Tooth Histology and Ultrastructure of a Paleozoic Shark, Edestus heinrichii, Taylor and Adamec 1977

Rainer Zangerl Tooth Histology and Ultrastructure of a Paleozoic Shark, EdestusheinrichiiKatherine Taylor1 Committee on Evolutionary Biology University of Chicago and Thomas Adamec2 Univ

FIELDIANA

Geology

Published by Field Museum of Natural History

Thisvolume is dedicated to Dr Rainer Zangerl

Tooth Histology and Ultrastructure

of a Paleozoic Shark, EdestusheinrichiiKatherine Taylor1

Committee on Evolutionary Biology

University of Chicago and

Thomas Adamec2

University of Chicago

Pritzker School of Medicine

INTRODUCTION Edestus heinrichii (Newberry and Worthen, 1866), is a Paleozoic

sharkknown from symphysealtoothisolatesandseveral articulated

toothbars Specimens attributed tothisgenus havebeendescribed

from Russia, Australia, England, and the mid-continental United

States E heinrichiiis oneof 15 specieswithingenus Edestus that

have been distinguished by variations in the dentition size andmorphology Teethremaintheonlyanatomicevidenceofthegenusthus far described This paper re-examines the symphyseal den-

titionbased on newmaterial from the Pennsylvanianshales of theIllinois Basin Aspects of histology, tissue ultrastructure, tooth

ankylosis,grossmorphology and embryologyofthefossilare

exam-ined Evidence is provided for the absence of orthodentine in the

symphysealteeth.Thisisthefirstelasmobranch knowntohavethis

condition The teeth are composed of only two types of dentine:

enameloid and trabecular The ultrastructure of the denteon in'Present address:Departmentof Pathology, University of Chicago.

442 FIELDIANA: GEOLOGY, VOLUME 33

trabecular dentine is shown to share a similar fundamental

struc-turewith theosteonofsecondarybone Thespecimens studied hereare Field Museum of Natural History (FMNH) PF 2848 and PF

2849, of E heinrichii They are from the Pennsylvanian shales of

Mecca Quarry in Parke County, Indiana, collected by Dr Rainer

Zangerl Recentmaterialforcomparisonof tissue structureisfrom Sphryna tudesandIsurid sharks, fromthe FieldMuseum'sDepart-mentof Fishes

MATERIALS AND METHODS

The Field Museum study collection has at least 27 individualteeth ofE heinrichii so faridentifiedby X-ray, includingfivepar-tial tooth whorls of from two to three teeth and one completely

articulatedwhorlofnine teeth(fig 1). Oneofthepartialtooth bars

of three articulated teeth with complete crowns and almost

com-plete roots waschosen for sectioning, along with a single isolatedtooth Thefossilsremainedcompletelyembeddedinshaleand were

identified by x-ray (pi 1). In PF 2849, the anterior teeth were cut

serially at 2 mm. intervals into 16 sections and light microscope

slides were hand ground(fig 2). Serialsections6, 7, and 12 didnot

survive the mounting andgrinding process andfragmentsofthem were used for electron field emission scanning. These fragmentswere put through successive24-hr periodsinpropylene oxideuntil

the embedded epoxide resins were removed, then dehydrated in

absolute alcohol Some of thespecimens at this stage wereetchedwithhydrochloricacid, thenairdried Driedmaterialwas mounted

on aluminiumdiscsandthen coatedwith gold:palladium(40:60) in

an Edward vacuum coating machine. The scanswere made by theseniorauthorand byDr.John M.ClarkoftheUniversityofChicago

Pritzker School of Medicine on the Hitachi HFS II scanningtronmicroscope, establishedbyagrantfromtheSloan Foundation,

elec-at the Enrico Fermi Institute The scans were done under PHS GrantNo 5T05 GM01939 from theNational Institute ofGeneralMedicalScience

CONDITION OF THE FOSSILS AND THEIR PRESERVATION

Thehard tissues werealmostperfectlypreservedinthetion process Both tooth specimens were laiddown parallel to the

fossiliza-shale's beddingplane, as is the case with the vast majority ofthe

specimens in the study collection X-ray photographs of similarly

embedded specimens were madeat various angles andchecked for

TAYLOR & ADAMEC: PALEOZOIC SHARK

angular deformation; none was found Thex-rays(pi. 1) represent

fully sagittal views Zangerl and Richardson (1963, p. 181) report

that a largecladodontid toothfromthesamequarrywas embeddedupright and showed no evidence of distortion due to compression.The shape dimensions are in complete agreement with teeth em- beddedlaterally.Plasticdeformationisthereforenegligible.

Diagenesis has onlyslightlymodifiedthemorphology and ogy The teeth are tosomeextent decalcifiedandbituminized The

histol-burial sediments and diagenetic replacement materials have

natu-rally stained histologic areas uniformly and consistently.

Micro-scopiccavitiesare neatly stainedwithironwhichisbrowntored to

orangeintransmittedlight. On PF2848, calcitehasfilledthe basalcanals and made them opaque, and filerite (zinc sulphate) hasformed betweenthe denticlesalongtheborders(pi 1). Thepresence

offileritefromdecompositioniscommonintheMecca fossils(

Zan-gerl,pers.comm.).

Thedepositionalenvironmentofthe blackshales was so acid the

bacterial degradation was not very destructive This permitted aslow steady impregnation with hydrocarbons, a condition most

favorable to preservation

Crackingofthe enameloid surfaceis grosslyvisiblewhenmatrix

is removed from the crown The cracks occur at regular intervals

remainingfairly equidistantandrunfrom the baseof the crown tothe tip (fig. 1). In sagittal view cracks in the trabecular dentine

lining the crown perforate the enameloidand open onto the crown

surface(pi. 4a). Theopenings are 40-50/u.wide andaverage .4 to .5

mm. in depth Electron scans of the enameloid surface (pi. 4b, c)

demonstratethat micro-cracks occur at intervals correspondingto

thechannelsinthe brightfield views Thereisnoindicationfromthe

examination here that these are anatomic structures They do notappeartobeinassociationwiththe vascularpatternofthe trabecu-lardentinetheypenetrate Zangerl foundingross examinationthat

the system of macro-cracks is arranged stress-coat fashion andprobablyresulted frompressure of the burial mud when it lost itsplasticity (Zangerl and Richardson, 1963, p. 181) The cracks are

presumedtobediagenetic ratherthan anatomic

GROSS MORPHOLOGY, VASCULARIZATION,

AND ANKYLOSIS

The tooth base presumably grows continually in a longitudinaldirection from the time the crown comes into place functionally

444 FIELDIANA: GEOLOGY, VOLUME 33

Fig 1.Edestusheinrichii,UF30(FMNH),showingacompletesymphysealtoothbarof nine successive teeth. Enameloidflangescan beseenextendingposteriorly;

the stress-coat-like cracks in theenameloidareapproximated

until thewhole tooth including its base is shed from the mostposition on the whorl The crown is full-sized when it comes

anterior-into placeintheposterior-mostposition.Thereplacement-sheddingprocess proceeds at a constant rate so that seven to nine teeth are

maintained on each bar The tooth crown is defined by the area

covered with enameloid The cusp is non-equilateral; the anterior

edgerisesatasharp angletotheroot; the posterioredgeslopes at a

widerangle. Thereareup to 1 1 denticlesonthe anteriorcrownder of the adult tooth and 13 along the posterior border Crenula-

bor-post

Fig 2.Edestusheinrichii,PF2849,showingpositionof coronal sections (A) seen

in Plate2,andthe position of thesagittalsection(B). The basal sinus seen in the

serial sections isapproximatedbydotted lines.

Plate 1 a, SagittalX-rayofEdestusheinrichii,PF2849.Threeadultsymphysealteeth are seen inanatomicarticulation. Thearrows alongthe posterior borderof

the third tooth indicate a radio-opaque area of pyrite Filerite, adecompositionnomenon, has formedbetween the denticles, b, Sagittal x-ray of E heinrichii, PF

phe-2848, isanisolated tooth thatwasshedanteriorlyfromtooth bar.

446 FIELDIANA: GEOLOGY, VOLUME 33

tions on the denticles are not apparent on x-ray but can be seenunder magnification on exposed specimens of E heinrichii The

denticles along at least the anterior border are crenulated The crownsare socloselyspacedthattheadjacent borders overlapallinthe samedirection(fig 1). Flanges ofenameloid extend out 1.5 cm.behind the crown on the top of thetoothbase troughs (fig 1) andoccur symmetrically on each side of the bar These flanges alsooccurinEdestusminor, although considerablyreduced

The teeth are well vascularized Thepattern is characterized by majorarterial branchingand venous anastomosingthroughout the

tooth base, with substantially smaller arterioles supplying the

centralcrownregionandafinernutrientnetworkgoingtothe apicalliningand terminating at theenameloidjunction. Thevessels runalongthe longitudinal axis of the root from backto front, diminish

in sizefrom frequentbranching, andslant upward into the crown.Thevesselsdonot convergetowardthecrown'sapexbutremainatrightangles to the posteriorborderascan be seeninasagittally sec-tionedtooth(pi. 3b) Thelargest canals are centrallyplaced inthe

root.Inthe centralvascularnetworkthereisclearlyasinglechannel

thatisthemajorarterialand venoussupplyforeachtooth.sky(1899, pp 404-421) described thepresenceof similar large single

Karpin-channels in Helicoprion without discussing their function The

channels' successivebranchingisclearlydemonstrated ontheserial

enlargements (pi 2). The central canal slants upward toward the

crown andrunsin thisspecimenjust toone sideofthe midline The

canalmayconductarteries,veins, andnervesasisthe typical

verte-bratecirculatoryandinnervation pattern

The trabeculation of the tooth bases is more rugged on the

ex-posedouter surface of the toothbar Thisisparticularly noticeable

on Plate 3a of the serial sections The external and internal rootsurfaces facing into the troughs have much smaller trabecles indi-

cating less stress between teeth than between the whorl and thejaws Theseinternal areas ofankylosis have uniform surfaces andemissary foramina(pi.3a)

The nature of the ankylosis of the teeth to one another has notbeen fully detailed before In his schematic drawing of what he

called "Protopirata heinrichii" C R Eastman (1902) reproduced

thepresenceofa basal sinuswhichhe does notname or discuss It

has otherwisebeen assumedthat thetooth bases werefully intact with each other (Newberry, 1889; Hay, 1910) This was notfoundtobethe casehere.Thetroughofatoothbaseandthebaseof

terior extension of theenameloidflangeonthecrown.

t i 500, /<

A PF 2849 slide 16

Plate3 a,PF2849, coronal section of toothshowingdistinctionbetweencrownandbase.Crowniscoveredbythinenameloid(seewidearrows),andiscomposedofTypes 1and2 trabecular dentine InterdenteonalhardtissuecharacterizingType2

is shown bythin arrows.Type3 trabecular dentine is restricted to the outer

milli-meterof thebaseandisan openspongiosumlacking denteons.Emissary foramina

inType 3 are associated with rough ligamentous attachment(the trabecles),and

with the vascularsupply (the foramina), b, PF2848, the vascular patternin this sagittally cut fossil toothshowsthat the vasculature within thedenteonlumen runperpendicular to the surface inType1 trabecular dentine,andatrightangles to the tooth surface inType2 c, PF2849, at higher magnification theabsenceof ortho- dentine isdemonstrated.Type1 trabecular dentine is subjacent to the enameloid.Hereagain the regular stress-coat crackingin theenameloidcan beseen.

distinct difference in fracture patternbetweenhypermineralizedenameloidandthemorefibrous trabecular dentine.Thejuncturebetweenthe tissuesshows upclearly.

450 FIELDIANA: GEOLOGY, VOLUME 33

the successivetoothitholdsarenot completely ankylosed formingabasal sinus(fig 2). Thesinusispatent onlybetweenadjacent toothbasesandisnotacontinuous channel throughouttheintermandibu-

lar whorl The successive basal sinuses are not artifacts of this

particularfossilnoraresultofthespecimenshavingpartiallyrotted

apart Tracings from blow-ups were cut out and a reassembly

at-temptedthat wouldclose offthebasalsinuses Sucha realignmentwas not structurally possible. Thebasal sinusis a real anatomical

feature.There may have been moremobilitybetweenteeththanhadbeen supposedwiththe basal sinus tissuescushioning compressive

and shearingstresses, acondition alsomoreconducive foranterior

toothshedding.

HISTOLOGY Remarkableconservatisminthe retention oftooth typesisa sub-

class character of elasmobranchs This conservatism over a long

stratigraphic sequenceseems tobethecaseforthe 110-million-year

spanofEdestus, fromtheMississippianthroughthe earlyTriassic

Edestus was a successful form Only two types of dentine —

tra-beculardentineandenameloid — occurredinits symphysealteeth

It isthefirstsharkforwhichthe lack oforthodentinehasbeen

docu-mented(pi.4a)

Inthe earlyliteraturetermsfordifferentdentinetypesproliferate

thatwereoftendefineddifferentlybyindividual researchers 0rvig's(1951, 1967a, c) consolidation andreordering ofterms for the hard

tissues of elasmobranchsis followedhere with one exception

Tra-becular dentine is used here for what would ordinarily be called

osteodentine We havenotbeenable to identify theinterstitiallular banding between the denteons as bone Osteoblasts may in

acel-certain instances transform into odontoblasts (Pflugfelder, 1930),

but invoking suchaprocess without evidenceisunwarrantedhere.The histology of edestid teeth has been examined previously(Hay, 1910; Nielson, 1932, 1952; Zangerl, 1966) Hay madesagittal

andcoronal sections ofonlythetoothbaseofE heinrichii,therefore

not observing the absence oforthodentinein thecrown His

speci-men came from the same general area, western Indiana, as thoseexaminedhere.The twocorrespondexactlyintoothbasestructure

Hayreferstothe trabeculardentineofthebaseas"vasodentine," a

tissuecontainingcapillarycanals instead of dentineal tubules; and from gross rather than histologic examination reports that the

toothcrowncovering"isprobablytrueenamel"(Hay, 1912,p.50).

TAYLOR & ADAMEC: PALEOZOIC SHARK 451

Zangerl(1966) described the histology of thecloselyrelated

edes-tid Ornithoprion hertwigi The outermost layer, "which probably

constituted the orthodentine with its vitrodentine surface" erl, 1966,p. 31), wasmissing In light ofitsabsence inE heinrichii

(Zang-itwasprobablyoriginally absentin 0 hertwigi also(Zangerl, pers

comm.) Asectionthroughthe trabeculardentineofalargeO

hert-wigi tooth shows trabecular dentine correspondingexactly to the

type1 (seepi.3a, b; 4a)crownliningfound inE.heinrichii Theclearinterstitial bandingof acellular calcifiedtissue isabsent, asit isin

E heinrichii, and the dentine tubules do not define the denteonmargins

Dentineis homologous among all vertebrates, the matrix being

secreted by mesodermally derived odontoblasts The odontoblasts

retreatalongthe front ofthematrix accumulation, leavinghair-likecellprocesses,calledTomes' fibers,behind(pi. 5b) Orthodentineisthesame histologically infish, reptiles, and mammals. Its absence

in this species andprobablythewhole familyisa feature forwhich

there isno ready explanation. Peyer (1968, p. 65) emphasizes that

coat of compact dentineis orthodentine It isundoubtedlylacking

inE heinrichii Some elasmobranchteeth consistalmostentirelyof

orthodentineandthereisa transition to teethofverylargelyulardentine withorthodentine formingaverythin coating E hein-richii is interpreted here as anevolutionaryform inwhich the ten-

trabec-dency towardreduction oforthodentine has culminated inits

com-plete absence Holocephalians characteristically lack orthodentine

also; thisis not to suggest thatEdestus ismore closely related to

themthantoelasmobranchs, butthatthisisa feature ofconvergent

histo-tooth organ. Type 1 trabecular dentine is a dense packing of teons enclosing a fine capillary system lining the tooth crown (pi.

den-3a, 4a) There is diagnostically no interstitial tissue between the

denteons inType 1 and thecalcified peritubular liningis much

TAYLOR & ADAMEC: PALEOZOIC SHARK

A.

453

Plate 6. PF2849, a, Fiber-mineralbundleswithin thedenteonwall arearranged

in circular fashion, b, Scan at 2,000 magnifications of the denteon wall shows

branchingfiber bundles, c,Thefracture pattern of the interdenteonal tissue is that

of a woven-fibered hard tissue. The interstitium between denteons seen here is

characteristic ofType2 trabecular dentine.

duced and frequently absent. Type 2 is immediately subjacent to

Type 1 and constitutes the central crown region and most of the

tooth base The denteons are separated by an acellular teonal hard tissue (pi. 3a) The typeofinterstitium foundhere hasbeenreferred toby Radinsky(1961) as interosteonalhard substanceand Peyer (1968) as cell-free interosteonal hard substance The

interden-a, Type brightfieldTome'sfibersquiteclearly.Theblack dots are radio-opaque pyrite b, In polarizing

light thedenteonis seen tobecomposedofaninnerdarkringof different refractionandtherefore different fiber-crystal orientationthanthe bright outer ring, c,Recent

Type2 trabecular dentinefrom thehammerhead shark, shows a consistent inner ring of transversely oriented fibers, and anouter ring ofmorelongitudinally ori-

entedfibers, d,e, Inmoderntissue as in thefossil,denteons withlamellae of

com-monfiber orientation are interspersedwithlamellae ofalternatingpitch.The

inter-denteonal hard tissue is the frothy materialbetween the denteons f, A naturalgrowthsurface of adenteonfroma modern Isuridshark shows therope-likesub- structure of thedenteonwall.

appears composedtinuous super-bundles in left-handed coils,PF2848 b,Lamellae arrangedcircularly

aroundthelumenarecomposedofspirallingleft-handed super-bundles.