diversity and evolution of hunter−schreger band configuration in … · 2011-02-14 · mon...

Diversity and evolution of HunterminusSchreger Bandconfiguration in tooth enamel of perissodactyl mammals

WIGHART VON KOENIGSWALD LUKE T HOLBROOK and KENNETH D ROSE

Koenigswald W von Holbrook LT and Rose KD 2011 Diversity and evolution of HunterminusSchreger Band configuminusration in tooth enamel of perissodactyl mammals Acta Palaeontologica Polonica 56 (1) 11ndash32

Four different HunterminusSchreger Band (HSB) configurations were observed in the teeth of fossil and extant PerissodactylaThis variability exceeds that observed in Artiodactyla or Proboscidea The four HSB configurations represent two differentevolutionary pathways Transverse HSB found in many mammalian taxa outside the Perissodactyla represents the mostprimitive HSB configuration It occurs in several primitive perissodactyl families and is retained in Palaeotheriidae and exminustant Equidae Curved HSB evolved from transverse HSB and occurs in Tapiridae Helaletidae and Lophiodontidae as wellas in Ancylopoda and Titanotheriomorpha This likely indicates independent evolution of curved HSB in two or more linminuseages but the number of instances of parallelism of this configuration is obscured by uncertainty in the relationships amongthese taxa and by a lack of data for some important basal taxa A second evolutionary pathway leads from transverse HSBvia compound HSB to vertical HSB Compound HSB were detected in Hyrachyidae Deperetellidae and the earlyrhinocerotid Uintaceras Vertical HSB configuration characterizes the molar dentition of other Rhinocerotidae Hyraminuscodontidae Indricotheriidae and Amynodontidae Often the incisors of rhinocerotids retain traces of compound HSB Thusthe HSB configuration reflects phylogenetic relationships to some degree The selective value of the modified HSB configuminusrations is interpreted functionally as a mechanism to reduce abrasion during mastication assuming that the perpendicular inminustersection of prisms with the actual grinding surfaces resists wear better than prisms running parallel to the occlusal surface

Key words Mammalia Perissodactyla HunterminusSchreger Bands HSB tooth enamel microstructure functional adaptaminustion phylogeny

Wighart von Koenigswald [Koenigswalduniminusbonnde] Steinmann Institut (Paleontology) University of Bonn Nussminusallee 8 Dminus53115 Bonn GermanyLuke T Holbrook [holbrookrowanedu] Department of Biological Sciences Rowan University Glassboro NJ 08028 USAKenneth D Rose [kdrose jhmiedu] Center for Functional Anatomy and Evolution Johns Hopkins University Schoolof Medicine Baltimore MD 21205 USA

Received 18 February 2010 accepted 23 June 2010 available online 24 June 2010

IntroductionThe shiny enamel of mammalian teeth is the hardest and mostresistant material mammals can produce The functional qualminusity of the enamel is determined by the hardness of the materialand by its internal structure The decussating layers of prismsserve as a crack stopping mechanism (Pfretzschner 1988) Alminusthough the internal structures are of functional significancethey are genetically controlled since the tooth is formed in thecrypt where no mechanical forces are active Despite the comminusmon occurrence of parallel and convergent evolution variaminustion in enamel microstructure may still provide insights intothe phylogeny of particular groups of mammals such asperissodactyls (Koenigswald 2004)

Most internal structures in the enamel are only visible usminusing high magnification The HunterminusSchreger Bands we disminuscuss here for perissodactyls are visible under low magnificaminustion as light and dark bands They were originally figured byHunter (1778) and Schreger (1800) for humans and bovidstwo centuries ago and accordingly are named HunterminusSchreminus

ger Bands (HSB) These bands occur in the enamel of mostlarge mammals (Koenigswald et al 1987)

The configuration of the HSB in perissodactyls shows anunusual extent of variation compared to other mammalianorders though there is general consistency within perissominusdactyl clades HSB are oriented vertically in rhinos (Rensminusberger and Koenigswald 1980 Fortelius 1984 Boyde andFortelius 1986) a phenomenon originally observed and deminusscribed in some detail by Quenstedt (1852) He illustrated thevertically oriented bands in molars of rhinoceroses (Fig 1)The specific HSB configuration of chalicotheres and brontominustheres was described as Uminusshaped (Koenigswald 1994) Asshown below different configurations occur in other perissominusdactyl clades In this paper we concentrate on two aspects ofHSB the phylogenetic significance and the functional valueof reoriented HSB

The complex structure of the enamel can be studied on varminusious levels (Koenigswald and Clemens 1992) The schmelzminusmuster describes the occurrence of different enamel typeswithin a tooth In this study we concentrated on one aspect of

doi104202app20100021Acta Palaeontol Pol 56 (1) 11ndash32 2011

the schmelzmuster namely the configuration of HSB (as deminusfined in the next section) and we surveyed the variability ofthis character in a wide diversity of perissodactyls We fominuscused on cheek teeth (molars and premolars) because theseare best represented for the greatest number of taxa but wealso made observations on the anterior dentition (incisors andcanines) whenever possible since the schmelzmuster may difminusfer in the various teeth at the dentition level We then usedthese observations to make inferences regarding the evolutionof HSB configurations in perissodactyls

Institutional abbreviationsmdashAMNH American Museum ofNatural History Department of Paleontology New YorkNew York BSPG Bayerische Staatsammlung fuumlr Palaumlontominuslogie und Geologie Muumlnchen Germany CM Carnegie Muminusseum Section of Vertebrate Paleontology Pittsburgh Pennminussylvania GMH Geiseltalmuseum Halle Germany HHZMZoologisches Museum der Universitaumlt Hamburg GermanyHLMD Hessisches Landesmuseum Darmstadt GermanyKOE Koenigswald enamel collection of the STIPB BonnGermany MB Museum fuumlr Naturkunde Berlin GermanyMCZ Museum of Comparative Zoology Harvard UniversityCambridge Massachusetts MR Michael Rummel collectionNaturminusMuseum Augsburg Germany NHMB Naturhistoriminussches Museum Basel Switzerland NHMW Naturhistoriminussches Museum Wien Austria PMM Palaeontological Muminusseum Moscow Russia SDSM South Dakota School ofMines Museum of Geology Rapid City South DakotaSTIPB Steinmann Institut Paleontology University of BonnGermany UM University of Michigan Museum of Paleontolminusogy Ann Arbor Michigan USGS United States GeologicalSurvey Denver Colorado specimens now housed at USNMUSNM National Museum of Natural History SmithsonianInstitution Department of Paleobiology Washington DCZFMK Zoologisches Museum Alexander Koenig BonnGermany ZSTUuml Zoologische Sammlung Universitaumlt Tuumlbinminusgen Germany

Other abbreviationsmdashBr Bridgerian EDJ enamelminusdentinejunction HSB HunterminusSchreger bands if interface betweenfields of HSB OES extend almost to the outer enamel surminusface SEM Scanning Electron Microscope Wa WasatchianIncisors canines premolars and molars are designated as IC P M for uppers i c p m for lowers

The nature of HunterminusSchregerBandsHunterminusSchreger Bands are an optical phenomenon producedby refraction of light due to the internal structure of theenamel The term HSB is not only used for this phenomenonbut is traditionally also used for the underlying structureformed by layers of decussating prisms In the terminology reminuslated to enamel structures we follow Koenigswald and Sander(1997b) Enamel is a highly mineralized material Several

structural levels must be differentiated to understand the pheminusnomenon of HSB The mineral hydroxyapatite forms very thincrystallites that are organized into rods called enamelldquoprismsrdquo although these structures are not prisms in the minminuseralogical sense These prisms have a diameter on the order of5 μm Many studies have been devoted to the changing shapeof the crossminussection of the enamel prisms (eg Shobusawa1952 Boyde 1965 Boyde and Martin 1984 Wood and Stern1997) The enamel prisms start at the enamelminusdentine junction(EDJ) and extend almost to the outer enamel surface (OES)They are normally arranged in groups with the same prism oriminusentation or in a very symmetrical arrangement Occasionallythe orientation of the prisms is irregular eg in proboscideans(Koenigswald 1997a Tabuce et al 2007 Ferretti 2008) Theorientation of the prisms defines the various enamel types(Koenigswald and Sander 1997a 1997b) The enamel cap ofa tooth may be formed by two or three different enamel typesThese can be arranged in layers within the thickness of theenamel band or occur in specific areas of the teeth Thearrangement of enamel types in a tooth was defined asschmelzmuster (Koenigswald 1980) The different tooth famiminuslies within the same dentition may show differences in theschmelzmuster (Koenigswald and Clemens 1992)

The visual phenomenon of HSB (Fig 2) is caused by theoptical properties of the crystallites within the prisms Thiseffect would hardly be visible in single crystallites but it ismagnified when crystallites are packed in prisms and it isstrongly increased when bodies of prisms are oriented in parminusallel If the direction of the light coincides more or less withthe long axis of the prisms it will disappear in the depth of theenamel Thus the crossminussection appears dark Light fallingperpendicular or at an angle to the prisms is reflected andthus the prisms appear bright Thus prisms effectively act inthe same manner as fiber optic light guides

The enamel type defined as HSB is formed by layers ofenamel prisms which decussate at a high anglemdashoften about90mdashwith the prisms of the adjacent layer The generalbiomechanical function of the layers of decussating prisms isto serve as an important crackminusstopping mechanism compaminus

12 ACTA PALAEONTOLOGICA POLONICA 56 (1) 2011

Fig 1 Vertical HSB configuration as figured by Quenstedt (1852 pl 2 1 [A]pl 3 35 [B]) A Occlusial view with HBS in the extoloph B Orienationand bifiurcation of the HSB in tangential aspect

rable to plywood structure (Koenigswald and Pfretzschner1987 Koenigswald et al 1993 Pfretzschner 1988 1994)

The light or dark appearance of the bands depends onwhere the light source is situated If this is changed fromone side to the other light bands become dark and viceversa (Fig 2A C) The thickness of these bands varies andis traditionally measured in the number of prisms per bandIn rodent incisors the bands may be only one prism thick(Korvenkontio 1934) In most mammals with HSB thickminusness is about 6 to 15 prisms with larger mammals tending tohave thicker HSB (Kawai 1955) In the vertical HSB of

Coelodonta antiquitatis we counted 11 to 13 prisms perband

The optical effectmdashthe light and dark bandingmdashis mostobvious when the angle between prisms of adjacent bands islarge and when the bands are thick and can be observed unminusder low magnification Quenstedt (1852) observed and figminusured vertical HSB in rhinocerotid molars using low magniminusfication He even correctly observed that these bands bifurminuscate and that intermediate layers occur between the lightand dark bands These layers are formed by prisms changminusing from one band to the next by a more or less sharp turn

doi104202app20100021

KOENIGSWALD ET ALmdashHUNTERminusSCHREGER BAND IN PERISSODACTYLS 13

05

mm

ED

JE

DJ

ED

JE

DJ

ED

JE

DJ

Fig 2 Appearance of the HSB in variable light A Scheme of the fiber optic light guide effect of enamel prisms Those prisms illuminated perpendicular tothe long axis reflect brightly while those illuminated parallel to the long axis appear dark B Transverse HSB illuminated from the left side in an incisor ofthe artiodactyl Myotragus Note the regular bifurcation of the light bands to the left of the dark bands to the right CndashE Vertical HSB in an etched groundsection of a molar of Coelodonta antiquitatis (Blumenbach 1799) (Upper Pleistocene Germany KOE 59) illuminated from different sides Light source onthe left (C) light source on the right (D) light source perpendicular to the direction of the bands (E) highlighting the transitional zones White dotted linesconnect identical spots

(Rensberger and Koenigswald 1980) Under proper illumiminusnation this narrow transitional zone of turning prisms beminustween two bands is visible as a thin reflecting line betweenthe vertical bands (Fig 2B)

The different prism orientation in HSB might cause differminusential wear resulting in a structure defined here as crossminusridgesin the occlusal surface of the enamel band They are most obminusvious in vertical HSB as in rhinocerotids where they can oftenbe felt when running a fingernail (Fig 3) along the enamelband Crossminusridges are not restricted to vertical HSB they mayoccur wherever the HSB intersect the occlusal surfaces of theenamel band On an oblique portion of the enamel band eventransverse HSB might create crossminusridges Therefore crossminusridges are not unequivocal evidence of vertical HSB

HunterminusSchreger Bands have another important featurethat differentiates them from other structural elements TheHSB bifurcate in a regular fashion as was figured by Quenminusstedt (1852 table 3) One group of bands (such as the lightones) always bifurcates to one side while the other (the darkones) bifurcates in the other direction If the light comes fromthe other side the optical effect is reversed (Fig 2B) This regminusular bifurcation of the HSB is related to the primary directionof prisms from the EDJ towards the OES (Koenigswald andPfretzschner 1987 fig 14)

We introduce the term ldquoconfiguration of HSBrdquo to refer tothe course of HSB (as it intersects the OES or a tangentialplane parallel to the EDJ) when viewed through the side of atooth (buccal lingual mesial or distal) This describes theorientation of HSB in relation to the growing direction of thetooth as seen from the outside or from tangential sectionsThe configuration often can be studied directly from the outminusside but the layer of HSB is sometimes overlain by a thicklayer of a different enamel type (such as radial enamel) thatobscures the HSB In such cases a tangential section throughthe enamel (ie a section parallel to the OES and EDJ) passminusing through the layer with HSB is required to see the HSB

configuration Specific types of configuration are describedbelow Configuration does not refer to the fact that HSB canrun relatively straight or can be wavy in appearance nor doesit describe the angle of inclination defined by Korvenkontio(1934) which relates to the angle that the plane of the HSBforms with the EDJ in vertical sections

Based on external observation and examination of tanminusgential sections we found four different configurations ofHSB (Fig 4)

Transverse HSB (Figs 4 5)mdashThe HSB are generally parminusallel to the occlusal surface and the base of the enamel crownThis is essentially horizontal in premolars and molars TheHSB often undulate or show other minor differentiations butotherwise remain transverse When the worn occlusal surminusface cuts obliquely through the enamel these HSB intersectthe enamel band

Curved HSB (Fig 4 see also Figs 5ndash7 11)mdashIn severalgroups the basically transverse HSB curve toward the occlusalsurface of the enamel band and thus intersect the shearingblades at a large angle The curved HSB configuration isstrictly related to specific areas of the tooth morphology and isalways combined with transverse HSB in other parts of theteeth Where HSB curve from different directions (what we reminusfer to here as different ldquofields of HSBrdquo) they may meet at acharacteristic interface The interface may be indicated by adistinct groove on the OES These curved HSB occur mostly inprominent crests such as wellminusdeveloped ectolophs and crossminuslophs in upper and lower cheek teeth Koenigswald (1994) deminusscribed the most strongly curved HSB in chalicotheres andbrontotheres and referred to them as Uminusshaped HSB Fortelius(1985) mentioned curved HSB in several groups as ldquohorizontal(concave)rdquo HSB but did not describe them in detail

Compound HSB (Fig 4 see also Fig 8)mdashWe found a speminuscific type of HSB configuration with transverse HSB as aninner zone and vertical HSB in an outer zone The occurrenceof vertical HSB may be related to enamel thickness but not tospecific areas in the tooth morphology The relative thickminusness of the inner and outer zones may differ and this in turnaffects how easily one can detect the corresponding HSB

Vertical HSB (Fig 4 see also Fig 9)mdashIn this configurationHSB are vertically oriented and are more or less straightrather than wavy or curving on all sides of the tooth from the


1 mm1 mm

Fig 3 Typical crossminusridges on the occlusal surface of the enamel bandcaused by vertical HSB in a lower molar of Rhinoceros sondaicus Desminusmarest 1822 (KOE 71) Pleistocene Saniran Java The vertical HSB arehere superimposed by thick radial enamel

transverse HSB curved HSB vertical HSBcompound HSB

Fig 4 Schematic illustration of the four configurations of HunterminusSchregerBands (HSB) found in Perissodactyla A Transverse HSB configurationB Curved HSB configuration with interface C Compound HSB configuminusration with transverse HSB in an inner layer and vertical HSB in an outerlayer D Vertical HSB configuration

basal cingulum (where present) up to the occlusal surfaceThe occurrence of vertical HSB is not related to the toothmorphology Like transverse HSB they exhibit unidirecminustional bifurcation Since the HSB do not converge no interminusfaces are present as are found regularly in the curved HSBconfiguration Crossminusridges caused by the intersection of theHSB with the occlusal surface are very characteristic

The configuration of the HSB may differ among the difminusferent tooth categories within the dentition especially whendentitions are heterodont (Koenigswald and Clemens 1992)Thus incisors and canines may show a different HSB configminusuration than premolars and molars Our survey shows thatthe presence or absence of differences between incisors andmolars makes the characterization of different groups easier

Methods of investigationAppendix 1 lists the specimens investigated for this studyThe specimens studied were selected to represent a widespectrum of perissodactyl diversity emphasizing the earliestmembers of the order and sampling the various lineages Inaddition several phenacodontid condylarths were examinedas an outgroup

Derived mammalian enamel is often composed of two orthree different enamel types forming separate superimposedlayers parallel to the EDJ (Koenigswald and Clemens 1992)The threeminusdimensional prism orientation is studied best fromvarious oriented sections under the scanning electron microminusscope (SEM) The sections are polished and etched followingprocedures outlined by Koenigswald (2004) The configuraminustion of HSB can be studied under the binocular microscopeunder low magnification and often sections are not necesminussary Thus specimens do not need to be sacrificed Most taxastudied here were examined in this way However if thelayer with HSB is covered by another enamel type or theenamel is not translucent nonminusdestructive methods may not

be adequate for revealing HSB configuration In such caseswhenever possible sections were made These sections wereoriented tangentiallymdashthat is parallel to the EDJ and theOES Small teeth such as those of several early perissominusdactyls had to be sectioned as well since the HSB are moredifficult to identify in uneven and small areas

HSB close to the OES can be investigated using the deminusscribed fiber optic light guide effect of the prism layers Oneof the various techniques is to hold the tooth in one hand withthe enamel surface in focus under the binocular lens withvarying magnification The light source is held in the otherhand It is best to direct the narrow opening of a light tube of afiber optic lamp from one side immediately beside the enaminusmel The light should be applied tangentially to a corner orfracture of the enamel Most of the light should penetrate intothe enamel tangentially HSB show their light and dark patminustern when the light falls at a very low angle onto the crossminussection of the enamel band It takes practice to turn the speciminusmen until the best view is available It is not easy howeverto document the results photographically

A magnification of 10 to 20 times is most effective In relminusatively clear enamel the bands may become visible at slightcracks within the enamel There is no single way to make theHSB visible due to the modification of the enamel duringfossil diagenesis but with experience and persistence the oriminusentation of HSB usually can be identified

All tooth surfaces were studied in order to follow HSBthroughout the enamel HSB are best seen when they areclose to the outer enamel surface Transverse HSB often runparallel to the perikymata superficial ridges on the OES thatusually develop perpendicular to the growth axis and whichare related to time intervals of enamel formation In contrastto perikymata HSB of all configurations show very distinctunidirectional bifurcations (Koenigswald and Pfretzschner1987) In rhinos where HSB are vertical the two structuresmay form a grid pattern (Koenigswald 2002)

doi104202app20100021


1 mm

HSB

1 mm

HSB

HSB

perikymata

paracone

Fig 5 Transverse HSB configuration in Equoidea A Lower molar of Mesohippus sp (KOE 1509) late Eocenendashearly Oligocene Toadstool Park areaNebraska USA The transverse HSB are to be seen in the tangential section Note also the transversely oriented perikymata on the outer enamel surfaceBoth structures are independent from each other B Upper molar of Palaeotherium sp (KOE 4050) upper Eocene Frohnstetten Germany transverse HSBvisible in the translucent enamel of the paracone from the outside

ObservationsOur observations are arranged using the classification seminusquence given in Rose (2006) with the following exceptionsLophiodontidae are placed after Tapiroidea based on the reminussults of Holbrook (2009) that called into question a relationminusship with chalicotheres Similarly Deperetellidae are placedwith rhinocerotoids because of the similarities of deperetellidschmelzmuster to that of Hyrachyus We include Colodonwithin Tapiridae following Colbert (2005) The results ofour observations are summarized in the next section in theconclusions

PhenacodontidaemdashOnly transverse HSB were observed incheek teeth of Phenacodus Ectocion and Meniscotherium asnoted earlier for Tetraclaenodon (Koenigswald et al 1987)Transverse HSB were observed in incisors of Meniscotheriumand canines of Meniscotherium and Phenacodus

EquidaemdashPfretzschner (1994) observed transverse HSBoverlain by radial enamel in molars of Hyracotherium andPalaeotherium Our own observations on various incisorspremolars and molars of Hyracotherium (sensu lato) confirmthis orientation but HSB are partially developed only weaklyIn Mesohippus all investigated teeth show only transverseHSB (Fig 5A) The outer layer of radial enamel presumablyhas been lost Prominent perikymata may hide the HSB butthe refraction on cracks confirms the transverse orientation InHippotherium and Equus the transverse orientation of theHSB was confirmed

In addition to the predominant transverse orientation ofthe HSB some genera eg Anchitherium aurelianense

present a specific convex bending in upper molars (Fortelius1985) In the ectoloph HSB bend downwards from the tips ofparacone and metacone to the parastyle and mesostyle butdo not form distinct interfaces By this bending the HSB arealmost parallel to the oblique shearing bladesmdashin contrast tothe curved HSB in brontotheres or chalicotheres We regardthis as a variation of the transverse HSB as Fortelius (1985)used the classification ldquohorizontal (convex)rdquo Thus all studminusied members of the Equidae share a similar transverse orienminustation of the HSB regardless of whether they are hypsodontor brachydont It occurs in upper and lower incisors as wellas premolars and molars

PalaeotheriidaemdashThe Eocene Propalaeotherium from theGeiseltal and Palaeotherium from Frohnstetten Germanyshow wellminusdeveloped transverse HSB in molars (Fig 5B)premolars partially combined with radial enamel In caninesand incisors HSB are dominantly transverse but we observedin one upper incisor a slight upward curvature at the lateralmargin so that the HSB intersect the occlusal edge obliquelyIn the pronounced ridge of the mesostyle and parastyle theHSB are slightly curved downwards Fortelius (1985) listedthe HSB of palaeotheres as ldquohorizontal (concave)rdquo as he didfor brontotheres and chalicotheres We did not observe a simminusilar curvature in palaeotheres as in the other two groupswhich we classified as curved HSB because of the distinct inminusterface

IsectolophidaemdashHomogalax protapirinus was difficult toinvestigate externally because most of the material availablewas very dark Thus the enamel of lower molars had to besectioned tangentially From these sections it is clear that the


A B1 mm 1 mm

if

Fig 6 Curved HSB configuration in Heptodon calciculus Cope 1880 (KOE 4035 4036) early Eocene Willwood Formation Bighorn Basin WyomingUSA A Tangential section of the posterior loph of a lower molar with two fields of curved HSB with the typical interface B Tangential section of theprotoconid of a lower molar with the transverse HSB Abbreviation if interface between fields of HSB

HSB are transversely oriented on the lingual and buccalsides The crossminuslophs of the lower molars were studied withspecial emphasis No deviation from the transverse orientaminustion could be identified in any of the several sections Lowerincisors and canines also exhibit transverse HSB

Lower molars of Cardiolophus showed transverse HSBSpecimens of Isectolophus annectens have molars withtransverse HSB that do not appear to exhibit the curvedHSB

HelaletidaemdashThe lower molars of Heptodon calciculusshow curved HSB The HSB are more transverse on the linminusgual and buccal sides of the cusps In the crossminuslophs the HSBrise diagonally towards the cutting edge forming a clear interminusface in the middle of the loph This is the typical curved HSBconfiguration as defined above and was corroborated in a tanminusgential section (Fig 6) North American specimens of Helaminusletes exhibit the same curved HSB Dashzeveg and Hooker(1997) erected the genus Irdinolophus for specimens previminusously referred to Helaletes mongoliensis and they assignedanother Mongolian species Helaletes fissus to the genusDesmatotherium They considered Irdinolophus to be closelyrelated to deperetellids but we include it here in our discussionof helaletids because its HSB configuration is more similar tothat of helaletids than that of deperetellids Fortelius (1985)listed ldquohorizontal (concave)rdquo HSB for Helaletidae

Lower molars of Selenaletes scopaeus which was origiminusnally placed in Helaletidae by Radinsky (1966) have onlytransverse HSB and do not exhibit the curved HSB Thereforethe placement of this genus in Helaletidae may be questioned

Lophialetidae and other endemic Asian ldquotapiroidsrdquo (exminuscept Deperetellidae)mdashLophialetids (including LophialetesSchlosseria and Breviodon) all exhibit transverse HSB intheir cheek teeth without any of the curving toward the occluminussal surface that is characteristic of the tapiroid condition Thisis also true of Rhodopagus and Pataecops two genera ofAsian Eocene ldquotapiroidsrdquo of uncertain affinity

TapiridaemdashExtant and Pleistocene Tapirus were studiedfrom complete and partial dentitions In the lower molars thebuccal and lingual sides are characterized by curved HSBwhich start as transverse on the cusps but curve upward in thecrossminuslophs from both lingual and buccal sides to meet thecutting surface almost vertically (Fig 7A) Since the HSB ofboth fields curve in different directions an interface betweenthese two fields is present in the middle of the loph The samestructure is found on the mesial as well as on the distal side ofthe loph In molars where the loph is heavily worn this interminusface is less obvious In upper molars the ectoloph also showscurved HSB with an interface just mesial to the point wherethe ectoloph meets the metacone The curved HSB are mostevident closer to the occlusal edge and the HSB are transminusverse near the root Thus wear may obscure the curved HSBon the ectoloph giving the appearance of only transverseHSB Upper and lower incisors and canines show transverseHSB only In the upper molars the ectoloph and buccal sides

of protocone and metacone show transverse HSB In thecrossminuslophs the HSB curve upwards from the buccal side Inthe protoloph they cover the entire loph until it meets theectoloph In the metaloph the curved HSB do not extend asfar to the ectoloph and meet the transverse HSB in theectoloph before both lophs join but there is no distinct interminusface between the two fields Incisors and canines show domiminusnantly transverse HSB as do p2 and p3 In unworn incisorshowever curved HSB were evident at the occlusal tip

In Colodon occidentalis the curved configuration is welldeveloped in the lower molars The p2 does not show twolophs like the other molariform premolars Nevertheless aslight indication of the curved configuration was seen at thedistal wall of the trigonid Upper molars of Colodon exhibitcurved HSB on both the cross lophs and the ectoloph with adistinct interface present on the ectoloph In Colodon cinguminuslatum the incisors have transverse or slightly curved HSBMolars of Haagella peregrina show very typical curvedHSB with an interface in the crossminuslophs of lower molars andoneminussided curved HSB in the upper molars

The curved configuration is also present in molars ofTapiravus from the upper Eocene and in lower molars andpremolars of Protapirus from the lower Oligocene

LophiodontidaemdashAll studied species of Lophiodon showthe typical configuration of curved HSB in the molar lophs(Fig 7B) In the buccal and lingual sides of the lower premolminusars and molars the HSB are transverse but in the lophs thebands curve upward at the ends forming an interface beminustween the fields of HSB from both sides In the cutting edgesof the lophs the crossminusridges are often visible In the uppermolars the ectoloph shows transverse HSB at the base and

doi104202app20100021


2 mmif

if

Fig 7 Curved HSB configuration with the typical interface in the transverselophs of lower molars in of tapirs A Tapirus sinensis Owen 1870 (MB Ma33219) Pleistocene Junnan China B Lophiodon remensis Lemoine 1878(KOE 4052) middle Eocene Geiseltal Germany Abbreviation if interfacebetween fields of HSB

slightly curved HSB in the upper part There an interface wasfound between paracone and metacone In the lophs thetransverse HSB from the buccal side of the protocone andmetacone bend upwards into the lophs to intersect the cuttingedge where they occur as crossminusridges The field of curvedHSB reaches almost to the ectoloph In the thick part of theenamel especially in Lophiodon rhinocerodes vertical eleminusments originating from zigzag HSB were observed Thus thetransverse HSB partly are transitional to a compound HSBconfiguration Lophiodontids are listed by Fortelius (1985)as having ldquohorizontal (concave)rdquo HSB

In incisors and canines the HSB are oriented transminusversely This is visible although the enamel has a rough surminusface texture

HyrachyidaemdashHyrachyus is characterized by the newlyrecognized compound HSB configuration in all tooth posiminustions (Fig 8) A superficial investigation of the outer surfaceof molar enamel indicated that European Hyrachyus miniminusmus and North American H eximius and H modestus havevertical HSB The vertical HSB are seen in all sides andlophs of the upper and lower molars On the occlusal surfaceof the enamel band even the crossminusridges formed by the interminussecting vertical HSB are visible However a more detailedinvestigation showed that these vertical HSB are only presminusent in an outer layer whereas transverse HSB form an innerlayer This combination was corroborated by a series of secminus

tions made parallel to the OES in molar teeth of HyrachyusIt is difficult to observe this condition with low magnificationand a light source because the inner and outer layers canvary in thickness to a degree that one layer may be easily obminusserved but not the other Compound configuration was alsoobserved in incisors and canines of Hyrachyus with the verminustical component appearing most strongly Consequently ourobservations do not confirm the classification of Fortelius(1985) as ldquohorizontal (concave)rdquo HSB

DeperetellidaemdashDeperetella was listed as having verticalHSB by Fortelius (1985) As reported by Holbrook (2007)specimens of Deperetella and Teleolophus exhibit crossminusridges on the occlusal surface of the enamel band that arecharacteristic of rhinocerotoids and their vertical HSBCloser examination of AMNH specimens of Deperetella andTeleolophus confirm the presence of vertical HSB but aspart of the compound HSB configuration Cheek teeth inthese specimens clearly possess vertical HSB but there alsois evidence of horizontal HSB deep to the vertical layer asobserved in Hyrachyus The horizontal component is mostevident in specimens of Teleolophus and in the enamel closminusest to the root Thus cheek teeth of both genera are characterminusized by the compound HSB configuration

HyracodontidaemdashHyracodon nebraskensis was represenminusted by all tooth positions The vertical HSB are present in theectoloph as well as in the buccal side of the protocone and the


CA B

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oute

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laye

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iddl

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r la

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1 m

m1

mm

Fig 8 Compound HSB configuration in Hyrachyus minimus (Fischer 1829) (KOE 4050) middle Eocene Geiseltal Germany Tangential section of theprotoconid of a lower molar in three sequential levels A Outer layer with vertical HSB B Middle level with a transitional orientation of the HSB C Innerlayer with transverse HSB

metacone (Fig 9A) The HSB tend to continue to the outersurface There vertical ridges are visible which correlate withthe HSB In some areasmdashespecially on the buccal sidemdashthese ridges in the outer surface are crossed by transverseperikymata Special care was taken to examine incisors andcanines available from a juvenile mandible vertical HSBshowing the typical bifurcations were found in all tooth posiminustions The same is true for all tooth positions of the genusArdynia from Mongolia

In Eggysodon from the Oligocene of Germany and Switminuszerland the molars show vertical HSB butmdashin contrast toHyracodonmdashin the lower incisor only transverse HSB were

detected Triplopus proficiens exhibits vertical HSB in themolars other teeth could not be assessed Cheek teeth asminussigned to Epitriplopus uintensis as well as a specimen asminussigned to Triplopus sp (CM 11955) exhibit the combinationof transverse and vertical HSB observed in Hyrachyus deminusscribed as compound HSB above

IndricotheriidaemdashForstercooperia exhibits vertical HSBon the molars and premolars An isolated incisor assigned toForstercooperia totadentata (AMNH 20118) appears to havetransverse HSB Juxia sharamurenense also has vertical HSBin the cheek teeth but on incisors certainly vertical HSB occur

doi104202app20100021


1 mm

1 mm1 mm

Fig 9 Vertical HSB configuration in Rhinocerotoidea A Hyracodon nebrascensis (Leidy 1850) (STIPB M 1772) late Eocenendashearly Oligocene WhiteRiver Group Toadstool Park area Nebraska USA Vertical HSB in the shearing blade of the ectoloph in the right M1 Note the bifurcations of the HSBB Floridaceras whitei Wood 1964 (KOE 357) early Miocene Gilchrist County Florida USA Strictly vertical HSB in the shearing blade of the ectolophof the upper P3 C Detail of B

(AMNH 20286 and AMNH 20287) The HSB configurationof the canines varies between these two specimens The firstone has transverse HSB whereas the second one appears tohave vertical HSB One other anterior tooth of AMNH 20287possibly a P1 or p1 also exhibits transverse HSB

AmynodontidaemdashIn Metamynodon and Cadurcodon themassive canines of the mandible show transversely orientedHSB whereas vertical HSB are evident in the worn tip of anisolated i1 (AMNH 1092) Vertical HSB are found in theenamel of all upper and lower cheek teeth They form an inminusner layer of the schmelzmuster covered by an outer layer ofradial enamel On the occlusal surface of the enamel band thecharacteristic crossminusridges of the HSB formed as the verticalHSB intersect the occlusal plane are evident to the nakedeye Molars of Amynodon advenum and Caenolophus prominusmissus also exhibit vertical HSB

In the Asian Armania asiana we found vertical HSB alminusthough the enamel is partially corroded in the available maminusterial The outer enamel surface is characterized by slightvertical ridges indicating that the vertical HSB extend to

the outer enamel surface (and therefore radial enamel is abminussent) Perikymata observed on the lingual side are orientedtransversely forming a grid pattern with the vertical HSB

RhinocerotidaemdashDetails about the various rhinocerotidsstudied are summarized in Table 1 All rhinocerotids arecharacterized by vertical HSB in premolars and molars (Fig9B C Rensberger and Koenigswald 1980) including verystrong crossminusridges in most specimens The milk dentition ofRhinoceros unicornis also showed vertical HSB in the decidminusuous premolars and transverse HSB in the incisors

Incisors however differ in the HSB configuration andmay have transverse vertical or compound HSB configuraminustion Compound HSB were found in Trigonias and in Subminushyracodon lower and upper incisors especially where theenamel is thin In thicker parts of the enamel especially inthe enlarged upper incisors the HSB tend to change from unminusdulating into a zigminuszag structure Since these zigminuszag HSB areparallel the aligned crests and troughs give the appearanceof vertical structures which are different from the strictlyvertical HSB in the cheek teeth In Menoceras from Agate


CA

B 5 mm

Fig 10 HSB configuration in the incisors of the rhinocerotid Menoceras arikarense (Barbour 1906) (USNM 412981) early Miocene Arikaree FormationAgate Nebraska USA A The lower incisor with an almost vertical shearing blade has transverse HSB B C In the upper incisor with a shearing bladeoblique to the growing axis the HSB are almost vertical

Springs in Nebraska both upper and lower incisors exhibitdifferentiation in the compound HSB configuration In I1the vertical component is dominant whereas in the i2 thetransverse component is strongest (Fig 10)

Uintaceras radinskyi differs from other rhinocerotids inits schmelzmuster The molars of the type specimen CM

12004 display clear vertical HSB but the upper molars alsoclearly exhibit an inner enamel layer that displays transverseHSB and thus exhibit compound HSB configuration Thelower molars are not clear with regard to any horizontalHSB The anterior teeth are isolated and their exact loci arenot clear but some that appear to be upper incisors clearly

doi104202app20100021


Table 1 The HSB configuration in molars and incisors of the studied Rhinocerotidae

Taxon Age HSBin cheek teeth

HSBin incisors

Eocene

Uintaceras radinskyi Middle Eocene Myton Pocket Utah USA compound vertical

Trigonias osborni Late Eocene Weld Co Colorado USA vertical compound

Penetrigonia dakotensis White River Badlands USA vertical

Oligocene

Subhyracodon occidentale lower Oligocene Toadstool Park area Nebraska USA vertical compound

Epiaceratherium magnum Oligocene MP 22 Moumlhren 13 Germany vertical transverse

Ronzotherium filholi Oligocene Moumlhren 7 Germany vertical transverse

Miocene

Menoceras arikarense Miocene Agate Nebraska USA vertical compound

Aceratherium incisivum upper Miocene MN 11 Eppelsheim Germany vertical compound

Aceratherium tetradactylum middle Miocene MN 6 Sansan France vertical compound

Aceratherium cf tetradactylum middle Miocene MN 5 Muumlnzenberg near Leoben Austria vertical compound

Aceratherium sp middle Miocene MN 7 Steinheim im Albuch Germany vertical transverse

Chilotherium sp Miocene Asia (no more data) vertical transverse

Floridaceras whitei lower Miocene Gilchrist Co Florida USA vertical

Plesiaceratherium fahlbuschi middle Miocene MN 5 Sandelzhausen Germany vertical compound

Dihoplus (= Dicerorhinus) schleiermacheri Mainz Mombach Germany vertical compound

Lartetotherium sansaniense middle Miocene MN 5 Sandelzhausen Germany vertical transverse

Brachypotherium brachypus middle Miocene MN 7 Steinheim im Albuch Germany vertical compound

Prosantorhinus germanicus middle Miocene MN 5 Sandelzhausen Germany vertical compound

Pliocene

Teleoceras fossiger upper and lower dentition Pliocene Janna Hills Kansas USA vertical transverse

Quaternary

Rhinoceros unicornis Recent vertical transverse

Dicerorhinus kirchbergensis maxilla Upper Pleistocene Burgtonna Germany vertical

Coelodonta antiquitatis tooth fragments Upper Pleistocene Urspringhoumlhle Germany vertical no incisors

Elasmotherium sibiricum molar fragment Pleistocene Russia vertical

10 mm 1 mm

interface

interface

paraconeparacone

Fig 11 Curved HSB configuration in Moropus elatus A Buccal aspect of M2 B detailed mapping of visible HSB in the paracone (modified fromKoenigswald 1994)

have vertical HSB The other conical teeth that might repreminussent the canines and lower incisors are either inconclusive orshow some evidence of horizontal HSB

EomoropidaemdashIn Eomoropus and Litolophus there is eviminusdence of transverse HSB but in no specimen could the HSBbe followed into the lophs to ascertain whether it is curvedThe m3 of the holotype of Eomoropus amarorum has whatcould be interpreted as a groove representing the interfacebetween two Uminusshaped fields of HSB but even this is quesminustionable

ChalicotheriidaemdashThe curved configuration of HSB in themolars of Moropus elatus from Agate Springs (Fig 11) wasdescribed in detail by Koenigswald (1994) and was conminusfirmed by the investigation of additional material of Chalicominustherium Ancylotherium pentelicum Nestoritherium sinenseand Metaschizotherium from Europe The thick protoconehas transverse HSB whereas in the ectoloph the HSB arestrongly curved on either side of the paracone In the uppermolars one interface on the ectoloph occurs on the preminusparacrista close to the parastyle and another occurs distal tothe mesostyle In the lower molars two interfaces are veryclose on either side of the twinned metaconid In additionthere are interfaces in the middle of the protolophid andhypolophid as mentioned by Koenigswald (1994) He usedthe term ldquoUminusshaped HSBrdquo for this extreme form of curvedHSB In contrast to the premolars and molars the incisorsshow only transverse HSB Fortelius (1985) listed chalicominustheres as having ldquohorizontal (concave)rdquo HSB which in thiscase is a synonym of our curved configuration

LambdotheriidaemdashLambdotherium from the late earlyEocene (biozone Waminus7) of Wyoming has clearly transverseHSB in various upper and lower molars and premolars Insome upper molars however a slight curvature of the HSBwas observed Thus these bands intersect the occlusal facet ata high angle No interface as in the more derived brontominustheriids could be detected No information on incisors wasavailable but the canines have transverse HSB

BrontotheriidaemdashThe lower molars of Eotitanops showtransverse HSB on the lingual side The HSB on protoconidand hypoconid are transverse but curve upwards in the lominusphids forming the typical curved HSB configuration In upminusper premolars and molars of Palaeosyops transverse HSBwere seen on the lingual side The buccal side of the uppermolars is formed by two cones with an angled cutting edgeHere the HSB are clearly curved with a distinct interfaceFortelius (1985) listed brontotheres as having ldquohorizontal(concave)rdquo HSB

The large brontothere Megacerops from the upper Eoceneincluding several genera synonymized by Mihlbachler (2008)has curved HSB in upper and lower molars with distinct interminusfaces The canines and incisors both show transverse HSB

Discussion

Perissodactyl phylogeny in the light of HSBconfiguration

In addition to documenting the HSB configuration in fossiland Recent Perissodactyla a major goal of this paper is totrace the evolution of HSB configuration in this order ofmammals (Fig 12) Because this goal is obviously dependminusent on our understanding of perissodactyl phylogeny a briefreview is given here Schoch (1989) provided a more deminus


Fig 12 Cladogram summarizing relationships among major lineages ofPerissodactyla and the evolution of various HSB configurations Boxes onthe right indicate HSB configurations in various perissodactyl taxa Boxeson the tree itself indicate changes in HSB configuration as inferred fromthe distribution of HSB configurations given this phylogeny The phylogminuseny is a conservative estimate of perissodactyl relationships drawn fromHooker (1989 1994) Froehlich (1999) and Holbrook (1999 2009)

tailed review of the history of perissodactyl systematics priorto 1989 and we refer the reader to that paper and to Hooker(2005) for more information

Wood (1934) divided perissodactyls into two subordersCeratomorpha including ldquotapiroidsrdquo (sensu lato) and rhinominuscerotoids and Hippomorpha including equoids chalicominustherioids and brontotherioids While the general concept of aclose relationship between the tapir and rhinoceros cladesrelative to the horse clade has been generally accepted (andeven corroborated by molecular studies Norman and Ashley2000) the relationships among the sominuscalled ldquohippomorphrdquotaxa as well as the relationships of certain putative fossilmembers of Ceratomorpha are unclear or controversial

Hooker (1989 1994) published the first computerminusgenerminusated cladistic analyses of early perissodactyl interrelationminusships based primarily on Eurasian taxa and dental characminusters Hooker concluded that (i) what was then called Hyracominustherium actually represents multiple genera and that theholotype of the type species Hyracotherium leporinum isactually a palaeotheriid (ii) lophiodontids historically clasminus

sified as ldquotapiroidsrdquo sensu lato are closely related to chalicominustherioids and are grouped together with them in the cladeAncylopoda (Hooker 1984) and (iii) Hookerrsquos Ancylopodaformed a clade with an emended Ceratomorpha and Isectominuslophidae which he called Tapiromorpha Froehlich (1999)came to similar conclusions in a study that focused on NorthAmerican taxa but Holbrook (1999 2001) was not able torecover Hookerrsquos concept of Tapiromorpha from data emminusphasizing characters from the cranial and postcranial skeleminuston Hooker (Hooker and Dashzeveg 2003 2004 Hooker2005) subsequently modified his view of Ancylopoda reminustaining the lophiodontidminuschalicotherioid relationship but alminuslying this group with a ceratomorphminusequoid clade he calledEuperissodactyla Euperissodactyla and Ancylopoda form alarger clade Lophodontomorpha to the exclusion of Brontominustherioidea

Within specific groups of perissodactyls there are otherphylogenetic issues relevant to this study Lambdotheriumknown from the early Eocene of North America has historiminuscally been interpreted as the earliest brontotherioid but somestudies have challenged this and suggested that this taxon ismore closely allied with palaeotheriids (Mader 1989 Lucasand Holbrook 2004)

Tapiroidea is a term that was historically applied to allnonminusrhinocerotoid ceratomorphs (Radinsky 1963) but morerecently this taxon has been restricted to a more exclusivemonophyletic group including tapirids and helaletids (Colminusbert and Schoch 1998 Holbrook 1999 2001) As a resultldquoisectolophidsrdquo including the Wasatchian Homogalax andCardiolophus as well as the Bridgerian Isectolophus havebeen removed from the Tapiroidea and probably do not repminusresent a monophyletic family (Holbrook 1999 2001) Inaddition the relationships of a variety of endemic Asianldquotapiroidsrdquomdashspecifically lophialetids and deperetellidsmdashtoother perissodactyls are no longer clear (Holbrook 1999)

Within Rhinocerotoidea the main phylogenetic issuesconcern the relationships among various taxa assigned to theHyracodontidae Radinsky (1966) broadened Hyracodontidaeto include any rhinocerotoids that could not be assigned toRhinocerotidae or Amynodontidae These included smallcursorial forms like Hyracodon from North America andEggysodon from Eurasia as well as the large to giganticindricotheres of Asia Though Hyracodontidae was clearly awastebasket taxon others adopted Radinskyrsquos (1966) compominussition of the family when attempting to establish it as monominusphyletic (Prothero et al 1986 1989) Some recent studies havecast doubt on the monophyly of this concept of Hyracominusdontidae especially with regards to the inclusion of indricominustheres (Holbrook 1999 2001) Thus we here treat indricominustheres as a separate family (Indricotheriidae) and considerNorth American hyracodontines and Eurasian eggysodontinesseparately

Given the current state of knowledge of perissodactyl phyminuslogeny and considering the distribution of HSB configurationobserved in this study several of the unresolved phylogeneticissues impact our ability to trace the evolution of HSB configminus

doi104202app20100021


Table 2 Generalized HSB configuration in cheek teeth canines and inminuscisors of the various perissodactyl families

premolarsand molars incisors canines

CONDYLARTHRAPhenacodontidae transverse transverse transversePERISSODACTYLAEQUOIDEAEquidae transverse transverse transversePalaeotheriidae transverse transverse transverseTAPIROMORPHAIsectolophidae transverse transverse transverseCERATOMORPHATAPIROIDEAHelaletidae curved transverse transverseLophialetidae and otherendemic Asian ldquotapiroidsrdquo transverse transverse

Tapiridae curved transverse transverseLophiodontidae curved transverse transverseRHINOCEROTOIDEAHyrachyidae compound compound compoundDeperetellidae compoundHyracodontidae vertical compound compoundIndricotheriidae vertical transverse comminus

poundAmynodontidae vertical compound transverseRhinocerotidae vertical compound and

transverseANCYLOPODAEomoropidae transverse

curvedChalicotheriidae curved transverse transverseTITANOTHERIOMORPHALambdotheriidae transverse transverseBrontotheriidae curved transverse transverse

uration In particular the phylogenetic positions of lophiominusdontids chalicotherioids and brontotherioids are importantfor interpreting HSB evolution Even with these limitationswe can still make some inferences regarding HSB evolutionand we summarize these below (Fig 13)

The ancestral HSB configurationmdashPhenacodontids exhibitthe tranverse HSB configuration which is consistent with thenotion that this configuration is the ancestral condition forperissodactyls Equids and palaeotheriids consistently exhibitthe transverse configuration throughout their history effecminustively retaining the ancestral condition from bunolophodontforms in the early Eocene through hypsodont forms right up toRecent times (Pfretzschner 1993) Other taxa that appear tohave retained the ancestral condition include LambdotheriumHomogalax Cardiolophus lophialetids Rhodopagus andPataecops Unfortunately the retention of the ancestral condiminustion does not clarify the relationships of these taxa to otherperissodactyls

The evolution of curved HSBmdashCurved HSB generally ocminuscur together with transverse HSB and thus presumably origiminusnated from transverse HSB They are evident in chalicominustheriids brontotheriids lophiodontids and tapiroids sensustricto (ie helaletids and tapirids) (Figs 13 14) The natureand extent of the curving differs among these groups thoughthis is at least partly due to the differences in the developmentof specific lophs Chalicotheriids and brontotheriids for inminusstance have very strong ectolophs and weaker cross lophswhereas the opposite is true for tapiroids Lophiodontids havestrong cross lophs and fairly strong ectolophs Thus it is mucheasier to detect curved HSB in the ectolophs of chalicotheriidsand brontotheriids than in the cross lophs and vice versa fortapiroids Consequently it is difficult to ascertain whether obminusserved differences in HSB are due to distinct HSB patterns orto molar morphology In any case it seems certain that curved

HSB arose independently from the transverse HSB configuraminustion at least twice since no recent phylogenies place all ofthese taxa together However on the basis of these observaminustions we cannot rule out either of the two proposed affinitiesof lophiodontids (either with tapiroids or with chalicotheres)The number of times that the curved HSB arose could be moreeasily determined if we could determine (i) the HSB configuminusration of eomoropids and (ii) the position of some putativebasal members of these lineages such as LambdotheriumHomogalax and Cardiolophus

The compound HSB configuration and the origin of vertiminuscal HSBmdashArguably the most interesting issue arising fromthese data is the evolution of HSB configurations In rhinominuscerotoids we see a close linkage between the compound HSBconfiguration (transverse HSB in the inner zone and verticalHSB in the outer zone) and the vertical HSB configurationThese configurations are similar in that they are not restrictedto specific functional areas of the dentition The evolution ofthe more derived vertical configuration probably occurred byreducing the inner layer of transverse HSB (Fig 13) The preminusvious interpretation (Rensberger and Koenigswald 1980)mdashthat vertical HSB derived from a tapirminuslike configurationmdashmust be rejected

Vertical HSB have long appeared to be a distinctive featureof rhinocerotoids and a synapomorphy uniting all members ofthe superfamily from the basalmost Hyrachyus to modernforms The observation of vertical HSB in deperetellids (Forminustelius 1985 Holbrook 2007) suggested that these unusual enminusdemic Asian ldquotapiroidsrdquo might actually be rhinocerotoids aswell Recognition of the compound HSB configuration howminusever calls into question any simple interpretation The comminuspound HSB configuration is found in Hyrachyus Uintacerasand deperetellids

Holbrook and Lucas (1997) described Uintaceras radinminusskyi from the Uintan of North America as the sisterminusgroup toRhinocerotidae and later analyses considered it to be thebasalmost member of the family (Holbrook 1999 2001Prothero 2005) The presence of compound HSB in Uintaminusceras is interesting because if Uintaceras is a basal rhinominuscerotid it suggests that one of the following is true (i) Thevertical HSB configuration evolved from the compound conminusdition independently in rhinocerotids and in the other mainfamilies of rhinocerotoids (Hyracodontidae Amynodontiminusdae and Indricotheriidae) or (ii) the vertical HSB configuraminustion characterizes all of these families and a reversal to thecompound configuration occurred in the lineage leading toUintaceras (Figs 12 14)

The presence of the compound HSB configuration indeperetellids may very well be evidence of a unique relationminusship with rhinocerotoids Considering that deperetellids sharevery few other characters with rhinocerotoids and are otherminuswise quite derived dentally this may indicate that depereminustellids are a derived offshoot of the lineage that led to convenminustional Rhinocerotoidea It would also indicate an Asian originfor the superfamily


compound HSB

transverse HSB

transverse HSB

curved HSB vertical HSB

Fig 13 Schematic hypothesis of the evolutionary interrelationship of thefour configurations of HunterminusSchreger Bands (HSB) found in Perissominusdactyla From the basal transverse HSB configuration evolved the curvedHSB configuration on the one hand On the other hand the compound HSBconfiguration evolved and gave rise to the vertical HSB configuration inRhinocerotidae

In contrast to the vertical HSB in rhinocerotoid cheekteeth some genera with enlarged incisors modified the comminuspound HSB configuration in a very different way Functionalreasons as described below led to the reduction of the vertiminuscal HSB in the outer layer and gave preference to the transminusverse HSB of the inner layer

Functional interpretation of HSB configurationsfound in Perissodactyla

HSB are an optical phenomenon but they reflect the arrangeminusment of enamel prisms which is important for the biomechaminusnical properties of the enamel Although prisms change diminusrection on their way from the EDJ to the OES thus passingthrough various HSB the sections of the prisms within aband share the same direction The functional interpretationoffered here is not based on the course of individual prismsbut rather on the major structural units represented by theHSB in which the prisms are oriented parallel to each other

Cracking and abrasion reduce the functionality of theenamel HSB are recognized as an effective crackminusstoppingmechanism in enamel The decussating prisms cause an iniminustial crack to radiate reducing its strength and thus stoppingthe progression (Fortelius 1985 Pfretzschner 1988) HSBoccur in most placental mammals in which the adult bodysize exceeds 1ndash2 kg (Koenigswald et al 1987) Among inminussectivores only the largest erinaceids have this structure andin primates early and small forms lack HSB This restrictionof HSB to larger mammals together with the distribution inthe fossil record indicates that HSB evolved in various plaminus

cental lineages independently But there is no strict relationminusship between body size and the occurrence of HSB (Maasand Thewissen 1995) For example rodents are a prominentexception they have HSB in their incisors regularly Veryfew large placental mammals lack HSB In perissodactylsHSB are regularly present although they may be developedonly weakly in the small Hyracotherium

Abrasion is affected by the prism direction Several indicaminustions and preliminary measurements indicate that enamel ismore resistant to abrasion when prisms intersect the occlusalsurface at an almost right angle Prisms with their long axismore or less parallel to the occlusal surface are abraded moreeasily (Osborn 1965 Rensberger and Koenigswald 1980Boyde 1984)

An impressive example illustrating this correlation isprovided by the euhypsodont molars of the rodent PedetesIn the occlusal surface the crossminussection of the enamel band isexposed around the dentine core In the inner layer formed byradial enamel the steeply rising prisms intersect the occlusalsurface almost at a right angle The outer layer is formed bytransverse HSB and here the prisms are oriented almost parminusallel to the occlusal surface In most naturally worn teeth theinner layer is distinctly higher and less abraded than the outerlayer (Koenigswald and Clemens 1992)

The transverse configurationmdashOf the various HSB conminusfigurations transverse HSB is the most common one and ocminuscurs in most placental lineages Even in wombats the onlyextant marsupial with HSB they are transversely oriented(Koenigswald 2000)

doi104202app20100021


Fig 14 Schematic diagram of the stratigraphic occurrence of the four configurations of HunterminusSchreger Bands (HSB) found in the various perissodactylfamilies The range data of the families are taken from McKenna and Bell (1997) All four types occurred during the Paleogene in several families The comminuspound HSB configuration did not reach the Neogene The three other types are represented by one family each in the extant fauna the transverse HSB conminusfiguration in Equidae the curved HSB configuration in Tapiridae and the vertical HSB configuration in Rhinocerotidae

The transverse orientation reflects a basic functional reminusquirement as a crackminusstopping mechanism in teeth coveredwith an enamel cap and loaded from the occlusal surface durminusing mastication (Pfretzschner 1988 Koenigswald and Pfretzminusschner 1991) The vertical load causes tensile stresses in ahorizontal plane and thus the transverse HSB with their layminusers of decussating prisms have the optimal orientation towithstand the tension Although this biomechanical model issomewhat simplistic it serves well to explain some observaminustions Muroid molars are characterized by a basal ring oflamellar enamel (very thin HSB) at the base of the crownwhile the enamel in the upper part of the crown does notshow this differentiation The ring of HSB occurs exactlywhere the intensity of the transverse stresses is at a maximumaccording to this simple model since the stresses increase tominuswards the base of the crown (Pfretzschner 1988 Koenigminusswald 2004)

This initial model for teeth covered with an enamel capmust be modified when the dentine core is exposed due toabrasion as in hypsodont teeth Then the surrounding enamelband is loaded from the crossminussection Besides compensatingfor tension stresses resistance to abrasion gains increasingsignificance in order to maintain the functional properties Intransverse HSB most prisms are often more or less parallel tothe occlusal surface and thus less resistant to abrasion Abraminussion can be reduced by the modification of the prism directionThus only the reorientation of the HSB may combine the beneminusfit of the crackminusstopping mechanism related to decussatingprisms and a steep angle of the prisms when they penetrate theocclusal surface

Transverse HSB are widely distributed among earlyperissodactyls Most perissodactyl clades however tend tomodify the orientation of the HSB Equoids are the onlygroup within the Perissodactyla that retains the transverseprism orientation into the Neogene Their phylogenetic sucminuscess may be related to the development of hypsodont teethand specific modification of the radial enamel within theenamel (Pretzschner 1994)

Curved HSB configurationmdashWe recognized curved HSBin tapirs lophiodontids chalicotheres and brontotheres Thecurved HSB are conspicuously developed in the main funcminustional shearing blades These are the transverse lophs of taminuspirs and lophiodontids and the ectolophs in chalicotheres andbrontotheres In the latter the curved HSB evolved to theUminusshaped pattern (Koenigswald 1994) The functional sigminusnificance of these curved HSB is probably to bring as manyprisms as possible in a steep angle to the shearing blade reminusducing abrasion Consequently the lophs can function for alonger time

Compound HSB configurationmdashThe compound HSBconfiguration is composed of an inner layer with transverseHSB and an outer layer of vertical HSB This compoundHSB is dominant in the cheek teeth of early HyrachyidaeDeperetellidae and Uintaceras It occurs in all sides of theteeth and seems not to be related to the tooth morphology as

with the curved HSB configuration The compound HSBevolved from transverse HSB The functional advantage ofthe two layers with a different orientation of the HSB is twominusfold first it forms an additional protection against cracksand second prisms of either the inner or the outer layer areoriented nearly perpendicular to horizontal or strongly inminusclined shearing blades thus reducing abrasion

The advantage of prisms oriented almost perpendicular toshearing blades can be tested in the rhinocerotid incisors(Fig10) In Trigonias and Subhyracodon both layers of thecompound HSB are present whereas the derived rhinos withlarge incisors show some differentiation In Menodus Aceraminustherium Chilotherium and many other genera the enlargedlower incisors are covered by enamel on the mesial side whilethe dentine is exposed on the posterior side The enamel formsa sharp edge beside the exposed dentine on both sides Theshearing blades formed by the crossminussection of the enamelband are almost parallel to the growing axis The transverseHSB are dominant and only a few ldquovertical structuresrdquo suggestthe outer layer of the compound HSB configuration Due tothe dominance of transverse HSB most of the prisms are oriminusented perpendicular to the shearing blade

The upper incisors are shaped very differently The teethare short and the shearing blade is oriented at an oblique anminusgle or perpendicular to the growing axis Both layers of thecompound HSB configuration are present in several areas ofthe tooth In the shearing blade the vertical HSB dominatethus most of the prisms form a large angle with the shearingblade

The contrasting differentiation of the compound HSBconfiguration in rhinocerotid upper and lower incisors seemsto be related to the advantage of having prisms (and HSB)perpendicular to the actual shearing blade in order to reduceabrasion The compound HSB configuration offers an ademinusquate layer of prisms in the inner or the outer layer The layerwhich is less advantageous tends to be the one reduced

The compound HSB configuration occurs sporadically invarious perissodactyls Traces of this type were found in acanine of Hyracotherium and as a minor component of theschmelzmuster in Lophiodon rhinocerodes especially wherethe enamel was thick

Comparable compound HSB configurations are alsoknown in some carnivores (Stefen 1995 1997a b 1999) Esminuspecially in the robust coneminusshaped premolars of hyaenids thetransverse HSB undulate only slightly at the EDJ The ampliminustudes increase with the distance from the EDJ and form aldquozigminuszag HSBrdquo With increasing amplitudes the vertical setsof prisms gain significance eventually forming verticalHSB This structure obviously is suited to cope with highpressure during boneminuscracking but comparable structureshave also been observed in some other mammals that wereclearly herbivorous such as the Eocene pantodont Coryminusphodon (Koenigswald and Rose 2005)

Vertical HSB configurationmdashThe vertical HSB configuraminustion is characteristic for cheek teeth of the Rhinocerotidae (Taminus


ble 1) The shearing blades of these teeth are mostly parallel tothe occlusal plane Due to the vertical arrangement of the HSBa great number of prisms intersect the occlusal surface at highangles Therefore the prisms are oriented very suitably for reminusducing abrasion The small differences in the angle of theprisms of adjacent bands are often accentuated by differentialwear They form the characteristic crossminusridges in the crossminussection of the enamel band (Quenstedt 1852 Rensberger andKoenigswald 1980) Fortelius (1985) is correct in stressing thepoint that a decussation of the prisms between the bands in theHSB structure would not be necessary to increase wear resisminustance Certainly radial enamel would have been appropriate aswell but the HSB was an inherited structure The bend of theHSB brought prisms into a much more effective direction thanprisms in transverse HSB Whether this functional propertyhowever caused the reorientation of the HSB remains an openquestion

Vertical HSB do not occur exclusively in Rhinocerotidaebut are also found in a few other nonminusrelated mammalian taxaeg in Astrapotherium Carodnia and Pyrotherium (Fortelius1984 1985 Lindenau 2005 Line and Bergqvist 2005 Rensminusberger and Pfretzschner 1992) The functional advantage ofvertical HSB is probably the same as in rhinocerotoid cheekteeth reducing the abrasion by an optimum prism orientationperpendicular to the occlusal surface Vertical HSB were deminustected also in the incisors of some rodents (Bruijn and Koenigminusswald 1994 Kalthoff 2000 Koenigswald 1993)

ConclusionEarly in their evolution perissodactyls modified the orientaminustion of the transverse HSB inherited from phenacodontidsThe four types of HSB configuration were fully developedduring the Eocene but several of the perissodactyl familiesvanished at the end of the Eocene or during the Oligocene Inthe extant fauna the transverse HSB configuration is retainedin Equoidea the curved HSB configuration is preserved onlyin Tapirus and the vertical HSB configuration characterizesthe Rhinocerotidae The compound HSB configuration is notpresent in any living perissodactyls (Fig 14)

Of the various HSB configurations found in Perissominusdactyla the transverse HSB are the least derived form Thesetransverse HSB are retained in equoids palaeotheriids andisectolophids Most other perissodactyl lineages modifiedthis basal pattern From the transverse HSB configuration thecurved HSB configuration arose in helaletids tapirs lophiominusdontids chalicotheres and brontotheres It is characterizedby curved fields of HSB with distinct interfaces The fields ofcurved HSB are closely correlated with tooth morphologyThe evolution of the curved HSB configuration may have ocminuscurred several times independently

A second way of reorganising the transverse HSB isfound in the compound HSB configuration where a secondlayer of vertical HSB is superimposed on an inner layer oftransverse HSB These vertical HSB characteristically occur

on all sides of the teeth and are not related to the tooth morminusphology We found this HSB configuration in hyrachyidsdeperetellids and Uintaceras We infer that the vertical HSBconfiguration typical for the cheek teeth of hyracodontidsamynodontids rhinocerotids and indricotheriids evolvedfrom the compound HSB configuration

The analysis of the HSB configuration provides new eviminusdence for the phylogenetic position of some genera andhigher taxa of perissodactyls but it also leaves some of thesequestions still very much unanswered Lophiodontids showsimilarities in HSB to both tapiroids and chalicotheresthough all three groups are distinct from rhinocerotoids andequoids The presence of compound HSB in deperetellids isvery suggestive of a close relationship between this familyand rhinocerotoids since the compound and vertical HSBconfigurations are likely closely related

This study also raises a number of new phylogenetic quesminustions Are the various instances of curved HSB homologousand if so does this indicate a close relationship betweenbrontotheres chalicotheres lophiodontids and tapiroidsSince rhinocerotoids are thought to be closely related to tapiminusroids how are the evolution of curved HSB on the one handand compound and vertical HSB on the other related Bettersampling should provide more insights especially data onEocene chalicotherioids and endemic Asian ldquotapiroidsrdquo

The adaptative value of the reorganization of the HSB conminusfiguration in perissodactyls is interpreted functionally as an efminusficient reduction of the abrasion during mastication assumingthat prisms intersecting the actual grinding surfaces almostperpendicularly resist wear better than prisms parallel to theocclusal surface It should be mentioned that the enamelmicrostructure is formed in the crypt an area free of externalstresses Enamel is not remodelled under stress like the strucminusture of bones In Perissodactyla various types of HSB configuminusrations were selected for in different clades but all of themshare this specific relationship between the prisms and theocclusal surface The various HSB configurations are not reminuslated to specific diets but rather to phylogenetic lineages

AcknowledgementsWe are very grateful to the many curators who provided material out ofthe collections in their care or property or allowed studying material forthis project We want to name especially Barbara Beasley (Nebraska Naminustional Chadron Nebraska USA) Chris Beard and Mary Dawson (CM)Loiumlc Costeur (NHMB) Philip D Gingerich and Gregg Gunnell (UM)Robert Emry (USNM) Uschi Goehlich (NHMW) Kurt Heissig andGertud Roumlszligner (BSPG) Meinolf Hellmund (GMH) Rainer Hutterer(ZFMK) Thomas Kaiser (HHZM) Michael Rummel (MR) and lateKarl Hirsch (Denver) We thank greatly Georg Oleschinski (STIPB)who provided several photos for the figures Finally we are thankful forthe valuable comments of the two reviewers Kurt Heissig and MikaelFortelius This research was supported for WvK by the ldquoDeutscheForschungsgemeinschaftrdquo (DFG German Research Foundation) and ispublication no 16 of the DFG Research Unit 771 ldquoFunction and performinusmance enhancement in the mammalian dentitionmdashphylogenetic andontogenetic impact on the masticatory apparatusrdquo KDR acknowledgesmultiple grants from the US National Science Foundation (especially

doi104202app20100021


IBNminus9419776 EARminus0000941 and EARminus0616376) in support of fieldwork and research on early Eocene faunas of the Bighorn Basin Wyominusming Bighorn Basin fossils were collected under permits from the USBureau of Land Management (Wyoming office)

ReferencesBoyde A 1965 The structure of developing mammalian dental enamel In

M Stark and R Fearnhead (eds) Tooth Enamel 163ndash194 WrightBristol

Boyde A 1984 Dependence of rate of physical erosion on orientation anddensity in mineralised tissues Anatomy and Embryology 170 57ndash62[CrossRef]

Boyde A and Fortelius M 1986 Development structure and function ofrhinoceros enamel Zoological Journal of the Linnean Society 87181ndash214 [CrossRef]

Boyde A and Martin L 1984 The microstructure of primate dentalenamel In D Chivers B Wood and A Bilsborough (eds) Food Acminusquisition and Processing in Primates 341ndash367 Plenum PublishingNew York

Bruijn H de and Koenigswald W von 1994 Early Miocene rodent faunasfrom the eastern Mediterranean area Part V The genus Enginia (Murominusidea) with a discussion of the structure of the incisor enamel Proceedminusings of the Koninklijke Nederlandse Akademie van Wetenschappen 97381ndash405

Colbert M 2005 The facial skeleton of the early Oligocene Colodon (Perissominusdactyla Tapiroidea) Palaeontologia Electronica 8 (12A) 1ndash27

Colbert M and Schoch R 1998 Tapiroidea and other moropomorphs In CJanis K Scott and L Jacobs (eds) Evolution of Tertiary Mammals ofNorth America Vol 1 Terrestrial Carnivores Ungulates and Ungulateminuslike Mammals 569ndash582 Cambridge University Press Cambridge

Dashzeveg D and Hooker J 1997 New ceratomorph perissodactyls (Mamminusmalia) from the middle and late Eocene of Mongolia their implications forphylogeny and dating Zoological Journal of the Linnean Society 120105ndash138 [CrossRef]

Ferretti M 2008 Enamel structure of Cuvieronius hyodon (ProboscideaGomphotheriidae) with discussion on enamel evolution in elephantoidsJournal of Mammalian Evolution 15 37ndash58 [CrossRef]

Fortelius M 1984 Vertical decussation of enamel prisms in lophodontungulates In R Fearnhead and S Suga (eds) Tooth Enamel IV427ndash431 Elsevier Amsterdam

Fortelius M 1985 Ungulate cheek teeth developmental functional andevolutionary interrelations Acta Zoologica Fennica 180 1ndash76

Froehlich D 1999 Phylogenetic systematics of basal perissodactyls Jourminusnal of Vertebrate Paleontology 19 140ndash159

Holbrook L 1999 The phylogeny and classification of tapiromorph perissominusdactyls (Mammalia) Cladistics 15 331ndash351 [CrossRef]

Holbrook L 2001 Comparative osteology of early Tertiary tapiromorphs(Mammalia Perissodactyla) Zoological Journal of the Linnean Society132 1ndash54 [CrossRef]

Holbrook L 2007 Rhinocerotoid affinities of Deperetellidae (MammaliaPerissodactyla) based on enamel microstructure Journal of VertebratePaleontology 27 90A

Holbrook L 2009 Osteology of Lophiodon Cuvier 1822 (Mammalia Perminusissodactyla) and its phylogenetic implications Journal of Vertebrate Paminusleontology 29 212ndash230 [CrossRef]

Holbrook L and Lucas S 1997 A new genus of rhinocerotoid from theEocene of Utah and the status of North American ldquoForstercooperiardquoJournal of Vertebrate Paleontology 17 384ndash396

Hooker J 1984 A primitive ceratomorph (Perissodactyla Mammalia) fromthe early Tertiary of Europe Zoological Journal of the Linnean Society 82229ndash244 [CrossRef]

Hooker J 1989 Character polarities in early perissodactyls and their signifminusicance for Hyracotherium and infraordinal relationships In D Prominus

thero and R Schoch (eds) The Evolution of Perissodactyls 79ndash101Oxford University Press New York

Hooker J 1994 The beginning of the equoid radiation Zoological Journalof the Linnean Society 112 29ndash63 [CrossRef]

Hooker J 2005 Perisssodactyla In K Rose and J Archibald (eds) TheRise of Placental Mammals 199ndash214 Johns Hopkins University PressBaltimore

Hooker J and Dashzeveg D 2003 Evidence for direct mammalian faunalinterchange between Europe and Asia near the PaleocenendashEoceneboundary Geological Society of America Special Paper 369 479ndash500

Hooker JJ and Dashzeveg D 2004 The origin of chalicotheres (Perissominusdactyla Mammalia) Palaeontology 47 (6) 1363ndash1386 [CrossRef]

Hunter J 1778 The Natural History of Human Teeth Explaining theirStructure Use Formation Growth and Diseases Second edition 128pp Johnson London

Kalthoff D 2000 Die Schmelzmikrostruktur in den Incisven der hamminussterartigen Nagetiere und anderer Myomorpha (Rodentia Mammalia)Palaeontographica Abteilung A 259 1ndash193

Kawai N 1955 Comparative anatomy of bands of Schreger OkajimasFolia Anatomica Japonica 27 115ndash131

Koenigswald W von 1980 Schmelzstruktur und Morphologie in denMolaren der Arvicolidae (Rodentia) Abhandlungen SenckenbergischeNaturforschende Gesellschaft 539 1ndash129

Koenigswald W von 1993 Die Schmelzmuster in den Schneidezaumlhnen derGliroidea (Gliridae und Seleviniidae Rodentia Mammalia) und ihresystematische Bedeutung Zeitschrift fuumlr Saumlugetierkunde 58 92ndash115

Koenigswald W von 1994 Uminusshaped orientation of HunterminusSchregerBands in the enamel of Moropus (Mammalia Chalicotheriidae) incomparison to some other Perissodactyla Annals of Carnegie Muminusseum 63 49ndash65

Koenigswald W von 1997a Brief survey of the enamel diversity at theschmelzmuster level in Cenozoic placental mammals In W vonKoenigswald and P Sander (eds) Tooth Enamel Microstructure137ndash161 Balkema Rotterdam

Koenigswald W von 1997b Evolutionary trends in the differentiation of themammalian enamel ultrastructure In W von Koenigswald and P Sander(eds) Tooth Enamel Microstructure 203ndash235 Balkema Rotterdam

Koenigswald W von 2000 Two different strategies in enamel differentiaminustion Marsupialia versus Placentalia In M Teaford M Smith and MFerguson (eds) Development Function and Evolution of Teeth107ndash118 Cambridge University Press New York

Koenigswald W von 2002 Besonderheiten der Schmelzoberflaumlche beiSaumlugetieren Lynx NS 32 (2001) 171ndash181

Koenigswald W von 2004 The three elementary types of schmelzmusterin rodent molars and their occurrence in the various rodent cladesPalaeontographica Abteilung A 270 95ndash132

Koenigswald W von and Clemens W 1992 Levels of complexity in themicrostructure of mammalian enamel and their application in studies ofsystematics Scanning Microscopy 6 195ndash218

Koenigswald W von and Pfretzschner H 1987 HunterminusSchregerminusBaumlnder imZahnschmelz von Saumlugetieren (Mammalia) Anordnung und Prismenminusverlauf Zoomorphology 106 329ndash338 [CrossRef]

Koenigswald W von and Pfretzschner H 1991 Biomechanics in the enamelof mammalian teeth In N SchmidtminusKittler and K Vogel (eds) Conminusstructional Morphology and Biomechanics 113ndash125 Springer Berlin

Koenigswald W von and Rose K 2005 The enamel microstructure of theearly Eocene pantodont Coryphodon and the nature of the zigzagminusenamel Journal of Mammalian Evolution 12 419ndash432 [CrossRef]

Koenigswald W von and Sander P (eds) 1997a Tooth Enamel Microminusstructure 280pp Balkema Rotterdam

Koenigswald W von and Sander P 1997b Glossary In W von Koenigminusswald and P Sander (eds) Tooth Enamel Microstructure 267ndash280Balkema Rotterdam

Koenigswald W von Martin T and Pfretzschner H 1993 Phylogeneticinterpretation of enamel structures in mammalian teeth possibilitiesand problems In F Szalay M Novacek and M McKenna (eds)Mammal Phylogeny 303ndash314 Springer New York


Koenigswald W von Rensberger J and Pfretzschner H 1987 Changesin the tooth enamel of early Paleocene mammals allowing increased dietdiversity Nature 328 150ndash152 [CrossRef]

Korvenkontio VA 1934 Mikroskopische Untersuchungen an Nagerminusincisiven unter Hinweis auf die Schmelzstruktur der BackenzaumlhneHistologischminusphyletische Studie Annales Zoologici Societatis ZoominuslogicaeminusBotanicae Fennicae ndash Vanamo 2 1ndash274 Helsinki

Lindenau C 2005 Zahnschmelzmikrostrukturen suumldamerikanischer Hufminustiere 193 pp PhD thesis University Bonn Bonn httphssulbunibonnde200505570557htm

Line S and Bergqvist L 2005 Enamel structure of Paleocene mmammalsof the Săo Joseacute de Itaboraiacute Basin Brazil Journal of Vertebrate Paleonminustology 25 924ndash928 [CrossRef]

Lucas S and Holbrook L 2004 The skull of the Eocene perissodactylLambdotherium and its phylogenetic significance New Mexico Muminusseum of Natural History and Science Bulletin 26 81ndash87

Maas M and Thewissen J 1995 Enamel microstructure of Pakicetus(Mammalia Archaeoceti) Journal of Paleontology 96 1154ndash1163

Mader B 1989 The Brontotheriidae a systematic revision and preliminaryphylogeny of North American genera In D Prothero and R Schoch(eds) The Evolution of Perissodactyls 458ndash484 Oxford UniversityPress New York

McKenna MC and Bell SK 1997 Classification of Mammals Above theSpecies Level 631 pp Columbia University Press New York

Mihlbachler M 2008 Species taxonomy phylogeny and biogeography ofthe Brontotheriidae (Mammalia Perissodactyla) Bulletin of the Ameriminuscan Museum of Natural History 311 1ndash475 [CrossRef]

Norman J and Ashley M 2000 Phylogenetics of Perissodactyla and testsof the molecular clock Journal of Molecular Evolution 50 11ndash21

Osborn C 1965 The nature of the HunterminusSchreger Bands in enamel Arminuschive of Oral Biology 10 929ndash933 [CrossRef]

Pfretzschner H 1988 Structural reinforcement and crack propagation inenamel Meacutemoirs Museacuteum national drsquoHistoire naturelle (seacuter C) 53133ndash143

Pfretzschner H 1993 Enamel microstructure in the phylogeny of EquidaeJournal of Vertebrate Paleontology 13 342ndash349

Pfretzschner H 1994 Biomechanik der Schmelzmikrostruktur in den Backenminuszaumlhnen von Grossaumlugern Palaeontographica Abteilung A 234 1ndash88

Prothero D 2005 The Evolution of North American Rhinoceroses 218 ppCambridge University Press Cambridge

Prothero D Manning E and Hanson C 1986 The phylogeny of the Rhinominuscerotoidea (Mammalia Perissodactyla) Zoological Journal of the Linminusnean Society 87 341ndash366 [CrossRef]

Prothero D Guerin C and Manning E 1989 The history of the Rhinominus

cerotoidea In D Prothero and R Schoch (eds) The Evolution ofPerissodactyls 321ndash340 Oxford University Press New York

Quenstedt F 1852 Handbuch der Petrefaktenkunde 792 pp Laupp andSiebeck Tuumlbingen

Radinsky L 1963 Origin and early evolution of North American Tapiroiminusdea Peabody Museum of Natural History Yale University Bulletin17 1ndash106

Radinsky L 1966 The families of the Rhinocerotoidea (Mammalia Perissominusdactyla) Journal of Mammalogy 47 631ndash639 [CrossRef]

Rensberger J and Koenigswald W von 1980 Functional and phylogeneticinterpretation of enamel microstructure in rhinoceroses Paleobiology6 477ndash495

Rensberger J and Pfretzschner H 1992 Enamel structure in astrapotheresand its functional implications Scanning Microscopy 6 495ndash510

Rose K 2006 The Beginning of the Age of Mammals 428 pp JohnsHopkins University Press Baltimore

Schoch R 1989 A brief historical review of perissodactyl classification InD Prothero and R Schoch (eds) The Evolution of Perissodactyls13ndash23 Oxford University Press New York

Schreger D 1800 Beitrag zur Geschichte der Zaumlhne Beitraumlge zur Zergliederminuskunst 1 1ndash7

Shobusawa M 1952 Vergleichende Untersuchungen uumlber die Form derSchmelzprismen der Saumlugetiere Okaijamas Folia Anatomica Japonica24 371ndash392

Stefen C 1995 Zahnschmelzdifferenzierungen bei Raubtieren Carnivoraim Vergleich zu Vertretern der Dreodonta Arctocyonidae Mesonychiminusdae Entelodontidae (Placentalia) Thylacoleodontidae Dasyuridaeund Thylacinidae (Marsupialia) 190 pp Unpublished PhD thesisUniversitaumlt Bonn Bonn

Stefen C 1997a The enamel of Creodonta Arctocyonidae and Mesominusnychidae (Mammalia) with special reference to the appearance ofHunterminusSchreger Bands Palaumlontologische Zeitschrift 71 291ndash303

Stefen C 1997b Differentiations in HunterminusSchreger Bands of carnivoresIn W von Koenigswald and P Sander (eds) Tooth Enamel Microminusstructure 123ndash136 Balkema Rotterdam

Stefen C 1999 Enamel microstructure of recent and fossil Canidae (Carniminusvora Mammalia) Journal Vertebrate Paleontology 19 576ndash587

Tabuce R Delmer C and Gheerbrant E 2007 Evolution of the toothenamel microstructure in the earliest proboscideans (Mammalia) Zoominuslogical Journal of the Linnean Society 149 611ndash628 [CrossRef]

Wood H 1934 Revision of the Hyrachyidae Bulletin of the American Muminusseum of Natural History 67 181ndash295

Wood C and Stern D 1997 The earliest prisms in mammalian and reptilminusian enamel In W von Koenigswald and P Sander (eds) ToothEnamel Microstructure 63ndash83 Balkema Rotterdam

doi104202app20100021


Appendix 1PhenacodontidaePhenacodus vortmani USGS 26100 (incisors canines) early Eocene

Willwood Formation Bighorn Basin WyomingPhenacodus almiensis USNM 16691 (maxillae with canines and cheek

teeth) late Paleocene (Clarkforkian) La Barge area western Wyominusming

Phenacodus sp UM 66761 (dentaries) early Eocene Willwood Forminusmation Bighorn Basin Wyoming

Phenacodus primaevus KOE 3668 (fragment of upper molar) earlyEocene Wyoming

Ectocion parvus USNM 525599 525600 527656 (dentaries) earliestEocene Willwood Formation Bighorn Basin Wyoming

Ectocion osbornianus USNM 494921 487874 487875 (dentaries andmaxillae) early Eocene Willwood Formation Bighorn Basin Wyominusming

Ectocion sp KOE 4058 (lower molar) early Eocene Willwood Forminusmation Bighorn Basin Wyoming

Meniscotherium chamense USNM 22699 22712 22725 (skulls anddentaries) early Eocene Wasatch Formation Sublette County Wyminusoming

Meniscotherium robustum USNM 19508 19510 (skull and mandiminusbles) early Eocene Wasatch Formation Sublette County Wyoming

EquidaeHyracotherium sandrae USNM 511099 527653 533617 (dentaries

and maxilla) earliest Eocene Willwood Formation Bighorn BasinWyoming

Hyracotherium vasacciense USNM 336136 336137 (dentary and rosminustrum) early Eocene Wasatch Formation Huerfano Colorado

Hyracotherium sp KOE 1022 3669 3670 (various upper and lowermolars) early Eocene Willwood Fm Wyoming

Xenicohippus grangeri holotype USNM 531628 (= USGS 292) (manminusdible with premolars) early Eocene Willwood Formation Wyominusming

Mesohippus bairdii SDSM V 9626 (cranium and mandible) earlyOligocene (Orellan) Brule Formation White River Badlands SouthDakota

Mesohippus sp STIPB 6522 (jaws and isolated teeth) late Eocenendashearly Oligocene Toadstool Park area Nebraska

Anchitherium aurelianense STIPB M 3301 (lower molar) MiddleMiocene Petersbuch Germany

Anchitherium aurelianense BSPG not catalogued (upper molar) Midminusdle Miocene Sandelzhausen Germany

Equus caballus KOE 38 3365 (various dentitions) Recent Germany

PalaeotheriidaePropalaeotherium sp GMH uncataloged KOE 4047 (left upper mominus

lar) middle Eocene (MP 13) Geiseltal GermanyPalaeotherium sp STIPB M2106 M2111 KOE 60 1255 1665 (isominus

lated teeth from all tooth positions and fragments) late EoceneFrohnstetten Germany

IsectolophidaeHomogalax sp KOE 881 1301 3671 (jaw fragments and isolated teeth)

early Eocene Willwood Formation Bighorn Basin WyomingHomogalax protapirinus USGS 5034 25032 (partial skulls and mandiminus

bles) early Eocene Willwood Formation Bighorn Basin WyomingIsectolophus annectens CM 2337 3043 11752 (maxillae and mandiminus

bles with cheek teeth and canine) middle Eocene (Uinta C) MytonPocket Uinta Basin Utah

Isectolophus latidens AMNH 12221 (skull with P3ndashM3) early middle

Eocene (Bridgerian) Twin Buttes Henryrsquos Fork Lone Tree Wyominusming

HelaletidaeHeptodon calciculus KOE 4035 4036 and USNM 522718minusKOE 4037

(isolated teeth and fragments) early Eocene Willwood FormationBighorn Basin Wyoming AMNH 294 4850 4855 14868 (maxillaeand dentaries with almost all tooth positions) early Eocene WindRiver Formation Wind River Basin Wyoming USNM 22782 (skulland dentary) early Eocene Wasatch Formation Sublette CountyWyoming

Heptodon posticus AMNH 14874 14971 (maxilla and mandibule)early Eocene Wind River Formation Wind River Basin Wyoming

Selenaletes scopaeus AMNH 8229 8230 (holotype) 8231 8232 (lowerdentitions) early Eocene Wind River Formation Wind River BasinWyoming

Helaletes nanus AMNH 12130 (maxilla) middle Eocene (Bridgerian)Bridger Formation Middle Cottonwood Creek Wyoming AMNH12663 13125 (dentary and isolated teeth) middle Eocene (Bridgerian)Bridger Formation Granger area Wyoming

Desmatotherium fissum AMNH 20161 81804 (maxilla and dentary)early middle Eocene (Bartonian) Irdin Manha Camp MargettsMongolia

Irdinolophus mongoliensis AMNH 19161 (holotype maxilla withP2ndashM2) middle Eocene Irdin Manha Iren Dabasu Nei MongolChina

Lophialetidae and other endemic Asian ldquotapiroidsrdquoLophialetes expeditus AMNH 21569 81675 (maxilla and mandibule)

middle Eocene Ulan Shireh beds Shara Murun region Nei MongolSchlosseria magister AMNH 20241 (holotype maxilla and lower jaw)

AMNH uncatalogued (maxilla) early middle Eocene (Bartonian)Irdin Manha Telegraph Line Camp Nei Mongol China

Breviodon acares AMNH 26113 (holotype mandible) middle Eominuscene Ulan Shireh beds Shara Murun region Nei Mongol

Breviodon minutus AMNH 20139 (holotype upper molar probablyM2) early middle Eocene (Bartonian) Irdin Manha Telegraph LineCamp Nei Mongol China

cf Breviodon sp AMNH 81751 (skull with cheek teeth) early middleEocene (Bartonian) Irdin Manha Telegraph Line Camp Nei Monminusgol China

Pataecops parvus AMNH 21747 (holotype maxilla with P2ndashM3)21746 81861 (maxilla and dentary) middle Eocene KholobolchiFormation Orok Nor Mongolia

TapiridaeColodon sp USNM uncatalogued (field no Wy 71minus358) middle

Eocenendashearly Oligocene WyomingColodon cf occidentalis MB Ma 33150 (lower molars) early Oligominus

cene White River Group South Dakota AMNH 42893 (m3) midminusdle Oligocene (Whitneyan) Protoceras beds South Dakota

Haagella peregrina BSPG 1975 XXII (holotype) and BSP1974 XXIV(fragments of mandible and maxilla) early Oligocene Moumlhren 19and 20 Germany

Protapirus bavaricus BSPG1949 I 9 1952 II 176a (mandible andmaxilla) late Oligocene (MP 28) Gaimersheim Germany

Dilophodon minusculus USNM V17826 V17827 (maxillae) middleEocene (late Bridgerian) Bridger Formation Wyoming

Tapirus terrestris ZSTUuml 7135 HH ZM Mam 351 ZFMK 79450 skullsand mandibles of different ontogenetic ages) Recent South America

Tapirus sinensis MB Ma 33219 33222 33244 (teeth) PleistoceneJunnan China


Tapirus sp USNM uncatalogued (isolated teeth) Pleistocene Melminusbourne Florida

LophiodontidaeLophiodon remensis KOE 4052 (several dentitions isolated teeth and

tooth fragments) middle Eocene (MP 13) Geiseltal GermanyLophiodon rhinocerodes MB Ma 33179 HLMDminusRO 1ndash17 (maxillae

mandibule and isolated teeth) upper Eocene (MP 14ndash16) RobiacSt Mamert Gard France

HyrachyidaeHyrachyus eximius AMNH 1645 (skull and jaws) early middle Eocene

(Bridgerian) Twin Buttes Wyoming AMNH 12355 (mandible) earlymiddle Eocene (Bridgerian) Twin Buttes CatminusTail Springs WyomingAMNH 12362 (holotype of ldquoMethyrachyus troxellirdquo maxilla) earlymiddle Eocene (Bridgerian Bridger C) Henryrsquos Fork WyomingAMNH 12364 (skull) early middle Eocene (Bridgerian Bridger D)Henryrsquos Fork Wyoming AMNH 12371 (skull) early middle Eocene(Bridgerian) Bridger Formation Summers Dry Creek Wyoming

Hyrachyus modestus AMNH 12359 (holotype of ldquoEphyrachyuscristalophusrdquo maxilla) early middle Eocene (Bridgerian BridgerC) Twin Buttes Wyoming AMNH 12664 (skull and jaws) earlymiddle Eocene (Bridgerian Bridger B2minus3) Grizzly Buttes WestWyoming AMNH 12667 (mandible) early middle Eocene (Bridgeminusrian Bridger B) Millersville Wyoming USNM nos 417319 (manminusdible) 417328 (right dentary ) early Eocene (early Bridgerian)Sheep Pass Formation Elderberry Canyon Nevada

Hyrachyus minimus GMH XXXVI 52 and 265 XXIIminus87 and 401XIVminus497 and KOE 4049 4050 (various dentitions isolated teethand tooth fragments) middle Eocene (MP 13) Geiseltal Germany

Hyrachyus affinis USNM 365033 (maxilla with upper molars) earlymiddle Eocene (Bridgerian Bridger C) Bridger Basin Wyoming

Hyrachyus sp KOE 882 (upper molar) middle Eocene (Bridgerian)Cedar Mountain Sweetwater Co Wyoming UM 32989minusKOE 4033and UM 32989minusKOE 4034 (lower and upper molar) middle Eocene(Bridgerian Brminus2) Green River Basin Wyoming USNM 487381(maxilla) middle Eocene (Bridgerian) Bridger Basin Wyoming

Fouchia elyensis USNM 417339 (holotype dentary) 417340 417341417342 (maxillae and dentaries) early Eocene (early Bridgerian)Sheep Pass Formation Elderberry Canyon Nevada

DeperetellidaeTeleolophus magnus AMNH 26063 (holotype maxillary fragment and

mandible) late Eocene or early Oligocene ldquoUlan Gochurdquo bedsUrtyn Obo Shara Murun region Nei Mongol

Teleolophus medius AMNH 20166 (holotype dentary with p1ndashm3)early middle Eocene (Bartonian) Irdin Manha Telegraph Line CampNei Mongol China

cf Teleolophus medius AMNH 81799 81853 81854 (mandibles andM2ndash3) early middle Eocene (Bartonian) Irdin Manha Camp Marminusgetts Mongolia

Teleolophus medius AMNH 26128 (M3) 26129 (M3) 26286 2628781797 (maxillae) middle Eocene Ulan Shireh beds Shara Murunregion Nei Mongol

Deperetella cristata AMNH 20290 (holotype right maxilla) 20292(mandible) early middle Eocene (Bartonian) Ula Usu Mongolia

HyracodontidaeHyracodon nebrascensis STIPB M 1778 M 1779 M 6513 M 6606

(jaws) late Eocenendashearly Oligocene White River Group ToadstoolPark area Nebraska (skull and dentary) Oligocene ldquonear HarrisonrdquoNebraska 42911 (skull and dentary) Oligocene Sioux County Neminusbraska

Triplopus proficiens AMNH 26123 (mandible) middle Eocene Chimminus

ney Butte North Mesa Ulan Shireh beds Shara Murun region SuiyanProvince Nei Mongol China

Triplopus sp CM 3240 (upper molar probably M1) 11955 (skull andjaw fragments) middle Eocene (Uinta C) Uinta Formation MytonPocket Uinta Basin Utah

Epitriplopus uintensis CM 3007 (juvenile skull and jaw fragments)middle Eocene (Uinta C) Uinta Formation Myton Pocket Uinta Baminussin Utah

Ardynia praecox AMNH 26039 (skull and mandible) middle Eocene(Ludian) Urtyn Obo Nei Mongol China

Ardynia kazachstanensis AMNH 26183 (mandible) middle Oligominuscene Baron Sog beds Nom Khong Obo Nei Mongolia China

Eggysodon osborni BSPG 1972 XI 1951 (lower incisor) Oligocene(MP 22) Moumlhren 13 Germany NHMB KB18 (upper and lower mominuslars) Oligocene Kleinblauen Switzerland

IndricotheriidaeForstercooperia totadentata AMNH 20116 (rostrum with premolars

and anterior teeth) 20118 (maxilla) middle Eocene Irdin ManhaTelegraph Line Camp Nei Mongol China

Juxia sharamurunense AMNH 20286 20287 (dentaries) middle Eominuscene Shara Murun Mongolia

AmynodontidaeAmynodon advenum CM 3107 (maxillary) middle Eocene (Uinta C)

Uinta Formation Myton Pocket Uinta Basin UtahMetamynodon planifrons HLMDminusWT 515 (mandible) AMNH 1092

(isolated i1) late Eocene White River Group South Dakota USNM6719 (dentary) early Oligocene Brule Formation South Dakota

Cadurcodon sp PMM 473 707minusKOE 486 (ectoloph of P3) lateEocenendashearly Oligocene Mongolia AMNH 19155 (juvenile skull)middle Eocene Ardyn Obo Formation Ardyn Obo Dorono GobiProvince Mongolia

Cadurcotherium cayluxi MB Ma 26318 (upper molars) late EoceneCaylux Quercy France

Armania asiana KOE 3648 (from Dashzeveg field no 1991 No17minus31) (two right upper premolars) late Eocene ErgilinminusDzo Forminusmation Mongolia

Caenolophus promissus AMNH 20297 (holotype maxilla with P3ndashM3)early middle Eocene (Bartonian) Ula Usu Mongolia

Rhinocerotidae

EoceneUintaceras radinskyi CM 12004 (holotype most of the dentition)

middle Eocene (Uinta C) Uinta Formation Myton Pocket UintaBasin Utah

Trigonias osborni USNM 4815 (mandible) latest Eocene (Chadronian)South Dakota

Penetrigonias dakotensis MB Ma 42545 (cranium) late Eocene WhiteRiver Badlands South Dakota

OligoceneSubhyracodon occidentale STIPB M 1781 M 6576 (lower deciduous

and permanent molars) early Oligocene Toadstool Park area Neminusbraska USNM 16826 (skull) early Oligocene (Orellan) Brule Forminusmation Niobrara County Wyoming MCZ uncataloguedminusKOE 556(M3) early Oligocene Brule Formation Torrington Wyoming

Subhyracodon sp USNM 15967 (skull) early Oligocene (Orellan)Brule Formation Niobrara County Wyoming USNM uncataloguedfield no 213minus42 (dentition including incisors) horizon and localityunknown

Epiaceratherium magnum BSPG 1972 XI 1912 (upper and lower inciminussors and molars) Oligocene (MP 22) Moumlhren 13 Germany

Ronzotherium filholi BSPG 1969 XXIV 153 (lower incisor) Oligominuscene Moumlhren 7 Germany

doi104202app20100021


MioceneMenoceras arikarense USNM 412981 (incisors) early Miocene Ariminus

karee Formation Agate NebraskaAceratherium incisivum MB Ma 26302 (enlarged lower incisor) STIPB

1690 (cranium with molar dentition) late Miocene (MN 11) Eppelminussheim Germany

Aceratherium tetradactylum MB Ma 42562 (two enlarged lower inciminussors) middle Miocene (MN 6) Sansan France

Aceratherium cf tetradactylum MB Ma 26430 (incisors) middle Miominuscene (MN 5) Muumlnzenberg near Leoben Austria

Aceratherium sp MB Ma 28030 and 28029 (a small and a very largelower incisor) middle Miocene (MN 7) Steinheim im Albuch Germinusmany

Chilotherium sp PMMminusKOE 492 (lower incisor and molar fragments)Miocene Asia

Floridaceras whitei MCZ 4052minusKOE 357 (lower and upper premolminusars) early Miocene Gilchrist County Florida

Plesiaceratherium fahlbuschi BSPG 1959 II and KOE 452 (severallower and upper incisors and molars) middle Miocene (MN 5)Sandelzhausen Germany

Gaindatherium vidali BSPG 1956 II 263 (lower incisor) late MioceneNagri Formation northern India

Dihoplus schleiermacheri STIPB M 1787 (fragmentary lower molars)Mainz Mombach Germany

Lartetotherium sansaniense BSPG 1959 II 4977 3912 (upper and lowerdentitions) middle Miocene (MN 5) Sandelzhausen Germany

Brachypotherum brachypus MB Ma 26348 and 26347 (upper molars andpremolars) middle Miocene (MN 7) Steinheim im Albuch Germany

Prosantorhinus germanicus BSPG 1959 II 3582 2542 5183 (severaldentitions) middle Miocene (MN 5) Sandelzhausen Germany

PlioceneTeleoceras fossiger MB Ma 228165 (upper and lower dentition) Pliominus

cene Janna Hills Kansas

QuaternaryRhinoceros unicornis ZMFK VIII 1935 (skull with mandibles) Reminus

centDicerorhinus kirchbergensis MB Ma 32 (maxilla) late Pleistocene

Burgtonna GermanyCoelodonta antiquitatis KOE 52 (tooth fragments) late Pleistocene

Urspringhoumlhle GermanyElasmotherium sibiricum PMMminusKOE 1253 (molar fragment) Pleistominus

cene Russia

EomoropidaeEomoropus amarorum AMNH 5096 (holotype skull and mandible)

early middle Eocene (Bridgerian) Mammoth Buttes Wyoming CM3109 (holotype of ldquoE annectensrdquo maxillae) middle Eocene (UintanUinta A) Wagonhound Member Uinta Formation Utah

Litolophus gobiensis AMNH 26644 26645 26647 26648 26649ndash26652 (skulls and mandibles) early middle Eocene (Bartonian)Irdin Manha Camp Margetts Mongolia

ChalicotheriidaeMoropus sp CM 1831 1740minusKOE 1638 (several dentitions) early

Miocene lower Harrison Formation Agate Springs Quarry SiouxCounty Nebraska

Chalicotherium grande NHMB C 53 NHMW C25a B4 (upper andlower dentitions) middle Miocene (MN6) Neudorf Slovakia

Chalicotherium goldfussi HLMD Din 3168 (left maxilla) late Miominuscene (MN11) Eppelsheim Germany

Metaschizotherium fraasi MR P 239Aminus003 and 004 (upper dentition)middle Miocene (MN6) Petersbuch 71 Germany

Ancylotherium pentelicum AMNH uncatalogued (left dP4 and dp4)late Miocene (Turolian) Samos Greece

Nestoritherium sinense AMNH 18453 (lower molar) PleistoceneChungminusKingminusFoo Szechuan China

LambdotheriidaeLambdotherium popoagicum KOE 4032 (upper molars) late early

Eocene (ldquoLostcabinianrdquo Waminus7) Willwood Formation Bighorn Baminussin Wyoming AMNH 4863 (mandible) 4880 (M1 and M2) earlyEocene (Wasatchian Waminus7) Wind River Basin Wyoming USNM1976119772 (skulls and mandible) late Wasatchian (Waminus7) KnightFormation Wyoming

Lambdotherium sp UM 78903minusKOE 4027 (fragmentary lower and upminusper molars) early Eocene Wasatch Formation Daniel Wyoming

BrontotheriidaePalaeosyops fontinalis UM 111893minusKOE 4029 4030 (upper premolminus

ars) late early Eocene (Gardnerbuttean Brminus1a) Wasatch FormationGreen River Basin Wyoming

Palaeosyops robustus AMNH 11710 (maxillary) early middle Eocene(Bridgerian Bridger C) Twin Buttes Wyoming USNM 1346626138 26303 (maxillae and dentary) middle Eocene (late Bridminusgerian) Bridger Formation Wyoming

Palaeosyops sp KOE 3894 (left P4 and M3 fragment) late early ormiddle Eocene Bridger Formation road cut near Lonetree Wyominusming

Eotitanops borealis UMminusKOE 4028 (m1) late early Eocene (Gardnerminusbuttean Br1a) Wasatch Formation Green River Basin Wyoming

Eotitanops gregoryi AMNH 14887 (holotype maxillary and mandiminusble) late early Eocene (Wasatchian) Wind River Basin Wyoming

Eotitanops minimus AMNH 17439 (holotype left p4ndashm3) late earlyEocene (Wasatchian) Huerfano B Colorado

Eotitanops sp AMNH 4772 (lower molar) early Eocene (Wasatminuschian) Wind River Formation Wind River Basin Wyoming

Telmatherium cf cultridens USNM V13463 (dentary) middle Eocene(late Bridgerian) Bridger Formation Wyoming

Megacerops proutti HLMD uncatalogued (cranium and upper andlower molars) late Eocene Big Badlands South Dakota

Megacerops sp UM10999 (upper premolars) late Eocene Big Badminuslands South Dakota

Incertae sedisToxotherium hunteri USNM 244352 (dentary) 244359 (maxilla with

molars) 244361 (dentary with p4ndashm2) late Eocene (Chadronian)Flagstaff Rim Wyoming

Toxotherium woodi AMNH 42901 (dentary fragment) late Eocene(Chadronian) White River Formation Wyoming

Rhodopagus pygmaeus AMNH 21554 (holotype maxilla) 26112 (manminusdible) 20391 20392 (assorted jaw fragments and isolated molars)middle Eocene Ulan Shireh beds Shara Murun region Nei Mongol


the schmelzmuster namely the configuration of HSB (as deminusfined in the next section) and we surveyed the variability ofthis character in a wide diversity of perissodactyls We fominuscused on cheek teeth (molars and premolars) because theseare best represented for the greatest number of taxa but wealso made observations on the anterior dentition (incisors andcanines) whenever possible since the schmelzmuster may difminusfer in the various teeth at the dentition level We then usedthese observations to make inferences regarding the evolutionof HSB configurations in perissodactyls

Institutional abbreviationsmdashAMNH American Museum ofNatural History Department of Paleontology New YorkNew York BSPG Bayerische Staatsammlung fuumlr Palaumlontominuslogie und Geologie Muumlnchen Germany CM Carnegie Muminusseum Section of Vertebrate Paleontology Pittsburgh Pennminussylvania GMH Geiseltalmuseum Halle Germany HHZMZoologisches Museum der Universitaumlt Hamburg GermanyHLMD Hessisches Landesmuseum Darmstadt GermanyKOE Koenigswald enamel collection of the STIPB BonnGermany MB Museum fuumlr Naturkunde Berlin GermanyMCZ Museum of Comparative Zoology Harvard UniversityCambridge Massachusetts MR Michael Rummel collectionNaturminusMuseum Augsburg Germany NHMB Naturhistoriminussches Museum Basel Switzerland NHMW Naturhistoriminussches Museum Wien Austria PMM Palaeontological Muminusseum Moscow Russia SDSM South Dakota School ofMines Museum of Geology Rapid City South DakotaSTIPB Steinmann Institut Paleontology University of BonnGermany UM University of Michigan Museum of Paleontolminusogy Ann Arbor Michigan USGS United States GeologicalSurvey Denver Colorado specimens now housed at USNMUSNM National Museum of Natural History SmithsonianInstitution Department of Paleobiology Washington DCZFMK Zoologisches Museum Alexander Koenig BonnGermany ZSTUuml Zoologische Sammlung Universitaumlt Tuumlbinminusgen Germany

Other abbreviationsmdashBr Bridgerian EDJ enamelminusdentinejunction HSB HunterminusSchreger bands if interface betweenfields of HSB OES extend almost to the outer enamel surminusface SEM Scanning Electron Microscope Wa WasatchianIncisors canines premolars and molars are designated as IC P M for uppers i c p m for lowers

The nature of HunterminusSchregerBandsHunterminusSchreger Bands are an optical phenomenon producedby refraction of light due to the internal structure of theenamel The term HSB is not only used for this phenomenonbut is traditionally also used for the underlying structureformed by layers of decussating prisms In the terminology reminuslated to enamel structures we follow Koenigswald and Sander(1997b) Enamel is a highly mineralized material Several

structural levels must be differentiated to understand the pheminusnomenon of HSB The mineral hydroxyapatite forms very thincrystallites that are organized into rods called enamelldquoprismsrdquo although these structures are not prisms in the minminuseralogical sense These prisms have a diameter on the order of5 μm Many studies have been devoted to the changing shapeof the crossminussection of the enamel prisms (eg Shobusawa1952 Boyde 1965 Boyde and Martin 1984 Wood and Stern1997) The enamel prisms start at the enamelminusdentine junction(EDJ) and extend almost to the outer enamel surface (OES)They are normally arranged in groups with the same prism oriminusentation or in a very symmetrical arrangement Occasionallythe orientation of the prisms is irregular eg in proboscideans(Koenigswald 1997a Tabuce et al 2007 Ferretti 2008) Theorientation of the prisms defines the various enamel types(Koenigswald and Sander 1997a 1997b) The enamel cap ofa tooth may be formed by two or three different enamel typesThese can be arranged in layers within the thickness of theenamel band or occur in specific areas of the teeth Thearrangement of enamel types in a tooth was defined asschmelzmuster (Koenigswald 1980) The different tooth famiminuslies within the same dentition may show differences in theschmelzmuster (Koenigswald and Clemens 1992)

The visual phenomenon of HSB (Fig 2) is caused by theoptical properties of the crystallites within the prisms Thiseffect would hardly be visible in single crystallites but it ismagnified when crystallites are packed in prisms and it isstrongly increased when bodies of prisms are oriented in parminusallel If the direction of the light coincides more or less withthe long axis of the prisms it will disappear in the depth of theenamel Thus the crossminussection appears dark Light fallingperpendicular or at an angle to the prisms is reflected andthus the prisms appear bright Thus prisms effectively act inthe same manner as fiber optic light guides

The enamel type defined as HSB is formed by layers ofenamel prisms which decussate at a high anglemdashoften about90mdashwith the prisms of the adjacent layer The generalbiomechanical function of the layers of decussating prisms isto serve as an important crackminusstopping mechanism compaminus


Fig 1 Vertical HSB configuration as figured by Quenstedt (1852 pl 2 1 [A]pl 3 35 [B]) A Occlusial view with HBS in the extoloph B Orienationand bifiurcation of the HSB in tangential aspect





doi104202app20100021


05

mm

ED

JE

DJ

ED

JE

DJ

ED

JE

DJ













1 mm1 mm












doi104202app20100021


1 mm

HSB

1 mm

HSB

HSB

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paracone










A B1 mm 1 mm

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2 mmif

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CA B

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Eocene




Oligocene




Miocene













Pliocene


Quaternary





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Discussion













doi104202app20100021


















compound HSB

transverse HSB

transverse HSB











doi104202app20100021


























doi104202app20100021

















































































doi104202app20100021


























































































Rhinocerotidae










doi104202app20100021






















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mm

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DJ













1 mm1 mm












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HSB

1 mm

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Eocene




Oligocene




Miocene













Pliocene


Quaternary





10 mm 1 mm

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interface

paraconeparacone








Discussion













doi104202app20100021


















compound HSB

transverse HSB

transverse HSB











doi104202app20100021


























doi104202app20100021

















































































doi104202app20100021


























































































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HSB

HSB

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paracone










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Eocene




Oligocene




Miocene













Pliocene


Quaternary





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Discussion













doi104202app20100021


















compound HSB

transverse HSB

transverse HSB











doi104202app20100021


























doi104202app20100021

















































































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Rhinocerotidae










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1 mm

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A B1 mm 1 mm

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Eocene




Oligocene




Miocene













Pliocene


Quaternary





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Discussion













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compound HSB

transverse HSB

transverse HSB











doi104202app20100021


























doi104202app20100021

















































































doi104202app20100021


























































































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Oligocene




Miocene













Pliocene


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compound HSB

transverse HSB

transverse HSB











doi104202app20100021


























doi104202app20100021

















































































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Rhinocerotidae










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Eocene




Oligocene




Miocene













Pliocene


Quaternary





10 mm 1 mm

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Discussion













doi104202app20100021


















compound HSB

transverse HSB

transverse HSB











doi104202app20100021


























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CA B

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Eocene




Oligocene




Miocene













Pliocene


Quaternary





10 mm 1 mm

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Discussion













doi104202app20100021


















compound HSB

transverse HSB

transverse HSB











doi104202app20100021


























doi104202app20100021

















































































doi104202app20100021


























































































Rhinocerotidae










doi104202app20100021






















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doi104202app20100021


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1 mm1 mm









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Eocene




Oligocene




Miocene













Pliocene


Quaternary





10 mm 1 mm

interface

interface

paraconeparacone








Discussion













doi104202app20100021


















compound HSB

transverse HSB

transverse HSB











doi104202app20100021


























doi104202app20100021

















































































doi104202app20100021


























































































Rhinocerotidae










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Eocene




Oligocene




Miocene













Pliocene


Quaternary





10 mm 1 mm

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Discussion













doi104202app20100021


















compound HSB

transverse HSB

transverse HSB











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doi104202app20100021

















































































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Rhinocerotidae










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Eocene




Oligocene




Miocene













Pliocene


Quaternary





10 mm 1 mm

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interface

paraconeparacone








Discussion













doi104202app20100021


















compound HSB

transverse HSB

transverse HSB











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doi104202app20100021

















































































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compound HSB

transverse HSB

transverse HSB











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Rhinocerotidae










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cene Russia






































doi104202app20100021


















compound HSB

transverse HSB

transverse HSB











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compound HSB

transverse HSB

transverse HSB











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doi104202app20100021


























































































Rhinocerotidae










doi104202app20100021






















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Rhinocerotidae










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cene Russia






















































































































Rhinocerotidae










doi104202app20100021






















cene Russia


















































cene Russia






























diversity and evolution of hunter−schreger band configuration in … · 2011-02-14 · mon...

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