VERTEBRAL DEVELOPMENT IN THE DEVONIAN ...palanth/Paleolab/susy_files/...487 Journal of Vertebrate Paleontology 22(3):487–502, September 2002 q 2002 by the Society of Vertebrate Paleontology

487

Journal of Vertebrate Paleontology 22(3):487–502, September 2002q 2002 by the Society of Vertebrate Paleontology

VERTEBRAL DEVELOPMENT IN THE DEVONIAN SARCOPTERYGIAN FISHEUSTHENOPTERON FOORDI AND THE POLARITY OF VERTEBRAL EVOLUTION IN

NON-AMNIOTE TETRAPODS

S. COTE1*, R. CARROLL1, R. CLOUTIER2, and L. BAR-SAGI1†1Redpath Museum, McGill University, 859 Sherbrooke St. W., Montreal, Quebec, H3A 2K6, Canada;

2Departement de Biologie, Universite de Quebec a Rimouski, 310 allee des Ursulines, Rimouski, Quebec, G5L 3A1, Canada

ABSTRACT—Study of a growth series of twenty-seven specimens from the Upper Devonian of Escuminac Bay,Quebec documents a complex pattern of vertebral development in the osteolepiform fish Eusthenopteron foordi. Os-sification begins with elements associated with the caudal, anal, and second dorsal fins. Development of the haemalarches, caudal radials, and caudal neural arches continues anteriorly and posteriorly from near the level of the anteriormargin of the caudal fin. Trunk neural arches ossify later than the caudal neural arches and as a separate sequence.Trunk intercentra most likely begin ossification posteriorly and continue forward after the ossification of haemal archesis complete. Comparisons of many different patterns of vertebral development within the modern actinopterygiansdemonstrates that the sequence of development in Eusthenopteron foordi is unique. The diverse patterns of vertebraldevelopment observed in fossil and modern fish presumably result from an interplay between the inherent anterior toposterior sequence of development controlled by the Hox genes, and varying selective forces imposed by the physicaland biological environment in which the fish develop. Initiation of vertebral development in the caudal region ofEusthenopteron foordi can be attributed to selection for early function of the tail in propulsion. In contrast, vertebraldevelopment in Carboniferous amphibians typically proceeds from anterior to posterior. This may reflect developmentin the still water of ponds and lakes in contrast with the coastal environment inhabited by the hatchlings of Eusthen-opteron foordi. The sequences of vertebral development seen in Carboniferous labyrinthodonts and lepospondyls aredivergently derived from that observed in Eusthenopteron foordi.

INTRODUCTION

Amphibians are unique among tetrapods in commonly ex-pressing a biphasic life history with fossilizable larval stagesthat document early ontogenetic development. The sequence ofdevelopment of vertebral elements differs markedly among themajor taxa of both Paleozoic and modern amphibians. Differ-ences in developmental patterns provide a potential means ofinferring phylogenetic relationships, but also reflect major dif-ference in their ways of life that are significant in tracing theirevolutionary history.

Carroll et al. (1999) attempted to establish relationships be-tween Paleozoic and modern amphibian orders on the basis ofdifferent patterns of vertebral development. They documenteda consistent pattern in the timing and direction of ossificationof the arches and centra in anurans and the larvae of labyrin-thodonts, specifically temnospondyl branchiosaurs, in which thearches ossify before the multipartite centra in a clearly anteriorto posterior sequence. They contrasted this pattern with thatseen in lepospondyls (particularly microsaurs) and specific sal-amanders, in which cylindrical centra ossify at a very earlyontogenetic stage, prior to the neural arches (Fig. 1).

The early formation of cylindrical centra in many salaman-ders was used to suggest that they might share a common an-cestry with lepospondyls (Carroll et al., 1999) since this patternwas certainly a derived character relative to the presence ofmultipartite centra in both labyrinthodonts and their putativesister-taxa, such as the osteolepiform Eusthenopteron foordi.However, a sister-group relationship between frogs and labyrin-thodonts could not be supported by the common pattern of ver-

*Current address: Harvard University, Department of Anthropology,Peabody Museum, 11 Divinity Avenue, Cambridge, Massachusetts,02138.

†Current address: Angell Memorial Animal Hospital, 350 S.Huntington Ave., Boston, Massachusetts, 02130.

tebral development if the sequence of development seen in Car-boniferous labyrinthodonts were primitive for tetrapods.

Knowledge of the early history of Chondrichthyes, Ostei-chthyes, and Placodermi indicates that neural arches evolvedlong before centra (Goodrich, 1930; Remane, 1936; Carroll,1988). This suggests that the pattern of vertebral developmentseen in Carboniferous labyrinthodonts, in which the arches os-sify before the centra, and in an anterior to posterior direction,is probably primitive for tetrapods. However, the sequence anddirection of vertebral development has never been described inthe closest sister-group of tetrapods, the osteolepiform sarcop-terygians. Large numbers of immature specimens of the bestknown of osteolepiforms, Eusthenopteron foordi Whiteaves, arepresent in numerous collections and have been used for studyof the pattern of development of both the body proportions(Thomson and Hahn, 1968) and the skull (Schultze, 1984).However, vertebral development has been largely ignored. An-drews and Westoll’s (1970) description of the skeleton of Eusth-enopteron foordi remains the most comprehensive and widelyaccepted (Fig. 2), however it deals only with mature specimens.The current study documents the sequence and direction of ver-tebral ossification in Eusthenopteron foordi and compares thisdata with the pattern of development seen in modern fish, am-phibians, and Carboniferous labyrinthodonts and lepospondyls.

VERTEBRAL DEVELOPMENT IN EUSTHENOPTERON

Extensive collections of Eusthenopteron foordi from the Up-per Devonian (middle Frasnian) locality of Miguasha in Quebecwere examined from the parc de Miguasha, Quebec (MHNM)(approximately 800 specimens), the Natural History Museum,London (BM(NH)), and the Museum of Comparative Zoology,Harvard (MCZ). Study was concentrated on 27 specimens rang-ing from less than 3 cm to 29.5 cm in length. The smallestshowed no trace of ossificiation of the internal skeleton, but inthe largest, all elements of the endochondral skeleton had be-

488 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 22, NO. 3, 2002

FIGURE 1. Vertebral development in Paleozoic and modern amphibians. A, dorsal view of a larva of the temnospondyl labyrinthodont Bran-chiosaurus salamandroides from the Westphalian D of Nyrany, Czech Republic. Neural arches ossify from anterior to posterior; they are justbeginning to form at the base of the tail. Centra ossify later, from paired, crescentic intercentra and pleurocentra. B, dorsal view of a late larvalstage of the modern anuran Rana pipiens. The neural arches ossify from anterior to posterior in the trunk region, cylindrical centra form only atmetamorphosis. Neither centra or arches form in the tail. C, ventral view of a juvenile specimen of the lepospondyl microsaur Hyloplesionlongicostatum, from the Westphalian D of Nyrany, Czech Republic. Even the smallest known specimens of this species have cylindrical centra,but loosely attached neural arches. The poor resolution of the last preserved caudal vertebrae indicate that the centra ossify in an anterior toposterior direction. D, the hynobiid salamander Salamandrella keyserlingii. Both arches and centra develop from anterior to posterior, but incontrast with the frog, the centra form first, and extend to the end of the tail. The most posterior centra initially chondrify as small paired elements.Only a few paired arches can be seen just behind the skull. Reproduced from Carroll et al., 1999.

Larval temnospondyl labyrinthodonts resemble anurans in that the arches form prior to the centra, and chondrification and ossification of botharches and centra proceed from anterior to posterior. Microsaurs resemble some salamanders in having cylindrical centra that form as early orearlier than the arches. Vertebral development in all these groups is derived relative to that of Eusthenopteron foordi.

come ossified and resembled the shape of bones in previouslydescribed adults (Figs. 3A–H, 4A–E). Isolated bones of Eusth-enopteron suggest adults reached a size of approximately 1.5m (Schultze, 1984), although the largest complete specimen, ondisplay at parc de Miguasha, is only 1.06 m long.

As others have done in the past, it was assumed that a seriesof different sized specimens, belonging to a single species froma single locality, represent differences in age. It has previouslybeen shown that the changes accompanying size increase inEusthenopteron foordi are similar to those seen in growth andmaturation studies in modern fish (Schultze, 1984). This seriesallows comparison of juvenile to mature specimens and indi-cates the order in which different areas and elements of thevertebral column ossify. The specimens vary greatly in degreeof completeness and quality of preservation.

Thirty cm was the size limit of those specimens of this genusdesignated as ‘‘juvenile’’ by Thomson and Hahn (1968). Theybased their recognization of a juvenile stage on observationssuggesting that most pronounced modifications of body shapehad occurred before the 30 cm stage, but admitted that this was

an artibrary decision. Study of additional specimens by Schul-tze (1984) failed to show statistical support for changes in thelimb positions for which Thomson and Hahn had argued. How-ever, Schultze did recognize that changes in skull proportions,specifically the relative length of the orbit and the postorbitalregion of the skull, were characteristic of an early stage ingrowth that he also referred to as juvenile, although he did notindicate a specific size range for juvenile individuals. The cur-rent study suggests that the time at which all elements of theendochondral skeleton have become ossified may be a non-arbitrary means of differentiating between juvenile and adultindividuals. This occurs at a total body length between 27.4 and29.5 cm.

Not even the smallest specimens of Eusthenopteron, less than3 cm in length, show any features typically associated withlarvae, nor can any changes seen within the series be associatedwith a definable metamorphosis (Moser, 1984). On the basis ofcurrent evidence, development can be considered direct.

The size series (Table 1) shows a fairly even distributionfrom 3 cm to 29.5 cm, with some clustering of specimens at

489COTE ET AL.—EUSTHENOPTERON VERTEBRAL DEVELOPMENT

FIGURE 2. Eusthenopteron foordi Whiteaves. Reconstruction of the skeleton. Reproduced from Andrews and Westoll (1970). In the specimensused for our study the intercentra appeared to be closer together than is indicated in this reconstruction. Abbreviations (used in this and allfollowing figures): af, anal fin; cf, caudal fin.; cl, cleithrum; cna, caudal neural arch and associated spine; dd1, distal support (radial) of firstdorsal fin; df1, first (anterior) dorsal fin; df2 second (posterior) dorsal fin; f, femur; ha, haemal arch and associated spine; hu, humerus; ic,intercentrum; na, neural arch and associated spine; pc, pleurocentrum; pcf, pectoral fin; pd1, proximal support (basal plate) of first dorsal fin;pd2, proximal support (basal plate) of second dorsal fin; pra, proximal support (basal plate) of anal fin; pvf, pelvic fin; pvg, pelvic girdle; ran,radials (3) of anal fin; rd2, radials (3) of second dorsal fin; sa, sacral vertebra; vcr, ventral caudal radial; v1, 1st vertebra (trunk vertebrae arenumbered from 1 to 31 from anterior to posterior).

approximately 15 cm and 24 cm (see also Parent and Cloutier,1996:fig. 11). This may indicate that overall body growth isslowed at these time, or more likely, it could be an artifact ofsampling.

Description of Specimens

The four smallest specimens (e.g., Figs. 3A, 5A), rangingfrom 2.9 to 4.2 cm in total length, show body scales, clearlydefined fin structure, generally unjointed lepidotrichia, and thedermal bones of the skull, but no trace of vertebral elements orendochondral fin supports. These specimens are all preservedin dorsal or ventral view, with a broadly flattened head and anarrow body. The beginning of internal ossification can first benoted in the 5.0 cm specimen MHNM 06-535 (Figs. 3B, 5B),which shows the entire body exposed in lateral view, with welldefined dermal fin elements and the initiation of ossification ofthe posterior endochondral fin supports. These include threeneural arches with spines, extending posteriorly from the an-terior margin of the epichordal lobe of the caudal fin and fourradials extending posteriorly from the anterior margin of thehypochordal lobe, but no haemal arches. It cannot be deter-mined whether or not the radials of the anal fin were ossified,but two radials were present in the second dorsal fin. No en-dochondral supports were evident in the more anterior dorsalfin or the paired fins.

Specimen MHNM 06-238 (Figs. 3C, 5C; 6.4 cm in length)had ossified all three radials of the second dorsal, as well astwo of the radials of the anal fin. The outline of caudal neuralarches and ventral radials can be recognized through the over-lying scales, but their specific number is difficult to establish.The haemal arches were apparently not yet ossified. An increas-ing number of elements can be seen in the caudal region of thepoorly preserved MHNM 06-30 (Fig. 6A), estimated to be 9.0cm in length. These include the first appearance of haemal arch-es, in addition to the neural arches and radials of the caudal fin.Approximately six neural arches with spines and four caudalradials are ossified, spanning the anterior portion of the caudalfin, in addition to three caudal haemal arches. All three radialsof the anal fin are ossified. Two of the three radials in thesecond dorsal and both bones (one radial and the basal plate)supporting the first dorsal are ossified, but no bones are visiblein the pelvic fin.

In MHNM 06-59 (Fig. 6B; 12.0 cm), the caudal neural archesand radials have ossified further posteriorly and additional hae-

mal arches have been added anteriorly. The large proximal sup-port (basal plate) for the anal fin has begun to ossify, but thatfor the second dorsal fin has not. In MHNM 06-36 (Fig. 7; 16.8cm), almost the entire body is well preserved, but endochondralossification is limited to the posterior end of the animal. Neitherpectoral nor pelvic fins show endochondral bones. Supports forthe first dorsal are well formed, although the elements havebeen displaced and appear side by side. Anterior haemal archesare evident only to the level of the distal end of the proximalsupport (basal plate) for the anal fin. The proximal support forthe second dorsal fin is not ossified. BM(NH) P 15961 (notillustrated) is only 15.5 cm in length, but has an ossified prox-imal support for the second dorsal.

In MHNM 06-299 (Fig. 8; estimated total length 18.2 cm),in which the endochondral skeleton is very well exposed, allbut the most posterior caudal neural arches and ventral radialsare ossified. However, the last several posterior haemal archesremain unossified, showing that all of these elements ossifiedinitially in association with support for the anterior margin ofthe caudal fin, with subsequent ossification extending from thefront to the back within the caudal skeleton, and slightly laterfrom the anterior margin of the caudal fin forward toward thetrunk. In this specimen, 11 neural arches are ossified, but theydo not extend forward of the base of the second dorsal fin. Incontrast, the haemal arches extend to a level just behind thepelvis where they continue as intercentra, the main central el-ements in Eusthenopteron. Eleven trunk intercentra, includingthe sacral vertebra (as identified by Andrews and Westoll(1970)), are present anterior to the pelvis, at which point theblock ends. These would be vertebrae 22 through 32 in a fullydeveloped adult. Traces of ribs, the bases of the trunk neuralarches, and possibly also pleurocentra are ossified in the pos-terior trunk. By this stage, the supports for the dorsal and analfins have reached almost the adult form. In a marked advancedover the next smaller specimens, the paired elements of thepelvic girdle are fully formed, together with the proximal ele-ments of the pelvic fins. Both the proximal and distal endo-chondral supports for the first dorsal fin are clearly defined.

MCZ 5810 (Fig. 9; 19.3 cm) is a critical specimen, possess-ing most of the vertebral column, although in some places thevertebrae are covered by scales that could not be removed with-out damaging the underlying bone. The dermal bones of thehead are crushed and a break runs vertically through the skullbetween the parietals and postparietals. However, no bones are


FIGURE 3. Reconstructions of a series of specimens of Eusthenopteron foordi showing changes in degree of ossification of the endochondralskeleton in relation to increasing size. These changes are assumed to represent modifications during ontogeny. Body outline indicated in solidlines based on the fossil as preserved, with some amount of reconstruction. Dotted lines indicate missing portions of the fossil. Endochondralelements are identified in subsequent illustrations. A, MHNM 06-235 A/B; B, MHNM 06-535; C, MHNM 06-238 A/B; D, MHNM 06-30 A/B;E, MHNM 06-59 A/B; F, MHNM 06-36 A/B; G, MHNM 06-299 A/B; H, MCZ 5810.

entirely missing and it is clear that the full set of dermal ele-ments was ossified. On the other hand, it is evident that thebraincase and palatoquadrate were unossified between the well-defined bones of both sides of the dermal skull.

The supports for the anal and second dorsal fin are completeand the humerus and two other elements of the pectoral fin areossified. The pelvic girdle is missing, as is the distal elementof the first dorsal fin support, most likely the result of localbreakage of the specimen. Sixteen intercentra, which begin be-hind the opercular series and proceed posteriorly along the bodyare visible through the scales. This spans the positions of ver-tebrae 7 through 22 or 23 in an adult. There is a large gap

between the most posterior intercentra and the haemal arches.No centra or arches are present anterior to the back of the oper-culum, although approximately six would be present in this areaof an adult (Andrews and Westoll, 1970; Hitchcock, 1995).Neural arches are visible above what would be the seventh,eleventh, and fourteenth intercentra in an adult. In the caudalregion, nine neural arches with spines and twelve haemal archesare present, as well as eight ventral radials.

Although generally poorly preserved, with areas at the baseof the tail and in the region of the operculum obliterated by theformation of pyrite, MHNM 06-209 (Fig. 10; 21.0 cm) includesmost of the skeleton. Impressions of intercentra and neural


FIGURE 4. Continuation of Figure 3. A, MHNM 06-209; B, MHNM 06-121 A/B; C, MHNM 06-382 A; D, BM(NH) P. 6803; E, MHNM 06-636.

arches extend anteriorly to at least the front of the shouldergirdle, and may pass beneath the operculum. Unfortunately, theimpressions of the vertebrae are not preserved in the matrix,but against the medial surface of the dermal scales, and so showalmost no surface detail. Therefore, it is not possible to deter-mine whether or not pleurocentra were present. Endochondralsupports for both the pectoral and the pelvic fins are visible.

As in MCZ 5810, no endochondral bone of the skull is pre-served.

Ossification in the caudal region can next be seen in MHNM06-121 (Fig. 11; estimated total length 24 cm), an especiallywell-preserved specimen. The caudal fin is supported by sevento eight neural arches with spines, four to five haemal arches,and 11 to 12 radials. This compares, respectively, with 12, 10,


TABLE 1. Reconstructed length of Eusthenopteron foordi specimens.Abbreviations: MHNM, specimens from the collection of the Parc deMiguasha; BM(NM) P, specimens from the collection of the BritishMuseum of Natural History; MCZ, specimens from the Museum ofComparative Zoology at Harvard. Total length is measured from the tipof the snout to the end of the medial portion of the caudal fin in smallspecimens in which it extends beyond the dorsal and ventral lobes, andby the ends of the dorsal and ventral lobes of the caudal fins in largespecimens, where they exceed the length of the medial portion. Forincomplete specimens, total length was estimated on the basis of theproportions of the body that was preserved, accepting Schultze’s (1984)finding that the position of the fins did not change significantly duringgrowth.

RankSpecimennumber

Approximatelength (cm)

12345678

MHNM 06-234MHNM 06-235 A/BMHNM 06-13MHNM 06-90MHNM 06-535MHNM 06-238 A/BMHNM 06-30 A/BMHNM 06-59 A/B

2.93.33.64.15.06.49.0

12.09

101112131415161718192021222324252627

BM(NH) P. 15961BM(NH) P. 15957MHNM 06-36 A/BMHNM 06-299 A/BMCZ 6518 A/BMCZ 5810MCZ 9159BM(NH) P.7074MHNM 06-209MHNM 06-233 BMCZ 9265BM(NH) P. 60340MHNM 06-121 A/BMHNM 06-382 ABM(NH) P. 15960BM(NH) P. 6803BM(NH) P. 60341BM(NH) P. 6804MHNM 06-636

15.516.216.818.218.919.319.520.221.022.023.023.524.025.026.026.426.727.429.5

and 14 in the restoration of an adult specimen illustrated byAndrews and Westoll (1970). Based on the latter specimen, thelongest of each element in MHNM 06-121 is identified as themost anterior support for the caudal fin. The length of the neuralarches and the radials is reduced more anteriorly. Unfortunately,this specimen does not extend anterior to the fin supports forthe second dorsal and anal fins.

MHNM 06-382 (Fig. 12; estimated total length 25 cm) isuniquely preserved, showing the entire vertebral column to thebase of the tail as well as the palatoquadrate and the braincase,but without any dermal bones or any trace of fins. The cranialelements are preserved in dorsal view, to judge by the smooth,rather then tooth covered surface of the palatoquadrate. This isthe smallest specimen in which there is definite evidence thatthe braincase and palatoquadrate are ossified. The first four ver-tebrae are disarticulated, but all 31 trunk intercentra, and a pu-tative sacral vertebra, can be accounted for. The intercentra atthe anterior end of the column are visible in ventral view (incontrast with the skull). The first 16 are extensive crescents,continuous at the ventral midline. The next few are either bro-ken ventrally or were originally paired, while those more pos-terior (exposed in lateral view) were certainly paired. The lastthree elements presumably represent the most proximal portionof the tail, but the area of the haemal arch is not preserved.Small, paired, circular pleurocentra are visible in associationwith intercentra 23 to 33. Pleurocentra may have been presentmore anteriorly, but would not be exposed since only the ven-tral surface of the intercentra can be seen.

In specimens BM(NH) P. 6803 (Fig. 13; 26.4 cm) andBM(NH) P. 60341 (not illustrated; 26.7 cm), the vertebral col-umn is represented primarily by impressions showing the ex-ternal surface of the scales closely overlying the arches andcentra. This mode of preservation shows that they were rela-tively large and well ossified, but reveals no surface detail.BM(NH) P. 6803 shows a number of clearly defined distal ra-dials of the pectoral fin. More proximal elements are present,but reveal little detail. Neural arches are associated with manyof the the intercentra.

In the largest specimen studied, MHNM 06-636 (Fig. 14),estimated at 29.5 cm in total length, the entire column hadachieved an essentially adult condition, with probable ossifi-cation of all elements from the skull to the end of the tail,including the ribs. Unfortunately, due to the manner of initialpreparation, little surface detail remains. The elements of thepelvic fin distal to the femur are well exposed and fully ossified.

Summary of Ossification Sequences

Numerous, well-preserved specimens document the devel-opmental sequence of endochondral bones in the posterior por-tion of the vertebral column in Eusthenopteron foordi (Table 2;Figs. 3, 4, 15A). Ossification of caudal neural arches, haemalarches, and ventral radials begins at the anterior margin of thecaudal fin and proceeds both posteriorly and anteriorly. Anteriorto the caudal fin, there is a gap in the ossification of neuralarches in MHNM 06-299 until roughly the level of the sacralvertebra but the haemal arches and intercentra form a contin-uous series, ossifying from posterior to anterior, into the pos-terior trunk. The gap in the sequence of neural arches belowand just anterior and posterior to the second dorsal fin may berelated to the need for flexion in this area for effective swim-ming. The neural arches in this area are reduced in size relativeto those anterior and posterior to them in the adult stage as well(Fig. 2). Pleurocentra are only seen with certainty in the pos-terior trunk region after all the other elements are formed. Thedistal radials of both the anal and second dorsal fins ossifybefore the large proximal supports; in contrast, the proximaland distal elements of the first dorsal fin appear to ossify si-multaneously.

Few specimens clearly show the pattern of development inthe anterior portion of the column. Specimens MHNM 06-59and MHNM 06-36 show a complete covering of scales, but theendochondral elements of the caudal, dorsal, and haemal finsprotrude through them. No such protrusions are evident in thearea of the paired fins or the vertebral column anterior to thelevel of the base of the anal fin. MCZ 5810 (Fig. 9) showsintercentra in the area between the pectoral and pelvic fins,corresponding with vertebrae 7 through 22 or 23. This specimenis most simply interpreted as indicating that ossificiation of theanterior intercentra begins just behind the operculum and pro-ceeds both anteriorly and posteriorly. This appears to occur asa separate event from the ossification of the haemal arches.

However, MHNM 06-299 (Fig. 8), which is one centimetershorter than MCZ 5810, shows fully developed intercentra be-ginning with the sacral vertebra and extending anteriorly to the22nd intercentrum, where the block ends. This specimen may beinterpreted as demonstrating that the intercentra develop as acontinuation of the series of haemal arches, beginning at theend of the trunk and proceeding anteriorly. However, we cannotexclude the possibility that intercentra in this specimen beganossification near the anterior end of the trunk and continued ina posterior direction.

These two specimens seem to provide contradictory infor-mation regarding the sequence of development of the intercen-tra. However, further study of MCZ 5810 reveals that the gapseen between the haemal arches and the last preserved inter-


FIGURE 5. Three of the smallest, but fairly well preserved specimens of Eusthenopteron foordi. A, MHNM 06-235 A, preserved in ventralview, showing the impression of the dorsal surface of the skull. Long, essentially unjointed lepidotrichia of the pectoral and caudal fins are visible.No endochondral fin supports or vertebral elements are ossified at this stage; B, MHNM 06-535, complete skeleton in lateral view. Endochondralsupports for the caudal, anal, and second dorsal fin are visible through the scales. All fins are supported by unjointed lepidotrichia; C, MHNM06-238 B. Ventral view of head region, showing the underside of the skull roof and cheeks. The body is twisted so that the lateral surface of thecaudal region is exposed. Endochondral supports for the caudal, anal, and both dorsal fins can be seen through or between the scales. Noendochondral elements can be seen more anteriorly. Image reversed left to right for comparison with the other two specimens.


FIGURE 6. Eusthenopteron foordi. A, MHNM 06-30 A/B, showingthe support for the first dorsal fin and the first haemal arches in additionto the elements seen in smaller specimens; B, MHNM 06-59 A/B, alsoshows the proximal fin support for the anal fin.

FIGURE 7. Eusthenopteron foordi. MHNM 06-36 A. Nearly complete skeleton with continuous scale cover. Endochondral supports are clearlyevident posteriorly (darkened for emphasis), and can not be seen in association with the pelvic or pectoral fins.

centra may be an artifact of preservation, since there is damageto the specimen in that area. It is therefore possible that inter-centra may have extended back to the haemal arches. If thiswere the case, it would suggest that intercentra begin ossifica-tion posteriorly as part of the sequence of haemal arches andproceed anteriorly. This may have occurred quite rapidly, sinceMHNM 06-36 (Fig. 7), which shows no intercentra and an in-complete set of haemal arches, is less than two centimetersshorter than MHNM 06-299 which possessed all the haemalarches and at least the last 11 intercentra.

Trunk neural arches are one of the last elements to beginossification. This certainly occurred as a separate event fromthe ossification of the caudal neural arches. However, the di-rection in which they ossified is uncertain. The earliest appear-

ance of trunk neural arches is in MHNM 06-299 (Fig. 8), how-ever they appear irregularly over a few intercentra and no pat-tern can be established. This is also the case in MCZ 5810.Therefore, ossification of trunk neural arches could have oc-curred either from front to back or from back to front. Pleu-rocentra are first clearly seen at the posterior end of the trunkand anterior caudal region in MHNM 06-382, but they mayhave been present more anteriorly in this specimen and yet notbe visible. They too might have begun ossification from eitherthe anterior or posteriorly end of the body.

Based on the nearly universal anterior to posterior directionof expression of the Hox genes (which control major aspects ofdevelopment of the body axis; Shubin et al., 1997; Coates andCohn, 1999), and the geologically earlier appearance of chon-drification and/or ossification of the neural and haemal archesrelative to the centra in both Chondrichthyes and Osteichthyes,the pattern of development in Eusthenopteron foordi appearshighly derived relative to more primitive aquatic vertebrates.The sequence also appears very different from that seen in bothCarboniferous and modern amphibians, which is commonly an-terior to posterior. One immediate question is whether the pat-tern seen in Eusthenopteron foordi is common among modernbony fish or is a specialization of sarcopterygians or of thelineage leading to tetrapods.

Among sarcopterygians, neither fossil nor living coelacanthshave ossified centra, and so provide only a limited basis forcomparison (Andrews, 1977). Centra as well as neural and hae-mal arches are ossified in Devonian lungfish (Denison, 1968),but the relative sequence of their ossification has not been es-tablished. Recent work by Arratia (2001) will provide a basisfor establishing the pattern of vertebral development in themodern species. The primary basis for comparison thus lieswith the phylogenetically divergent living actinopterygian fish.

ACTINOPTERYGIAN FISH

Surprisingly, there is relatively little published informationregarding vertebral development in modern actinopterygianfish, and there has been no recent synthesis of the availabledata. Dunn (1984) listed work that had been published up tothat date and states that the pattern of ossification varies con-siderably among taxa. More recent studies further documentthis variability. In the following section, observations on ver-tebral development taken from the available literature are re-


FIGURE 8. Eusthenopteron foordi. MHNM 06-299 A/B. Caudal region and posterior trunk showing a gap in the neural arches between thecaudal fin and the area of the sacral vertebra and the first evidence of the pectoral girdle and proximal support for the second dorsal fin. Neuralarches begin to appear over some intercentra.

FIGURE 9. Eusthenopteron foordi. MCZ 5810. Complete skeleton covered with scales. Shows the humerus and several small bones of thepectoral support. Pelvic girdle is absent, most likely due to breakage of the specimen in this area. Intercentra can be seen from the area of thepectoral girdle back to the mid-trunk region. There are no intercentra in the opercular region, or in the area of the pelvic fin. The dermal skull isfully ossified, however there is no evidence of an ossified braincase or palatoquadrate.

viewed in a phylogenetic sequence beginning with the mostprimitive living actinopterygians.

Specific comparison of vertebral elements between sarcop-terygians and actinopterygians is complicated by the fact thatthe central elements are not homologous, and different patternsof development of both the arches and centra are indicated bya distinct terminology. Patterns of development among actin-opterygians, emphasising the caudal region, are documented indetail by Arratia and Schultze (1992) and by Schultze and Ar-ratia (1986). Where the terminology differs, the sarcopterygianterm is used, followed by the designation for the actinoptery-gian analogue in parentheses.

Polypterus (Polypteridae), considered the primitive sister-tax-on of all other living actinopterygians, provides an informativecontrast with Eusthenopteron foordi. Overall, the neural arches,vertebral centra, and ribs differentiate from anterior to posterior,while the lepidotrichia and endoskeletal supports of the dorsalfin form from posterior to anterior. Chondrification and ossifi-cation of the hypaxial caudal skeleton also occur in a posteriorto anterior direction (Bartsch and Gemballa, 1992). Chondrifi-

cation begins when the fish is 11.0 mm long with the occipitalarches and the bases of the next three neural arches. By 14.5mm, the first and second pair of neural arches and the posteriorfin rays of the dorsal fin are ossified. Body scales begin to formin specimens approximately 30 mm in length, in marked con-trast to their much earlier appearance relative to the centra andfin supports in Eusthenopteron foordi. Bartsch and Gemballa(1992:519) state that the development of the vertebral columnin Polypterus ‘‘is ruled by strict functional demand rather thanby the ‘ballast’ of evolutionary history.’’ They interpret the ear-ly completion of the caudal and posterior dorsal fin skeleton asbeing necessary adaptations for locomotion.

Development of the primitive chondrostean Polyodon spa-thula (Acipenseriformes: Polyodontidae), was recently de-scribed by Bemis and Grande (1999). The medial fins becomedistinguished from one another in an anterior to posterior se-quence- dorsal, anal, then caudal. However, as in Eusthenop-teron foordi, fin supports are initially elaborated in the caudalregion. The first visible skeletal elements are the hypurals andmiddle radials of the dorsal and anal fin, which are initially all


FIGURE 10. Eusthenopteron foordi. MHNM 06-209. Smallest specimen in which the vertebral column extends to the back of the skull, andthe proximal elements of the pectoral fin are well ossified. Most of the endochondral bone is preserved as an impression on the inside surface ofthe scales, which shows little structural detail. Dashed outline indicates pyrite. Head omitted.

FIGURE 11. Eusthenopteron foordi. MHNM 06-121 A/B. Posterior portion of the skeleton showing the endochondral supports for the caudal,anal, and second dorsal fin in nearly their adult configuration. Lepidotrichia conspicuously jointed in contrast with smaller specimens.


FIGURE 12. Eusthenopteron foordi. MHNM 06-382 A. Endochondral bones of axial skeleton, stripped of all elements of the dermal skeleton.Palatoquadrate seems to be preserved in dorsal view, anterior portion of column in ventral view, and posterior portion of column in lateral view.This is the smallest specimen to show pleurocentra unequivocally. Braincase is extensively ossified.

FIGURE 13. Eusthenopteron foordi. BM(NH) P. 6803, with full pectoral fin support and more visible neural arches over the intercentra.

cartilaginous. Hypurals, radials, and dermal fin rays all begindevelopment in the middle portion of the fin and spread bothposteriorly and anteriorly. Polyodon does not form vertebralcentra. The full adult complement of all caudal, anal, and dorsalfin structures are present by the time the fish is 47 mm. How-ever, only the dermal fin rays are ossified. Bemis and Grandebelieve that fish at this stage have completed metamorphosis,which indicates that ossification of endochondral structuresmust occur sometime in the juvenile stage.

Development of Amia calva has recently been described byGrande and Bemis (1998). As shown in their illustrations (oneof which is redrawn as Figure 15B), the abdominal centra (thoserunning from the occiput to the first centrum bearing a haemalcanal) mineralize in an anterior to posterior sequence. Ossifi-cation of the ural centra occurs separately and begins beforethe ossification of even the most anterior of the diplospondylouscentra (part of the preural caudal region). Chondrification andossification of the neural arches extends into the caudal region


FIGURE 14. Eusthenopteron foordi. MHNM 06-636. 29.5 cm in length. Skeleton is fully ossified.

TABLE 2. Sequence of first appearance of endochondral bones of theskeleton of Eusthenopteron foordi.

Skeletal element

Length (in cm)of smallestspecimen

expressing thiselement

Caudal neural archesVentral caudal radialsFirst two radials of second dorsal finThird radial of second dorsal finFirst two radials of anal finThird radial of anal finHaemal arches of caudal finSupports of first dorsal finProximal support for anal finProximal support of second dorsal finPelvic girdle and femurPosterior intercentraAnterior intercentraPectoral support (humerus)Endochondral skull (braincase and palatoquadrate)

5.05.05.06.46.49.09.09.0

12.015.518.218.219.319.325.0

prior to the centra. The supports for the caudal fin ossify beforethose of the paired or dorsal fins. More details of vertebraldevelopment are provided in Schultze and Arratia (1986).

Among teleost fish, the Catostomidae have been reported toossify their vertebral centra in an anterior to posterior direction,but in the guppy (Poeciliidae), ossification begins in the middleof the vertebral column and proceeds both anteriorly and pos-teriorly (Weisel, 1967). Crane (1966) describes yet another pat-tern in the viperfishes (Chauliodontidae). Ossification of thevertebrae occurs first in the caudal region and proceeds ante-riorly. In some specimens, the most anterior vertebrae remainunossified throughout life, which Crane suggests could be anadaptation for increased flexion required for efficient feeding.Therefore, in a phylogenetically and functionally diverse groupof teleost fishes, a variety of very different patterns of vertebralossification can be found.

Within the order Perciformes, we see a more consistent pat-tern of vertebral ossification. Most perciforms for which the

direction of vertebral ossification has been reported show ananterior to posterior direction of differentiation in both the arch-es and centra. For example, the swordfish, Xiphidae (Potthoffand Kelley, 1982), the closely related Scombridae (Wollom,1970), and the Anarhichadidae (Pavlov and Moksness, 1997).

Anisotremus virginicus (Haemulidae), known as the porkfish,shows a slightly different pattern (Potthoff et al., 1984). Carti-laginous neural arches (basidorsals) appear first both just behindthe skull and separately in the mid-trunk region, while cartilag-inous haemal arches (basiventrals) appear at the center and pos-terior end of the vertebral column. However, ossification of bothneural and haemal arches occurs after the ossification of allvertebral centra in an anterior to posterior direction. The pos-terior portion of the dorsal fin, as well as the anal and caudalfins are the first to develop rays, while the pelvic and pectoralfins are the last to do so. The elements of the caudal fin support,including the hypurals, normally ossify after the centra of thetrunk. Potthoff et al. (1984) cited several additional studies ofvarious perciforms in which vertebral elements ossify from an-terior to posterior.

The perciform Archosargus probatocephalus or sheepshead(Sparidae), also ossifies all its vertebral elements in an anteriorto posterior direction (Mook, 1977). Here, neural and haemalarches begin ossification soon after the centra, so that the an-terior neural and haemal arches are ossified before the posteriorcentra. Ossification of the caudal skeleton begins with the lep-idotrichia in 3.5 mm larvae, followed by the urostyle, hypurals,and finally the epurals- all in an anterior to posterior sequence.The hypurals are the last elements to complete ossification,when the fish is 25 mm in length.

In her comprehensive study of centrarchid fishes (Centrar-chidae), Mabee (1993) reported that all 30 species ossify theirvertebrae following the same pattern, although the number ofelements can vary among species. Vertebral centra ossify fromanterior to posterior in a continuous sequence, like other per-ciforms (Fig. 15C). However, the two urostylar centra ossifyearlier than the centra anterior to them, although the anteriorurostylar centrum does ossify first. Another important differ-ence from other perciforms is that ossification of the haemalarches begins in the middle of the series and then proceedssimultaneously in both anterior and posterior directions. This


FIGURE 15. Comparison of the sequence of vertebral development in Eusthenopteron foordi with two modern fish. A, vertebral developmentin Eusthenopteron foordi with arrows indicating the direction in which elements ossify; B, larval specimen of Amia calva, which illustratesvertebral centra and neural arches ossifying in an anterior to posterior direction. Bone is shown in solid black and thick lines, thin lines and whiteindicate cartilage. Dermal fin rays ossify first in the caudal region; (modified from Grande and Bemis, 1998:129); C, direction of ossification ofvertebral and fin elements in the Centrarchidae; (reproduced from Mabee, 1993).

pattern is also shared by the fin rays of the dorsal, anal, andcaudal fins, as well as the hypurals. The fin rays of the pectoralfin ossify in a dorsal to ventral direction. The earliest neuralarches to ossify are those at the very anterior part of the ver-tebral column, with ossification continuing in a posterior direc-tion. However, a second set of neural arches ossify in the mid-trunk region, from which ossification proceeds in both anteriorand posterior directions. The sequence of development beginswith the anterior neural arches and hypurals, followed by thehaemal arches and mid-trunk neural arches. Although centra arethe last elements to appear, they form initially as ossified struc-tures (autocentra) and so would be visible in fossilized speci-mens before the arches. Mabee states that this pattern of ossi-fication has also been reported in Trachurus symmetricus (Car-angidae) (Ahlstrom and Ball, 1954).

In contrast with the uniform axial development seen in allcentrarchids, Moser and Ahlstrom’s (1970) study of the lan-

ternfish (Myctophidae) showed that there can be variability inthe sequence of ossification within groups as well. Dermal finrays are always the first postcranial structures to ossify, but theorder in which the fins ossify is variable. The endochondralsupports of the caudal fin ossify before those of the other fins,but this occurs after the complete set of caudal dermal fin rayshas formed. Vertebral centra, neural arches, and haemal archesall ossify in an anterior to posterior direction. The timing ofossification can vary between species; however, in most thecentra, neural arches, and haemal arches ossify simultaneously.Generally, the ossification of the vertebral column occurs latein development relative to the ossification of other structures,however it is usually completed before the time of metamor-phosis, which varies with species.

Although this general pattern of anterior to posterior verte-bral column development is common to most lanternfishes, twospecies follow the opposite sequence. The vertebral centra of


FIGURE 16. Comparison between the body outlines of Eusthenopter-on foordi and Esox lucius showing the similarity in positioning of thedorsal and anal fins and overall appearance, which has been used asevidence to suggest their similar behavior as adults. Both species reachsimilar size as adults. A, Eusthenopteron foordi outline adapted fromSchultze (1984); B, Esox lucius outline adapted from Bry (1996).

Hygophum atratum and Hygophum reinhardti ossify from pos-terior to anterior, as do their neural arches (Moser and Ahls-trom, 1970). This pattern is unlike that seen in any of the otherperciforms. In addition, ossification begins very late in thesetwo species, normally just before metamorphosis. Therefore,the lanternfish show variation both in the sequence of ossifi-cation between elements and in the direction of ossificationwithin specific elements.

From this scattered sampling of bony fish, it is obvious thatthe sequence and direction of chondrification and ossificationof vertebral elements are extremely variable and are not obvi-ously tied to the degree of taxonomic affinity. The most com-mon pattern is for most elements to ossify in a predominantlyanterior to posterior direction, but in some fish a posterior toanterior sequence is seen. Frequently, some elements of the cau-dal region will ossify prior to those in the posterior part of thetrunk. The absence of a phylogenetically consistent pattern ofvertebral development among bony fish strongly suggests theimportance of functional controls, such as the feeding and lo-comotive needs of hatchlings and juveniles (Crane, 1966;Mook, 1977; Bartsch and Gemballa, 1992). Similarity of pat-terns of development must be supplemented by other data toprovide a reliable means of establishing relationships. Ontogenyof the vertebrae does not necessarily reflect phylogeny. In fact,very divergent patterns of vertebral development may give riseto very similar adult forms.

The pike and muskellunge, Esox (Esocidae), have long beenrecognized as similar to Eusthenopteron foordi in body formand probable behavior (Andrews and Westoll, 1970; Arsenault,1982). This is based on their large size and the far posteriorposition of the dorsal and anal fins that give a powerful thrustin lurk and lunge feeding (Fig. 16). One might expect that theywould also share the sequence of development of the vertebraeand fin supports seen in Eusthenopteron foordi. In fact, recentX-ray studies carried out by Alison Murray show that the ver-tebral column in the four North American species of Esox de-velops from anterior to posterior. This marked difference indevelopment suggests that factors other than adult feeding hab-its may be important in the selective control of development.Reproduction in pike generally occurs in shallow, thickly veg-etated habitats on submerged flood plains (Bry, 1996). Thiswould indicate that there would be little wave or current activityin the environment in which young Esox were undergoing earlydevelopment. In contrast, most specimens of Eusthenopteronfoordi are found in tidally influenced estuarine environments(Chidiac, 1996; Cloutier et al., 1996). It is probable that the

early ossification of the caudal region in Eusthenopteron foordimay be an adaptation necessary for early swimming in a fast-current marine environment.

VERTEBRAL DEVELOPMENT IN DEVONIAN ANDCARBONIFEROUS TETRAPODS

No fossils are yet known of larval or juvenile individuals ofeither Panderichthys, which is thought to be the closest knownsister-taxon to tetrapods, or of any of the Upper Devonian am-phibians. However, the high degree of development of the cau-dal fin in these genera strongly supports its importance in swim-ming, which Clack and Coates (1995) and Clack (2000) argueto be the primary, if not sole means of locomotion in Acan-thostega and Ichthyostega. This suggests that the pattern of ver-tebral development described in Eusthenopteron foordi, withthe early ossification of the tail region, may have been retainedin Late Devonian amphibians. This is in strong contrast to boththe adult structure and the patterns of development seen in mostmembers of the major groups of primitive Carboniferous am-phibians, the labyrinthodonts and lepospondyls. With the ex-ception of some embolomeres and the nectrideans, most mem-bers of these groups, from the Visean on, had long slender tailswith little evidence of adaptation for swimming.

Some 20 to 30 million years separate Eusthenopteron foordiand the Upper Devonian tetrapods from the earliest adequatelyknown members of the amphibian lineages that dominated themid- to late Carboniferous and include the ancestors of themodern orders. During this time, the reproductive environmentchanged from wave and current influenced marginal marineconditions to quiet inland bodies of fresh water, including coalswamps, oxbow lakes, and larger, semipermanent lakes. Thedifferent environments in which Eusthenopteron foordi andCarboniferous amphibians reproduced may have strongly influ-enced their patterns of vertebral development. These quiet wa-ters apparently did not require the early development of the tailas a major swimming structure, and their partial isolation mayhave limited the access of large aquatic predators. Reduction inthese selective pressures may have allowed the axial skeletonin Carboniferous amphibians to develop in direct accordancewith the anterior to posterior direction of expression of the Hoxgenes.

The relatively large adult size of most labyrinthodonts mayhave required a fairly long period of aquatic development, dur-ing which first the neural arches and later the multipartite centrachondrified and then ossified. Lepospondyls had a much differ-ent growth strategy, with precocial ossification greatly limitingadult size, and resulting in formation of fully cylindrical centraat a stage when vertebrae in labyrinthodonts had barely begunto ossify (Fig. 1).

With the description of vertebral development in Eusthen-opteron foordi, it is obvious that the patterns of developmentin both labyrinthodonts and lepospondyls are derived relativeto more primitive choanates. Hence, the pattern seen consis-tently in larval temnospondyls, in which development of thearches long precedes that of the centra, is a putative synapo-morphy linking them with anurans, which follow a comparablesequence in all families in which vertebral development hasbeen described.

Comparison with salamanders is more difficult. It has longbeen assumed that the pattern of vertebral development com-monly seen in advanced salamanders, including plethodontids,ambystomatids, and salamandrids, was typical for urodeles.This seemed to be borne out by the very early formation ofcylindrical centra, and later appearance of arches in the hyno-biid Salamandrella (Carroll et al., 1999). However, furtherstudy of a cleared and stained specimen of another hynobiid,


Ranodon showed very different patterns, in which the neuralarches in the anterior trunk form before the centra.

Most striking is the pattern of development seen in Dicamp-todon, generally considered a much more advanced salamanderallied with the radiation leading to salamandrids and ambysto-matids (Milner, 2000). Wake and Shubin (1998) show that earlystages in its vertebral development closely resemble that offrogs, with neural arches developing from anterior to posterior,well before the appearance of centra. Like bony fish, there isclearly a great variety in the patterns of vertebral developmentin salamanders that may be attributed to hatching and devel-oping in different environments. Accepting this degree of plas-ticity among salamanders, and the difficulty of establishing thepolarity of character transformation within this order, it is dif-ficult to use any particular mode of vertebral development forestablishing relationships with Paleozoic amphibians. On theother hand, it opens up the possibility for their being related totemnospondyls and frogs (as suggested by Trueb and Cloutier,1991), which seemed very unlikely if all the primitive sala-manders had a pattern resembling that of lepospondyls, withprecocial ossification of cylindrical centra. Work is now under-way to examine vertebral development in a much greater rangeof modern salamanders to see if a primitive salamander patterncan be established (Boisvert; in press).

Eusthenopteron foordi also differs significantly from laterCarboniferous tetrapods in the apparent absence of a recognizedlarval stages and a definitive metamorphosis. Bemis and Grande(1999:45) describe metamorphosis in the paddle fish Polyodonas occurring ‘‘when the external shapes of the fins reach theirapproximately adult appearance, and adult coloration and feed-ing mode are achieved.’’ In even the smallest known specimenof Eusthenopteron foordi (at 29 mm), the lepidotrichia coverall of the fins, which does not happen until after metamorphosisin Polyodon. This might indicate that all the specimens ofEusthenopteron foordi used in this study were post-metamor-phic, or that this species developed directly, with the hatchlingalreadying attaining the general body form of the adult.

Amphibian metamorphosis may only have became evidentwith the evolutions of a clearly biphasic life history, with along period of aquatic development, followed by emergence onland (Boy and Sues, 2000). This transformation is clearly evi-dent in labyrinthodonts, whose larvae had external gills, but lesswell defined in lepospondyls, whose small, frequently elongatebodies would have resulted in a sufficiently large surface tovolume ratio so that they may have been able to subsist oncutaneous respiration both in the water and on land.

CONCLUSIONS

The pattern of vertebral development seen in Eusthenopteronfoordi is different from that of any of the modern fish surveyedand also differs from that in both the modern and fossil am-phibians. Lepidotrichia appear in all fins very early in devel-opment. The first endochondral bones to ossify are the supportsfor the caudal fin, followed by those of the anal and dorsal fins.Centra most likely ossify from the pelvic region forward. Trunkneural arches and pleurocentra are the last elements of the ver-tebral column to begin ossification. Dermal skull bones appearearly in development, but the endochondral elements of thebraincase and palatoquadrate ossify significantly later. This se-quence of ossification suggests that effective aquatic locomo-tion is critical in young Eusthenopteron foordi. Although Hoxgenes are expressed in an anterior to posterior sequence in allvertebrates, the sequence of chondrification and ossification ofvertebral elements is prone to modification by environmentalconstraints and the functional needs of the animal. The diversityof patterns seen in modern fish indicates that both phylogenyand adaptive factors play roles in the vertebral development of

all fish. Salamanders also show a considerable variety of pat-terns of development, related to the environment in which theydevelop. Vertebral development in Eusthenopteron foordi isvery different from the patterns seen in Carboniferous amphib-ians. The patterns of development in lepospondyls and labyrin-thodonts are thought to have been derived divergently from thatof Eusthenopteron foordi.

ACKNOWLEDGMENTS

The authors wish to thank Johanne Kerr at the Parc de Mig-uasha, as well as Sandra Chapman at the Natural History Mu-seum, London and Charles Schaff at the Museum of Compar-ative Zoology for loan of specimens. Gloria Arratia, WilliamBemis, Lance Grande, and David Johnson were helpful in sug-gesting references on the development of actinopterygian fish.Alison Murray provided X-rays and information on pike de-velopment and Tamsin Rothery transported specimens fromLondon. This research has been supported by grants from theNatural Sciences and Engineering Research Council of Canada.

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Received 12 January 2001; accepted 25 September 2001.

Documents

VERTEBRAL DEVELOPMENT IN THE DEVONIAN ...palanth/Paleolab/susy_files/...487 Journal of Vertebrate Paleontology 22(3):487–502, September 2002 q 2002 by the Society of Vertebrate Paleontology