growth and patterning in the conodont skeleton

35
doi: 10.1098/rstb.1998.0231 , 633-666 353 1998 Phil. Trans. R. Soc. Lond. B Philip C. J. Donoghue Growth and patterning in the conodont skeleton References http://rstb.royalsocietypublishing.org/content/353/1368/633#related-urls Article cited in: Rapid response http://rstb.royalsocietypublishing.org/letters/submit/royptb;353/1368/633 Respond to this article Email alerting service here right-hand corner of the article or click Receive free email alerts when new articles cite this article - sign up in the box at the top http://rstb.royalsocietypublishing.org/subscriptions go to: Phil. Trans. R. Soc. Lond. B To subscribe to This journal is © 1998 The Royal Society on October 20, 2010 rstb.royalsocietypublishing.org Downloaded from

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Page 1: Growth and Patterning in the Conodont Skeleton

doi: 10.1098/rstb.1998.0231, 633-666353 1998 Phil. Trans. R. Soc. Lond. B

 Philip C. J. Donoghue Growth and patterning in the conodont skeleton  

Referenceshttp://rstb.royalsocietypublishing.org/content/353/1368/633#related-urls

Article cited in:

Rapid responsehttp://rstb.royalsocietypublishing.org/letters/submit/royptb;353/1368/633

Respond to this article

Email alerting service hereright-hand corner of the article or click Receive free email alerts when new articles cite this article - sign up in the box at the top

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This journal is © 1998 The Royal Society

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Page 2: Growth and Patterning in the Conodont Skeleton

Growth and patterning in the conodont skeleton

Philip C. J. Donoghue{Department of Geology, University of Leicester, University Road, Leicester LE1 7RH, UK

Recent advances in our understanding of conodont palaeobiology and functional morphology haverendered established hypotheses of element growth untenable. In order to address this problem, hardtissue histology is reviewed paying particular attention to the relationships during growth of the compo-nent hard tissues comprising conodont elements, and ignoring a priori assumptions of the homologies ofthese tissues. Conodont element growth is considered further in terms of the pattern of formation, ofwhich four distinct types are described, all possibly derived from a primitive condition after heterochronicchanges in the timing of various developmental stages. It is hoped that this may provide further means ofunravelling conodont phylogeny. The manner in which the tissues grew is considered homologous withother vertebrate hard tissues, and the elements appear to have grown in a way similar to the growingscales and growing dentition of other vertebrates.

Keywords: conodont; agnathan; histology; odontode; enamel; dentine

1. INTRODUCTION

Conodont a¤nity has been the subject of debate ever sincethe microscopic tooth-like elements were ¢rst discovered(Pander 1856; for a review, see Aldridge 1987). The topicremains controversial even after 140 years of research andthe discovery of soft tissue remains of conodonts. Morerecent discussion has narrowed the debate to theacraniate^craniate level within the chordates, basedprimarily on characters of soft tissue anatomy (Aldridge etal. 1993; Aldridge & Purnell 1996; Aldridge & Donoghue1997).

In the years preceding the discovery of preserved softtissues, the a¤nity of the tooth-like phosphatic microfos-sils remained enigmatic. Palaeobiologists had attemptedto resolve this conundrum using comparative anatomy ofthe architecture of the feeding apparatus (e.g. Schmidt1934, 1950; Schmidt & Mu« ller 1964), element morphologyand histology. Although there are some notable exceptions,histological studies failed to take full advantage ofcomparative histology. Without any degree of constraintover a¤nity this proved an unpro¢table line of research,resulting in a series of esoteric accounts of hard tissueultrastructure.

In retrospect, it would never have been possible to reachan unequivocal conclusion regarding conodont a¤nity justby analysing element morphology and internal structure.A parallel can be seen in the debate over the a¤nity ofHadimopanella Gedik, which is represented in the fossilrecord almost exclusively by microscopic phosphatic scler-ites. The sclerites are two-component hard tissuecomplexes composed of a microcrystalline base containingtubules, overlain by a hypermineralized glassy cap(Bengtson 1977). The structure and morphology of thesclerites, therefore, made Hadimopanella and related taxa

convincing micromeric agnathans (Dzik 1986; Ma« rss1988; van den Boogaard 1988). However, the discovery ofexceptionally preserved specimens composed of seconda-rily phosphatized soft tissues and articulated scleritesrevealed Hadimopanella to be a palaeoscolecid, a poorlyknown group of Early Palaeozoic worms (Hinz et al. 1990;Mu« ller & Hinz-Schallreuter 1993).

Now that we have a much clearer perception of cono-dont a¤nity, a new era in conodont comparativehistology has begun. Dzik (1986), Sansom et al. (1992)and, to a lesser extent, numerous others (e.g. Andres1988; Burnett & Hall 1992), have reviewed elementhistology in the context of our new phylogenetic under-standing. The drawback of these studies is their relianceon direct comparison between speci¢c structures withintissues, without considering other factors such as the inter-play between the component hard tissues during growth.Because they failed to consider relative growth, theseauthors were unable to reconcile their interpretationswith existing models of growth in conodont elements, orknowledge of tissue interaction in modern organisms.These studies have also been criticized because of theirfailure to consider the full spectrum of chordate hardtissues (Kemp & Nicoll 1995a).

One subject that has been ignored entirely is patterning.At present, we have only a broad understanding of how afew conodont elements grew, and then only at the simplestlevel. The growth of more complex elements can only beresolved by identifying recurrent patterns of growth inthe internal structure of the hard tissues. Furthermore,there are a number of recurrent morphological patternsexpressed by conodont elements through their fossilrecord. Do these re£ect common ancestry or convergence?The pattern of formation is potentially a useful tool indiscriminating homology from analogy. Knowledge ofpattern formation would also be useful in comparing thegrowth of conodont elements with other vertebrate hardtissue complexes, and would enable investigation of the

Phil.Trans. R. Soc. Lond. B (1998) 353, 633^666 633 & 1998 The Royal SocietyReceived 30 April 1997 Accepted 30 June 1997

{Present address: School of Earth Sciences, University of Birmingham,Edgbaston, BirminghamB152TT,UK([email protected]).

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complexity shown during this early craniate experimentwith skeletal mineralization.

The present study addresses the interpretation of thehard tissues after consideration of growth and patterning,and is organized into two sections. The ¢rst addressespattern and is concerned primarily with the descriptionof conodont hard tissues and their patterns of intergrowth.A new model of conodont hard tissue growth is presented,based on these patterns, and patterns of whole elementgrowth are described. The second section considersprocess and evaluates competing hypotheses of hardtissue homology in the light of results from the ¢rstsection, and a new interpretation of hard tissue histologyis outlined. Patterns of whole element growth are evalu-ated in the light of these results, and compared with thoseshown by the hard tissues of taxa outside the Conodonta.

2. A HISTORICAL REVIEW OF STUDIES OF

CONODONT HARD TISSUE HISTOLOGY

Conodont histology is currently in a state of disarray.Largely, this has arisen because the most recent studieshave failed to address previous observations and interpre-tations. It is therefore pertinent to review our accumulatedknowledge of conodont histology in an attempt to resolvedi¡erences in the current debate which persist for mainlyhistorical reasons.

In the ¢rst paper on conodonts, Pander (1856) noted thelamellar nature of crown tissue and the presence of cells orcavities within the albid white matter. However, he incor-rectly interpreted the direction of growth in the crown asinward, and it was more than 80 years before this wascorrected by the work of Furnish (1938) and Hass (1941).

Although intervening years were occupied by variouscontentions over the a¤nities of conodonts, 30 yearselapsed before Zittel & Rohon (1886) reviewed conodonthistology and a¤nities. They were the ¢rst to attempt tohomologize conodont hard tissues with those of anothergroup. They considered lampreys and annelids as possibledescendants, and compared the ultrastructure of thetoothlets of these two groups with the histology ofconodont hard tissues, concluding that conodonts wereannelids.

Stau¡er & Plummer (1932) provided an excellentreview of the conodont controversy to that time. Theycompared their own observations on element microstruc-ture with ivory (dentine), and also tentatively consideredconodont element growth, concluding that the denticles,which were composed of white matter, were inserted intoelements after the hyaline crown tissue had been fullyformed.

Branson & Mehl (1933) were the ¢rst to use histology asa taxonomic character in conodonts, recognizing a groupof `¢brous' conodonts, the Neurodontiformes, which theylater erected to the rank of suborder, distinct from allother conodonts (Branson & Mehl 1944).

Furnish (1938) brie£y considered the growth of cono-dont elements, clarifying the mode of outer apposition ofsuccessive crown tissue layers, and was probably also the¢rst to recognize internal discontinuities in the crown asevidence of in vivo damage and repair. This observation isnormally attributed to Hass (1941), who recognized therelevance of internal discontinuities as evidence of

external and not internal growth. Hass also noted theoccurrence of hollow spaces or tubules within whitematter and the presence of interlamellar spaces in lamellarcrown tissue. Beckmann (1949) later exhumed Pander'scontention of vertebrate a¤nity, interpreting allcomponent hard tissues as dentine. He was the ¢rst todevelop a model for conodont element growth, and thisremains the only synthesis of complex elementmorphogenesis (¢gure 1a). Beckmann identi¢ed cavitieswithin lamellar crown tissue that he believed to havebeen interconnected, and to have supplied nutrients fromthe pulp (basal cavity) to interconnected tubules withinwhite matter. He believed that the nutrients were ¢nallytransported to the outer surface of the element, whichwas covered by a temporary mesh-like secreting tissue.The renowned vertebrate histologist Òrvig consideredBeckmann's model `untenable' as, in his opinion, `thesubstance of which the cusps are built up is clearlydi¡erent from all hard tissues met with in vertebrates'(Òrvig 1951, p. 381). However, Òrvig's criticisms wereonly aimed at the ¢nal proposed homology of the hardtissues with dentine and did not consider the growthmodel itself. The presence of the cavities within lamellarcrown tissue has subsequently been veri¢ed by lightmicroscopy (Mu« ller & Nogami 1971, 1972) and electronmicroscopy (Barnes et al. (1973a), who similarly suggestedthat their function was to transport nutrients); that theyare interconnected has yet to be demonstrated. Inter-connections between the white matter cavities that couldfacilitate transport of £uids from the basal cavity to theexternal surface of the crown are not present, and Pietzneret al. (1968) failed to ¢nd any evidence of interconnectionwhatsoever. Therefore, Beckmann's (1949) model is unten-able not because the component tissues of conodontelements fail to resemble dentine, but because there is noultrastructural evidence to support it.

Gross (1954, 1957, 1960) published a series of studies onconodont microstructure, in which he compared conodonthard tissues with those of vertebrates, particularlyheterostracan dermal armour. Gross believed that growthincrements within the crown did not coincide with theridges apparent in the basal cavity or on the recessivebasal margin (¢gure 1b,c, part i) which align with theincremental layers in the basal tissue. He conceded thatthe ridges were parallel with the incremental layers of thecrown, but he concluded that incremental layers in thecrown and basal body were not secreted synchronously.Gross invoked an elaborate, ad hoc hypothesis wherebyspecial cells partly resorbed each incremental layer ofcrown tissue shortly after their secretion and prior tosecretion of the subsequent layer of basal tissue. In thisway, concentric ridges were formed over the base ofthe crown, parallel to the incremental layers, but not coin-ciding with them (¢gure 1c, part i). Hence the incrementallayers abut with these ridges, but are not con£uent withincremental layers within the crown. However, Grossbelieved that the earliest phase of growth was restrictedto the crown, although his contention was probably basedon oblique thin sections, or sections which failed to coin-cide with the growth centre of the elements. Furthermore,he did not perceive the basal body as a homogeneousstructure, and proposed instead that it was composed of a`Basistrichter' and `Trichterfu« llung' (basal cone and cone

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Growth and patterning in the conodont skeleton P. C. J. Donoghue 635

Phil.Trans. R. Soc. Lond. B (1998)

Figure 1. Previous growth hypotheses of Beckmann (1949), Gross (1957, 1960) and Mu« ller & Nogami (1971, 1972). (a) Beck-mann's was the only model to account for growth in multidenticulate elements. (b) Gross believed that growth increments withinthe crown had not been been secreted synchronously with those of the basal body. (c) Comparison of (i) Gross's and (ii) Mu« ller &Nogami's hypotheses of growth. (d) Mu« ller & Nogami ¢nally resolved the synchronous growth relationship between the crown andbasal body.

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¢lling). Gross rejected the idea that conodont hard tissueswere homologous with dentine and enamel as he erro-neously believed that the conodont mode of centrifugalgrowth was incompatible with such an interpretation. Heinstead concluded that the elements were composed ofexoskeletal bone. Gross's model of conodont elementgrowth was subsequently negated by Mu« ller & Nogami(1971) who clearly demonstrated the con£uent passage ofgrowth increments between crown and basal body (¢gure1c, part ii, and d).

Quinet (1962a) provided a detailed account of thehistology of Ancyrodella Ulrich & Bassler and PolygnathusHinde Pa elements, con¢rming much of Hass's work andconcluding that conodont elements could not have beenteeth, or have performed a tooth function, because oftheir outer-appositional mode of growth. He alsosuggested that the ultrastructure of the elements comparedwell with exoskeletal bone, which is also covered by softtissue in life. In a later publication, Quinet (1962b)described the histology of Belodus Ethington with whichhe compared the feeding elements of the polychaeteNereis, concluding that Belodus was a polychaete, and thatthe Conodonta represented a polyphyletic group.

One of the most unconventional interpretations of cono-dont a¤nity was proposed by Fahlbusch (1964) who partlyjusti¢ed his hypothesis on histological grounds. Fahlbuschcompared the histology of conodont elements to fossil algalmaterial, reinterpreting Gross's model of growth for cono-donts to ¢t his predilections. Fahlbusch's model was poorlyreceived and severely criticized (Beckmann et al. 1965).

Lindstro« m (1955) made preliminary observations on thehistology of Lower Ordovician conodont elements,describing basal bodies with lamellar and globularinternal structures. Later, Lindstro« m (1964) reviewed allaspects of earlier research and produced an excellentoutline of conodont ultrastructure. His conviction that`One may assume a priori that the inner structure musthave a great systematic signi¢cance, greater perhaps thanthat of the surface morphology' (Lindstro« m 1964, p.22),was to spark new interest in the histology of conodontelements that was sustained for the following twodecades. Amongst many other observations and conten-tions, he believed that white matter had been formed by aprocess of resorption of crown tissue resulting in a series ofhollows and inclusions within an otherwise lamellar struc-ture (following Gross 1954). He resolved Gross's (1957,1960) bizarre two-part division of the basal body into asingle structure with partly discontinuous growth incre-ments, and cast doubt on the basal resorption hypothesisby demonstrating the clear relationship between lamellarcrown increments and the ridges on the aboral surface ofelements. Lindstro« m also disagreed with Gross's sugges-tion that the conodont crown was homologous withexoskeletal bone, but followed Gross's erroneous reasoningin discounting enamel and dentine as component tissues ofthe conodont skeleton.

Schwab (1965) described lamellar structure in thecrowns of neurodontiformes, thereby reinstating them asconodonts. Schwab also distinguished the two structuralforms of basal body: a cartilage-like' lamellar structureand a `bone-like' spherular structure, later reinterpretedas atubular dentine (Sansom 1996) and globular calci¢edcartilage (Sansom et al. 1992), respectively. In a later

paper, Schwab (1969) described the histology of Panderodusdenticulatus Schwab as three-layered, including an innerlining surrounding the basal cavity, and inner and outerlamellar layers, the last containing what he believed to bedentine tubules. His distinction of separate layers istenuous, and the `dentine tubules' he described from theouter lamellar layer more probably represent alignment ofthe long (c) axes of the component crystallites.

Mu« ller & Nogami (1971, 1972) produced the last reviewsthat were primarily based on light microscope study.These were probably the most in£uential of all works onconodont histology, describing a wide range of conodonttaxa and producing a taxonomic grouping based solely onthe internal structures of elements. Although often attrib-uted to Gross, Mu« ller & Nogami were also responsible forresolving the pattern of synchronous growth between thecrown and basal body (¢gure 1c, part ii, and d). They alsoelaborated on Staesche's (1964) histological work bydistinguishing a number of di¡erent types of whitematter, which they proposed would be useful in taxonomy.Three years earlier than Mu« ller & Nogami (1971), the

¢rst of a series of studies which heralded a new era inultrastructural research had been undertaken by Pietzneret al. (1968).This work included geochemical, transmissionelectron microscope (TEM) and scanning electronmicroscope (SEM) analyses of conodont elements,through which these authors re¢ned knowledge ofchemical composition and of the varying organic contentof di¡erent tissues. They also described the discreteporous nature of white matter, and the structure of theother hard tissues. Structural di¡erences between thecrown and the basal body, including di¡erent crystal sizesand organic matter content, were also noted. Pierce &Langenheim (1969) were the only other authors toattempt a TEM study, in this case using Pa elements ofPalmatolepis Ulrich & Bassler and Polygnathus, but theirwork failed to reveal any new information.

An SEM study of fractured surfaces led Lindstro« m &Ziegler (1971) to conclude that white matter was seconda-rily derived from lamellar crown tissue by a process ofrecrystallization during the animal's life. In a later paper(Lindstro« m & Ziegler 1972), they documented variation incrystal structure throughout the various tissues andsuggested that the crown and basal body were not secretedsynchronously, although each corresponding increment ofthe two tissues had been secreted in step. They suggestedthat the basal tissue increment was secreted ¢rst, and wassubsequently matched by an increment of crown tissue.However, they presented no evidence in support of thismodel. They went on to review advances of conodonthistology published since Lindstro« m's (1964) monograph,paying particular attention to alternative interpretationsof the growth of protuberances on the surfaces of Paelements of Pseudopolygnathus Branson & Mehl (Ziegler &Lindstro« m 1975).

During the early 1970s, Barnes and his co-workerspublished a series of studies on conodont histology withthe aim of constructing a suprageneric classi¢cationscheme based on ultrastructure (Barnes et al. 1970,1973a,b, 1975). This work revealed a number of charactersthat appear unique to speci¢c groups, thereby at leastpartly ful¢lling their objective. Most notably, a newinternal microtexture was described from neurodontiform

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hyaline elementsöelongate crystallites containing micro-spheres 0.5 mm in diameter. Later, Wright (1989, 1990)interpreted these structures as microspherules expelled byGolgi apparatuses during mineralization. The Barnesteam advocated a secondary origin for white matter fromlamellar crown tissue, supporting the earlier contention ofLindstro« m (Lindstro« m 1964; Lindstro« m & Ziegler 1971;Lindstro« m et al. 1972).

Bengtson (1976, 1983) described and compared thehistology of proto-, para- and euconodonts, proposingthat they represented an evolutionary series. Szaniawski(1982, 1983, 1987) compared the most primitive group,protoconodonts, with the histology of modern chaetognathspines, concluding that protoconodonts were indeed thespines of fossil chaetognaths. Hence, if the proto-, para-and euconodont evolutionary series were correct, thiswould indicate that the a¤nity of true conodonts lay withthe chaetognaths. By 1993, protoconodonts were consid-ered a distinct group of animals, although theevolutionary relationship between para- and euconodontswas rea¤rmed (Szaniawski & Bengtson 1993).

The advances made in conodont hard tissue histologyduring the late 1960s and the 1970s led to the possibilityof using histology to distinguish conodonts from the scler-ites of other organisms. Clark et al. (1981) even went so faras to include the histological complexity of conodontelements as a character in his diagnosis of the Conodonta.Chau¡ & Price (1980) used histological characters tojustify the conodont a¤nity of their new Devonian genusMitrellataxis, which they brie£y compared microstructu-rally with ¢sh scales from the same deposits. Wang (inWang & Klapper 1987;Wang1989) similarly used internalstructure as a means of justifying the a¤nity of FungulodusGagiev. The presence of white matter, apparent in thinsections, was taken as unequivocal support for a conodonta¤nity, o¡ering a contrast with the histology of thelodontdermal denticles. However, this interpretation remainsequivocal (Wang & Turner 1985; Wang 1993). Addingfurther confusion, Wang (in Wang & Klapper 1987)disputed the conodont a¤nity of Mitrellataxis (Chau¡ &Price 1980) on histological grounds, concluding a verte-brate a¤nity. Histology was also used by Klapper &Bergstro« m (1984) to assess the a¤nity of ArcheognathusCullison. They described Archeognathus as bearing a`¢brous' crown and a lamellar basal body entirely lackingtubules or cell spaces. Klapper & Bergstro« m thusconcluded that dentine and bone were not present andthat the fossils represented the remains of a conodont,and not a vertebrate.

In contrast, Barskov et al. (1982) described spongy andlamellar forms of basal body in Neocoleodus Branson &Mehl and Coleodus Branson & Mehl, compared sphericalstructures in the spongy form with osteocyte lacunae, andhomologized the tissue with bone, concluding a vertebratea¤nity for conodonts.

Von Bitter & Merrill (1983) described the histology ofEllisonia Mu« ller using naturally fractured specimens. The¢brous nature of the crown tissue led them to suggest thatellisoniids were neurodonts, a group of conodontsconventionally deemed restricted to the Ordovician.Their observations suggested that the neurodonts werepresent at least as late as the Late Carboniferous(Pennsylvanian).

Before 1983, conodont histologists were evidently in astate of confusion; some authors recognized vertebratehard tissues amongst conodont elements and used this asevidence of vertebrate a¤nity for conodonts. Conversely,other authors recognized a distinct histology which theyused to discriminate conodonts from vertebrate microre-mains. This all changed with the discovery of conodontsoft tissues (Briggs et al. 1983; Aldridge et al. 1986; Aldridge& Briggs 1986); conodont histologists ¢nally had a contextin which to evaluate the histology of the feeding elements(Dzik 1986). Dzik was the ¢rst to take advantage of this,and began by homologizing conodont basal tissue withdentine, and comparing conodont crown tissue withenamel. Similarly, when Andres (1988) described thehistology of a number of Cambrian and early Ordovicianconodonts representative of para- and euconodonts, hehomologized basal tissue with dentine and crown tissuewith enamel. Again, followingDzik, Andres concluded thatparaconodonts were the ancestors of both euconodonts andvertebrates. Later, Burnett & Hall (1992) comparedlamellar crown tissuewith protoprismatic enamel.Krejsa et al. (1990a,b) introducedaneontological perspec-

tive to conodont palaeobiology, comparing andhomologizing the tissues of conodont elements with those ofmyxinoid keratinous toothlets (¢gure 2). They suggestedthat the basal body was a developing replacement tooth forthe overlying functional crown, enabling the conodontsperiodically to shedand replace their `teeth'.Theyalso inter-preted spaces within white matter as homologous with thegoblet-shaped pokal cells that underlie the keratinoustoothlet covering in hag¢sh, apparently con¢rming themyxinoid a¤nities of conodonts. However, Krejsa et al.'smodel ignores conodont histological features which renderit untenable, such as the con£uence of growth between thecrown and basal body indicating that the two structuresgrew synchronously, not as separate generations. Further-more, the histogenesis of hag¢sh toothlets is poorlyunderstood; attempts to draw homology between themand conodont elements should be reserved until the histo-genesis of hag¢sh toothlets has been properly documented.

In a series of papers, Sansom and his colleaguesreviewed element histology in the light of the chordatea¤nity of conodonts (Sansom et al. 1992, 1994; Sansom1996). Many of the observations of their 1992 paper hadbeen made earlier by other authors (Barnes et al. 1975;Dzik 1986; Jeppsson 1980; Smith et al. 1987; Smith 1990),but Sansom et al. (1994) were the ¢rst to describeunequivocal dentine from conodonts, most notably inNeocoleodus. Sansom (1996) also described protoprismaticenamel from the Ordovician^Devonian conodont lineagePseudooneotodus Drygant and placed the model of conodontelement growth established by Mu« ller & Nogami (1971,1972; ¢gure 1c, part ii, and d) into a biological and devel-opmental perspective. M. M. Smith et al. (1996) extendedthe number of conodont taxa covered, and reviewed therelevance of the a¤nity and relative antiquity of cono-donts to understanding the early evolution of thevertebrate skeleton.

The interpretations of conodont hard tissues by Sansomet al. (1992, 1994) remain controversial even though manyaccept conodonts as vertebrates (� craniates). Forey &Janvier (1993) aimed their criticisms primarily at theproposed homology between lamellar crown tissue and

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enamel. The extreme variation in the orientation of crys-tallites in lamellar crown tissue, ranging from parallel to ahighly angular relationship with the surface (particularlyevident in taxa ¢gured in Sansom et al. (1992); ¢gure 3i),was thought to be incompatible with enamel, neitherorientation corresponding precisely. The description ofprismatic structure in the lamellar crown of Pseudooneotodus(Sansom 1996) has demonstrated that the lamellar crowncan mirror the structure of some enamels. However,Sansom and his colleagues have still failed to reconcilethe wide variation in conodont crown structure with therange of known enamels. Further, although Sansom(1996) has been able to reconcile his interpretations ofhard tissue histology with both Mu« ller & Nogami's (1971)model of conodont growth, and modern developmentalsystems, he has achieved this reconciliation without apriori considering how the tissues grew. Janvier (1995,1996a,b) has further criticized the suggested homology ofwhite matter with cellular dermal bone, suggesting amesodentine a¤nity to be more likely. Schultze (1996)also disagreed with Sansom and his colleagues over theirinterpretations of conodont hard tissue histology. Most ofthese criticisms have been made earlier, but other pointsof contention result from Schultze's assumption that thework of Gross (1954, 1957, 1960) is correct, and heconcludes `the placement of conodonts in the animalkingdom will be solved as soon as a recent relative canbeen found' (Schultze 1996, p. 283).

Histological study of conodont elements has not beenrestricted to the mineralized hard tissues. FÔhraeus &FÔhraeus-Van Ree (1987) undertook a histochemicalstudy (using haemalum and eosin) of preserved soft tissueremnants from the organic components of the mineralized

tissues, ¢nding them to be histochemically reactive after415 Myr! Much of the tissue is very similar to moderncollagen and also appears to preserve cell spaces;however, many of the structures remain enigmatic, andFÔhraeus & FÔhraeus-Van Ree (1987, p.109) preferred towait `until stained tissue sections of early Palaeozoic verte-brate tissue (e.g. ostracoderms) have been produced',before ¢rm conclusions were reached. However, althoughthis work had already been undertaken over 20 yearsearlier (Tarlo & Tarlo 1961; Halstead Tarlo & Mercer1966), the ¢delity of preservation is too poor to be usefulin comparison.

Kemp & Nicoll (1995a,b, 1996) also attempted to iden-tify organic molecules within the mineralized matrix bystaining them in situ, applying histochemical tests forcollagen (picrosirius red), DNA (DAPI), keratin (Gram'sstain), cartilage (Alcian blue) and protein (toluidine blue).These tests used a series of positive and negative controls(Kemp & Nicoll 1993, 1995a,b, 1996). Lamellar crownstained positive for collagen, so Kemp & Nicoll rejectedthe hypothesis that lamellar crown tissue is homologouswith enamel, which is a purely epidermal product andcontains no collagen.White matter and basal tissue failedto stain for collagen, but bone, cartilage and dentine arederived from ectomesenchymal and epidermal interaction,and contain collagen in life. Kemp & Nicoll (1995a)concluded that conodont hard tissues are not comparablewith those of vertebrates. Attempts to repeat the results,even with modern vertebrate material and unequivocalfossil vertebrates, have failed (M. M. Smith, personalcommunication). Kemp & Nicoll have also failed todemonstrate the e¡ectiveness of this test on uncontestedfossil vertebrate material. Towe (1980) has shown that,

638 P. C. J. Donoghue Growth and patterning in the conodont skeleton

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Figure 2. (a) Lingual tooth ofMyxine Linnaeus in longitudinal section, after Dawson (1963) and Kresja (1990a,b). (b) Pa elementof Ozarkodina in transverse section, after Mu« ller & Nogami (1971). The functional keratin cap and replacement toothlet (pokal cellcone) of the myxinoid grow as distinct structures, whereas the crown and basal body (putative replacement crown of Kresja(1990a,b)) grew in intimate association.

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although tissues like collagen may be preserved physicallywith high ¢delity, biochemical preservation is negligible.Furthermore, the instability of collagen is such that it canonly be expected to survive biochemically intact for a fewmillion years (Bada 1991).Therefore, although FÔhraeus &FÔhraeus-Van Ree (1987, 1993) may well have been correctin interpreting their isolated organic residues ascontaining collagen, it is unlikely that Kemp & Nicoll'sresults are meaningful.Many questions regarding conodont hard tissue

histology remain unanswered: the primary or secondarynature of white matter has yet to be conclusively deter-mined; no clear model has been published to show howconodont elements grew, other than at the very simplestof levels (Mu« ller & Nogami 1971, 1972); and we need toaddress the problem of how more complex elements weregrown.

3. MATERIAL AND METHODS

(a) MaterialThe present study was based primarily on material from

the reference collection of the Micropalaeontology Unit,Leicester University Geology Department. Of the ¢guredmaterial, specimens with numbers pre¢xed by BU arereposited at the Lapworth Museum, University ofBirmingham; those with a ROM pre¢x are reposited atthe Royal Ontario Museum, Toronto, and those with a Cpre¢x are reposited at the Geological Survey of SouthAfrica, Pretoria.

(b) MethodsConodont element ultrastructure has been examined

using a variety of methods including thin sectioning, theexamination of naturally and arti¢cially fractured speci-mens, and the use of scanning electron, incident light,transmitted light and laser confocal microscopy.

Thin sections were made by embedding elements incold-curing polyester resin, set in nitrile Beam capsules,the elements oriented according to the required section.The polyester cylinders were then ground to the appro-priate level and polished on a rotating felt lap with0.05 mm alumina powder. The polished surface wasbonded to a frosted glass slide using cold-curing epoxyresin (Buelers' Epothin).The opposing side of the polyestercylinder was removed using a diamond-tipped annularsaw and the excess resin ground away using 600 and 1000grade carborundum powder until the desired level withinthe conodont element was reached. The exposed surfacewas polished as before, either by hand, or by using anautomated attachment to the rotating felt lap.Thin sections were studied using transmitted light and

laser-confocal microscopy. For SEM, the thin sectionswere etched using 0.5% orthophosphoric acid for varyingperiods, always less than 10min. The sections were eitherpermanently coated with gold, or temporarily coated withcarbon (following Repetski & Brown 1982) or silver(following Mills 1988).

Of the naturally and arti¢cially fractured specimensstudied, natural fractures were found to be less revealingdue to diagenetic alteration of element ultrastructure.Arti¢cial fractures were produced using an entomologicalneedle mounted in a pin vice; inverted conodonts elements

were fractured by applying pressure to the pin, which wasseated in the basal cavity of the element. Immersion of thespecimen in a small droplet of water was found to preventloss during this procedure. Specimens were subsequentlyetched using 0.5% orthophosphoric acid for 6^8min andcoated for SEM study.

There has been some discussion in the literature relatingto the relevant merits of the microstructural study via thinsection versus fractured surfaces (Lindstro« m & Ziegler1971; Barnes et al. 1973; Mu« ller 1981). Both methods havethe potential to produce artefacts' that do not truly re£ectmicrostructure. However, care in the interpretation of thinsections can obviate this problem. The use of fracturedsurfaces in studying microstructure is more contentious(see, for example, discussion in Barnes et al. (1973b)),although by employing etching techniques it is possible todiscern artefacts from true microstructure. In addition,despite the mistrust of the etch-fracture technique bysome conodont histologists, this methodology is commonlyused in vertebrate palaeohistology (e.g. Smith 1989). Thetechnique is also supported in theoretical consideration ofthe behaviour of brittle solids during failure (e.g. Dally &Riley 1991).

The simplest and most rapid method of studying micro-structure is by immersion of elements in oil of a refractiveindex close to that of apatite (1.68). It is also important forthe oil to have a relatively high viscosity, thus preventing£ow away from the specimen. In this way, tens of elementscan be studied at once using traditional light and laserconfocal microscopy. For laser confocal microscopy thespecimen was ¢rst bonded to the slide using a smallamount of gum tragacanth. In contrast with other techni-ques, this method is non-destructive and the oil canreadily be removed by washing the specimens in ethanol.

Light micrographs were taken using a Leitz Aristoplan¢tted with di¡erential interference contrast. Scanningelectron micrographs were taken on a Hitachi S-520.

4. PATTERN: THE CONODONT ELEMENT

Characteristically, conodont elements are constructedfrom two basic units: the crown and underlying basalbody (¢gure 3a^ c). The crown is composed either entirelyof hyaline lamellar crown tissue (¢gure 4e^ j), or of acombination of lamellar crown and white matter (¢gure3a^ c). The basal body is a single component structurecomposed from a hard tissue herein termed basal tissue.

(a) The component tissues(i) Lamellar crown tissue

This is the most coarsely crystalline of all conodonthard tissues and usually comprises the major componentof conodont elements. The length of individual crystallitesis extremely variable, ranging from less than 1 mm to inexcess of 30 mm, but they are usually no more than a fewmicrons long.The crystallites are bounded at either end bythe punctuating growth lines which de¢ne the lamellaethat are so characteristic of the tissue (e.g. ¢gure 3d,e).The orientation of the crystallites relative to the growthincrements, and thus the surface at the time of growth, isinconsistent (e.g. ¢gure 3i) and has in the past beenattributed to `the direction in which the main ontogeneticgrowth occurred at the place in the lamella where the

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crystal is located' (Hass & Lindberg1946, p. 501). In manysimple coniform elements the crystallites are arrangedwith their long (c) axes parallel or sub-parallel to thelong axis of the element, such that the entire crown iscomposed of a single homogeneous prism of crystallites ina fan-like arrangement. In complex' conodont elements,the prismatic structure of the element is broken up into anumber of individual prisms, each comprising a denticle(¢gure 3h). Because the crown of a multidenticulateelement is structurally more di¡erentiated than the crownof a coniform element, the main ontogenetic vector ofgrowth is not so extreme. As a result, the more extremevariations of crystallite arrangement, such as sub-parallelto the growth lines, are less prevalent than in coniformelements. In areas of complex elements that were simplybeing enlarged by successive increments of lamellarcrown tissue, without development of new morphologicalfeatures (e.g. growth around the main body of blade-likeor platform elements), the crystallites are usually orientedperpendicular to the outer surface (e.g. the variation in¢gure 3i,k). Crystallites adjacent to the basal cavity areinclined upwards and outwards relative to the junction ofthe crown with the basal body (¢gure 3j).

(ii) White matterWhite matter is a term derived from the appearance of

this tissue in re£ected light.White matter contrasts sharplywith lamellar crown tissue because of its more ¢nelycrystalline composition (¢gure 4a^d), its markedlygreater resistance to standard dental acid etchants (e.g.Stau¡er & Plummer 1932; ¢gure 4b), its lower organiccontent (Pietzner et al. 1968) and the lack of punctuatinggrowth increments. White matter occurs exclusively indenticles as cores (¢gure 5i) and has sharply de¢nedlateral margins. The cores appear dark in transmittedlight (¢gures 3a and 5i, j) because of the cavities enclosedwithin the ¢ne-grained groundmass (¢gure 4a,c,d). Thesecavities vary considerably in their size, shape andorientation. Most common are tubular cavities (¢gure4d), which occur in two size distributions both of whichare predominantly oriented with their long axes parallelto the long axis of the denticle: longer tubules, typically20^30 mm in length, and shorter tubules (¢gure 4c),usually only a few microns in length. The calibre of thetubules is usually in the order of 0.25 to 1 mm, but theysometimes expand into a large (3^7 mm diameter), some-times irregular, cell-shaped cavity, from which other

tubules may splay (¢gures 4c and 5l). These larger cavitiesare rare but ubiquitous, and usually occur at the oral endof connected tubules (¢gure 5l). It is likely that the tubulesand cavities represent the sites of mineral-secreting cells.

Although white matter and lamellar crown tissue areextremely distinctive tissues, the junction between the twois imperceptible in transmitted light (¢gure 5j,k). This isthe main reason why conodont histologists in the 1970sgenerally interpreted white matter as secondarily derivedfrom lamellar crown tissue. However, when these tissuesare studied in etched sections, their mutual boundary isextremely sharp (compare ¢gures 3b and c).

The transitional zone apparent to Barnes et al. (1973a)between the two tissues does not appear to be lamellar,coarsely crystalline or cancellate in transmitted light, so itis di¤cult to resolve whether it is lamellar crown, whitematter or a third, previously unrecognized tissue.However, in properly etched sections, no transitionaltissue is evident, and the boundary between white matterand lamellar crown is extremely sharp.The apparent tran-sitional zone is in fact white matter that lacks cavities.The problem of distinguishing white matter from

lamellar crown is further complicated because not all thetissues that appear albid in re£ected light are true whitematter; when they are examined in fracture or thin-section they can be seen to be forms of lamellar crowntissue (¢gure 4e^ j). In most cases, the albid area occupiesa site where crystallites in successive increments oflamellar crown are not aligned. An albid e¡ect can alsoresult from hypocalci¢cation (¢gure 13f ), and may addi-tionally occur at sites of radiating prismatic structure.Such `pseudo white matter' includes Mu« ller's (1981) whitematter categories 3a^d and can usually be distinguishedby transmitted light examination under immersion oil.True white matter is cancellated in appearance and canonly be identi¢ed unequivocally by thin sectioning andexamination of etched surfaces with a SEM.

(iii) Basal tissueBasal tissue comprises the entire basal body and is often

clearly punctuated by growth striae (¢gure 3a). The tissueis so ¢nely crystalline that individual crystallites cannot bediscerned under light microscopy. In complete specimens,successive increments extend over the lower surface of thebasal body, thereby encapsulating all previous increments(¢gure 3j). However, basal tissue is the most variable of allconodont hard tissues, both between taxa and within a

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Figure 3. (a) Longitudinal section through an Sc element of Coryssognathus dubius composed of a basal body (to left) and crown (toright); the crown includes an opaque core of white matter. Specimen BU 2616, frame width 547 mm. (b) Light micrograph, and(c, j) scanning electron micrographs of a transverse section through a Pa element of Ozarkodina con£uens. Note the relationshipbetween the white matter in (b) and (c), and the variation in crystallite orientation at the crown^basal body junction in ( j).Specimen BU 2617, (b, c) frame widths 458 mm, ( j) frame width 158 mm. (d) Perpendicular arrangement of crystallites in a Paelement ofOzarkodina con£uens. Specimen BU 2618, frame width 27 mm. (e) Pre-prismatic arrangement of crystallites in a Pa elementof Scaliognathus anchoralis Branson & Mehl. Specimen BU 2613, frame width 55 mm. ( f ) Protoprismatic arrangement of crystallitesin a Pa element of Idiognathodus sp. Specimen ROM 53261, frame width 114 mm. (g) Transverse section through the cusp of a Paelement of Ozarkodina con£uens. Note the oblique orientation of crystallites relative to the bounding incremental growth lines.Specimen BU 2615, frame width 22.5 mm. (h) Arrangement of crystallites into distinct prisms which form the denticles in the freeblade of a Pa element of Mestognathus beckmanni Bischo¡. Specimen BU 2620, frame width 284 mm. (i, k) Variation in crystallitearrangement in a horizontal section through a Pa element of Ozarkodina con£uens. (i) Changing from perpendicular at the margin ofthe element, and oblique at the core of the element. Specimen BU 2621, frame width 76 mm. (k) Subvertical arrangement of crys-tallites adjacent to the core of white matter. Specimen BU 2621, frame width 118 mm.

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single taxon. For instance, the structure of the CordylodusPander basal body is known to vary from coarse spheroids(Mu« ller & Nogami 1971; Sansom et al. 1992; ¢gure 5a^ c) tolaminated (Kemp & Nicoll 1995a); Pseudooneotodus exhibitsboth spheroidal structure (¢gure 5d,e) and lamellar formwith microspherules (Sansom 1996). Some specimens ofChirognathus Branson & Mehl possesses a basal body withlamellar structure and perpendicular ¢ne calibre tubules(Sansom et al. 1994; Mu« ller & Nogami 1971, 1972), butother specimens apparently have a clearly atubular lami-nated structure (Kemp & Nicoll 1995a). Mu« ller &Nogami ¢gured a single specimen of Neocoleodus with alamellar basal body, whereas Sansom et al. (1994) haverecorded a non-lamellar basal body that includesbranching tubules. Some basal tissue is neither laminated,spheroidal nor tubular.

The ¢ne calibre tubules described from the basal bodyof Chirognathus and Neocoleodus have only rarely beenrecorded in conodont elements, whereas coarser tubuleshave been recorded in many more taxa, including allthose claimed to possess dentine tubules prior to the workof Sansom et al. (1994) (e.g. Andres 1988; Dzik 1986). Thecoarser tubules are typically 50 mm diameter (too coarseto be dentine processes) and meander throughout thebasal body.

Most basal bodies are atubular, particularly those of theorder Ozarkodinida (sensu Sweet 1988), and they usuallyoccur within concentric growth increments equivalent togrowth striae in the crown (¢gure 5f,g). The basal tissuelamellae are rarely perfectly concentric and are discontin-uous or disrupted, usually because of incorporatedmicrocalcospheres that often occupy much of the area justbelow the crown^basal body junction, and frequentlyoccupy the core of the structure (¢gures 3j and 5e, f ).Intergradation between all forms can occur within asingle taxon, and sometimes within a single specimen(¢gures 3j and 5c), indicating that all the structures arefeatures of a common tissue possibly a¡ected by the time-scale of growth. The presence of the microspherules in ahomogeneous, unstructured matrix therefore indicatesrapid growth, and the well-organized lamellar andtubular structures represent slower, ordered growth.

Reduced mineralization of the basal body is a consistentfeature of Early to Late Palaeozoic conodont elements,and many lineages have no record of a basal body. Patho-logical features of crown morphology in elements of sometaxa (e.g. Polygnathus xylus xylus Stau¡er in Nicoll (1985),text-¢g.1H,V) indicate the presence of an in£exible struc-ture, and so a basal body was certainly present in vivo; thereason for lack of preservation of the structure is unknown,

although the most likely reason is that it was not comple-tely mineralized.

By the Carboniferous, very few taxa have any record ofthe presence of a mineralized basal body.This is evident inthe Carboniferous conodonts with soft tissue preservation(Aldridge et al. 1993), and the exceptionally preserved`bedding plane assemblages' that represent the undis-turbed but collapsed remains of the feeding apparatus(Purnell & Donoghue 1997, 1998). Not one of the manyhundreds of articulated skeletal remains of ozarkodinidspossesses even the remnants of a basal body. Interestingly,although gondolellid elements (order Prioniodinida) havebeen recovered with intact basal bodies from sediments ofthe Carboniferous and later (e.g. Mu« ller & Nogami 1971,pl. 15, ¢g. 4), the many bedding plane assemblages ofNeogondolella Bender & Stoppel and Gondolella Stau¡er &Plummer (Rieber 1980; Orchard & Reiber 1996; Merrill& von Bitter 1977) possess no basal tissue. This is also trueof all recorded fused clusters. However, this bias may betaphonomic as collections from the Devonian of WesternAustralia contain polygnathid clusters with no basaltissue, whereas isolated elements from the same samplehave fully preserved basal bodies (Nicoll 1985, personalobservation).

(b) Interrelationships of the tissues during growthThe crown is known to have grown by outer apposition

because many elements display evidence of episodes ofdamage and subsequent repair (Furnish 1938; Hass 1941;¢gure 5h). The con£uent passage of incremental growthstriae between the crown and basal body indicates thatthe two structures were grown synchronously (contra Gross1957, 1960; Krejsa et al. 1990a,b) and, by inference, that thebasal body also grew by outer apposition. The innermostcore of each element therefore represents the earliestgrowth stage, and the outermost layer the latest.

It is possible to determine the growth relationshipbetween the lamellar crown tissue and the junction withthe underlying basal body. At the base of the crown, crys-tallite orientation indicates growth up and away from thejunction with the basal body (¢gure 3j). Unfortunately, thecrystallites that compose the basal tissue are too small todetermine orientation, and the growth direction can onlybe resolved by inference. However, the nature of thegrowth relationship between the crown and the under-lying basal body indicates a mirroring of the pattern ofgrowth apparent in the crown.

The two basic units that compose a typical conodontelement therefore grew in opposing directions relative tothe crown^basal body junction (¢gure 1c, part i, and d;

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Figure 4. (a,b) Longitudinal section through an Sc element of Ozarkodina con£uens. The white matter cores are bound by a thinsheath of lamellar crown tissue (arrowed) which expands orally. Specimen BU 2622, (a) frame width 121 mm, (b) frame width233 mm. (c) Cell-shaped space incorporated within the ¢ne-grained groundmass of white matter from a Pa element of Ozarkodinacon£uens. Specimen BU 2615, frame width 26.7 mm. (d) White matter core of an Sc element of Ozarkodina con£uens. The tissue isdominated by vertically orientated tubules, many of which branch in the plane of the section. Specimen BU 2619, frame width50 mm. (e^g) Longitudinal section through an element of Cordylodus angulatus. Note the relationship between the opaque areas in (e)and the scanning electron micrograph in ( f ), which indicates a complete absence of true white matter. The opaque areas probablyresult from optical e¡ects produced by the prism bounadries in (g). Specimen BU 2623, (e, f ) frame widths 1541 mm, (g) framewidth 200 mm. (h^j) Longitudinal section through an element of Ligonodina sp. Bassler. As in (e^g), despite the presence of opaqueareas in (h), (i) reveals an absence of true white matter resulting from interfering crystallite arrangement in ( j). Specimen BU2624, (h, i) frame widths 805 mm, ( j) frame width 90 mm.

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cf. Sansom (1996), although his methodology followed apriori interpretations of the component tissues). Thispattern alone is evident in many coniform conodontelements that lack white matter, but elements with analbid component are far more complex structurally andtheir growth is much less well understood. Given theirantiquity and importance in our understanding of theearly evolution of vertebrates and their skeletons, this isan important area of investigation.

Although the £anks of white matter cores are usuallyplanar (¢gure 4a,b), more rarely they are stepped (¢gure5i^k), each step coinciding and con£uent with incrementallayers in the surrounding crown tissue, thereby providingan insight into the relationship between these two tissuesduring growth. This arrangement appears to indicate thatthe two tissues grew synchronously and at the same rate.Examples where increments of the lamellar crown passconformably into white matter have been ¢gured manytimes (e.g. Barnes et al. 1973a, ¢g. 6.6; Sansom et al. 1992,¢g. 3e), but in ¢gure 5i^k the white matter is bounded bythe growth increments. The length of the long tubuleswithin the white matter core greatly exceeds the thicknessof individual increments of the adjacent crown tissue(¢gures 4a and 5l). This indicates that growth of whitematter was more continuous than the punctuated growthof lamellar crown, and that the control over the secretionof the two tissues was distinct. Because of the outerappositional mode of growth of the surrounding tissue, itis likely that white matter also grew in this way. Thepolarized nature of the cell-shaped cavities within whitematter therefore suggests that the secreting cells retreatedorally, usually ahead of the mineralizing front, and henceonly the cell processes (the tubules) were commonlyincorporated into the mineralized matrix. Furthermore,the polarization of the shorter, perpendicular tubulesand attached cavities indicates that they grew away fromtheir junction with the lamellar crown tissue. Thiscontrasts strongly with the direction of growth of thelamellar crown tissue, which from the orientation of thecrystallites was usually perpendicular (¢gure 5j,k) orsub-perpendicular (¢gure 3g) to the £anks of the whitematter cores and long axes of the denticles.

White matter was therefore secreted as a continuous coreof mineralized tissue, partly controlled at the margins bythe secretion of lamellar crown. White matter, therefore,forms a series of upwardly tapering collars around, andmerging with, the core (¢gure 6). Although secretion ofthe two tissues was independently controlled, the lack of a

plane of weakness, such as at the junction of the crown andbasal body (¢gure 5g), suggests that mineralization of thetwo tissues was simultaneous rather than staggered.

5. PATTERN: GROWING THE CONODONT SKELETON

Although I have outlined the morphogenetic pattern ofintergrowth between the two structural units and threecomponent tissues comprising most conodont elements,this goes little further than explaining the morphogenesisof the conventional perception of a simple coniform

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Figure 5. (a^c) Longitudinal section through an Sc element of Cordylodus angulatus. The basal body is dominated by spheruliticstructure, each spherule indicated by an extinction cross in cross-polarized light (b). Specimen BU 2614, (a, b) frame widths644 mm, (c) frame width 204 mm. (d, e) Transverse section through an element of Pseudooneotodus sp. in plane-polarized light (d) andcross-polarized light (e). The basal tissue of this specimen also exhibits a spherulitic structure. Specimen BU 2625, (d) frame width531 mm, (e) frame width 337 mm. ( f, g) Longitudinal section through a Pa element of Ozarkodina con£uens with a basal body exhi-biting lamellar structure. Note the con£uence of growth increments between the basal tissue and lamellar crown tissue in (g).Specimen BU 2626, ( f) frame width 380 mm, (g) frame width 72 mm. (h) Pa element of Ozarkodina gulletensis Aldridge photomicro-graphed under oil. This element exhibits a conspicuous internal discontinuity with evidence of subsequent repair. Specimen lost,frame width 225 mm. (i^l) Pa element of Ozarkodina con£uens photomicrographed under oil. (i) Ventral portion of the elementviewed in plane polarized light, the denticle in the centre of the frame exhibits a staggered ventral margin where the increments ofwhite matter and lamellar crown tissue are clearly con£uent. Specimen BU 2627, frame width 453 mm. ( j, k) Denticle in (i) athigher magni¢cation. Specimen BU 2627, frame widths 88 mm. (l) Tubules and cell-shaped cavities within the white matter.Specimen BU 2627, frame width 35 mm.

Figure 6. Diagrammatic representation of relative growth ofwhite matter and surrounding lamellar crown tissue.

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element, or a single denticle in a complex element. Mostconodont elements are far more complex and theirmorphogenesis can only be explained by studyingrecurrent patterns of growth. This study has revealed arestricted number of morphogenetic patterns expressed bycomplex elements; these are described primarily withreference to conodonts of the order Ozarkodinida, butsome evidence from members of the orders Prioniodinida,Prioniodontida and Proconodontida is included.

Di¡erent groups of conodonts have followed di¡erentmorphogenetic pathways in the construction of theirfeeding elements and, as a result, there is a great diversityof element morphology. However, a number of elementmorphologies have been converged upon by di¡erentmorphogenetic paths; these can only be discriminated byconsidering pattern formation in reconstructing conodontphylogeny.

(a) Ramiform element morphogenesis(i) Type I

This ¢rst group includes taxabearing elements composedof numerous isolateddenticles.Thebest source of evidence isPromissum pulchrum Kovacs-Endro« dy, a balognathid with a19-element apparatus from the late Ordovician Soom Shaleof SouthAfrica,which is foundalmostexclusively inbeddingplane assemblages (Theron et al. 1990; Aldridge et al. 1995;¢gure 7a^d). The ramiform elements of Promissum pulchrumconsist of denticles that are united by a single underlyingstructure that appears to be neither part of the crownnor the basal body (¢gure 7a). The denticles themselvesare variable; those on the (conventional) posteriorprocesses are structurally di¡erentiated into tri-denticu-late units (¢gure 7a,b); denticles on other processes arestructurally distinct (¢gure 7a,c,d; Theron et al. 1990). Inboth cases, each denticle possesses a distinct crown andbasal body (¢gure 7b,d), indicating that they grew inde-pendently of adjacent denticles (¢gure 8a). Inontogenetically older specimens, the cusp and adjacentdenticles exhibit a tendency to fuse at the margins oftheir crowns and their basal bodies. Each denticle there-fore appears to be homologous with the conventional viewof a simple coniform element, although it represents onlypart of a complex element. It is likely that each denticlewould have been regarded as a single element if foundonly in a discrete element collection. Thus, Nicoll (1982)appears to have been correct in interpreting fused clustersof hundreds of simple cones in association with Pelements of Icriodus Branson & Mehl as component denti-cles comprising multidenticulate elements. Van denBoogaard (1990) and Miller & Aldridge (1993) reacheda similar conclusion in their interpretations of the rami-form elements of Coryssognathus Link & Druce.

(ii) Type IICarniodus Walliser is a Silurian conodont genus of

unclear a¤nity (family 6, order unknown of Aldridge &Smith (1993)). Like the ramiform elements of type I,Carniodus grew many of its denticles as morphogeneticallydistinct units (¢gure 8b), but unlike type I, the denticleson Carniodus ramiform processes are compound struc-tures (¢gure 7e). Each of the denticle units is de¢ned bya rostral and/or caudal border with adjacent units,conspicuous only in transmitted light (¢gure 7f,h, j ).Each of the units has its own basal cavity, and iscomposed from a distinct crown and basal body (¢gure7f,h, j ), indicating that each of the units grew indepen-dently. Unlike type I elements, the crowns of type IIelements were entirely fused prior to growth of thesubsequent unit. New units began to grow separatelyfrom the rest of the element, usually some distance caud-ally (¢gure 8b). The unit began to grow equally inrostral and caudal directions until eventually it reachedthe caudal edge of the preceding unit. Later incrementswould then envelop both the new unit and the entirepre-existing element, leaving the join between successiveunits imperceptible on the surface of the crown or basalbody.

Carniodus possesses a very characteristic, repetitivedenticulation that relates directly to the underlyingmorphogenetic units (¢gure 7e, f ). The basal cavity doesnot appear to be directly linked with any speci¢c denticlewithin the repeated unit, although the conspicuously largedenticle may be considered the cusp of each unit. Thebasal cavities instead relate to the growth of each morpho-genetic unit as a whole. Each of the denticles in a Carnioduselement cannot, therefore, be considered equivalent to thedenticles of elements conforming to type I growth, whichare instead homologous with each unit of type II growth.Denticle formation and addition within these units followsa pattern typical of type III elements (¢gure 8b; seebelow). This same pattern of growth is also found in theramiform elements of taxa including AmorphognathusBranson & Mehl and Prioniodus Pander. Alternatively, inearly representatives of Cordylodus (e.g. C. angulatusPander), the crown of each unit remains undi¡erentiated,each denticle composed of a distinct crown and basal body(e.g. Nicoll 1991).

Microzarkodina Lindstro« m also exhibits the type IImorphogenetic pattern in all but its M elements. In thisgenus, the successive units consist simply of a largeproximal and small distal denticle. The smaller denticle issubsequently encapsulated during growth of the nextmorphogenetic unit, resulting in an external pattern ofdenticulation more akin to Ozarkodina Branson & Mehland type III growth.

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Figure 7. (a^d) Details of elements of Promissum pulchrum. (a) Sc element with a posterior process composed from individual multi-denticulate units (b), and lateral processes composed from individual denticles (c, d). (a, b) Specimen C424, frame widths 21 234 mmand 2037 mm, respectively; (c, d) specimen C679, frame widths 836 mm and 495 mm, respectively. (e, f, h, j ) Sc elements of Carniodussp. Note the optical distinction between the multidenticulate units comprising these elements; each unit includes a distinct basalcavity. (e, f ) Specimen BU 2628, frame widths 1375 mm and 438 mm, respectively; (h) specimen BU 2629, frame width 288 mm; ( j )specimen BU 2630, frame width 294 mm. (g, i, k^m) Sc elements of Ozarkodina con£uens. (g, i) Plane-polarized light and cross-polar-ized light, respectively. Specimen BU 2631, frame widths 562 mm. (k, l) Growth cavities along the ventral margin of the element.Specimen BU 2632, (k) frame width 1406 mm, (l) frame width 225 mm. (m) Scanning electron micrograph of an etched groundsection exhibiting distinct white matter cores within the lamellar crown tissue. Specimen BU 2633, frame width 1098 mm.

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(iii) Type IIIThe ramiform elements of Ozarkodina con£uens (Branson

& Mehl) bear an undi¡erentiated denticulation pattern,with each denticle almost entirely composed of whitematter and surrounded marginally and aborally by asmall amount of lamellar crown tissue (¢gure 9a).Growth increments are clearly apparent within the crowntissue but are only rarely traceable through the blocks ofwhite matter (¢gures 7g,i,k,l,m and 10a,b). Unlike thegrowth patterns outlined above in types I and II, thetype III growth pattern produces a compound structurethat extends processes by marginal accretion of individualdenticles (¢gure 9a). The ¢rst stage of growth of anindividual denticle is marked by an evagination of anincremental layer of crown tissue at the distal extremityof the process. The evagination encloses a hollow cone-shaped, distally tapering cavity with step-shapedmargins representing the abutment of surrounding micro-lamellae, and crowned by an all-enveloping ¢nal layer(¢gures 7l and 10a,b). This is succeeded by a series ofthick growth increments encapsulating similar cone-shaped cavities. The successive cone-shaped cavities orgrowth cavities' are stacked one upon another, butaligned in an arcuate, distally convex pattern (¢gures 9aand 10a,b). The growth of an individual denticle ¢nisheswith a ¢nal phase of white matter secretion. The ¢rstpoint of denticle formation, enclosing the ¢rst cavity, isclose to the ¢rst point of white matter secretion becausegrowth is concentrated in an oral, and not distal, direc-tion (as in type IV; ¢gure 10a,b). No specimens have yetbeen discovered where the growth cavities contain any

mineralized tissue. This category also includes elementsof Plectodina', the putative ancestor of all ozarkodinids(Sweet 1988).

Type III growth also occurs in many of the taxa onceplaced within the now defunct order Neurodontiformes.Although the elements appear to have grown by marginalaccretion, such taxa remain histologically distinguishablefrom other euconodonts, and the separate classi¢cation of asubset of the defunct order may well be biologically valid. Inaddition to the more obvious Ordovician forms, manyMiddle and Late Palaeozoic forms retain this uniquehistology, particularly taxa that are assigned to the orderPrioniodinida (sensu Sweet 1988): e.g. Idioprioniodus Gunnell,Cryptotaxis Klapper & Philip, Ellisonia (cf. von Bitter &Merrill 1983). The structure of the crown di¡ers from mostconodonts in its `¢brous' nature; growth increments arepresent but very faint (¢gure 4h^ j). The tissue is dominatedby elongate ¢bre-like crystals (¢gure 4j) which can reach20^30 mm in length, and their arrangement is morecomplex than that seen in any other group of conodonts.Early growth, and growth along the axes of individualdenticles, exhibits a divergent arrangement of crystal ¢bres;subsequent growth records a reversal in arrangement of the¢bres so that they converge distally (note the subtle changein crystal ¢bre orientation to the left of ¢gure 4j). It is thisarrangement of crystallites that produces Mu« ller & Noga-mi's (1971; Mu« ller 1981) `M'-shaped type 3D white matter.Clearly it is not true white matter.

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Figure 8. (a) Growth type I typi¢ed by Promissum pulchrumramiform elements where individual denticles grew synchro-nously. (b) Growth type II typi¢ed by Carniodus ramiformelements where the repetitive sets of denticles graduallybecame incorporated into the rest of the element as itcontinued to grow.

(a)

(b)

Figure 9. (a) Type III growth typi¢ed by Ozarkodina ramiformelements where new denticles were added periodically duringmarginal secretion of lamellar crown tissue. Denticle genesis was¢rst instigated by evagination of normal lamellar growth andincorporation of a `growth cavity'. (b) Type IV growth typi¢edby gnathodid ramiform elements where denticles were addedcontinually during marginal accretion of crown tissue. The repe-titive denticulation results from di¡erentiation of the denticles.

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(iv) Type IVThis group includes gnathodids, Cavusgnathus Harris &

Hollingsworth, Vogelgnathus Norby & Rexroad, LochrieaScott, polygnathids, some palmatolepids and at least somecyrtoniodontids (e.g. Phragmodus Branson &Mehl). Most ofthese families andgeneraarederived fromOzarkodina (Sweet1988) but display a more complicated morphogeneticpattern of growth (¢gure 9b). The ramiform elements aregenerally much more elongate than those of their ancestorand possess a di¡erentiated pattern of denticulation,similar to that of Carniodus but apparently achieved via adi¡erent pattern of formation.The elements are composedpredominantly of lamellar crown tissue, and white mattergenerally becomes sparser fromMiddle to Late Palaeozoic.The denticles of palmatolepids and polygnathids are almostentirely composed of white matter extending deep into theelements, whereas the denticles of gnathodids usually onlyinclude white matter in the portion of the denticle emergingfromthemainbodyofanelement, andeventhenonlyduringlate ontogeny (¢gure10c).

Transmitted light clearly reveals the complex growthhistory of type IV elements (¢gure 10c^ j). Cone-shapedgrowth structures of the type seen in Ozarkodina arepresent, but in this case occurring in sets relating directlyto the overlying denticulation (¢gure 10c, j). The ¢rstevagination is palm-shaped (¢gure 11a,b), each digitrelating to, and ultimately resulting in, a single andspeci¢c denticle (¢gures 10j and 11g). The denticles withineach unit are distinct optical units, traceable as discreteprisms through ontogeny (¢gure 10f,i). During the onto-geny of each denticle set, the angle of inclination of eachdenticle increases progressively from nearly parallel withthe long axis of the element to the erect position moretypical of `mature' denticulation (¢gure 10j). This isexpressed in surface morphology by a transition fromsuberect to erect denticulation proximally (¢gure 10c,e).Elements conforming to type IV growth were constantlyundergoing morphological change by addition of newdenticles. This condition is di¡erent from type III growthwhere elements underwent enlargement between episodesof denticle addition.The long axis of a process in a type IVelement was the main axis of growth from which thedeveloping denticle sets diverged. The progressivedevelopment of the individual denticles within each unitcan be traced by the presence of the cone-shaped cavities(¢gure 10j). After the axis of growth of the large denticlediverged from the main axis of growth of the process, thegrowth axes of the smaller denticles diverged in turn fromthe growth axis of the larger denticle (¢gure 10e,f,g,i,j).The growth axes then translated their orientation into aprogressively higher angle relative to the process. As inOzarkodina, the proximal margins of the growth structuresare aligned in a convex-distal arrangement.The last cone-shaped cavity occurs exactly at the point at which whitematter secretion ¢rst occurred (¢gures 10g, j and 14e,g).The large denticle represents the distal extremity of eachunit.

Early growth distally occurs synchronously with lategrowth proximally. Because of the pattern of growthexhibited by type IV taxa, each unit of denticulation isconsidered equivalent to each unit in taxa with type IIgrowth, and to an individual denticle in taxa with types Iand III growth.

(b) Morphogenesis of elements in P positionsElements ¢lling P positions within the apparatuses of

complex conodonts can be broadly divided into blade-likeandplatform-bearingmorphologies and,more rarely, rami-form morphologies (prioniodinids, see earlier). Most, if notall platform-bearing P elements are essentially modi¢edtype III ramiforms and therefore exhibit similar growthpatterns. However, some attempts at platform constructionaremerelyelaborations of type III patternof element forma-tion. Instead of arranging denticles linearly, P elements ofthis type are composed of three-dimensionally arrangeddenticles; in Promissum, for example, these remain structu-rally distinct, but in Coryssognathus they are gradually fusedtogether during ontogeny (cf. van den Boogaard 1990).Despite the more variable morphology exhibited byelements ¢lling Pa positions, the morphogenetic patternsare much more conservative than those exhibited byelements in S andMpositions.

(i) Blade morphogenesisThe morphogenesis of blade-like elements and the blade

portion of platform-bearing elements is very similar totype III ramiform growth and is typi¢ed by the Pelements of Ozarkodina. Initial growth of the crowninvolved only lamellar crown tissue and very soonafterwards white matter secretion began. Denticles formedas distinct optical units as in ramiform elements.Maximumgrowth was in dorsal and ventral directions and newdenticles are added marginally by localized evagination ofa layer of lamellar crown tissue.Whitematter forms the coreof all denticles in juvenile elements, but later growth, whichmodi¢es the shape of an element, is generally restricted tothe ventral portion of the element and is devoid of whitematter. During late-stage growth, white matter depositionis halted and the cores are enveloped by layers of lamellarcrown tissue. The tips of denticles forming dorsal or mid-oral surfaces are generally devoid of crown tissue, althoughthis condition may be due to attrition resulting fromfunction rather than re£ecting a pattern of growth.The blade portions of platform elements were

constructed by a pattern of growth identical to that ofwholly blade-shaped elements (¢gure 9a). All thefollowing patterns are derived from this.

(ii) Type A platformsThis ¢rst category of platform morphogenesis represents

a modi¢cation of the standard blade pattern (¢gure 12a).In taxa such as Idiognathodus Gunnell (sensu Baesemann1973; Grayson et al. 1991), Gnathodus Pander and IcriodellaRhodes the platform is restricted to the dorsal portion ofthe element, and the internal construction of its crownincorporates a series of cavities within the lamellae, alongthe main growth axis of the element (¢gure 11d^ i). Thecavities mimic the arrangement of cone-shaped cavitiespresent in ramiform and blade-shaped elements, wherethe proximal margins of the cavities are aligned inascending fashion, with the structure ultimately produced(denticle or ridge; ¢gure 11e,h). However, these cavities arenot wholly encapsulated by the crown; they extend downto the base of the crown where they open into the basalcavity through a restricted opening which can often beobserved in SEM (¢gure 11e,g). The upper margins of thecavities are aligned in an undulating arrangement,

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directly re£ecting the overlying ridge morphology (¢gure11e,h).

In almost all platform elements that bear transverseridges, the ridges occur in pairs on either side of a centraltrough which directly overlies the axial cavities, and variesin its development from a large dividing depression to anarrow slit. The ridges have a structure similar to denti-cles, being formed as discrete and homogeneous prismsthat are centred about the apices of each set of growthcavities' (¢gure 11h,i). The symmetry or asymmetry ofeach prism is a direct re£ection of the shape of the over-lying structure; whether or not the prisms merge at theirmargins is dependent on whether the ridges are of lowrelief (e.g., gnathodids; ¢gure 11h), or whether the ridgesare more peg-like (e.g. Icriodella; ¢gure 11e).

Paired platform ridges occur in a number of di¡erenttaxa, particularly among Middle and Upper Carboni-ferous ozarkodinids. The signi¢cance of this is borne outby examination of the juvenile component of the internalgrowth record. For instance, the early growth stage of aCavusgnathus platform reveals an original blade-likemorphology (¢gure 13a^ c; and see Purnell (1992) for theontogeny of Taphrognathus Branson & Mehl, a closelyrelated taxon). Prismatic structure and maximum growthcoincide with the axis of the blade (¢gure 13b; in trans-verse view). However, after relatively few increments, theaxis of primary growth bifurcates into two distinct growthaxes, oblique to the original axis (¢gure 13c). The crystal-lites in subsequent layers of crown tissue are organized intwo prisms, disposed about the new primary growth axes,and with an intervening area which is aprismatic, whereall crystallites are organized approximately parallel toeach other, perpendicular to the outer surface. Ontoge-netic bifurcation of denticles appears to be the mainmethod of platform formation within type A platform-bearing taxa, and may have implications for deducingtheir evolutionary origin.Additional nodes may be incorporated into the plat-

form. Like the ridges, their internal structure is opticallydistinct from the surrounding crown tissue. Cross-crystal-lographic arrangement of the prisms of crystallites withinthe platform results in an albid appearance in re£ectedlight.True white matter is usually absent from the platformbut may occur in the blade (if one is present).

(iii) Type B platformsThis category includes such taxa as gondollelids, palma-

tolepids, polygnathids, and Siphonodella Branson & Mehl(¢gure 12b).They di¡er from type A in that their platformsare formed by lateral expansion of the incremental layers

of lamellar crown tissue (¢gure 13e,g). The axes of growthare dorsoventral in most of these elements (and a thirdlateral process in some taxa, e.g. palmatolepids), andcontain growth cavities strongly resembling those alongthe growth axis of type A platforms (¢gure 13d). Thesecavities are generally larger than their type A counter-parts and are overlain by fewer layers of crown tissue.

Away from the main axes of growth, successive incre-ments include patches of poor mineralization and oftenenclose large cavities, particularly in areas of maximumgrowth on the outer margins of elements (¢gure 13e, f ).As a result, prominent growth increments vary in thick-ness from a few microns to 30 or 40 microns. The outersurfaces of each of the increments in the areas ofmaximum growth parallel surface morphology.The internal structure of surface morphological struc-

tures such as ridges and nodes also di¡er from those oftype A elements that bear prismatic structure. Surfacemorphological features are produced by site-speci¢cincreases in the thickness of layers of the enamel relativeto adjacent regions of the enamel within these individuallayers (¢gure 13e).

Like type A platforms, type B platforms also lack truewhite matter within the platform although they exhibitareas of albid appearance in re£ected light. White matteris present in the free blade and carina.

The most conspicuous di¡erence between surfacemorphology of type A and B platforms is the absence andpresence of a carina, respectively. The platform in type Aplatforms often lack a carina because the denticles thatcomprised the dorsal blade in juvenile (and ancestral?)forms were split ontogenetically to form the paired ridgescommon to this element type. Type B elements retain aprominent carina throughout ontogeny because the denti-cles perform no role in formation of the platform.However, some forms appear to combine both morphoge-netic patterns, e.g. Gnathodus bilineatus (Roundy). Somespecies of Cavusgnathus, a typical type A platform, alsoexhibit evidence of a combination of the two growth typeswhere a small carina at the dorsal-most tip of the Paelement is developed in specimens representing late onto-geny. All work so far suggests that beside minorelaborations, such as platform development, pattern forma-tion is the same in all elements in a given apparatus.

6. PROCESS: INTERPRETATION OF THE HARD

TISSUES

Considering the widely diverging views of conodonta¤nity expressed over the past 140 years, there have been

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Figure 10. (a, b) Ozarkodina con£uens Sc element viewed (a) in plane-polarized light, and (b) in di¡erential interference contrast.Note the conspicuous growth cavities along the ventral margin of the element. Specimen BU 2634, frame widths 562 mm. (c) Selement of Idiognathodus photomicrographed under oil and in di¡erential interference contrast. Note the conspicuous growthcavities within the main body of the element, each set of growth cavities relate to the overlying sets of alternating denticulation.Specimen ROM 53262, frame width 1894 mm. (d^i) S element of Mestognathus beckmanni. (e, f ) Photomicrographed in plane-polarized light and cross-polarized light respectively. Note the extinction pattern exhibited by the prisms which represent thegradual development of denticles. Specimen BU 2635, (e) frame width 1894 mm, ( f ) frame width 1660 mm. (i) Detail of the caudalportion of the element in cross-polarized light. Specimen BU 2635, frame width 625 mm. (d, g, h) Detail of denticle structure.Specimen BU 2635, (d) frame width 225 mm, (g) frame width 225 mm, (h) frame width 225 mm. ( j) S element of Idiognathodusphotomicrographed in plane-polarized light and di¡erential interference contrast. Note the relationship between the sets of growthcavities and overlying alternating denticulation. Specimen ROM 53263, frame width 425 mm.

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surprisingly few competing hypotheses to explain elementhistology. Most authors have contended that the hardtissues represent forms homologous to those of vertebratesand, except for a few o¡-beat interpretations (Zittel &Rohon 1886; Quinet 1962b; Fahlbusch 1964; Bischo¡1973), all other considerations of conodont hard tissuehistology are refutations of the vertebrate hypothesis(Kemp & Nicoll 1995a,b, 1996; Schultze 1996).

Conodonts are now widely regarded as craniatesprobably most closely related to the extant agnathans(Aldridge et al. 1993; Forey & Janvier 1994; Gabbott et al.1995; Janvier 1995, 1996a,b), although some authorsbelieve that conodonts represent a more primitive condi-tion akin to amphioxus (Kemp & Nicoll 1995a,b, 1996;Nicoll 1995; Pridmore et al. 1997). However, there iscurrently consensus over the chordate a¤nity of conodontsand it is in this context that the following interpretation ofconodont hard tissues has been considered.

(a) Lamellar crown tissueAmong protochordates only the ascidiacean and

soberacean tunicates are able to secrete biomineralizedtissues (Lambert et al. 1990). Amongst these two groups,phosphatic biomineralization is largely restricted toamorphous deposits and in some cases dahllite. However,even this one record of mineralized phosphate may bequestionable because of the inherent instability ofamorphous calcium phosphate (e.g. Lowenstam & Weiner1985). In either case, lamellar crown tissue is clearly notcomposed from dahllite (Pietzner et al. 1968).

Although myxinoids are capable of secreting non-skeletal calcium phosphate in the form of statoliths andstatoconia (Carlstro« m 1963), this system is also unlikely tobe responsible for conodont hard tissues. Agnathanstatoliths are composed from an amorphous (polyhy-droxyl) calcium phosphate, which is highly unstable anddissolves in a solution of pH 8 or less (R. W. Gauldie,personal communication). Lamprey biomineralization issimilarly restricted to the formation of statoliths, althoughunder the right conditions (in vivo or in vitro) lampreys arecapable of skeletal biomineralization, in particular, calci¢-cation of cartilage (Langille 1987; Langille & Hall 1993;Bardack & Zangerl 1971).Considering the range of chordate hard tissues, the

only possible homologues of lamellar crown tissue areenameloid and enamel. Both enamel and enameloid arehypermineralized, but enameloid crystallites are gener-ally much larger than those of enamel, the crystallinestructure of which is punctuated by incremental growth

lines. Enamel crystallites are aligned in a preferred orien-tation, which is usually perpendicular to the growingsurface, although this alignment can vary considerably.Enameloid crystallites, which more usually resemble long¢bres, are not always aligned preferentially and can rangefrom a completely random arrangement (e.g. tangled¢bre enameloid; Preuschoft et al. 1974, pl. 8, ¢g. d) tohighly ordered woven and interwoven sheets (e.g. parallel¢bre enameloid; Preuschoft et al. 1974, pl. 8, ¢g. e).Lamellar crown tissue most closely resembles enamel,and I interpret them as homologous. This conclusion hasbeen reached by several authors in the past (e.g. Dzik

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Figure 11. (a^c) Etched ground-section of an S element of Mestognathus beckmanni. The growth cavities along the axis of theelement can clearly be seen, and individual denticles can be traced throughout growth as distinct prisms from inception. SpecimenBU 2636, frame width of (a) 410 mm. (b) Palm-shaped growth cavity representing one of the ¢rst growth stages of a forming set ofdenticles, each digit representing a distinct prism and denticle. Specimen BU 2636, frame width 32.5 mm. (c) Growth cavityrepresenting the inception of a new set of denticles at the caudoventral margin of the element. Specimen BU 2636, frame width93 mm. (d^g) Etched, arti¢cially fractured specimen of a Pa element of Icriodella inconstans Aldridge. (e) Growth cavities in sets alongthe dorsoventral axis of the element; each set relates to the overlying denticulation. Specimen BU 2637, frame width 388 mm. (d)Crystallite arrangement adjacent to the growth cavities. Specimen BU 2637, frame width 47 mm. (f ) Perpendicularly orientedcrystallites forming the walls of the growth cavities. Specimen BU 2637, frame width 27 mm. (g) Oblique view of the basal marginshowing that the growth cavities are open to the basal body (not preserved). Specimen BU 2637, frame width 185 mm. (h, i) Etched,arti¢cially fractured section of the platform component of a Pa element of Idiognathodus sp. (inset) exhibiting sets of growth cavitiesrelating to the overlying denticulation and intervening preprismatic structure. (h) Specimen ROM 53264, frame width 267 mm,width of inset 736 mm. (i) Specimen ROM 53264, frame width 153 mm.

Figure 12. (a) Growth type A typi¢ed by the platforms ofgnathodid Pa elements. The junction between the crown andthe (unpreserved) basal body is irregular, the basal bodyinvading the crown between successive increments of lamellarcrown tissue. The paired ridges are often derived from di¡er-entiation of individual denticles in juvenile stages. (b) Growthtype B typi¢ed by the platforms of Palmatolepis Pa elements.The crown^basal body junction is similarly irregular, but thecrown is formed by exaggerated lateral growth, often resultingin hypocalci¢cation within the enamel.

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1986; Burnett & Hall 1992; Sansom et al. 1992), butheavily criticized (e.g. Blieck 1992; Kemp & Nicoll 1993,1995a,b, 1996; Schultze 1996; Forey & Janvier 1993;Janvier 1995, 1996a,b).

Although Forey & Janvier (1993) felt that the apparentextreme variation' of crystallite orientation in conodontlamellar crown tissue was irreconcilable with enamel, it isnot without parallel in known enamels (e.g. Smith 1989),although the sub-parallel arrangement of crystallites isunusual. The dearth of comparable microstructures inother vertebrates probably results from the lack ofenamel-bearing structures of comparably intricatemorphology. Although other vertebrates may producedental and other structures that are as intricate, suchelements invariably lack enamel and are instead largelycomposed of various types of enameloid.

The presence of prismatic structure and elaboratesurface ornament in some conodont taxa indicates thatthe enamel organ responsible for secretion of the tissuewas relatively sophisticated, capable of controllingmineral secretion and mineral alignment in any onesite, and of producing textures comparable with thesurface ornamentation of the tooth enamel of gnathosto-mous ¢sh (cf. Smith 1989, text-¢g. 5, Laccognathusbiporcatus Gross).

(b) Basal bodyInterpretations of basal tissue have varied more than

those of any other tissues of conodont elements. Theyrange from bone (Barskov et al. 1982), to globular calci¢edcartilage (Sansom et al. 1992), and various dentines (Dzik1986; Sansom et al. 1994; Sansom 1996), to a mineralisedextracellular matrix, organised like connective tissue orthe inner core of embryonic or chordate notochord'(Kemp & Nicoll 1995a, p. 238).

The last interpretation warrants separate discussionbecause it is so conspicuously di¡erent from the othercompeting hypotheses. Kemp & Nicoll (1993, 1995a,b,1996) have followed earlier work (FÔhraeus & FÔhraeus-Van Ree 1987, 1993) concerned with organic remnantsretrieved after acid dissolution of conodont elements. Theorganic matrices retrieved from the basal tissue of Prio-niodus amadeus Cooper and Cordylodus sp. form the basis ofthis interpretation and are shown in ¢g. 3a^e of Kemp &Nicoll (1996) and pl. 1, ¢gs 4, 7, 8, pl. 2, ¢gs 9^12 of Kemp& Nicoll (1995a). It is remarkable that organic remnants orreplacements of original soft tissues could be preserved,but the least remarkable factor is the low ¢delity of preser-vation. Indeed the preservation is such that the organicremnant cannot be compared with any speci¢c moderntissue with any con¢dence because of the lack of distin-guishing characters. The organic remnant does, however,

compare well with connective tissue, which led to Kemp& Nicoll's interpretation of conodont basal tissue as theirhypothetical extracellular mineralised matrix' tissue;they pro¡er no homologous tissue from any animal extantor extinct.

The divergent growth relationship between the basaltissue and the enamel supports interpretations of basaltissue as bone, mineralized cartilage or dentine. All threetissues are involved in odontogenesis in extant and extinctvertebrates, are neural crest derived, and can often occurtogether with enamel/enameloid as a result of epithelial^ectomesenchymal interaction. Enamel overlying dentine isa pattern characteristic of the vertebrate dermal skeletonand, contrary to Kemp & Nicoll (1995a) and Schultze(1996), enamel overlying bone is not unparalleled amongthe vertebrates (Smith 1979; Sire 1994). Although hypothe-tically possible, no examples have been reported whereenamel can be observed directly overlying cartilage.

Sansom et al. (1994) contended that during the Ordovi-cian acme of vertebrate evolution (Halstead 1987) theconodonts, like all the other armoured agnathan groups,were experimenting with di¡erent tissue combinations.However, the other vertebrate groups were expressingthis experimental episode in the production of variablystructured dermal armour. Based on new histologicalevidence presented here and elsewhere, the scenariopresented by Sansom et al. (1994) would be extrapolatedto suggest that conodonts were directly substitutingdi¡erent tissues in a homologous site of an otherwiseentirely unchanged mineralized skeleton, sometimeswithin individual species. Clearly, this is highly unlikely.

The case for the interpretation of conodont basal tissueas bone, as made by Barskov et al. (1982), was based on thepresence of concentric hollow spheres and tubules within alamellar matrix, respectively suggested to be osteocytelacunae and vascular canals. However, the putative celllacunae bear little resemblance to structures in bone; thespheres are in¢lled, bear no processes and are better inter-preted as components of dentine. Evidence for thepresence of vascular tubules is also very poor, althoughstructures similar to these have been described in otherconodont taxa (e.g. Problematoconites Mu« ller in Andres(1988), and Semiacontiodus Miller in Dzik (1986)).

The case for the interpretation of basal tissue asmineralized globular cartilage is considerably stronger.Smith et al. (1987), Smith (1990) and Sansom et al. (1992)have all compared the basal tissue of C. angulatus (¢gure5a^ c) to the globular calci¢ed cartilage found in theHarding Sandstone vertebrate Eriptychius Walcott(Denison 1967). However, Smith & Hall (1990) havepostulated that cranial exoskeletal cartilage is always asso-ciated with bone, which, as we shall see below, was

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Figure 13. (a^c) Etched transverse section through a Pa element of Cavusgnathus altaHarris & Hollingsworth in progressively highermagni¢cation. Note the change from blade to paired-ridge morphology during ontogeny. Specimen BU 2638, (a) frame width436 mm, (b) frame width 150 mm, (c) frame width 76 mm. (d) Etched, arti¢cally fractured section through a Pa element of Palmato-lepis sp. (inset). Specimen BU 2639, frame with 472 mm, inset width 967 mm. (e, f ) Etched, arti¢cally fractured section through a Paelement of Palmatolepis sp. (e) Relationship between structure and morphology. Specimen BU 2640, frame width 285 mm. (f )Hypocalci¢cation within lamellar crown tissue. Specimen BU 2640, frame width 42 mm. (g, h) Transverse section through a Paelement of Palmatolepis sp. photomicrographed in plane-polarized light with di¡erential interference contrast. (g) Entire element.Specimen BU 2641, width 1523 mm. (h) Detail of the basal body exhibiting large internal cavities which indicate that the basaltissue was secreted both from the inside and outside. Specimen BU 2641, frame width 562 mm.

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evidently lacking in conodonts. Furthermore, as Sansom etal. (1992, p.1310) admitted,`it is possible that other miner-alisation processes could produce spherulitic structuressuch as these'.The strongest case is for an interpretation of conodont

basal tissue as dentine. Dentine exhibits a great variationin structure, including forms that do or do not includecells, i.e. mesodentine, semidentine and orthodentine (forreviews, see Òrvig 1967a; Smith & Hall 1990). Variationsalso occur within these categories due to factors such asenvironmental and physiological stress (e.g. Appleton1994). Although the claims of dentine in conodontelements by Dzik (1986) and Andres (1988) are equivocal,the identi¢cation of mesodentine in Neocoleodus (Sansom etal. 1994) is unequivocal. The assertion by Kemp & Nicoll(1995a) that the structure of the Chirognathus basal tissue isa preservational artefact is unfounded, unless the histolo-gical integrity of the whole Harding Sandstone vertebratefauna is called into question.

Thus, at least some basal bodies are demonstrablycomposed of dentine, and other structures, whichapparently support alternative interpretations, are alsosometimes displayed by dentine. The spheroidal structurecompares favourably in morphology and scale withdentine calcospherites which commonly occur withindentine (¢gure 14d) and result from poor mineralization(Halstead 1974), rapid growth or other factors such asdisease (Appleton 1994). Atubular dentine has beendescribed from the basal body of Pseudooneotodus (Sansom1996), but other material of Pseudooneotodus (¢gure 5d,e)reveals a spherulitic structure directly comparable withthe basal body of Cordylodus, also described by Sansom etal. (1992) but interpreted as globular calci¢ed cartilage.Most basal bodies are lamellar and lack evidence oftubules, but even these ¢t within the range of knowndentines, speci¢cally (atubular) lamellar dentine (e.g.Karatajute-Talimaa et al. 1990; Karatajute-Talimaa &Novitskaya 1992). In most dentines these structures canoccur together, so that lamellar dentine containscalcospheres, as do most tubular dentines. This is alsoobserved in conodont basal tissues. Interpretation of allconodont basal tissue as dentine is therefore supported bythe structural variation and integradation seen in a rangeof conodont taxa. However, the possibility remains thatdi¡erent tissue combinations were present in the earlyevolution of the Euconodonta, particularly if this clade isconsidered polyphyletic (e.g. Miller 1984), althoughfurther histological analysis of Early Ordovician cono-donts is required.

The pattern of growth displayed by the basal tissue isextremely variable. The basal body of Pseudooneotodus isdominantly lamellar but is spheritic at the crown junction,the site of the terminal dentine network (Sansom 1996).The basal body of Ozarkodina is usually lamellar, exceptfor the £anks of the structure below the contact with thecrown, which may result from either disruption of themineralizing dentine by vascular supply from the pulp, orrepresent the site of attachment ¢bres. Similarly, thecoarse structures previously interpreted as dentine tubules(Dzik 1986; Andres 1988) can be homologized with pulpcanals.

The basal body of Palmatolepis also has a variablestructure, although this may result fromprocesses of preser-vation. In optimally preserved specimens, the £anks of thesquat plate-like structure incorporate coarse calibre canal-like structures which are in¢lled from the outside inwards(¢gure 13g,h). Thin-sectioned elements reveal a hollowinternal structure which indicates that as the element grewrapidly laterally, the successive growth increments of basaltissue incorporated large spaces into the structure(mirroring hypocalci¢cation in the crown). The specimensexamined exhibit evidence of gradual enlargement withoutmorphologicalmodi¢cation, punctuatedby periodic lateralexpansion of the structure, again, by incorporation of alarge space. The spaces did not remain hollow, but weregradually in¢lled by successive lamellae, the secretingtissue probably maintained via the canals in the £anks ofthe basal body (¢gure 14a^ c). The rapid growth hasresulted in the incorporation of pulp tissue within themineralized structure. The lateral walls of the basal bodyoccupied by vascular canals are poorly or weakly minera-lized; this may explain the less completely mineralizedstate of most Palmatolepis basal bodies, where only theportion above the vascular region is present. In these speci-mens the growth increments do not exhibit closure aroundthe lower surface of the basal body. Either the lower half fellaway post mortem or it was never mineralized. Most often thebasal body is not preserved at all.

The temporal trend towards unmineralized basal bodiesis potentially a serious weakness in the interpretation ofbasal tissue as dentine, as this homology relies partly onevidence from relative growth between the componenttissues of elements. Within the vertebrate dermal skeletonthe signal for enamel secretion is believed to be thepresence of a mineralized surface, typically mineralizeddentine (Smith 1992). Reduced mineralization in cono-dont basal bodies poses no developmental problem aslong as dentine adjacent to the enamel^dentine junction

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Figure 14. (a, b) Detail of Pa element of Palmatolepis sp. (inset) exhibiting the position of in¢lled pulp canals. (a) Caudal margin.Specimen BU 2642, frame width 1650 mm, length of element in inset 2723 mm. (b) Rostroventral margin of element. Note thesection of a concentrically in¢lled tubule at upper left. Specimen BU 2642, frame width 492 mm. (c) Ventral view of a Pa element ofPalmatolepis sp. with a hollow basal body which opens to the venter. Specimen BU 2643, frame width 488 mm. (d) Ground sectionthrough a crushing tooth of Lissodus minimus (Agassiz), a Rhaetian elasmobranch. The scanning electron micrograph details mantledentine with remnants of the associated dentine tubules. Specimen BU 2644, frame width 153 mm. (e, g) Etched ground sectionthrough an S element of Polygnathus sp. exhibiting the recurrent relationship between growth cavities, the bounding crystallites andwhite matter. (e) White matter secretion appears to have been initiated immediately after a growth cavity. Specimen BU 2645,frame width 93 mm. (g) Typical arrangement of crystallites adjacent to growth cavity. Specimen BU 2645, frame width 23 mm. ( f )Thin section through the dermal scale of Gomphoncus sp. Pander, an acanthodian (inset). Specimen BU 2646, frame width 357 mm,inset width 586 mm. (h) Ground section through a Pa element of Idiognathodus sp. (inset) exhibiting growth cavities in¢lled by atissue similar to white matter. Specimen ROM 53265, frame width 37 mm, inset width 578 mm. (i, j ) Thin section through an Selement of Idioprioniodus exhibiting growth cavities in¢lled by a tissue similar to calcospheric dentine. Specimen ROM 53266, (i)frame width 55 mm, ( j ) frame width 23 mm.

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was mineralized. This could explain why many Devonianconodont taxa retain a thin remnant of basal tissue whichwould otherwise have performed no useful purpose (e.g.see Smith et al. 1987).

Enameloid displays a di¡erent relationship with dentineto that between enamel and dentine. In enameloid, theepidermal cells (ameloblasts) begin secretion beforemineralization of the dentine instead of after. As a result,the extracellular matrices of the two tissues intermix andthe resulting tissue mineralizes from the outer surfaceinwards, the opposite of how enamel grows.The di¡erencebetween enameloid and enamel, therefore, has beenproposed to be the result of a heterochronic shift in thetiming of secretion by the ameloblasts from post- to pre-mineralization of dentine (Smith1992,1995). In conodonts,all histological data point toward interpretation of crowntissue as enamel, but the lack of a basal body could not beexplained away even if the crown were enameloid becausethe growth increments of the crown are still sharply trun-cated by the basal cavity.

To explain the then apparent absence of dentine in cono-dont elements (only the basal body of C. angulatus had bythen been described), Smith & Hall (1993) suggested ashift in timing of ameloblast di¡erentiation to an evenearlier phase, prior to odontoblast di¡erentiation. In sucha scenario, epithelial^ectomesenchymal interaction wouldhave taken place to produce ameloblast and chondroblastprecursors, ultimately resulting in the secretion of enameland mineralized cartilage. Sansom et al.'s (1992) interpreta-tion of the C. angulatus basal body has just been discussedand so this scenario may no longer be necessary or appro-priate. However, could such a heterochronic shift in timingbe invoked to explain the absence of dentine in Middle andUpper Palaeozoic conodonts? Themechanism is not unpar-alleled (Smith 1992, 1995; M. M. Smith, personalcommunication) and it is certainly plausible, but it wouldindicate that the signal for enamel secretion is not thepresence of a mineralized surface. M. M. Smith et al.(1996) have attempted to homologize conodont elementswith odontodesöbasic units of the vertebrate dermalskeletonöwhich are viewed as `single, modi¢able morpho-genetic system[s]' (Schae¡er 1977). Odontodes aretheoretically (and often in practice) perceived as £exibleenough to allow any of their component tissues (enamel,dentine and bone) to have evolved before the others, or bepresent independently of the others, by uncoupling or inde-pendently regulating odontoblast and ameloblastdi¡erentiation (Smith & Hall 1993). If conodont elementsare homologous to odontodes, the lack of preserved miner-alized dentine in many conodont elements could quiteeasily be explained.

(c) White matterWhite matter is perhaps the most problematic of all

conodont hard tissues. The most recent interpretation ofwhite matter contends that the tissue is cellular dermalbone (Sansom et al. 1992, reiterated in 1994; Sansom 1996;M. M. Smith et al.1996).The polarized arrangement of theputative cell processes and cell spaces within white matter,however, argue against an interpretation of white matteras dermal bone.

Although the arrangement of cell spaces and processeswithin white matter adjacent to lamellar crown is like a

dentine, the inclusion of cell-shaped spaces within thegroundmass appears atypical. Most modern dentines arehighly organized in structure and include only spaces leftby cell processes. Cells themselves are not included withinthe matrix because they retreat ahead of the mineralizingfront. However, the fossil record of dentine reveals anevolutionary series of dentine types from a poorly orga-nized cell-including primitive condition, throughincreasingly more-organized arrangements of cells andcell processes, to a rigidly organized acellular advancedcondition (Òrvig 1967a). White matter resembles thedisorganized structure of mesodentine (e.g. ¢gure 14f ),the most primitive in this evolutionary lineage. However,the match is not exact because white matter lacks asso-ciated pulp canals which often occur in mesodentine. Theorganization of white matter indicates, however, that thetissue grew orally, so the lack of associated pulp structuresmay not be so surprising. The implication is that whitematter was dead once the sustaining vascularization hadbeen removed to facilitate element function.

The tissue lacks punctuating growth striae which(except for the most primitive types) commonly occur inmost dentines. The tissue also reacts di¡erently from thedentine of basal bodies when etched with acid. Onepossible alternative interpretation is that white matter is aform of enameloid, which commonly includes spaces leftby the processes of odontoblasts, close to the dentine^enameloid junction. However, the microcrystallinegroundmass of white matter is inconsistent with thishypothesis, as most forms of enameloid are composed ofelongate ¢bre-like crystals.

At present, the most likely interpretation, on the basisof growth pattern and structure, is that white matter is adentine-related tissue comparable with mesodentine, butexclusive to conodonts. Similarity to primitive enameloidsmay be shown in the future, e.g. tubercles of theheterostracomorph ¢sh Astraspis Walcott possess a glassycap', although the lack of large crystal ¢bre bundlessuggests that this tissue is not homologous with theenameloids of higher vertebrates (Smith et al. 1995), andis more similar to white matter. The interpretation ofwhite matter as enameloid appears £awed because whitematter is usually completely enveloped by enamel, and isnever in contact with the dentine basal tissue. However,there is a direct relationship between the occurrence ofgrowth cavities in the enamel crown and the initiation ofwhite matter secretion (¢gure 14e). The few examples inwhich such cavities are in¢lled reveal a mineralizedtissue resembling white matter (in Idiognathodus, ¢gure14g) or calcospheritic dentine (in Idioprioniodus, ¢gure14i, j). Furthermore, the step-sided margins of thecavities, resulting from the abutment of surroundingenamel increments, could represent appositional growthof enamel and dentine (¢gure 14g). These cavities could,therefore, represent a source of odontoblastic cells thatcombined with ameloblasts of the forming enamel toproduce an enameloid (bitypic enamel of Smith (1989)).Such a scenario may be analogous to the formation ofacrodin blisters on the dermal denticles of some fossilactinopterygians (e.g. Òrvig 1978a,b,c).Refutation of the presence of cellular dermal bone in

conodont elements negates the conclusions of Smith &Hall (1990) and M. M. Smith et al. (1996) with regard to

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the primacy of cellular over acellular bone, and bothtissues retain their previously established (coeval) anti-quity (Smith 1991).White matter is not ubiquitous amongst conodonts and

is absent from many taxa. The tissue was not essential tothe formation of denticles as elements of almost all taxacontain denticles without white matter. The presence ofwhite matter was, however, certainly bene¢cial in termsof structural integrity. Conodont element crowns arecomposed almost entirely from enamel, which is thehardest wearing of all vertebrate biominerals but isextremely brittle. Simple enamels that lack thestrengthening e¡ect of prismatic structure areparticularly weak. The incorporation of a second tissue,such as white matter, which has di¡erent rheological prop-erties, helps to strengthen the element and aids in thedecussation of propagating cracks. Through the UpperPalaeozoic, many conodont lineages, particularly ozarko-dinids, record a pattern of reduced white matter in Pelements in favour of increased complexity in enamelmicrostructure.

White matter appears to be unique to conodonts, butbecause it is not present in the earliest of conodontelements it cannot be considered an autapomorphy of thegroup.

(d) DiscussionExamination of patterns of growth recorded by cono-

dont hard tissues has facilitated testing of recenthypotheses of homology with tissues of other organisms.Patterns of growth displayed by individual tissues and bycombinations of tissues are consistent with homologieswith speci¢c vertebrate dermal hard tissues. This supportsthe main conclusions of Sansom and colleagues (Sansomet al. 1992, 1994; Sansom 1996) although some reinter-pretation of their results is necessary. The complexity inpatterns of growth previously unrecognized in multi-denticulate elements highlights the di¤culty inidentifying homology between the conodont skeleton andother vertebrate hard tissue systems. This study implies,however, that conodonts must have mineralized theirskeleton through the evolution of a suite of hard tissuesindistinguishable from those of vertebrates. To even themost ardent opponents of parsimony analysis, an entirelyindependent origin must appear unlikely. Nevertheless,whatever the outcome of the debate over a¤nities, thepatterns of growth of conodont hard tissues and ofelement morphogenesis remain valid.

7. PROCESS: UNDERSTANDING CONODONT

ELEMENT GROWTH

(a) Homology within the growing skeletonThe full interpretation of conodont hard tissues now

available allows reassessment of the morphogeneticpatterns described earlier, taking into considerationpatterns of growth of comparable tissues in extant andwell-documented extinct vertebrates. The descriptions ofthe morphogenetic growth patterns included someattempt to draw homology between the di¡erent cate-gories. It is clear that individual denticles of type Ielements represent the basic unit of the conodont skeleton.It is also apparent that these undi¡erentiated units are

homologous with the individual multidenticulate units,which collectively comprise type II elements. Further-more, these units are homologous with multidenticulateelements of more derived taxa such as the ozarkodinids,representative of types III and IV. This last stage ofhomology is, however, misleading as both type III andIV elements exhibit evidence of repair. These repairevents are reinterpreted as episodes of post-functionalgrowth indicating that these elements, like type IIelements underwent post-eruptive growth, by envelop-ment by subsequent odontodes. Whereas juvenilemultidenticulate elements of type III and IV taxa arehomologous to individual units of type I taxa, geronticspecimens are composed of several such units. Elementsof type III and IV are homologous at coeval stages inontogeny, but the di¡erentiated denticle units of type IVare homologous to individual denticles of type IIIelements.

The basic structural component of the conodontskeleton can now be seen as a denticle consisting of anenamel lamellar crown cap and a dentine base.Incremental lines within both the enamel crown anddentine basal body meet at the enamel^dentine junction(basal cavity surface), indicating that the two tissues grewin opposing directions, beginning at the enamel^dentinejunction with a layer of dentine, followed by a layer ofenamel. This pattern is widely recognized amongstvertebrate dermal units and is known as appositionalgrowth. In the vertebrate dermal skeleton, the incrementallines within the two tissues usually share an angularrelationship. This is dependent on the shape of theenamel^dentine junction, which is rarely as evaginated inconodont elements. In conodonts, an acute angularrelationship is restricted to coniform elements with deeppulp (basal) cavities.

Discrete dermal units within the vertebrate skeletonconsisting of enamel and dentine are known as odontodes(Òrvig 1967a) and are the basic building blocks of thedermal skeleton. Odontodes usually include a thirdcomponent, bone, which acts as a tissue of attachment.However, bone is not ubiquitous within odontodes and isabsent from the scales of thelodonts, a group of extinctjawless ¢sh, and the scales and teeth of most chondrich-thyans. On this basis, M. M. Smith et al. (1996) haveargued for a homology between conodont elements andodontodes, but in the light of morphogenetic patternsdescribed here, their contention is clearly an oversimpli¢-cation. Type I elements are composed of up to tens ofindividual odontodes, but they remained structurally aswell as histogenically distinct from each other, unitedonly by an underlying supporting structure. Although theindividual odontodes of type II elements were histogeni-cally distinct, their lack of structural identity makes theresulting element an odontocomplex (sensu Òrvig 1977;Reif 1982). Odontocomplexes vary in their mode offormation such that successive odontodes may be added toone side, from above or circumferentially. Type III and IVelements are also odontocomplexes and exhibit circumfer-ential addition of successive odontodes. The establishmentof the new dental papilla for each odontode, at theboundary between the pre-existing crown and basalbody, makes distinguishing the successive odontodes di¤-cult, although pathological specimens con¢rm this

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pattern, e.g. Mu« ller & Nogami (1971, pl. 11, ¢g. 1) andMu« ller (1981, ¢g. 30), where the succeeding odontode hasadded to one side of the growth centre in a Pa element ofSiphonodella.

(b) DiscussionIf the growth patterns described here are to be

considered in terms of current hypotheses of conodontphylogeny their arrangement from primitive to advancedwould be II^(I)^III^IV; the simplest form, type I, is anevolutionary o¡shoot, apparently restricted to forms suchas Promissum, Coryssognathus and Icriodus. The di¡erencesbetween the four categories are most easily rationalizedas resulting from heterochronic changes in the timing ofvarious developmental stages. Type II is found inC. angulatus, one of the earliest taxa bearing multidenticu-late elements. It has been interpreted as either anevolutionary dead-end (Sweet 1988), or as the stem groupof all conodonts (Dzik 1991). C. angulatus elements exhibit apattern of morphogenesis typical of type II, suggestingthat either the slightly later forms exhibiting the samepattern are convergent (after Sweet 1988), or else C. angu-latus is ancestral to all subsequent multidenticulateelement-bearing taxa (or possibly they have a commonancestor and C. angulatus is divergent). This pattern waselaborated upon in later forms and perhaps within Cordy-lodus itself, where the growth units di¡erentiatedmorphologically producing multidenticulate units, as inCarniodus. Type I appears to be secondarily simple,derived from type II stock and representing a conditionwhere preceding units continued growth after subsequentunits were added. This change may have been facilitatedby an extension of the early ontogenetic stage of odontodegrowth in a type II ancestor. Type III probably representsa change in the timing of development in a type IIancestor such that the adult stage is delayed and theprimary unit allowed to extend its growth. As there areno spatial restrictions on growth, the element maycontinue extending along its growth axes. At ¢rst itappears as though both III and IV have abandoned theancestral condition of adding odontodes after primarygrowth. However, the pattern of periodic repair andenlargement exhibited by these taxa is evidently a vestigeof the ancestral growth strategy. The subsequent growthstages are adapted from marginal accretion to completelysurround the existing structure, homologous with thegrowth of acanthodian scales (see below).

The timing of white matter secretion is potentiallyanother important character when comparing the di¡erentgrowth categories, particularly as it consistently representsthe latest stage of growth in individual denticles.Whereasdenticles in type III elements are dominated by whitematter, denticles of type IVelements contain less.Throughthe Devonian and Carboniferous white matter is furtherreduced, until by the Carboniferous, many taxa boreelements where only in late stage growth and only theportion of denticles emergent from the main body of theelement, containwhitematter. As a result, type IVelementsresemble the juvenile stage of denticle growth in type IIIelements, suggesting a heterochronic shift in the timing ofsecretion of the di¡erent tissues.

The complexity of denticle genesis, described here,clearly contradicts Szaniawski & Bengtson's (1993)

hypothesis on the origin and genesis of denticulation ineuconodonts. Their model proposed that denticles origi-nated in early euconodonts by the accretion of layers oflamellar crown tissue onto a worn, jagged region of primi-tive coniform elements. If early euconodonts do indeedexhibit this pattern of growth, it is more likely that thedenticles formed by repair, having replaced pre-existing,but worn denticles. The pattern of denticle genesisproposed by Szaniawski & Bengtson (1993) is certainlynot present in any of the ozarkodinids, prioniodinids, prio-niodontids, panderodontids, belodellids or proconodontidsobserved by this author.

8. COMPARISON OF THE MORPHOGENESIS OF

CONODONT ELEMENTS AND OTHER VERTEBRATE

HARD TISSUES

The pattern of periodic regrowth in conodont elements,which facilitates repair and enlargement, is unusual in thevertebrate dental record, particularly as the elements aredominated by enamel. In most systems that includeenamel, the enamel organ is destroyed during the processof eruption and even in those where the enamel organsurvives eruption, enamel secretion is spatially restricted(e.g. rodent teeth), and it cannot facilitate repair to thefunctional surface. There are very few dental systems thatfacilitate repair, mainly because most craniates haveadopted a strategy of shedding and replacement.However, growing' scales are much more common thangrowing teeth' in the vertebrate record and include afacility for post-eruptive repair (if the scale does indeederupt): for example, some acanthodian (e.g. ¢gure 14f )and actinopterygian scales. After some period of time, anerupted scale sinks within the dermis and is enlarged bythe growth of another odontode around, above, or to oneside of the pre-existing structure. As a result, scales areenlarged and can thus be repaired by successive layers ofganoine (a homologue of enamel; Sire et al. 1987; Sire1994) over the outer surface, occurring in step withsuccessive layers of dentine around the lower surface.Such scales must have spent much time enclosed withinsoft tissue, in contrast with conodont elements, which,although not teeth in the strictest sense, functioned assuch. Conodont elements must periodically have sunkwithin the dermis, or else the dermis must have grownover the surface of the element, to facilitate growth andrepair. As many elements, particularly types I and II,exhibit marginal growth independent of the remainder ofthe structure, it is possible that at least some elements werepartly enclosed within soft tissue throughout life.

The pattern of denticulation in type II and IV is paral-leled in a great number of gnathostome dentitions,particularly amongst teleosts. In most cases each denticleis a structurally distinct odontode (tooth), which is situatedin a jaw and individually shed and replaced. Conodontelements were not situated within a jaw apparatus andwere permanent, not shed and replaced (M. M. Smith etal. 1996). Some acanthodian dentitions were also perma-nent and bear a remarkable similarity to conodonts in`tooth' arrangement and pattern of growth. Ischnacanthidacanthodians bore dentigerous jaw bones in which theteeth were incorporated and remained undi¡erentiablefrom the jaw proper (¢gure 15a); it is largely for this

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reason that these groups were believed to have possessedpermanent dentition. Like type II and IV conodontelements, the jaw bone grew by marginal accretion anddental units comprising alternating dentition were addedsequentially (¢gure 15b(i)^b(iv)). The sequential units arenot divisible into distinct teeth and are considered multi-denticulate teeth (Òrvig 1973). The dentigerous jaw bonesgrew rostrally in contrast to the caudal direction ofmarginal accretion in type I^IV conodont ramiformelements. Acanthodian tooth spirals also exhibit the samepattern of marginal accretion, although the dentigerousunits are unidenticulate and grew by accretion on thecaudal margin of the spiral. The tooth spirals di¡er fromthose of elasmobranchs because the successive teeth arefused together in a single structural unit (¢gure 15c), andso, as each tooth was replaced by its successor, it was notimmediately shed but retained and shed with the wholespiral when the last tooth was no longer functional(Òrvig 1973). Although growth of acanthodian denti-gerous jaw bones has been poorly documented, thereappears to be no evidence of repair to existing dentitionduring the addition of new dental units, a signi¢cantdi¡erence from conodont elements. In addition, acantho-dian jaws are entirely composed of dentine and bone in theupper and lower portions respectively; they completelylack enamel and there is no evidence for enameloid,again, di¡ering considerably from the condition of cono-dont elements.

The pattern of growth displayed by the toothplates ofmodern lung¢sh represents another possible analogue tothe pattern of formation of some conodont elements. Thelung¢sh toothplate is a permanent tooth that grows byaccretion of odontodes onto the growing margin (labial inthis case). The new odontodes are aligned with ridges ofthe toothplate, which represent fusion of previouslyformed odontodes; each ridge is thereby interpreted ashomologous with a tooth family (Kemp 1977). Lung¢shtoothplates are also capable of some degree of repair, butthis is achieved by hypermineralizing the dentine, in¢llingthe spaces left by the cell processes that were responsiblefor the secretion of the original tissue (Smith 1979). Thepattern of odontode addition is directly comparable withthe addition of denticles in type II conodont ramiformelements and the bifurcation of toothplate toothfamiliescomparable with the addition of secondary and tertiaryprocesses in conodont elements such as ramiform elements.Young et al. (1996) challenged the primacy of the odon-

tode as the plesiomorphic patterning component of thevertebrate dermal skeleton. Their new model of theprimitive dermal skeleton is based upon fragments ofputative dermal armour from the Late Cambrian ofAustralia, slightly younger than the ¢rst records of Anato-lepis Bockelie & Fortey, another putative vertebrate(Bockelie & Fortey 1976; Repetski 1978; Smith & Sansom1995; M. P. Smith et al. 1996), and the ¢rst true conodonts.These broken plates are composed of a tripartite tissuecomplex including a laminated basal layer, calcospheriticmiddle layer and continuous hypermineralized cappinglayer. The middle layer is composed of a series of poly-gonal ¢elds, radially arranged about vertical canals thattraverse the capping layer and open onto the surfacethrough tubercles. The capping tissue is considered homo-logous to enamel, and althoughYoung et al. (1996) refrain

from attempting to draw homology between the middleand basal layers and the tissues of other vertebrates, theyconsider dentine absent. The lack of dentine or bone ofattachment in this material is taken as evidence thatthey are not primitive for the dermal skeleton of verte-brates, and thus an unreliable indicator of vertebratea¤nity. In the light of this, one wonders on what basisthe new Cambrian material from Australia is ascribed tothe vertebrates? The identi¢cation is based largely oncomparative morphology of surface ornament, and thetripartite tissue combination from which the sclerites arecomposed. Comparative morphology has, in the past,been recognized as an unreliable indicator of a¤nity(e.g. Schallreuter 1983, 1992). Furthermore, the tripartitetissue combination is typical of vertebrate dermal armourbecause odontodes are three-layered, and yet Young et al.(1996) conclude that odontodes are not plesiomorphic inthe vertebrate exoskeleton.Yet on this basis,Young et al. goon to reinterpret the hard tissue histology of Anatolepisand conodonts, concluding that the two groups `representdivergent specialisation's with the early diversi¢cation of

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Figure 15. (a) Part of a dentigerous jaw bone in Xylancanthusgrandis Òrvig, after Òrvig (1967b, 1973) with omission of thesupporting jaw cartilage. Dashed lines delineate units ofgrowth. (b(i)^b(iv)) Illustration of growth of acanthodiandentigerous jaw bone by marginal accretion at the anterior endof the jaw. Illustration also includes successive wearing-downof the teeth, after Òrvig (1973). (c) Illustration of growth ofacanthodian tooth whorl, based on Nostolepis Pander. Shadingdelineates units of growth that were added to the posterior ofthe whorl, after Òrvig (1973).

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vertebrate hard tissues' (p. 812) and that conodont hardtissues are unique. Even if the new Cambrian materialwere vertebrate, there is no evidence, stratigraphic orotherwise, that it is any less derived than Anatolepis orthe hard tissues of conodonts. It could as easily havebeen derived from Anatolepis. The evidence from Anatolepisand from conodonts suggests that odontodes are plesio-morphic patterning units of the vertebrate dermalskeleton.

9. DISCUSSION

The apparent complexity inherent within the structureof conodont elements is remarkable. Conodonts werecapable of producing elements of diverse shape and struc-ture, from unidenticulate coniform elements tomultidenticulate ramiform elements, through the additionof any number of odontodes. However, the basic architec-tural plan of the feeding apparatus remained conservativethroughout the conodont record. The architecture of thefeeding apparatus of ozarkodinids is known to haveremained stable in element number and positionthroughout much of its record (Silurian^Carboniferousfrom a record extending latest Ordovician to Permian;Purnell & Donoghue 1998). Given the variety of morpho-genetic patterns exhibited by di¡erent conodont taxa,architectural stability is even more remarkable.

Prioniodinids also bore a standard 15-element appa-ratus (Purnell & von Bitter 1996), and although Promissumpossessed a 19-element apparatus, other evidence suggeststhat this apparatus is representative of balognathids aloneand not the prioniodontid order as a whole (Stewart 1995).Current available evidence indicates, however, that thisplan is not plesiomorphic for the Euconodonta as taxarepresentative of ancestral stocks, such as PanderodusEthington, may have had up to 17 elements (Sansom et al.1994).

Theremust havebeenacontrolling factor in thegrowthofthe conodont apparatuswhichpreventeddeviation from thestandard 15-element PMS division through much of theconodont record.The elements as unitary structures are notdirectly comparable with teeth or dermal teeth, but withaggregations of them, so it is convenient to consider eachelement position to be analogous to a gnathostome toothfamily, where growth is restricted to within the `tooth posi-tion'. Growth between such positions in conodontelements, as in tooth families, may have been preventedby a `zone of inhibition'. However, unlike most toothfamilies, functional teeth were not replaced in successivegenerations, but added to by new teeth, as in the denti-gerous jaw tooth families of ischnacanthid acanthodians.

The di¡erence between teeth and other odontodes is thelocus of formation; teeth are formed only within a dentallamina, which probably did not evolve until after themandibular arch (Reif 1982). However, if conodontelements are homologous to vertebrate teeth (e.g. Gaengler& Metzler 1992), they must have formed within a dentallamina. Such a dental lamina would have had to bepermanent, but instead of facilitating growth of replace-ment teeth, it would have been responsible for periodicgrowth and repair of damaged elements. If such a scenariois realistic, it is likely that the dental lamina was discontin-uous and the proposed 15-element plan of the conodont

feeding apparatus, autapomorphic to all complex cono-donts, was a result of segregated dental laminae of thesame number.

10. THE REST OF THE CONODONT SKELETON

The feeding elements are the only part of the conodontskeleton to have been consistently mineralized, but is thereany other evidence of skeletal biomineralization? Phos-phatic spheres found associated with conodont elementshave been attributed to the conodont animal and havebeen coined conodont pearls' (Glenister et al. 1976, 1978).Glenister et al. further proposed that the structures repre-sented the animal's response to irritation, whether bydetritus or parasitic invasion. The animal alleviated theirritation by secretion, around the stimulus, of themineral normally used to grow the feeding elements. Thepearls have since been demonstrated as belonging to anextinct group of bryozoans (Donoghue 1996).

The only other mineralized structure associated withconodonts is a small phosphatic object found adjacent tothe feeding apparatus in one of the Scottish conodontanimals. This sphaeroid strongly resembles lamprey stato-liths which are also phosphatic, and appears in a positionwithin the head consistent with the otic capsules (Aldridge& Donoghue 1997), organic remnants of which may also bepreserved in another of the Scottish specimens (Briggs etal. 1983; Aldridge et al. 1993). However, otoliths, statolithsand statoconia are non-skeletal (Maisey 1987).

The conodont animal must also have possessed someform of internal skeleton, if for no other reason than tohave provided support and articulation for manipulationof the feeding apparatus (Purnell & Donoghue 1997) andalso support to the gills. Despite preservation of soft tissues(Briggs et al. 1983; Aldridge et al. 1986, 1993; Aldridge &Theron 1993), sometimes in exquisite detail (Gabbott etal. 1995), there is still no record of such an internalskeleton, mineralized or otherwise. It is likely that theanimal possessed a cartilaginous endoskeleton much likethat of the extant agnathans, hag¢sh and lampreys. Fossilrepresentatives of these groups also lack preservedevidence of their cartilaginous endoskeleton (Bardack &Zangerl 1968, 1971; Bardack & Richardson 1977; Bardack1991).

11. CONCLUSIONS

Description of growth patterns in conodont elementshas provided a means of testing competing hypotheses ofhard tissue histology which were originally based simplyon isolated morphological characters. The results of thestudy have vindicated the suggestion that there ishomology between conodont and vertebrate hard tissues.Conodont elements are more complex structures thanpreviously recognized. They are not homologous with`odontodes' (contra M. M. Smith et al. 1996), but eachelement appears to comprise one or a number of odon-todes, analogous (or homologous) to a tooth family. Thedi¡erent patterns of formation are believed to re£ectheterochronic shifts in the timing of developmental stages.The growth patterns in conodont elements were evolvedentirely independently from similar patterns in moreadvanced vertebrates. Conodont elements o¡er closer

662 P. C. J. Donoghue Growth and patterning in the conodont skeleton

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comparison with dermal scales and oral odontodes thanwith true teeth.

I thank Professor R. J. Aldridge and Dr M. A. Purnell for theirhelp throughout the course of this project, and particularly R. J.Aldridge for providing most of the material on which this studywas based. I also thank Stefan Bengtson, Jerzy Dzik, Peter Forey,Philippe Janvier, Anne Kemp, Klaus Mu« ller, Bob Nicoll, IvanSansom, Moya Smith, Paul Smith and Hubert Szaniawski fordiscussion. Both Derek Briggs and Paul Smith provided carefulreviews of the manuscript; with R. J. Aldridge their help in beat-ing the manuscript into a shape suitable for human consumptionis greatly appreciated. Funded by a University of Leicester stu-dentship and a Royal Commission for the Exhibition of 1851Research Fellowship.

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666 P. C. J. Donoghue Growth and patterning in the conodont skeleton

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