Inmesial and distal view the tooth curves towards the lingual side creating a convex labialand concave lingual side The cross-section is oval at the base to D-shaped at the apex TheSI is 238 and the CI 069 see Table 1

Both carinae are worn exposing dentine on both sides and a prominent oval wear facetis present on the lingual side (F2 abrasion stage) This tooth could have been a premaxillaryone Another worn surface is present on the apex of the labial surface where the enamel isworn away to expose the dentine

The enamel wrinkling consists of rugose protruding continuous anastomosingridges which are flattened by wear andor abrasion throughout Between these ridgesdiscontinuous grooves and pits are visible


PIMUZ AIII 0823c (Fig 3C) The crown of this well-preserved unworn tooth is blackwhilst the root is cream-coloured to beige The crown is more or less apicobasally straightin labial and lingual view however a faint convexity is seen on the medial side showinga curvature of the entire tooth from root to apex towards the distal side Towards theapex the crown tapers sharply creating a triangular apical tip In mesial and distal viewthere is only a faint convexity visible on the labial side whereas the lingual side remainsapicobasally straight The cross-section at the base is oval and the cross-section at the apexis lemon-shaped (sensu Diacuteez Diacuteaz Tortosa amp Loeuff 2013) It presents a SI of 378 and a CIof 067 See Table 1

As no wear facets are present this tooth has a F1 abrasion stage No more informationabout its placement in the jaw can be deduced Both carinae are well-preserved as sharplyprotruding ridges where the distal carina is more pronounced than the mesial and showsa faint sinusoidal curvature Furthermore the distal carina shows ridges inclining fromthe apicobasally oriented wrinkling towards the carina creating denticle-like structuresor pseudodenticles (Bonaparte Gonzaacutelez Riga amp Apesteguiacutea 2006) The enamel wrinklingconsists of rugose discontinuous sinusoidal rounded protrusions and islets which areintersected by shallow but broad anastomosing grooves and pits The enamel is mostpronounced on the lingual side whilst the labial side shows a polished surface on the upperhalf of the crown where the wrinkling is worn away This tooth was probably used beforeit was lost despite the lack of wear facets because of its labial polished surface (indicatingfood-to-tooth contact)

PIMUZ AIII 0823d (Fig 3D) This reddish to chocolate-brown worn and polished toothcrown is apicobasally straight in labial and lingual view In labial view the tooth is morerectangular in shape whilst in lingual view the mesiodistal width increases from the basetowards the middle after which it tapers towards the apex The apex of the crown inclinesslightly towards the distal side especially in lingual view In labial view two grooves arepresent the distal of which is slightly displaced towards the middle of the tooth In mesialand distal view the labial side is mildly convex and the lingual side is more apicobasallystraight The cross-section from base to apex remains similar being oval to ellipticalwithout protruding carinae on mesial and distal sides The SI is 233 and the CI 067 seeTable 1

Symmetrical oval wear facets are present on the lingual and labial apices The presenceof both labial and lingual wear facets in the same tooth is an interesting feature that hasnot been considered in the five abrasion stages (Wiersma amp Sander 2016) Garciacutea amp Cerda(2010) and Garciacutea amp Cerda (2010b) described several apical wear patterns from a sample oftitanosaurian teeth from Argentina and the morphology of the crown and wear facets ofPIMUZ AIII 0823d is highly similar to the tooth MPCA-Pv-55 (fig 54) The apex of theseteeth (with both labial and lingual apical wear facets) is usually straight and perpendicularto the apicobasal axis of the crown and the inclination and development of both wear facetsis normally different Garciacutea amp Cerda (2010) and Garciacutea amp Cerda (2010b) suggested thatthe presence of both a labial and a lingual wear facet on the same tooth could be related tothe position of the teeth on the tooth row the occlusal pattern and the replacement of the


opposite teeth (seeGarciacutea amp Cerda 2010Garciacutea amp Cerda 2010b) fig 7 for a more graphicexplanation of this hypothesis) The absence of mesial and distal wear facets suggests thatit was probably anteriorly located in the dentary or (pre)maxilla (it is not possible to bemore accurate as both wear facets are equally developed) The mesial and distal sides ofthe apex do not taper which further adds to the rectangular appearance of the tooth Themesial and distal carinae are worn down to smooth polished ridges however the dentineis not exposed

The enamel wrinkling pattern ismostly polished away by (food-to-tooth or taphonomic)abrasion and only at the base of the labial and lingual sides a faint wrinkling is presentThis consists of rounded anastomosing protrusions giving a pebbly textural shape withwide but shallow grooves and pits in between At the base of the carinae the wrinklingbecomes slightly more rugose showing angular protrusions angling at sim30 degrees withrespect to the apicobasal axis towards the carinae with deep wide grooves running parallelto these

PIMUZ AIII 0823e (Fig 3E) The crown of this greyish-brown tooth tapers gently towardsthe apex in labial and lingual view and inclines slightly towards the distal side In labialand lingual view the tooth crown is apicobasally straight In mesial and distal view thetooth is labially strongly convex but lingually only mildly concave The apex tapers to apoint labiolingually The cross-section at the base is elliptical to cylindrical whilst the apexis more D-shaped to elliptical It has a SI of 411 and a CI of 078 see Table 1 Both carinaeare worn showing marginal grooves where dentine almost appears through the enamel

A large oval wear facet is present on the lingual apical side However the labial side alsoshows a less pronounced wear facet symmetrically placed to that of the lingual side Thistooth was probably placed anteriorly in the upper part of the mouth (possibly premaxilla)as can be deduced from the more developed lingual wear facet and the absence of mesialand distal facets The poor development of the labial wear facet indicates that its lower newopposite tooth probably erupted only shortly prior to its loss We consider a F2 abrasionstage to be appropriate for this tooth due to the poor development of the labial wearfacet and its placement in the premaxilla (because of the absence of mesial and distal wearfacets)

The enamel wrinkling pattern is finely reticulate with a symmetrical distribution ofsmall rounded protrusions surrounded by thin grooves However at the base of the crownthe enamel shows deep continuous grooves interspersed with pits whilst the protrusionsare worn away Part of the enamel at the root is damaged or gone

PIMUZ AIII 0823f (Fig 3F) This black smooth tooth crown shows traces of redsediment In labial and lingual views the lower half of the tooth crown is straight afterwhich it shows a strong inclination towards the distal side giving the mesial apical half aconvex and the distal apical half a straight to concave shape In mesial and distal viewsthe tooth is rather apicobasally straight only a faint labial convexity and lingual concavityis seen The cross-section at the base is round to elliptical and more cylindrical to a veryfaint lemon-shape (due to the carinae) at the apex Apically the tooth tapers to a sharp tip


which is inclined distally The SI is 475 and the CI is 088 Both mesial and distal carinaeshow a prominent but smooth ridge protruding towards mesial and distal sides on theapical half of the crown the lower half of the crown does not show carinae

As no apical wear facets are present we consider this tooth to show a F1 abrasion stageDue to this the placement of this tooth in the snout cannot be hypothesized The enamelis completely smooth suggesting together with the lack of clear wear facets that this toothwas relatively unused and unworn

PIMUZ AIII 0823g (Fig 3G) This grey to reddish brown tooth crown follows the samegeneralmorphology as PIMUZAIII 0823f in that the lower half of the crown is apicobasallystraight in both labial and lingual views as well as in mesial and distal views The upperhalf of the crown bends towards the distal side providing the mesial side with a convexcurvature The apex tapers to a sharp tip in labial and lingual view as well as in mesialand distal view Both mesial and distal carinae are present which are prominently butsmoothly protruding at the apical half of the crown The cross-section is elliptical at thebase to strongly lemon-shaped at the apex This tooth has a SI value of 483 and a CI valueof 083 see Table 1

An apicobasally-elongated mesiolabially-oriented wear facet as well as an equallyelongated distallingual wear facet is present giving the apical half of the crown a moreconstricted shape and creating a faint buttress at the base of the mesial and distalconstriction Finally a faint small round apical wear facet is present The presence ofthese three wear facets place this tooth in a F4 abrasion stage as the apex is already gentlyrounded This tooth probably was placed in the maxilla The slight displacement of bothmesial and distal wear facets indicate that this tooth was rotated The enamel is completelysmooth however apicobasal striations in the enamel are present on the labial apical sideof the tooth

PIMUZ AIII 0823 h (Fig 3H) The smallest tooth of the sample this reddish-browncrown shows a similar morphology to PIMUZ AIII 0823f and PIMUZ AIII 0823g Thecrown is straight in labiolingual and mesiodistal views with only the mesial apical endinclining towards the distal side in labiolingual view The apex tapers to a sharp tip Thecross-section is elliptical to cylindrical at the base and at the apex The SI is 433 and the CIis 075 see Table 1

The tooth is completely smooth and nearly unworn only a small circular apical wearfacet is present (F1ndashF2 abrasion stage) This information is not sufficient to propose itslikely placement in the snout Due to its small size and unworn state this tooth mightoriginate from a juvenile

PIMUZ AIII 0823i (Fig 3I) This rectangular red tooth is the second smallest of theErfoud sample It has a rectangular shape showing almost no tapering in labial and lingualview and only a slight apical tapering in mesial and distal view In mesial and distal viewthe labial side is mildly convex and the lingual side is mildly concave The cross-section isoval at the base to oval to lemon-shaped at the apex It has a SI of 382 and a CI of 073 seeTable 1


The labial apical side shows a high-angled oval wear facet whilst a low-angled elongatedwear facet is present on the lingual side which stretches to halfway down the apicobasallength of the crown This tooth presents the same condition as PIMUZ AIII 0823d withboth labial and lingual apical wear facets As the apical labial wear facet is more developedthis tooth may have been placed in the lower jaw The absence of mesial and distal wearfacets suggests that it was probably anteriorly located in the dentary The enamel of thetooth is completely smooth

PIMUZ AIII 0823j (Fig 3J) This dark brown to black tooth tapers gently towards theapex from the base whilst being slightly mesiodistally constricted at around the middleThe labial side is convex whilst the lingual side remains apicobasally straight Both mesialand distal carinae are present as smooth ridges which do not protrude The cross-sectionis elliptical both at the base as well as at the apex It presents a SI value of 378 and a CIvalue of 111 see Table 1

The upper half of the tooth crown is polished However only on the lingual side a lowangled wear facet is present Both at the mesial and distal apical sides a low-angled ovalpolished surface is present as well indicating tooth overlapping (F4 abrasion stage as thecrown apex is rounded) The location and development of these three wear facets indicatethat this tooth was probably located in the maxilla

The enamel wrinkling pattern is only visible at the base of the tooth as similar toBSPG 1993 IX 331C there is a mesiodistally-positioned chevron-like pattern of deep widegrooves and ridges which disperse towards the carinae

Algerian sampleBSPG 1993 IX 2A (Fig 2E) The tooth is covered in black enamel and has a reddish-brownbase The crown is apicobasally straight The mesial and distal sides taper strongly towardsthe apex whereas the labial and lingual sides taper slightly The mesial side howevershows a slight convexity and curves towards the distal side which is straight apically Thetooth is mesiodistally widest at the middle after which it tapers towards the apex Carinaeare present on the mesial and distal edges of the upper third of the crown as smoothprotruding ridges The carina on the distal side shows a slightly sinusoidal curvature atabout halfway of the apicobasal length of the tooth which is also seen in PIMUZ AIII0823c The distal carina reaches slightly further basally The cross-section at the base is ovalbecoming lemon-like at the apex due to the carinae (sensu Diacuteez Diacuteaz Tortosa amp Loeuff2013) The SI is 435 and the CI 078 (see Table 1)

A wear facet is present on the lingual side angled at around 50 degrees with respect tothe labiolingual axis The presence of only one wear facet the occlusal one groups thistooth within the F2 abrasion stage As this facet is located lingually and there are no mesialand distal wear facets this tooth was probably placed in the maxilla

The apical part of the labial side also shows a polished surface as in PIMUZ AIII0823c The enamel wrinkling pattern on both the labial and lingual sides consists ofapicobasally-oriented grooves and ridges which are less broad and more sinuous onthe labial side than on the lingual side (see Figs 4Gndash4H) While unworn was probably


similar to the crown enamel of BSPG 1993 IX 2B (Figs 4Indash4J) but it has been worn bytooth-to-food contact (like BSPG 1993 IX 313A Figs 4Endash4F) The enamel on the labialside is slightly thicker than on the lingual side

BSPG 1993 IX 2B (see Fig 2F) This worn tooth is grey to beige in colour The tooth iscurved lingually with the labial side convex and the lingual side concave This curvatureincreases towards the apex A very slight mesiodistal tapering can be seen at the apical partof the crown however the tooth appears rectangular when observed from the labial andlingual side Labiolingual tapering appears due to the presence of a labial and lingual wearfacet intersecting at the apex The lingual side of the tooth is relatively flat in the mesiodistaldirection when compared to the labial side This gives the tooth an oval cross section atthe base becoming D-shaped toward the centre and more cylindrical to lemon-shapedapically due to the presence of carinae Carinae are present on the mesial and distal edgesalthough the distal carina is more pronounced and continues further basally It has a SI of365 and a CI of 071 (see Table 1)

Two distinct wear facets are present on BSPG 1993 IX 2B one on the labial and the otheron the lingual side The labial wear facet is larger (almost 15 mm in apicobasal length) andangled toward the mesial side The labial wear facet is angled at around 72 degrees withrespect to the labiolingual axis of the crown The lingual wear facet is smaller It cuts thelabiolingual axis at almost 90 degrees This tooth presents the same condition as PIMUZAIII 0823d and PIMUZ AIII 0823i with both labial and lingual apical wear facets As theapical labial wear facet is more developed in BSPG 1993 IX 2B this tooth may have beenplaced in the lower jaw The absence of mesial and distal wear facets suggests that it wasprobably anteriorly located in the dentary

The enamel wrinkling pattern consists mainly of apicobasally-oriented sinuous groovesand ridges The ridges are sharply protruding and are triangular in shape (see Figs 4Indash4J)The enamel wrinkling pattern of BSPG 1993 IX 2B appears quite similar to BSPG 1993 IX331A BSPG 1993 IX 331B and the labial side of BSPG 1993 IX 2A The enamel wrinklingof BSPG 1993 IX 331A and of BSPG 1993 IX 331B is slightly more pronounced than theenamel wrinkling of BSPG 1993 IX 2B a difference perhaps caused by greater wear on thelatter A noteworthy difference between the enamel wrinkling patterns of this tooth andall other teeth from this sample is that the enamel wrinkling is more pronounced on whatseems to be the lingual side instead of the labial side

BSPG 1993 IX 2C (Fig 2G) This grey to beige coloured tooth is badly preserved andlargely covered with reddish sediment The crown is fairly straight apicobasally and tapersapically (mesiodistally as well as labiolingually) The mesial apical side shows a curvaturetowards the distal side as seen in BSPG 1993 IX 2A From the base to the middle thewidth of the crown expands slightly labiolingually after which it tapers to the apex Thisexpansion mainly seems to occur on the convex (probably labial) side and is also seen inBSPG 1993 IX 2A The distal edge shows faint traces of a carina but that cannot currentlybe accurately determined The cross-section at the base is slightly oval becoming almost


circular at the middle of the crown and then becoming more lemon-like apically due tothe presence of carinae The SI is 409 and the CI is 087 (see Table 1)

A possible wear facet can be seen on the labial side cutting the labiolingual axis of thecrown at a low angle (35 degrees) so it was probably at a F2 abrasion stage The absence ofmesial and distal wear facets and the labial position of the one present indicate that thistooth probably belonged to the anterior part of the dentary Because of the damaged stateof this tooth no SEM pictures were taken

BSPG 1993 IX 2D (Fig 2H) This reddish-brown coloured crown tapers mesiodistallytowards the apex as well as labiolingually resulting in a sharp apical tip The labial sideis convex whilst the lingual side is more concave The upper third of the crown showsstronger mesiodistal tapering on the mesial side Distinctly protruding carinae are presenton the mesial and distal edges of the crown The mesial carina is slightly more distinct dueto the curvature of the mesial apical part however it only runs halfway along the toothtowards the base whereas the distal carina continues further basally to the upper 34th ofthe tooth The tooth has an oval cross section at the base becoming strongly lemon-shapedapically due to the distinct carinae It presents a SI of 362 and a CI of 071 (see Table 1)

Wear facets are not present (F1 abrasion stage) so its position on the snout cannotbe deduced The enamel is smooth except for some pits (see Figs 4Kndash4L) This feature isinteresting not only because this tooth is the one that has the most worn crown enamelbut also for the presence of pits on it The individual probably fed on low vegetation witha significant quantity of grit This tooth had clearly been used for feeding but occlusionfeatures are not present so it was probably located anteriorly in the snout with its oppositetooth unerupted throughout its functional life

DISCUSSIONSystematic discussion and comparisonsThe tooth sample from northwestern Africa shares the presence of mesial and distalmargins extending parallel to each other along almost the entire length of the crown withneosauropod (diplodocoid and titanosauriform) sauropods together with the absence ofa mesiodistal expansion at the base of the crown (Calvo 1994 Upchurch 1995 Upchurch1998 Salgado amp Calvo 1997 Wilson amp Sereno 1998 Upchurch amp Barrett 2000 Barrett etal 2002 Wilson 2002 Upchurch Barrett amp Dodson 2004) These teeth also share withdiplodocoids and titanosaurs the loss of some plesiomorphic features of Sauropoda whichare retained in some but not all basal titanosauriforms (eg Giraffatitan Euhelopus) suchas the presence of a lingual concavity with a median ridge and labial grooves (Upchurch1998 Barrett et al 2002)

The general crown outline is similar in all the teeth of the sample parallel-sided crownsshowing slight labiolingual compression with mesial and distal carinae which express ahigher amount of protrusion in BSPG 1993 IX 331B BSPG 1993 IX 2A BSPG 1993 IX2D PIMUZ 0823c and PIMUZ AIII 0823 h The labiolingual compression (seen in apicalview) is more conspicuous in the Algerian teeth though PIMUZ AIII 0823a from ErfoudMorocco also shows this amount of compression BSPG 1993 IX 331B and BSPG 1993


IX 2D PIMUZ AIII 0823d PIMUZ AIII 0823 h PIMUZ AIII 0823i present a differentcrown morphology from the rest of the sample (see below) However this difference in thecrown morphology between these teeth and the rest of the sample could be due to differentpositions in the tooth row as occurs in most eusauropods and other sauropodomorphs(eg Carballido amp Pol 2010 Chure et al 2010 Holwerda Pol amp Rauhut 2015 Martiacutenezet al 2016 Mocho et al 2016 Carballido et al 2017 Wiersma amp Sander 2016) Lingualbuttresses seen in titanosauriforms from the Lower Cretaceous of Japan (Barrett et al2002) South Korea (Lim Martin amp Baek 2001) in Giraffatitan Janensch 1935 and inAstrodon (Carpenter amp Tidwell 2005) or circular bosses as seen in Euhelopus (Barrett ampWang 2007 Poropat amp Kear 2013) a possible macronarian from the Upper Jurassic ofPortugal (Mocho et al 2016) and an unknown (possible euhelopodid) titanosauriformfrom the Barremian of Spain (Canudo et al 2009) are not seen in any of our Moroccanor Algerian tooth samples Neither do the Algerian and Moroccan tooth samples showmesial and distal buttresses such as in an isolated tooth from the Santonian of Hungary(Oumlsi Csiki-Sava amp Prondvai 2017) Moreover diplodocoid pencil-like or needle-like teethas in Limaysaurus (Calvo amp Salgado 1935 Salgado et al 2004) are not found in this sampleeither In addition two further enamel types can be found in the sample rugosely orreticulately wrinkled (BSPG 1993 IX 331A 331B 331C PIMUZ AIII 0823abce BSPG1993 IX 2B and 2C) or smooth (BSPG 1993 IX 313A PIMUZ AIII 0823dfghi BSPG1993 IX 2A and 2D) enamel The differences between more rugose and more reticulatewrinkling in the enamel ornamentation could be due to the wear of the tooth and the dietof the individual animal

Finally although the CI is similar in both morphotypes the SI range is wider in theMoroccan Erfoud sample whilst remaining within a similar range between the MoroccanTaouz and the Algerian sample

After the morphological descriptions and similarities two main morphotypes couldbe distinguished based on shared features of shape expression of wear facets carinaeand enamel wrinkling One morphotype however may harbour further submorphotypeswhich are also discussed however without further sampling this could not be provenvalid It should also be noted that the morphotypes proposed here might not always reflectbiological morphotypes The morphotypes are here discussed and compared to othersauropods including but not restricted to biogeographically similar and contemporaneoussauropods (eg of Spain France northwest and central Africa)

Morphotype I BSPG 1993 IX 331A BSPG 1993 IX 331B BSPG 1993IX 313A BSPG 1993 IX 2A BSPG 1993 IX 2C BSPG 1993 2D PIMUZAIII 0823a PIMUZ AIII 0823b PIMUZ AIII 0823c PIMUZ AIII 0823ePIMUZ AIII 0823f PIMUZ AIII 0823g PIMUZ AIII 0823hGeneralThis is the most abundant morphotype in the sample It consists of teeth with highSI (22-49) and CI (06-09) rugose enamel wrinkling (but see discussion on this)prominent mesial and distal carinae together with a labial convexity and a slightly distalinclination of the apex and a subcylindrical to lemon-shaped cross-section There are


many intra-group specific morphological differences within this morphotype howeveras teeth both differ morphologically within one toothrow as well as between upper andlower toothrows (Sereno amp Wilson 2005 Wilson 2005 Zaher et al 2011 Holwerda Pol ampRauhut 2015 Martiacutenez et al 2016 Mocho et al 2016 Wiersma amp Sander 2016) enamelwrinkling as well as the presence of carinae are taken as the main drivers for comparisons(see Carballido amp Pol 2010 Holwerda Pol amp Rauhut 2015) Moreover enamel wrinklingcan be demonstrated to change over ontogeny with indications that juveniles have smoothor smoother enamel wrinkling in comparison with adult animals (Fiorillo 1991 Fiorillo1998 Diacuteez Diacuteaz et al 2012 Diacuteez Diacuteaz Pereda Suberbiola amp Sanz 2012 Diacuteez Diacuteaz Ortegaamp Sanz 2014 Holwerda Pol amp Rauhut 2015) As stated above this abundant MorphotypeI arguably still hosts several (sub)morphotypes which are also discussed below

DiscussionBSPG 1993 IX 331A and BSPG 1993 IX 331B (Figs 2A 2B) show a different SI and differentCI However they share a similar morphology in terms of expression of carinae labialconvexity and enamel wrinkling pattern and most likely belong to the same morphotypeSimilarly PIMUZ AIII 0823a shares the same apicobasal elongation of BSPG 1993 IX331A as well as a worn-down version of the rugose and highly sinuous enamel wrinklingThis reticulate worn-down version of the rugose type of enamel wrinkling is further foundin BSPG IX 1993 313A BSPG IX 1993 2B as well as in PIMUZ AIII 0823b and PIMUZAIII 0823e BSPG 1993 331A resembles a large Campanian-Maastrichtian titanosaur toothfrom Riacuteo Negro Argentina (Garciacutea 2013) in having a similar crown-root transition aswell as having high CI and SI ratios (073 vs 085 and 373 vs 436 for the tooth describedby Garciacutea (2013) and BSPG 1993 IX 331A respectively) However the enamel wrinklingpatterns between these two teeth show great differences the enamel of BSPG 1993 IX331A shows highly sinuous patterns not visible on the Argentine tooth The tooth alsoresembles the cylindrical morphotype with circular cross-section of the southeasternFrench Campanian-Maastrichtian Fox-Amphoux-Meacutetisson morphotype (FAM 03060311 and 0417 Diacuteez Diacuteaz Pereda Suberbiola amp Sanz 2012 fig 9) The SI ratios are highin both the AlgerianMoroccan and the French sample (sim4 excepting BSPG 1993 IX331B) These teeth also display a similar labial convexity which becomes stronger towardsthe apex in both the AlgerianMoroccan and the French sample The enamel wrinklingdiffers between these two however as the Kem Kem teeth show a much more pronouncedenamel wrinkling The apicobasal elongation slight labial convexity and presence on mostof these teeth of an apically based labial and lingual wear facet also resembles that of theLate Cretaceous Mongolian Nemegtosaurus (Wilson 2005) Finally the moderate tapering(or lack thereof) resembles that of teeth of the Late Cretaceous Alamosaurus from the USA(Kues Lehman amp Rigby 1980) although the enamel wrinkling on Alamosaurus is smootherthan in the MoroccanAlgerian sample though apicobasal striations are present on both

Even though the reticulate enamel wrinkling could be a worn-down version of therugose wrinkling described for this morphotype BSPG 1993 IX 313A PIMUZ AIII0823b and PIMUZ AIII 0823e (Figs 2D 3B 3E) slightly deviate from the generalshape of this morphotype in displaying a mesiodistally constricted apex in labial and


lingual view A difference in order of tooth row might explain this as teeth from themesial side of the toothrow are larger and more robust than teeth from the distal endof the toothrow This is not seen in titanosaurs (Garciacutea amp Cerda 2010 Garciacutea amp Cerda2010b) however it is observed in titanosauriforms (eg Giraffatitan MBR218121Abydosaurus (Chure et al 2010) This shape is further seen in more robust (lower SIhigher mesiodistal and labiolingual width) titanosauriform morphotypes such as theCenomanian titanosauriform indet tooth from France described by Vullo Neraudeauamp Lenglet (2007) Astrodon (Carpenter amp Tidwell 2005) the more robust tooth formof the Late Cretaceous Asian Mongolosaurus (Mannion 2011) Europatitan from theBarremian-Aptian of Spain (Torcida Fernaacutendez-Baldor et al 2017) the posterior maxillaryteeth of the Cenomanian-Turonian Patagonian Sarmientasaurus (Martiacutenez et al 2016)Ligabuesaurus from the Aptian-Albian of Neuquen Argentina (Bonaparte Gonzaacutelez Rigaamp Apesteguiacutea 2006) an unnamed titanosaurian tooth sample from the Upper CretaceousBissekty Formation Uzbekistan (Averianov amp Sues 2017) and lastly the robust types ofthe Massecaps and Ampelosaurus morphotypes from the Campanian-Maastrichtian ofsoutheastern France (Diacuteez Diacuteaz Tortosa amp Loeuff 2013) Finally BSPG 1993 IX 313A withits strong apical labial convexity is morphologically similar to both the small tooth typeof the Cenomanian-Campanian Chinese Huabeisaurus (DrsquoEmic et al 2013) as well asthe small Campanian-Maastrichtian Atsinganosaurus tooth type from France by sharinga labiolingual compression (CI 076) a high-angled apical wear facet and lemon-shapedcross section due to the presence of apical carinae (Diacuteez Diacuteaz Tortosa amp Loeuff 2013 fig3 MHN-AIX-PV199922) It also matches Huabeisaurus and Atsinganosaurus in havingsmooth enamel One hypothesis for this smooth enamel could be the tooth-to-food contactthat could have worn a previously more coarse enamel like the ones of BSPG 1993 IX 331Aand BSPG 1993 IX 331B (Figs 4Andash4D) However the enamel of BSPG 1993 IX 313A doesnot present the conspicuous pits that appear on the enamel of BSPG 1993 IX 2D (Figs4Kndash4L) from the Algerian sample This could be due to a diet with a greater quantity ofgrit in the Algerian individual as happens in many sauropods especially the ones that fedin the lower levels of the trees (Fiorillo 1998 Upchurch amp Barrett 2000 Garciacutea amp Cerda2010 Garciacutea amp Cerda 2010b) The individual of BSPG 1993 IX 313A may have fed on softvegetation as has been suggested for Diplodocus (Fiorillo 1998)

Also included in Morphotype I are BSPG 1993 IX 2A BSPG 1993 IX 2C PIMUZ AIII0823c (Figs 2E 2G 3C) These teeth deviate from the general cylindrical and general apicaltapering shape of Morphotype I in that they all display a mesiodistally slender base afterwhich the width increases towards the middle and then tapers towards the rounded apicaltip This is also arguably seen in Rinconsaurus (Calvo amp Gonzaacutelez Riga 2003) as well asin an unnamed titanosaur tooth sample from the Upper Cretaceous Bissekty FormationUzbekistan (Averianov amp Sues 2017) although the latter teeth show a lingual median ridgewhich the Moroccan and Algerian samples do not BSPG 1993 IX 2A and BSPG 1993 IX2C display a similar low angled lingual wear facet (sim50 degrees relative to the labiolingualtooth axis) and both BSPG 1993 IX 2A and PIMUZ AIII 0823c show a similar labialpolished surface BSPG 1993 IX 2C is too worn however the carinae of the well-preservedBSPG 1993 IX 2A and PIMUZ AIII 0823c are prominently present as mesially and distally


offset ridges Moreover the distal carina is more developed than the mesial one in bothshowing a sinusoidal curvature in distal view as seen to a lesser extent in Huabeisaurus(DrsquoEmic et al 2013) Note however that the carinae are not as prominent as in Euhelopus(Barrett amp Wang 2007 Poropat amp Kear 2013) Furthermore the distal carina of PIMUZAIII 0823c shows pseudodenticles a feature seen in the Late Jurassic South AfricanGiraffatitan (Janensch 1935) the Lower Cretaceous Patagonian Ligabuesaurus (BonaparteGonzaacutelez Riga amp Apesteguiacutea 2006) an unnamed titanosauriform from the Early Cretaceousof Denmark (Bonde 2012) the Late Jurassic French Vouivria (Mannion Allain amp Moine2017) and the Early Cretaceous AfricanMalawisaurus (Gomani 2005)

Furthermore BSPG 1993 IX 2A resembles the morphotype B of Lo Hueco Spain(MCCM-HUE 2687 Diacuteez Diacuteaz Ortega amp Sanz 2014 Fig 5) Both morphotypes arecylindrical have a high SI (gt43) a strong apical distal or medial inclination of the tooth(giving the tooth a far from straight outline) with a high-angled wear facet Moreover theenamel wrinkling of BSPG 1993 IX 2A matches that of the Lo Hueco morphotype in thatboth morphotypes show coarse but not rugose discontinuous wrinkling with smoothlongitudinal ridges although BSPG 1993 IX 2A shows more pronounced enamel wrinklingthan Lo Hueco morphotype B

PIMUZ AIII 0823c also resembles Lo Hueco morphotype A in the general morphologyof the crown and its length its labiolingual compression and its SI and CI values (see egHUE-685 Diacuteez Diacuteaz Ortega amp Sanz 2014 fig 2)

It could be argued that due to the differences of BSPG 1993 IX 2A BSPG 1993 IX 2CPIMUZ AIII 0823c from the rest of Morphotype I these teeth could be gathered in aseparate morphotype however as the sample size is low with only three teeth furtheranalysis to help distinguish any (sub)morphotypes is not possible and lies outside of thescope of the current study until a higher tooth sample can be examined Therefore althoughthese teeth are discussed as potentially separate the most parsimonious conclusion is toleave them in Morphotype I

Finally BSPG 1993 2D PIMUZAIII 0823f PIMUZAIII 0823g PIMUZAIII 0823 h areassigned toMorphotype I although the enamel wrinkling differs from the rugose type (boththe worn and unworn expression of it) BSPG 1993 IX 2D PIMUZ AIII 0823f PIMUZAIII 0823g and PIMUZ AIII 0823 h (Figs 2H 3F 3G 3H) all share a smooth enamel typea strong distal displacement of the apex in labial and lingual view an acutely tapering sharpapical tip and a distally inclined base of 45 degrees One tooth (PIMUZ AIII 0823h) islikely to be a juvenile tooth This is interesting as thus far teeth of juvenile sauropods showa difference in expression of enamel wrinkling as found by Fiorillo (1991) Fiorillo (1998)Diacuteez Diacuteaz et al (2012a) Diacuteez Diacuteaz Pereda Suberbiola amp Sanz (2012) Diacuteez Diacuteaz Ortega ampSanz (2014) and Holwerda Pol amp Rauhut (2015) in several titanosaurian teeth from theIbero-Armorican Island The smoothness of enamel wrinkling in juvenile teeth thereforecould express differently in adults further supporting the most parsimonious conclusionof including these last teeth in Morphotype I Barrett et al (2016) described some juvenile(hatchling or even embryonic) sauropod teeth of titanosauriformscamarasaurids fromthe Berriasian of southern France which match the apical morphology of this Moroccantooth However the Moroccan tooth lacks the basal mesial constriction and the lingual


Figure 5 Dispersion plot of Cretaceous sauropod tooth morphotypes with Jurassic outgroups Seecoloured boxes in legend for sauropod groups (A) All groups highlighted (B) Morphotype I and II high-lighted


buttress of juvenile teeth described by Barrett et al (2016) Juvenile teeth are also describedby Garciacutea amp Cerda (2010) and Garciacutea amp Cerda (2010b) for sauropod embryos from AucaMahuevo however these small teeth show a more acutely tapering apical tip than theMoroccan sample

PIMUZAIII 0823f andPIMUZAIII 0823 h resemble the Spanish LoHuecomorphotypeA in the general morphology of their crowns and their slight apical asymmetry (which


could be due to wear) PIMUZ AIII 0823f also reflects the Lo Hueco morphotype A in thatit has a similar length labiolingual compression and SI and CI values (Diacuteez Diacuteaz Ortegaamp Sanz 2014) As PIMUZ AIII 0823 h probably belonged to a juvenile specimen the sizeof this tooth is smaller when compared to the other ones and this changes the SI and CIvalues Juvenile teeth need to be used with caution when included in comparative studiesespecially when using quantitative variables such as the SI and CI (see statistical analysis)

PIMUZ AIII 0823g is the only tooth with smooth enamel that shows striations onthe surface providing the cross-section with a slightly rhomboid shape however thestrongly protruding carinae also still give a lemon-shaped cross section Striations areseen on teeth of Huabeisaurus (DrsquoEmic et al 2013) brachiosaurid teeth from SouthKorea (Lim Martin amp Baek 2001) smooth enamel type titanosaur teeth from the BissektyFormation Uzbekistan (Averianov amp Sues 2017) and in combination with smooth enamelin Atsinganosaurus (though some teeth do display gentle wrinkling on the middle see DiacuteezDiacuteaz Tortosa amp Loeuff (2013) as well as in Demandasaurus (Torcida Fernaacutendez-Baldor etal 2011) although the carinae are less conspicuous on the latter taxon Smooth enamel incombination with a sharp apex is further seen in the Albian Karongasaurus from Malawi(Gomani 2005) Smooth enamel exists on Limaysaurus (Salgado et al 2004) however thistooth is more needle-shaped than the teeth of theMoroccanAlgerian sample As these teethare not worn the apical morphology differs from the other teeth of Morphotype I whichare all mostly worn apically However as worn versus unworn teeth cannot be properlymorphologically distinguished with isolated teeth these are still assigned to Morphotype I

Given the resemblance of Morphotype I to predominantly Cretaceous sauropodsand moreover given the size and shape range this morphotype is difficult to assignto any particular group The size and shape range suggests a titanosauriform origin asderived titanosaurians usually show a more conservative morphological range (Garciacutea ampCerda 2010 Garciacutea amp Cerda 2010b) However given the similarity between some teeth ofMorphotype I with those of titanosaurians it is more likely that both non-titanosauriantitanosauriforms as well as titanosaurians are present in the tooth sample of Morphotype Iwhich reflects sauropod postcranial diversity of the Cretaceous of northwest Africa recordedby previous studies as both titanosauriforms (Mannion amp Barrett 2013 Fanti Cau ampHassine 2014 Lamanna amp Hasegawa 2014) as well as derived titanosaurians (Ibrahimet al 2016) have been reported to be present Even though some of the teeth resemblemore specific groups (eg Euhelopus Huabeisaurus) the general morphotype cannot beassigned to any more specific group No affinity with other groups (eg diplodocidsrebbachisaurids) is found for Morphotype I either

Morphotype II BSPG 1993 IX 331C BSPG 1993 IX 2B PIMUZ AIII0823d PIMUZ AIII 0823i PIMUZ AIII 0823jGeneralA smaller tooth sample from both the Moroccan and Algerian sample deviatesmorphologically from Morphotype I These teeth show a more rectangular morphology alack of apical tapering and distinct labial and lingual wear facets


DiscussionBSPG 1993 IX 331C and PIMUZ AIII 0823j (Figs 2C 3J) both show a distinctive enamelwrinkling not seen in the other teeth of the sample It displays a lsquochevronrsquo pattern on thelabial and lingual surfaces with rugose striations anastomosing towards the carinae Thispattern is arguably present on the labial side of the enamel of another Moroccan KemKem sauropod tooth tentatively (but not conclusively) assigned to rebbachisauridae byKellner amp Mader (1997) This latter tooth however also shows striations (Kellner amp Mader1997) which are not seen on BSPG 1993 IX 331C and PIMUZ AIII 0823j As Carballidoamp Pol (2010) and Holwerda Pol amp Rauhut (2015) showed enamel wrinkling on sauropodteeth can be an autapomorphic diagnostic feature As both teeth are worn however theother morphological features besides enamel wrinkling must be taken into account Theteeth do share morphological similarities in crown shape with the tooth described byKellner amp Mader (1997) which is apicobasally straight The rectangular morphology ofthese teeth caused by a lack of mesiodistal tapering towards the apex together with aslightly higher CI due to higher labiolingual compression than the other teeth from theMoroccanAlgerian sample showing an oval to cylindrical cross-section is shared withBSPG 1993 IX 2B as well as PIMUZ AIII 0823d and PIMUZ AIII 0823i (Figs 2F 3D3I) These five teeth further share labial and lingual wear facets which are symmetricallyplaced though in PIMUZ AIII 0823i as well as in BSPG 1993 IX 2B one high-angledand low-angled wear facet is seen which is characteristic of the Aptian-Albian Nigersaurus(Sereno amp Wilson 2005 p166 fig 57 Sereno et al 2007 Fig 2) The size of PIMUZ AIII0823i matches that of Nigersaurus however the other teeth are much larger than theisolated Nigersaurus tooth described by Sereno amp Wilson (2005) The enamel asymmetrya diagnostic feature for Nigersaurus could not be accurately measured on the Moroccanand Algerian tooth sample To a lesser degree the labial and lingual wear facet symmetryis seen in both the Brazilian Aptian Tapuisaurus (Zaher et al 2011) as well as the LateCretaceous Maxakalisaurus (Kellner et al 2006 Franca et al 2016) However these teethshow a higher SI than the MoroccanAlgerian sample as well as stronger labial convexityThe morphology of Morphotype II also does not closely match the conical peg-shapedteeth of Demandasaurus (Torcida Fernaacutendez-Baldor et al 2011) a rebbachisaurid from theEarly Cretaceous of Spain However the enamel is relatively smooth on both MorphotypeII and Demandasaurus and moreover the teeth of Morphotype II are unworn whereasthe Demandasaurus teeth are relatively unworn

The morphological features on BSPG 1993 IX 2B further show a set of derivedtitanosaurian characteristics with a D-shaped cross-section in the middle of the toothas seen in Mongolosaurus (Mannion 2011) but also seen in a titanosauriform toothfrom Argentina (Garciacutea amp Cerda 2010 Garciacutea amp Cerda 2010b MPCA-Pv-55 fig 5) Aspreviously stated differences in tooth shape can be explained by their relative placementin the toothrow as seen in Mongolosaurus (having both a cylindrical as well as a D-shaped tooth (Barrett et al 2002 Mannion 2011 and Nemegtosaurus Wilson 2005) BothMongolosaurus as well as Nemegtosaurus however show a distinct tapering of the apexwhich BSPG 1993 IX 2B does not show Furthermore differences in shape betweenupper and lower toothrows is also observed in diplodocoids such as Diplodocus and


Nigersaurus (Sereno amp Wilson 2005) The labial wear facet in particular is characteristicfor diplodocids and dicraeosaurids (Sereno amp Wilson 2005) and while diplodocids are notknown from the Cretaceous rebbachisaurids and dicraeosaurids are (eg Sereno amp Wilson2005 Gallina et al 2014) As rebbachisaurids such as Rebbachisaurus garasbae are foundin the Kem Kem beds of Morocco (Lavocat 1954 Mannion amp Barrett 2013 Wilson ampAllain 2015) the Aptian-Albian of Niger (Nigersaurus and rebbachisaurids (Sereno et al1996 Wilson 2005 Sereno et al 2007) and also the Aptian-Albian of Tunisia (Fanti Cauamp Hassine 2014 Fanti et al 2015) and tentatively in the late Barremian-early Aptian ofSpain (Pereda Suberbiola et al 2003 Torcida Fernaacutendez-Baldor et al 2011) they are bothbiogeographically close as well as originating from beds near-contemporaneous to thoseof our tooth sample Morphotype II therefore is tentatively assigned to Rebbachisauridaeindet

Quantitative analysisThough quantitative analysis has been applied to theropod teeth in several previousstudies (eg Hendrickx amp Mateus 2016 Samman et al 2005 Fanti amp Therrien 2007 OumlsiApesteguiacutea amp Kowalewski 2010 Hendrickx Mateus amp Arauacutejo 2015) a statistical approachto sauropod tooth diversity has thus far only been applied through using one variablemdashtheSI - by Chure et al (2010) and the number of wear facets on the apex (Averianov amp Sues2017) Quantitative analyses on sauropod teeth with two or more variables is thereforean area of study that has not received much attention Here we conduct an analysis ofsauropod teeth based on multivariate statistical tests The one-way PERMANOVA revealedsignificant differences between some of the tested groups (F = 1446 p= 00001) Specificcomparisons for each pair of groups are listed in Table 2 Morphotype I shows significantdifferences in SI and CI ratios with the D-shaped Morphotype from Fox-AmphouxPatagosaurus Euhelopus the Shiramine morphotype and Maxakalisaurus (Table 2)Differenceswith someof these groups are congruentwith the qualitative approach describedabove On the other hand the SI and CI values of Morphotype I did not significantly differfrom those of Atsinganosaurus Lirainosaurus Astrodon the cylindrical Morphotype fromFox-Amphoux both tooth morphotypes from Lo Hueco and the titanosaurian teethfrom Massecaps Neuqueacuten Uzbekistan and the Bauru Formation Brazil (see Table 2)This is in agreement with the qualitative discussion of Morphotype I where the robusttooth type showed morphological similarities with Astrodon and the elongated cylindricaltype was shown to be morphologically comparable to the Neuqueacuten and Uzbekistan toothtypes It also reinforces the morphological similarities found between Morphotype I withIbero-Armorican titanosaurs

ConcerningMorphotype II the SI andCI ratios differ significantly fromAtsinganosaurusPatagosaurus Euhelopus and Maxakalisaurus (see Table 2) confirming that even thoughthe wear facets of Morphotype II match those of Maxakalisaurus there is no furthermorphological overlap Unfortunately the available sample size of Nigersaurus and otherrebbachisaurids was not large enough to statistically test their similarities with confidence(see Table S1)


Table 2 One-way PERMANOVA comparisons for each pair of sauropod groups

Morph_I Morph_II Atsinga-nosaurus

Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus

Euhelopus Shiramineform

Astrodon Neuquentitanoindet

UzbekistanNeosauropod

Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763

Atsinganosaurusc 08383 00083 03888 00427 06971 00347 00006 00022 00093 01399 00495 06864 00165 00357

FoxAmphoux C-Morphc 00172 01892 00532 06458 00954 00054 00122 00268 01423 0106 06005 00176 01028

FoxAmphoux D-Morphc 01474 00792 00143 0144 00009 00074 03581 01112 09855 00057 00082 01545

Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212

Massecaps titanosaurc 00059 00117 01099 07491 04618 00936 00198 05032

Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527

Neuquen titanosaur c 00219 00072 047

Uzbekistan Neosauropodd 00008 00968

Maxakalisaurusc 00174

Bauru titanosaurc

Notesanon-neosauropod eusauropodbnon-titanosaurian titanosaurifomctitanosaurdunknown or resolved in this study

Holw


OI107717peerj5925

2843

However the very small sample size of this study is not well-suited to this type ofapproach therefore the results of this analysis must be taken with caution and anyrelationships found between sauropod taxa of our sample must be regarded as tentativeThe sauropod relationships suggested by the qualitative and quantitative analysis mightnot be supported if the sample size is increased For example most of the tooth groups ofthe studied sample were not distinguished after the Bonferroni correction on the post-hoctests This might mean that titanosaurian teeth do not possess any clear diagnostic featuresor more likely that only two variablesmdashthe SI and the CImdashare not enough to distinguishbetween titanosaurs as most taxa and morphotypes strongly group together (see Fig 5)In Fig 5 most teeth from the MoroccanAlgerian samples cluster together and there isalso overlap with other sauropod taxa andor tooth morphotypes The teeth with highSI and high CI are Maxakalisaurus Rapetosaurus Petrobasaurus and Limaysaurus whilstteeth with low SI and low CI are Patagosaurus and Jobaria (see Fig 5) The taxon withlow SI but high CI is Lapparentosaurus (Fig 5) From the central cluster MorphotypeI and II overlap mostly with the Shiramine teeth the Uzbekistan teeth Astrodon andthe Franco-Iberian teeth (ie the Lo Hueco Massecaps Fox-Amphoux-Meacutetissons andAtsinganosaurus types Fig 5) Titanosauriform teeth are known to show a large range inmorphology and moreover they show some convergence in morphology with more basalsauropod teeth (Garciacutea amp Cerda 2010 Garciacutea amp Cerda 2010b) However it is possibleafter the qualitative and quantitative analyses here that titanosaurian teeth show a similarconvergence Finally as mentioned previously the large range of size and shape within onetoothrow could also cause taxa to accrete in Fig 5 though postcranial morphology wouldcause more morphological scatter To resolve these issues a larger sample size not only ofthe case study at hand but also of other (Cretaceous) sauropod teeth could possibly aidin obtaining a better resolution of future quantitative analyses however this is beyond thescope of the present study

Euro-Gondwanan Cretaceous sauropod diversity andpalaeobiogeographical implicationsTo summarize the described tooth sample from the AlbianndashCenomanian Kem Kembeds of Morocco and the Continental Intercalaire of Algeria shows a predominantlynon-titanosaurian titanosauriformtitanosaurian assemblage with only one morphotype(II with four teeth) showing tentative rebbacchisaurid affinities When compared withthe biogeographically nearest tooth assemblages namely titanosaurian teeth found inthe Ibero-Armorican Island as well as northwest and central Africa several probablepalaeobiogeographical patterns can be assessed

Morphotype I shows morphological affinities with titanosauriforms Titanosauriansauropods in the Campanian Kem Kem beds of Morocco have been reported previously(Ibrahim et al 2016) This titanosaurian predominance is also seen in the later stagesof the Cretaceous of Egypt (Lamanna et al 2017 Sallam et al 2018) as well as Spainand France (see eg Le Loeuff 1995 Le Loeuff 2005 Sanz et al 1999 Garcia et al 2010Diacuteez Diacuteaz et al 2016 Vila Selleacutes amp Brusatte 2016) As fourteen teeth from our sampleshare several similarities with the cylindrical morphotype from Fox-Amphoux-Meacutetisson


with the morphotype A from Lo Hueco and with the D-shaped morphotype fromFox-Amphoux-Meacutetisson as well as with Atsinganosaurus and the morphotype B fromLo Hueco (Diacuteez Diacuteaz et al 2012 Diacuteez Diacuteaz Pereda Suberbiola amp Sanz 2012 Diacuteez DiacuteazTortosa amp Loeuff 2013 Diacuteez Diacuteaz Ortega amp Sanz 2014) this might suggest a possible closeaffinity between the Cenomanian North African titanosaurian faunas and those from theCampanian-Maastrichtian of southern Europe

Morphotype II shows affinities with rebacchisaurids Rebbachisaurid presence hasalready been noted from the Early Cretaceous of Niger (Sereno et al 1999 Sereno ampWilson 2005) Tunisia (Fanti et al 2013 Fanti et al 2015 Fanti Cau amp Hassine 2014)and Morocco (Lavocat 1954 Kellner amp Mader 1997 Mannion amp Barrett 2013 Wilson ampAllain 2015) as well as the United Kingdom (Mannion Upchurch amp Hutt 2011) and Spain(Pereda Suberbiola et al 2003 Torcida Fernaacutendez-Baldor et al 2011) Again the NorthAfricanmdashsouthern European connection is a tentative explanation for the dispersion ofrebbachisaurids between Gondwana and Europe in the Cretaceous (see Fig 6) in additionrebbachisaurids also seem to be a relatively diverse clade within North and Central Africaduring the end of the Aptian-Cenomanian (eg Mannion amp Barrett 2013 Fanti Cau ampHassine 2014 Wilson amp Allain 2015)

In previous studies faunal connections have been demonstrated to exist between NorthAfrica and Italy such as temporary continental connections during the Barremian (125Ma the so-called Apulian route) or more permanent connections caused by carbonateplatforms in the peri-Adriatic (Gheerbrant amp Rage 2006 Canudo et al 2009 Zarcone etal 2010 Torcida Fernaacutendez-Baldor et al 2011) These last authors suggested that thisroute could have allowed for the divergence of the rebbachisaurids Demandasaurusand Nigersaurus Moreover Fanti et al (2016) point to a rebbachisaurid dispersal eventleading from Gondwana to a European lineage in the Early Cretaceous Perhaps thehypothesized continental connection also allowed titanosaurs to migrate betweenLaurasia and Gondwana Furthermore next to European sauropods also theropodscrocodyliforms amphibians and snakes and even batoids from southern Europe (FranceSpain Italy Croatia) have been found to show Gondwanan affinities (Soler-Gijoacuten ampLoacutepez-Martiacutenez 1998 Gardner Evans amp Sigogneau-Russell 2003 Pereda-Suberbiola 2009Pereda-Suberbiola et al 2015 Sweetman amp Gardner 2013 Csiki-Sava et al 2015 Blanco etal 2016 Blanco et al 2017 Dal Sasso et al 2016 Blanco In Press)

The discovery of titanosaurian teeth with similar morphologies from the Cenomanianof Algeria and Morocco and from the late Campanian-early Maastrichtian of the Ibero-Armorican Island could indicate that some of these European titanosaurian faunas hada Gondwanan origin However this hypothesis needs to be taken with some cautionuntil more postcranial remains (with associated cranial specimens) are found anddescribed from the Early-Late Cretaceous of North Africa and southwestern Europeas our statistical analysis does not show a high support of any definite grouping betweenthe North African and southern European tooth morphotypes Csiki-Sava et al (2015)suggested that European titanosaurs do not seem to have a southern influence andpalaeobiogeographical analyses as well as this study show both a Gondwanan (South


Figure 6 Palaeobiogeographical reconstruction of northwest Africa and southern Europe using sauro-pod tooth morphotypes (A) northwest Africa and southern Europe during the Cenomanian (black line)and Campanian-Maastrichtian (grey line) with possible migration routes (dotted green line) adaptedfrom Csiki-Sava et al 2015 (B) Tooth morphotype I next to tooth morphotypes A and B from Lo Hueco(from Diacuteaz Ortega amp Sanz 2014) Fox-Amphoux-Meacutetissons cylindrical type and D-shaped morphotype(from Diacuteaz Suberbiola amp Sanz 2012b) the Massecaps titanosaur and Atsinganosaurus (from Diacuteaz Tor-tosa amp Loeuff 2013) (C) Tooth morphotype II next to Nigersaurus from Sereno et al 2007 and Deman-dasaurus (From Torcida Fernaacutendez-Baldor et al 2011)


American) and North American input in European Cretaceous fauna (egUpchurch 2008Ezcurra amp Agnoliacuten 2011) which might cautiously be supported by our qualitative andquantitative analyses as well However more recent studies have added more informationabout the North African-southern European connection between these sauropod faunasin the Late Cretaceous (see eg Sallam et al 2018 Diacuteez Diacuteaz et al 2018) In Fig 6 atentative palaeobiogeographical construction is shown using the Algerian and Moroccanmorphotypes and their morphological counterparts from northwest and central Africa aswell as southern Europe and possible migratory routes based on previous hypotheses

CONCLUSIONSA sample of eighteen teeth from the Cretaceous Kem Kem beds from Erfoud andTaouz Morocco and from the Continental Intercalaire Algeria has been studied Theoverwhelming majority of this sample shows titanosauriformtitanosaur affinities with asmaller group showing rebacchisaurid affinities This is congruent with the results of thestatistical analyses However the small size of the comparative samples and the relative


scarcity of this type of analysis in studies thus far begs for caution in interpreting resultsuntil further study is possible

On the other hand similarities between tooth samples from northwestern and centralAfrica and southwestern Europe do strongly hint at a possible sauropod faunal exchangethrough continental connections in the early Late Cretaceous between North and CentralAfrica and between North Africa and southwestern Europe These results support previoushypotheses from earlier studies on faunal exchange and continental connections

Institutional abbreviations

BSPG Bayerische Staatssammlung fuumlr Palaumlontologie und GeologieMunich Germany

FAM Fox-Amphoux-Meacutetisson FranceMBR Museum fuumlr Naturkunde Berlin GermanyMCCM-HUE Museo de las Ciencias de Castilla-la Mancha SpainMHN-AIX-PV Natural History Museum Aix-en-Provence FranceMPCA-Pv Museo Provincial lsquolsquoCarlos Ameghinorsquorsquo coleccioacuten de paleovertebra-

dos Riacuteo Negro ArgentinaPIMUZ Palaeontological Institute and Museum University of Zuumlrich

Switzerland

ACKNOWLEDGEMENTSOliver Rauhut (BSPG Munich Germany) Christian Klug and Torsten Scheyer (PIMUZZuumlrich Switzerland) are profoundly thanked for kindly allowing us to use material fromtheir collections We are indebted to Enrico Schwabe (ZSMMunich Germany) for his kindassistance in SEM imaging Many thanks also to Daniela Schwarz and Jens Koch (Museumfuumlr Naturkunde Berlin Germany) for allowing us to use their Giraffatitan specimen Weare grateful to Matt Dale and Charlie Underwood for their aid in Kem Kem palaeoecologyJeff Liston kindly checked the English The comments and recommendations of editorKenneth de Baets and reviewers Paul Barrett Attila Oumlsi and one anonymous reviewergreatly improved this manuscript This work was part of the BSc thesis of RM at UtrechtUniversity (the Netherlands)

ADDITIONAL INFORMATION AND DECLARATIONS

FundingAlejandro Blanco is supported by the program Axudas postdoutorais da Xunta de Galicia2017mdashModalidade A Additional funding for Alejandro Blanco came from the SynthesysProject DE-TAF-7025 and from the program Axudas aacute investigacioacuten da UDC 2017 2018The other authors received no funding for this work The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript


Grant DisclosuresThe following grant information was disclosed by the authorsAxudas postdoutorais da Xunta de Galicia 2017mdashModalidade ASynthesys Project DE-TAF-7025Axudas aacute investigacioacuten da UDC 2017 2018

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Femke M Holwerda conceived and designed the experiments performed theexperiments analyzed the data prepared figures andor tables authored or revieweddrafts of the paper approved the final draftbull Veroacutenica Diacuteez Diacuteaz performed the experiments analyzed the data prepared figuresandor tables authored or reviewed drafts of the paper approved the final draftbull Alejandro Blanco and Roel Montie performed the experiments analyzed the dataprepared figures andor tables approved the final draftbull Jelle WF Reumer conceived and designed the experiments approved the final draft

Data AvailabilityThe following information was supplied regarding data availability

Raw data consists of Slenderness Index (SI) and Compression Index (CI) of sauropodteeth mainly from the Cretaceous with some outgroups from the Jurassic The datasetis compiled using all literature and personal observations that to our knowledge exist ofCretaceous sauropod teeth This dataset was used for the quantitative analysis to compareMorphotype I andMorphotype II of the sauropod tooth sample fromMorocco and Algeriato other sauropods The Taouz Morocco and Algerian tooth sample of eight teeth is storedin the collections of the Palaeontological Museum Munich (BSPG) the Erfoud Moroccotooth sample of 10 teeth is stored in the collections of the Palaeontological Museum of theUniversity of Zurich (PIMUZ) and both are free and openly accessible upon request tothe curators in Munich and Zurich

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj5925supplemental-information

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vertebrates from the Algerian Kem Kem beds A new procoelous salamander fromthe Cenomanian with remarks on African Caudata Cretaceous Research 84384ndash388DOI 101016jcretres201711019

Apesteguiacutea S 2007 The sauropod diversity of the La Amarga Formation (Barremian)Neuqueacuten (Argentina) Gondwana Research 12533ndash546 DOI 101016jgr200704007


Averianov A Sues H-D 2017 Sauropod teeth from the Upper Cretaceous BissektyFormation of Uzbekistan Historical Biology 29641ndash653DOI 1010800891296320161229777

Barrett PM Hasegawa Y ManabeM Isaji S Matsuoka H 2002 Sauropod dinosaursfrom the Lower Cretaceous of eastern Asia taxonomic and biogeographical implica-tions Palaeontology 451197ndash1217 DOI 1011111475-498300282

Barrett PM Pouech J Mazin J-M Jones FM 2016 Teeth of Embryonic or HatchlingSauropods from the Berriasian (Early Cretaceous) of Cherves-de-Cognac FranceActa Palaeontologica Polonica 61591ndash596 DOI 104202app002572016

Barrett PM Upchurch P 2005 Sauropodomorph diversity through time In CurryRogers K Wilson J eds The Sauropods evolution and paleobiology Berkeley Univof California Press 125ndash156

Barrett PMWang X-L 2007 Basal titanosauriform (Dinosauria Sauropoda) teeth fromthe Lower Cretaceous Yixian Formation of Liaoning Province China Palaeoworld16265ndash271 DOI 101016jpalwor200707001

Belvedere M Jalil N-E Breda A Gattolin G Bourget H Khaldoune F Dyke GJ 2013Vertebrate footprints from the Kem Kem beds (Morocco) a novel ichnologicalapproach to faunal reconstruction Palaeogeography Palaeoclimatology Palaeoecology383ndash38452ndash58 DOI 101016jpalaeo201304026

Benyoucef M Laumlng E Cavin L Mebarki K Adaci M BensalahM 2015 Overabundanceof piscivorous dinosaurs (Theropoda spinosauridae) in the mid-Cretaceous ofNorth Africa The Algerian dilemma Cretaceous Research 5544ndash55

Blanco A Igdabatis marmii sp nov (Myliobatiformes) from the lower Maas-trichtian (Upper Cretaceous) of northeastern Spain an Ibero-Armoricanorigin for a Gondwanan batoid Journal of Systematic Palaeontology In PressDOI 1010801477201920181472673

Blanco A Bolet A Blain HA Fondevilla V Marmi J 2016 Late Cretaceous (Maas-trichtian) amphibians and squamates from northeastern Iberia Cretaceous Research57624ndash638 DOI 101016jcretres201507005

Blanco A SzaboacuteM Blanco-Lapaz Agrave Marmi J 2017 Late Cretaceous (Maastrichtian)Chondrichthyes and Osteichthyes from northeastern Iberia PalaeogeographyPalaeoclimatology Palaeoecology 465278ndash294 DOI 101016jpalaeo201610039

Bonaparte JF Gonzaacutelez Riga BJ Apesteguiacutea S 2006 Ligabuesaurus leanzai gen et spnov (Dinosauria Sauropoda) a new titanosaur from the Lohan Cura Formation(Aptian Lower Cretaceous) of Neuqueacuten Patagonia Argentina Cretaceous Research27364ndash376 DOI 101016jcretres200507004

Bonde N 2012 Danish dinosaurs a review Bernissart Dinosaurs and Early CretaceousTerrestrial Ecosystems 464435ndash451

Buffetaut E 1989 Archosaurian reptiles with Gondwanan affinities in the UpperCretaceous of Europe Terra nova 169ndash74 DOI 101111j1365-31211989tb00328x

Buffetaut E Mechin P Mechin-Salessy A 1988 Un dinosaure theacuteropode drsquoaffiniteacutesgondwaniennes dans le Creacutetaceacute supeacuterieur de Provence Comptes rendus de lrsquoAcademie


des sciences Seacuterie 2 Meacutecanique Physique Chimie Sciences de lrsquounivers Sciences de laTerre 306153ndash158

Calvo JO 1994 Jaw mechanics in sauropod dinosaurs Gaia 10183ndash193Calvo JO Gonzaacutelez Riga BJ 2003 Rinconsaurus caudamiru s gen et sp nov a new

titanosaurid (Dinosauria Sauropoda) from the Late Cretaceous of PatagoniaArgentina Revista geologica de Chile 30333ndash353

Calvo JO Salgado L 1995 Rebbachisaurus tessonei sp nov a new Sauropoda from theAlbian-Cenomanian of Argentina new evidence on the origin of the DiplodocidaeGaia 1113ndash33

Canudo JI Barco JL Pereda-Suberbiola X Ruiz-Omentildeaca JI Salgado L Fernaacutendez-Baldor FT Gasulla JM 2009What Iberian dinosaurs reveal about the bridge said toexist between Gondwana and Laurasia in the Early Cretaceous Bulletin de la SocieteGeologique de France 1805ndash11 DOI 102113gssgfbull18015

Carballido JL Holwerda FM Pol D Rauhut OW 2017 An Early Jurassic sauropodtooth from Patagonia (Cantildeadoacuten Asfalto Formation) implications for sauropoddiversity Publicacioacuten Electroacutenica de la Asociacioacuten Paleontoloacutegica Argentina 1750ndash57

Carballido JL Pol D 2010 The dentition of Amygdalodon patagonicus (DinosauriaSauropoda) and the dental evolution in basal sauropods Comptes Rendus Palevol983ndash93 DOI 101016jcrpv201001003

Carpenter K Tidwell V 2005 In Thunder-lizards ed Reassessment of the Early Creta-ceous sauropod Astrodon johnsoni Leidy 1865 (Titanosauriformes) Bloomington andIndianapolis Indiana University Press 78ndash114

Cau A Maganuco S 2009 A new theropod dinosaur represented by a single unusualcaudal vertebra from the Kem Kem Beds (Cretaceous) of Morocco Atti della Societaitaliana di scienze naturali e del museo civico di storia naturale di Milano 150239ndash257

Cavin L Forey PL 2004 New mawsoniid coelacanth (Sarcopterygii Actinistia) remainsfrom the Cretaceous of the Kem Kem beds Southern MoroccoMesozoic Fishes3493ndash506

Cavin L Tong H Boudad L Meister C Piuz A Tabouelle J AarabM Amiot RBuffetaut E Dyke G Hua S Le Loeuff J 2010 Vertebrate assemblages from theearly Late Cretaceous of southeastern Morocco an overview Journal of African EarthSciences 57391ndash412 DOI 101016jjafrearsci200912007

Chure D Britt B Whitlock J Wilson J 2010 First complete sauropod dinosaur skullfrom the Cretaceous of the Americas and the evolution of sauropod dentitionNaturwissenschaften 97379ndash391 DOI 101007s00114-010-0650-6

Csiki-Sava Z Buffetaut E Ősi A Pereda-Suberbiola X Brusatte SL 2015 Island lifein the Cretaceous - faunal composition biogeography evolution and extinctionof land-living vertebrates on the Late Cretaceous European archipelago ZooKeys4691ndash161 DOI 103897zookeys4698439

Dalla Vecchia FM 2002 Cretaceous dinosaurs in the AdriaticndashDinaric carbonate plat-form (Italy and Croatia) paleoenvironmental implications and paleogeographicalhypothesesMemorie della Societa Geologica Italiana 5789ndash100


Dalla Vecchia FM Cau A 2011 The first record of a notosuchian crocodyliform fromItaly Rivista Italiana di Paleontologia e Stratigrafia 117309ndash321

Dal Sasso C Pierangelini G Famiani F Cau A Nicosia U 2016 First sauropod bonesfrom Italy offer new insights on the radiation of Titanosauria between Africa andEurope Cretaceous Research 6488ndash109 DOI 101016jcretres201603008

De Broin F Grenot C Vernet R 1971 Sur la deacutecouverte drsquoun nouveau gisement deVerteacutebreacutes dans le Continental Intercalaire saharien la Gara Samani (Algeacuterie)Comptes Rendus de lrsquoAcademie des Sciences de Paris 2721219ndash1221

De Lapparent AF Gorce F 1960 The dinosaurs of the lsquolsquoContinental Intercalaire of thecentral SaharaMemoirs of the Geological Society of France 391ndash57

DrsquoEmicMDMannion PD Upchurch P Benson RBJ Pang Q Zhengwu C 2013Osteology of Huabeisaurus allocotus (Sauropoda Titanosauriformes) from the UpperCretaceous of China PLOS ONE 8e69375 DOI 101371journalpone0069375

Diacuteez Diacuteaz V Garcia G Pereda Suberbiola X Jentgen B Stein K Godefroit P ValentinX 2018 The ttitanosaurian dinosaur Atsinganosaurus velauciensis (Sauropoda)from the Upper Cretaceous of southern France new material Phylogenetic affinitiesand palaeobiogeographical implications Cretaceous Research 91429ndash456

Diacuteez Diacuteaz VD Mocho P Paacuteramo A Escaso F Marcos-Fernaacutendez F Sanz JLOrtega F 2016 A new titanosaur (Dinosauria Sauropoda) from the Up-per Cretaceous of Lo Hueco (Cuenca Spain) Cretaceous Research 6849ndash60DOI 101016jcretres201608001

Diacuteez Diacuteaz V Ortega F Sanz JL 2014 Titanosaurian teeth from the Upper Cretaceous ofLo Hueco (Cuenca Spain) Cretaceous Research 51285ndash291

Diacuteez Diacuteaz V Pereda Suberbiola X Sanz JL 2012 Juvenile and adult teeth of thetitanosaurian dinosaur Lirainosaurus (Sauropoda) from the Late Cretaceous ofIberia Geobios 45265ndash274DOI 101016jgeobios201110002

Diacuteez Diacuteaz V Tortosa T Le Loeuff J 2013 Sauropod diversity in the Late Cretaceousof southwestern Europe the lessons of odontology Annales de Paleontologie99119ndash129 DOI 101016jannpal201212002

Diacuteez Diacuteaz VD Garcia G Knoll F Suberbiola X Valentin X 2012 New cranial remainsof titanosaurian sauropod dinosaurs from the Late Cretaceous of Fox-Amphoux-Meacutetisson (Var SE France) Proceedings of the Geologistsrsquo Association 123626ndash637DOI 101016jpgeola201204002

Erickson GM 1996 Incremental lines of von Ebner in dinosaurs and the assess-ment of tooth replacement rates using growth line counts Proceedings of theNational Academy of Sciences of the United States of America 9314623ndash14627DOI 101073pnas932514623

Ezcurra MD Agnoliacuten FL 2011 A new global palaeobiogeographical model for the latemesozoic and early tertiary Systematic Biology 61553ndash566

Fanti F Cau A Cantelli L Hassine M Auditore M 2015 New information onTataouinea hannibalis from the Early Cretaceous of Tunisia and implications for the


tempo and mode of rebbachisaurid sauropod evolution PLOS ONE 10e0123475DOI 101371journalpone0123475

Fanti F Cau A Hassine M 2014 Evidence of titanosauriforms and rebbachisaurids(Dinosauria Sauropoda) from the Early Cretaceous of Tunisia Journal of AfricanEarth Sciences 901ndash8 DOI 101016jjafrearsci201310010

Fanti F Cau A Hassine M Contessi M 2013 A new sauropod dinosaur from theEarly Cretaceous of Tunisia with extreme avian-like pneumatization NatureCommunications 42080 DOI 101038ncomms3080

Fanti F Cau A Panzarin L Cantelli L 2016 Evidence of iguanodontian dinosaurs fromthe Lower Cretaceous of Tunisia Cretaceous Research 60267ndash274DOI 101016jcretres201512008

Fanti F Therrien F 2007 Theropod tooth assemblages from the Late CretaceousMaevarano Formation and the possible presence of dromaeosaurids in MadagascarActa Palaeontologica Polonica 52155ndash166

Fiorillo AR 1991 Dental microwear on the teeth of Camarasaurus and Diplodocusimplications for sauropod paleoecology In Fifth symposium on mesozoic terrestrialecosystems and biota Contributions from the Palaeontological Museum University ofOslo 24

Fiorillo AR 1998 Dental micro wear patterns of the sauropod dinosaurs Camarasaurusand Diplodocus evidence for resource partitioning in the Late Jurassic of NorthAmerica Historical Biology 131ndash16 DOI 10108008912969809386568

Forey PL Cavin L 2007 A new species of Cladocyclu s (Teleostei Ichthyodectiformes)from the Cenomanian of Morocco Palaeontologia Electronica 101ndash10

Forey PL Loacutepez-Arbarello A MacLeod N 2011 A new species of Lepidotes (Actinoptery-gii Semiontiformes) from the Cenomanian (Upper Cretaceous) of MoroccoPalaeontologia Electronica 141ndash12

Franca MA Juacutelio C de A Riff D Hsiou AS Langer MC 2016 New lower jaw and teethreferred toMaxakalisaurus topai (Titanosauria Aeolosaurini) and their implicationsfor the phylogeny of titanosaurid sauropods PeerJ 4e2054 DOI 107717peerj2054

Freire PC Medeiros MA Lindoso RM 2007 Sauropod teeth diversity in the Laje doCoringa fossiliferous site Eocenomanian of northeastern Brazil PaleontologiaCenarios de Vida 1523e532

Gallina PA Apesteguiacutea S Haluza A Canale JI 2014 A diplodocid sauropodsurvivor from the Early Cretaceous of South America PLOS ONE 9e97128DOI 101371journalpone0097128

Garciacutea RA 2013 A giant tooth from the Late Cretaceous (middle Campanian-lowerMaastrichtian) of Patagonia Argentina an enormous titanosaur or a large toothedtitanosaur Cretaceous Research 4182ndash85

Garcia G Amico S Fournier F Thouand E Valentin X 2010 A new titanosaur genus(Dinosauria Sauropoda) from the Late Cretaceous of southern France and its paleo-biogeographic implications Bulletin de la Societeacute Geacuteologique de France 181269ndash277DOI 102113gssgfbull1813269


Garciacutea RA Cerda IA 2010a Denticioacuten de titanosaurios (Dinosauria Sauropoda) delCretaacutecico Superior de la provincia de Riacuteo Negro Argentina morfologiacutea insercioacuten yreemplazo Ameghiniana 4745ndash60 DOI 105710AMGHv47i16

Garciacutea RA Cerda IA 2010b Dentition and histology in titanosaurian dinosaur embryosfrom Upper Cretaceous of Patagonia Argentina Palaeontology 53335ndash346DOI 101111j1475-4983201000937x

Gardner JD Evans SE Sigogneau-Russell D 2003 New albanerpetontid amphibiansfrom the Early Cretaceous of Morocco and Middle Jurassic of England ActaPalaeontologica Polonica 48301ndash319

Gheerbrant E Rage J-C 2006 Paleobiogeography of Africa how distinct from Gond-wana and Laurasia Palaeogeography Palaeoclimatology Palaeoecology 241224ndash246

Gomani EM 2005 Sauropod dinosaurs from the early Cretaceous of Malawi AfricaPalaeontologia Electronica 827A-37p

Hammer Oslash Harper DAT 2006 Paleontological data analysis Oxford BlackwellPublishing 351

Hammer Oslash Harper DAT Ryan PD 2001 Past paleontological statistics softwarepackage for education and data analysis Palaeontologia Electronica 41ndash9

Hendrickx C Mateus O 2016Morphofunctional analysis of the quadrate of Spinosauri-dae (Dinosauria Theropoda) and the first definitive evidence of two cohabitingspinosaurids in the Cenomanian of North Africa PLOS ONE

Hendrickx C Mateus O Arauacutejo R 2015 A proposed terminology of theropodteeth (Dinosauria Saurischia) Journal of Vertebrate Paleontology 35e982797DOI 101080027246342015982797

Holwerda FM Pol D Rauhut OWM 2015 Using dental enamel wrinkling to definesauropod tooth morphotypes from the Cantildeadoacuten Asfalto Formation PatagoniaArgentina PLOS ONE 10e0118100 DOI 101371journalpone0118100

IbrahimN Dal Sasso C Maganuco S Fabbri M Martill DM Gorscak E LamannaMA2016 Evidence of a derived titanosaurian (Dinosauria Sauropoda) in the lsquolsquoKem Kembeds of Morocco with comments on sauropod paleoecology in the Cretaceous ofAfrica Cretaceous period biotic diversity and biogeography New Mexico Museum ofNatural History amp Science 71149ndash159

IbrahimN Varricchio DJ Sereno PCWilson JA Dutheil DB Martill DM Baidder LZouhri S 2014 Dinosaur footprints and other ichnofauna from the Cretaceous KemKem Beds of Morocco PLOS ONE 9e90751 DOI 101371journalpone0090751

JanenschW 1935 Die Schaumldel der Sauropoden Brachiosaurus Barosaurus und Di-craeosaurus aus den Tendaguruschichten Deutsch-Ostafrikas PalaeontographicaSupplement 7145ndash298

Kellner A Campos D Azevedo S Trotta M Henriques D Craik M Silva H 2006 On anew titanosaur sauropod from the Bauru Group Late Cretaceous of Brazil Boletimdo Museu Nacional 741ndash31

Kellner AWMader BJ 1997 Archosaur teeth from the Cretaceous of Morocco Journalof Paleontology 71525ndash527 DOI 101017S0022336000039548


King T Andrews P Boz B 1999 Effect of taphonomic processes on dental microwearAmerican Journal of Physical Anthropology 108359ndash373

Kues BS Lehman T Rigby JK 1980 The teeth of Alamosaurus sanjuanensis a LateCretaceous sauropod Journal of Paleontology 54864ndash869

LamannaMC Gorscak E Diacuteez Diacuteaz V Schwarz D El-Dawoudi I 2017 Reassessmentof a partial titanosaurian sauropod dinosaur skeleton from the upper Cretaceous(Campanian) Quseir formation of the Kharga Oasis Egypt XV In Annual Meetingof the European Association of Vertebrate Palaeontologists Zitteliana 50

LamannaMC Hasegawa Y 2014 New titanosauriform sauropod dinosaur materialfrom the Cenomanian of Morocco implications for paleoecology and sauropoddiversity in the Late Cretaceous of north Africa Bulletin of Gunma Museum ofNatural History 181ndash9

Laumlng E Boudad L Maio L Samankassou E Tabouelle J Tong H Cavin L 2013Unbalanced food web in a Late Cretaceous dinosaur assemblage PalaeogeographyPalaeoclimatology Palaeoecology 381ndash38226ndash32 DOI 101016jpalaeo201304011

Lavocat R 1954 Reconnaissance geacuteologique dans les Hammadas des confins algeacutero-marocains du Sud Notes et Memoires du Service Geacuteologique du Maroc 1161ndash147

Le Loeuff J 1991 The Campano-Maastrichtian vertebrate faunas from southern Europeand their relationships with other faunas in the world palaeobiogeographicalimplications Cretaceous Research 1293ndash114 DOI 101016S0195-6671(05)80019-9

Le Loeuff J 1995 Ampelosaurus atacis (nov gen nov sp) a new titanosaurid (Di-nosauria Sauropoda) from the Late Cretaceous of the Upper Aude Valley (France)Comptes Rendus de lrsquoAcademie des Sciences-Serie II-Sciences de la Terre et des Planetes321693ndash700

Le Loeuff J 2005 Osteology of Ampelosaurus atacis (Titanosauria) from southernFrance In Tidwell V Carpenter K eds Thunder-Lizards The SauropodomorphDinosaurs Bloomington and Indianapolis Indiana University Press 115ndash137

Le Loeuff J Laumlng E Cavin L Buffetaut E 2012 Between Tendaguru and Bahariya onthe age of the Early Cretaceous dinosaur sites from the Continental Intercalaire andother African formations Journal of Stratigraphy 36e502

Lefranc JP Guiraud R 1990 The Continental Intercalaire of northwestern Sahara andits equivalents in the neighbouring regions Journal of African Earth Sciences (and theMiddle East) 1027ndash77 DOI 1010160899-5362(90)90047-I

Lim J-D Martin LD Baek K-S 2001 The first discovery of a brachiosaurid from theAsian continent Naturwissenschaften 8882ndash84 DOI 101007s001140000201

Mahler L 2005 Record of Abelisauridae (Dinosauria Theropoda) from the Cenomanianof Morocco Journal of Vertebrate Paleontology 25236ndash239DOI 1016710272-4634(2005)025[0236ROADTF]20CO2

Mannion PD 2009 A rebbachisaurid sauropod from the Lower Cretaceous of the Isle ofWight England Cretaceous Research 30521ndash526 DOI 101016jcretres200809005


Mannion PD 2011 A reassessment ofMongolosaurus haplodon Gilmore 1933 atitanosaurian sauropod dinosaur from the Early Cretaceous of Inner Mongo-lia Peoplersquos Republic of China Journal of Systematic Palaeontology 9355ndash378DOI 101080147720192010527379

Mannion PD Allain R Moine O 2017 The earliest known titanosauriform sauropod di-nosaur and the evolution of Brachiosauridae PeerJ 5e3217 DOI 107717peerj3217

Mannion PD Barrett PM 2013 Additions to the sauropod dinosaur fauna of the Ceno-manian (early Late Cretaceous) Kem Kem beds of Morocco palaeobiogeographicalimplications of the mid-Cretaceous African sauropod fossil record CretaceousResearch 4549ndash59 DOI 101016jcretres201307007

Mannion PD Upchurch P Hutt S 2011 New rebbachisaurid (Dinosauria Sauropoda)material from the Wessex Formation (Barremian Early Cretaceous) Isle of WightUnited Kingdom Cretaceous Research 32774ndash780 DOI 101016jcretres201105005

Martiacutenez RDF LamannaMC Novas FE Ridgely RC Casal GA Martiacutenez JE Vita JRWitmer LM 2016 A basal lithostrotian titanosaur (Dinosauria Sauropoda) witha complete skull implications for the evolution and paleobiology of TitanosauriaPLOS ONE 11e0151661 DOI 101371journalpone0151661

McGowan AJ Dyke GJ 2009 A surfeit of theropods in the Moroccan Late CretaceousComparing diversity estimates from field data and fossil shops Geology 37843ndash846DOI 101130G30188A1

Meister C Piuz A Cavin L Boudad L Bacchia F Ettachfini EM Benyoucef M2017 Late Cretaceous (Cenomanian-Turonian) ammonites from southernMorocco and south western Algeria Arabian Journal of Geosciences 101ndash46DOI 101007s12517-016-2714-1

Mocho P Royo-Torres R Malafaia E Escaso F Silva B Ortega F 2016 Turiasauria-liketeeth from the Upper Jurassic of the Lusitanian Basin Portugal Historical Biology28861ndash880 DOI 1010800891296320151049948

Novas FE Dalla Vecchia F Pais DF 2005 Theropod pedal unguals from the LateCretaceous (Cenomanian) of Morocco Africa Revista del Museo Argentino deCiencias Naturales 7167ndash175 DOI 1022179REVMACN7333

Oumlsi A Apesteguiacutea S Kowalewski M 2010 Non-avian theropod dinosaurs fromthe early Late Cretaceous of Central Europe Cretaceous Research 31304ndash320DOI 101016jcretres201001001

Oumlsi A Csiki-Sava Z Prondvai E 2017 A sauropod tooth from the Santonian of Hungaryand the European Late Cretaceous lsquoSauropod Hiatusrsquo Scientific Reports 73261DOI 101038s41598-017-03602-2

Pereda-Suberbiola X 2009 Biogeographical affinities of Late Cretaceous continentaltetrapods of Europe a review Bulletin de la Societeacute Geacuteologique de France 18057ndash71DOI 102113gssgfbull180157

Pereda-Suberbiola X Corral JC Astibia H Badiola A Bardet N Berreteaga ABuffetaut E Buscalioni AD Cappetta H Cavin L 2015 Late Cretaceous continentaland marine vertebrate assemblages of the Lantildeo Quarry (Basque-Cantabrian RegionIberian Peninsula) an update Journal of Iberian Geology 41101ndash124


Pereda Suberbiola X Torcida F Izquierdo LA Huerta P Montero D Peacuterez G 2003First rebbachisaurid dinosaur (Sauropoda Diplodocoidea) from the early Cretaceousof Spain paleobiogeographical implications Bulletin de la Societe Geologique deFrance 174471ndash479 DOI 1021131745471

Poropat SF Kear BP 2013 Photographic atlas and three-dimensional reconstructionof the holotype skull of Euhelopus zdanskyi with description of additional cranialelements PLOS ONE 8e79932 DOI 101371journalpone0079932

Rabi M Seboumlk N 2015 A revised Eurogondwana model Late Cretaceous notosuchiancrocodyliforms and other vertebrate taxa suggest the retention of episodic faunallinks between Europe and Gondwana during most of the Cretaceous GondwanaResearch 281197ndash1211 DOI 101016jgr201409015

Richter U Mudroch A Buckley LG 2013 Isolated theropod teeth from the KemKem Beds (Early Cenomanian) near Taouz Morocco Palaumlontologische Zeitschrift87291ndash309 DOI 101007s12542-012-0153-1

Rodrigues T Kellner AWMader BJ Russell DA 2011 New pterosaur specimens fromthe Kem Kem beds (Upper Cretaceous Cenomanian) of Morocco Rivista Italiana diPaleontologia e Stratigrafia 117149ndash160

Russell DA 1996 Isolated dinosaur bones from the Middle Cretaceous of the TafilaltMorocco Bulletin du Museum National drsquoHistoire Naturelle 4349ndash402

Saegusa H Tomida Y 2011 Titanosauriform teeth from the Cretaceous of Japan Anaisda Academia Brasileira de Ciencias 83247ndash265DOI 101590S0001-37652011000100014

Salgado L Calvo JO 1997 Evolution of titanosaurid sauropods II the cranial evidenceAmeghiniana 3433ndash48

Salgado L Garrido A Cocca SE Cocca JR 2004 Lower Cretaceous rebbachisauridsauropods from Cerro Aguada del Leoacuten (Lohan Cura Formation) Neuqueacuten Provincenorthwestern Patagonia Argentina Journal of Vertebrate Paleontology 24903ndash912

SallamHM Gorscak E OrsquoConnor PM El-Dawoudi IA El-Sayed S Saber S KoraMA Sertich JJ Seiffert ER LamannaMC 2018 New Egyptian sauropod revealsLate Cretaceous dinosaur dispersal between Europe and Africa Nature Ecology ampEvolution 2445ndash451

Samman T Powell GL Currie PJ Hills LV 2005Morphometry of the teeth of westernNorth American tyrannosaurids and its applicability to quantitative classificationActa Palaeontologica Polonica 50757

Sanz J Powell J Le Loeuff J Martinez R Pereda Suberbiola X 1999 Sauropod remainsfrom the Upper Cretaceous of Lantildeo (northcentral Spain) Titanosaur phylogeneticrelationships Estudios del Museo de Ciencias Naturales de Alava 14235ndash255

Sereno PC Beck AL Dutheil DB Larsson HC Lyon GHMoussa B Sadleir RW SidorCA Varricchio DJ Wilson GP 1999 Cretaceous sauropods from the Sahara andthe uneven rate of skeletal evolution among dinosaurs Science 2861342ndash1347DOI 101126science28654431342

Sereno PC Dutheil DB IarocheneM Larsson HCE Lyon GHMagwene PMSidor CA Varricchio DJ Wilson JA 1996 Predatory dinosaurs from the


Sahara and Late Cretaceous faunal differentiation Science 272986ndash991DOI 101126science2725264986

Sereno PCWilson JA 2005 Structure and evolution of a sauropod tooth battery InCurry Rogers K Wilson JA eds The sauropods evolution and paleobiology BerkeleyUniversity of California Press

Sereno PCWilson JAWitmer LMWhitlock JA Maga A Ide O Rowe TA2007 Structural extremes in a Cretaceous dinosaur PLOS ONE 2e1230DOI 101371journalpone0001230

Smith JB Dodson P 2003 A proposal for a standard terminology of anatomical notationand orientation in fossil vertebrate dentitions Journal of Vertebrate Paleontology231ndash12

Soler-Gijoacuten R Loacutepez-Martiacutenez N 1998 Sharks and rays (chondrichthyes) from theUpper Cretaceous red beds of the south-central Pyrenees (Lleida Spain) indicesof an India-Eurasia connection Palaeogeography Palaeoclimatology Palaeoecology1411ndash12 DOI 101016S0031-0182(98)00007-8

Sweetman SC Gardner JD 2013 A new albanerpetontid amphibian from the Barremian(Early Cretaceous) Wessex Formation of the Isle of Wight southern England ActaPalaeontologica Polonica 58(2)295ndash324

Torcida Fernaacutendez-Baldor F Canudo JI Huerta P Montero D Pereda SuberbiolaX 2011 Demandasaurus darwini a new rebbachisaurid sauropod from the EarlyCretaceous of the Iberian Peninsula Acta Palaeontologica Polonica 56535ndash552DOI 104202app20100003

Torcida Fernaacutendez-Baldor FT Canudo JI Huerta P Moreno-AzanzaMMonteroD 2017 Europatitan eastwoodi a new sauropod from the lower Cretaceous ofIberia in the initial radiation of somphospondylans in Laurasia PeerJ 5e3409DOI 107717peerj3409

Upchurch P 1995 The evolutionary history of sauropod dinosaurs PhilosophicalTransactions of the Royal Society of London Series B Biological Sciences 349365ndash390DOI 101098rstb19950125

Upchurch P 1998 The phylogenetic relationships of sauropod dinosaurs ZoologicalJournal of the Linnean Society 12443ndash103 DOI 101111j1096-36421998tb00569x

Upchurch P 2008 Gondwanan break-up legacies of a lost world Trends in Ecology ampEvolution 23229ndash236 DOI 101016jtree200711006

Upchurch P Barrett PM 2000 The evolution of sauropod feeding mechanisms In SuesH-D ed Evolution of herbivory in terrestrial vertebrates perspectives from the fossilrecord Cambridge Cambridge University Press 79ndash122

Upchurch P Barrett PM Dodson P 2004 Sauropoda In Weishampel DB Dodson POsmoacutelska H eds The Dinosauria Second edition Berkeley Dodson University ofCalifornia Press 259ndash322

Vila B Selleacutes AG Brusatte SL 2016 Diversity and faunal changes in the latest Cre-taceous dinosaur communities of southwestern Europe Cretaceous Research57552ndash564 DOI 101016jcretres201507003


Vullo R Neacuteraudeau D Allain R Cappetta H 2005 Un nouveau gisement agrave microrestesde verteacutebreacutes continentaux et littoraux dans le Ceacutenomanien infeacuterieur de Fouras(Charente-Maritime Sud-Ouest de la France) Comptes Rendus Palevol 495ndash107DOI 101016jcrpv200411006

Vullo R Neraudeau D Lenglet T 2007 Dinosaur teeth from the Cenomanian ofCharentes western France evidence for a mixed Laurasian-Gondwanan assemblageJournal of Vertebrate Paleontology 27931ndash943DOI 1016710272-4634(2007)27[931DTFTCO]20CO2

Wellnhofer P Buffetaut E 1999 Pterosaur remains from the Cretaceous of MoroccoPalaumlontologische Zeitschrift 73133ndash142 DOI 101007BF02987987

Wiersma K Sander PM 2016 The dentition of a well-preserved specimen of Cama-rasaurus sp implications for function tooth replacement soft part reconstructionand food intake PalZ 91(1)145ndash161 DOI 101007s12542-016-0332-6

Wilson JA 2002 Sauropod dinosaur phylogeny critique and cladistic analysis ZoologicalJournal of the Linnean Society 136215ndash275 DOI 101046j1096-3642200200029x

Wilson JA 2005 Redescription of the Mongolian sauropod Nemegtosaurus mon-goliensis Nowinski (Dinosauria Saurischia) and comments on Late Creta-ceous sauropod diversity Journal of Systematic Palaeontology 3283ndash318DOI 101017S1477201905001628

Wilson JA Allain R 2015 Osteology of Rebbachisaurus garasbae Lavocat 1954 adiplodocoid (Dinosauria Sauropoda) from the early Late Cretaceousndashaged KemKem beds of southeastern Morocco Journal of Vertebrate Paleontology 35e1000701DOI 1010800272463420141000701

Wilson JA Sereno PC 1998 Early evolution and higher-level phylogeny of sauropoddinosaurs Journal of Vertebrate Paleontology 181ndash79

Zaher H Pol D Carvalho AB Nascimento PM Riccomini C Larson P Juarez-ValieriR Pires-Domingues R Da Silva NJ De Almeida CD 2011 A complete skull of anEarly Cretaceous sauropod and the evolution of advanced titanosaurians PLOS ONE6e16663 DOI 101371journalpone0016663

Zarcone G Petti FM Cillari A Di Stefano P Guzzetta D Nicosia U 2010 A possiblebridge between Adria and Africa new palaeobiogeographic and stratigraphicconstraints on the Mesozoic palaeogeography of the Central Mediterranean areaEarth-Science Reviews 103154ndash162 DOI 101016jearscirev201009005


INTRODUCTIONThe early Late Cretaceous of northwestern Africa is well-known for its rich vertebratefauna many taxa having been described in particular from the AlbianndashCenomanian(sim113ndash939 Ma) Kem Kem beds of Morocco and the AlbianndashCenomanian equivalentcontinental intercalaire of Algeria The Moroccan Kem Kem beds include aquatic faunasuch as sharks lungfish coelacanths bony fish amphibians turtles crocodylomorphs aswell as terrestrial vertebrates such as squamates pterosaurs sauropods and an abundanceof theropods (Lavocat 1954 Russell 1996 Sereno et al 1996Wellnhofer amp Buffetaut 1999Cavin et al 2010 Richter Mudroch amp Buckley 2013 Laumlng et al 2013 Mannion amp Barrett2013) Despite this large diversity most fossil material consists of isolated elements fromtheropods and chondrichthyans (eg Spinosaurus Carcharodontosaurus OnchopristisLaumlng et al 2013 C Underwood pers comm 2018) Laumlng et al (2013) attributed thisto the deltaic palaeoenvironment being unsuitable for the setting of stable terrestrialvegetation Because of this the herbivorous fauna has not received much attention thusfar and sauropod material is rare (C Underwood pers comm 2018 but seeMcGowan ampDyke 2009) Studies of sauropod material from this region thus far found Rebbachisaurusgarasbae and other rebbachisaurids (Lavocat 1954 De Lapparent amp Gorce 1960 Russell1996 Mannion amp Barrett 2013 Wilson amp Allain 2015) as well as several titanosauriformremains and also a possible titanosaurian (De Broin Grenot amp Vernet 1971 Kellner ampMader 1997 Mannion amp Barrett 2013 Lamanna amp Hasegawa 2014 Ibrahim et al 2016)De Lapparent amp Gorce (1960) also mentioned brachiosaurid finds however these remainsare now considered to be rebacchisaurid or titanosauriform (Mannion 2009 Mannion ampBarrett 2013)

Sauropod body fossils are restricted to mostly isolated elements or if associatedmaterial is not as numerous as with theropod material (see egMahler 2005 Novas DallaVecchia amp Pais 2005 Cau amp Maganuco 2009) Sauropod teeth however are preservedin relative abundance One isolated sauropod tooth had already been reported on byKellner amp Mader (1997) Sauropod teeth are commonly preserved in the fossil record dueto their hardness resilience against weathering and due to their high tooth replacementrates (see eg Calvo 1994 Erickson 1996 Garciacutea amp Cerda 2010 Garciacutea amp Cerda 2010b)Studying isolated teeth has previously been applied to assessing theropod species diversity inNorth Africa (Richter Mudroch amp Buckley 2013) Sauropod teeth can be used for a similarpurpose as well as morphological classifications based on shape size and position of wearfacets (Calvo 1994 Salgado amp Calvo 1997 Chure et al 2010Mocho et al 2016 Carballidoet al 2017) and enamel wrinkling patterns (Carballido amp Pol 2010 Diacuteez Diacuteaz PeredaSuberbiola amp Sanz 2012Diacuteez Diacuteaz Tortosa amp Loeuff 2013Holwerda Pol amp Rauhut 2015)have classified tooth assemblages into morphotypes or even down to family or genus level(eg Amygdalodon Patagosaurus)

Mannion amp Barrett (2013) suggested that the Cretaceous North African titanosauriformsmay not be closely related to southern African forms as the lineages were cut off fromeach other by the trans-Saharan seaway Moreover close relations are suggested betweenCretaceous North African sauropods and Italian sauropods (Zarcone et al 2010 Dal






carbonate



sandstones

Cenomanian-

Turonian

Upper m

arly unitLow

er sandstone unit

Cenomanian-(A

lbian-Aptian)

D

Morocco

Algeria

Spain

Kem Kem


Lo Hueco


France

A

Erfoud

Taouz



Cenomanian

and teeth

C

A B










1cm

A B

C D

E F

G H













Specimennr

Apico-basallength

Abrasionstage

Mesio-distalbase

Mesio-distalmiddle

Mesio-distalapex

Labio-lingualbase

Labio-lingualmiddle

Labio-lingualapex

SI CI Abrasionstage




Enamelornamentation








Lemonshaped

Longitudinal ridges


Lemonshaped

















Lemonshaped

Smooth


Chevron-like

Holw


OI107717peerj5925

943





































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland





































































































































































carbonate



sandstones

Cenomanian-

Turonian

Upper m

arly unitLow

er sandstone unit

Cenomanian-(A

lbian-Aptian)

D

Morocco

Algeria

Spain

Kem Kem


Lo Hueco


France

A

Erfoud

Taouz



Cenomanian

and teeth

C

A B










1cm

A B

C D

E F

G H













Specimennr

Apico-basallength

Abrasionstage

Mesio-distalbase

Mesio-distalmiddle

Mesio-distalapex

Labio-lingualbase

Labio-lingualmiddle

Labio-lingualapex

SI CI Abrasionstage




Enamelornamentation








Lemonshaped

Longitudinal ridges


Lemonshaped

















Lemonshaped

Smooth


Chevron-like

Holw


OI107717peerj5925

943





































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland

































































































































































carbonate



sandstones

Cenomanian-

Turonian

Upper m

arly unitLow

er sandstone unit

Cenomanian-(A

lbian-Aptian)

D

Morocco

Algeria

Spain

Kem Kem


Lo Hueco


France

A

Erfoud

Taouz



Cenomanian

and teeth

C

A B










1cm

A B

C D

E F

G H













Specimennr

Apico-basallength

Abrasionstage

Mesio-distalbase

Mesio-distalmiddle

Mesio-distalapex

Labio-lingualbase

Labio-lingualmiddle

Labio-lingualapex

SI CI Abrasionstage




Enamelornamentation








Lemonshaped

Longitudinal ridges


Lemonshaped

















Lemonshaped

Smooth


Chevron-like

Holw


OI107717peerj5925

943





































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland






































































































































































1cm

A B

C D

E F

G H













Specimennr

Apico-basallength

Abrasionstage

Mesio-distalbase

Mesio-distalmiddle

Mesio-distalapex

Labio-lingualbase

Labio-lingualmiddle

Labio-lingualapex

SI CI Abrasionstage




Enamelornamentation








Lemonshaped

Longitudinal ridges


Lemonshaped

















Lemonshaped

Smooth


Chevron-like

Holw


OI107717peerj5925

943





































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland

































































































































































1cm

A B

C D

E F

G H













Specimennr

Apico-basallength

Abrasionstage

Mesio-distalbase

Mesio-distalmiddle

Mesio-distalapex

Labio-lingualbase

Labio-lingualmiddle

Labio-lingualapex

SI CI Abrasionstage




Enamelornamentation








Lemonshaped

Longitudinal ridges


Lemonshaped

















Lemonshaped

Smooth


Chevron-like

Holw


OI107717peerj5925

943





































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland









































































































































































Specimennr

Apico-basallength

Abrasionstage

Mesio-distalbase

Mesio-distalmiddle

Mesio-distalapex

Labio-lingualbase

Labio-lingualmiddle

Labio-lingualapex

SI CI Abrasionstage




Enamelornamentation








Lemonshaped

Longitudinal ridges


Lemonshaped

















Lemonshaped

Smooth


Chevron-like

Holw


OI107717peerj5925

943





































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland






































































































































































Specimennr

Apico-basallength

Abrasionstage

Mesio-distalbase

Mesio-distalmiddle

Mesio-distalapex

Labio-lingualbase

Labio-lingualmiddle

Labio-lingualapex

SI CI Abrasionstage




Enamelornamentation








Lemonshaped

Longitudinal ridges


Lemonshaped

















Lemonshaped

Smooth


Chevron-like

Holw


OI107717peerj5925

943





































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland


































































































































































Specimennr

Apico-basallength

Abrasionstage

Mesio-distalbase

Mesio-distalmiddle

Mesio-distalapex

Labio-lingualbase

Labio-lingualmiddle

Labio-lingualapex

SI CI Abrasionstage




Enamelornamentation








Lemonshaped

Longitudinal ridges


Lemonshaped

















Lemonshaped

Smooth


Chevron-like

Holw


OI107717peerj5925

943





































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland





































































































































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland

































































































































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland






























































































































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland























































































































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland















































































































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland










































































































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland



































































































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland



























































































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland



















































































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland













































































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland






































































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland

































































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland





























































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland


























































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland




















































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland















































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland










































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland







































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland



































































































































































Fox-AmphouxC-Morph

Fox AmphouxD-Morph

Liraino-saurus

LHMorph A

LHMorph B

Massecapstitanosaur

Patago-saurus




Maxakali-saurus

Baurutitanosaur

Morph_Id 03975 01917 02584 00383 0751 04729 03556 04127 00001 00002 00096 06408 00774 02623 00006 04152

Morph_IId 00228 00752 01809 08623 08758 01156 1 00008 00038 01131 08568 03702 00909 00087 0763




Lirainosaurusc 06662 02362 05032 00224 00374 01364 09338 04363 0374 005 05989

LoHueco Morph Ac 00932 07119 00015 00019 00366 09081 0321 00913 00079 06607

LoHueco Morph Bc 00707 0001 00024 0009 0189 00765 09515 0009 01212


Patagosaurusa 00233 00105 00021 00047 00002 0001 00061

Euhelopusb 01902 00051 00818 00002 0002 00128

Shiramine formb 01433 05639 00014 00086 01707

Astrodonb 03297 01885 00077 06527




Bauru titanosaurc


Holw


OI107717peerj5925

2843





















Switzerland





















































































































































































Switzerland

















































































































































































Switzerland












































































































































































Switzerland







































































































































































Switzerland












































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































Documents

Late Cretaceous sauropod tooth morphotypes may …Femke M. Holwerda1,2 3, Verónica Díez Díaz4 5, Alejandro Blanco2,6, Roel Montie1,2 3 and Jelle W.F. Reumer1 1 Faculty of Geosciences,