Thin Section Microscopy of the Fossil Fish Cylindracanthus

130 Proceedings of the South Dakota Academy of Science, Vol. 96 (2017)

THIN SECTION MICROSCOPY OF THE FOSSIL FISH CYLINDRACANTHUS

Barbara S. Grandstaff1, Rodrigo A. Pellegrini2, David C. Parris2*, and Donald Clements2 1School of Veterinary Medicine University of Pennsylvania 3800 Spruce Street Philadelphia, PA 19104-6045 2New Jersey State Museum 205 West State Street PO Box 530 Trenton, NJ 08625-0530 *corresponding author email: [email protected]

ABSTRACT

Since discovery of the definitive specimen of Cylindracanthus in the Verendrye Formation of Hyde County, South Dakota, new interest has been focused this genus, known only from its distinctive rostral spines. Hypothetically linked to ascip- enseriform (sturgeon-like) fishes, the spines, found in circum-Atlantic Cretaceous to Eocene marine formations, have been examined in thin sections for more than a century. We have expanded this range of microscopy to include detailed description of the tooth pedicels, examination of possible lesions and healed bony tissue, and petrography of the fossil, and probable functional anatomy. We have repeated the historical comparative studies with modern billfish specimens. Billfish rostral structure has no real resemblance (structural or mineralogical) to Cylindracanthus. The tooth base attachments in billfish are subdermal. In contrast, the tooth base structures and the lesions and damaged surfaces in Cylindracanthus give no evidence of having been subdermal. We have also expanded our comparative histological research to include Polyodon (paddlefishes) and Acipenser (sturgeons). Although fish teeth are typically acrodont (i. e., fused to the oral surfaces of the jaw and palatal elements), the teeth of Cylindracanthus are functionally pleur- odont, attached along (in fact, within) a groove, from which they protrude only slightly. The teeth point backwards toward the mouth (away from the tapered end of the rostrum). Hypothetically, the teeth could function in predation by causing damage during a stabbing motion of the rostral spine; they would be useless in a striking and/or slapping motion. The teeth would be highly effective in head-on attacks of shelled cephalopods, such as ammonites. This would have been advan- tageous during the Cretaceous Period but of no value later during the Eocene, after the ammonites had become extinct. We conjecture that the teeth became vestigial after the K-Pg event, as they are unknown in Cenozoic specimens.

Keywords Cylindracanthus, Cretaceous, Eocene, histology Proceedings of the South Dakota Academy of Science, Vol. 96 (2017) 131

INTRODUCTION Agassiz (1833-1843) used the name Coelorhynchus for fossils which he identi- fied as probable rostral elements. Leidy (1857a) independently gave the name Cylindracanthus to fossils from New Jersey and Alabama which he interpreted as dorsal fin spines. He later (1857b) noted that his Cylindracanthus fossils resem- bled figures of Coelorhynchus published by Dixon (1850). Leriche (1905) proposed the name Glyptorhynchus to replace Coelorhynchus because Coelorhynchus was preoccupied by a chimaeroid, and noted that Glyptorhynchus is similar to the rostrum of Blochius. Glyptorhynchus is now considered a junior synonym of Cylindracanthus (Purdy et al. 2001). Smith-Woodward (1888, 1891) believed that Cylindracanthus (Coelorhynchus) was a fin spine. Histologic studies by Williamson (1849) and Carter (1927) did not clearly identify these fossils as either fin spines or rostra. Thus both anatomic and taxonomic interpretations of Cylindracanthus remain subject to question (Friedman 2012). Our understanding of Cylindracanthus has advanced greatly in recent years. A specimen from South Dakota (SDSM 30638) was instrumental in confirming that this enigmatic fossil is a rostrum: this specimen preserves both teeth and ring-shaped tooth pedicels (Figure 1A). The tooth pedicels form elevations on the bottoms of two wider grooves that extend over the entire preserved length of the specimen. Teeth occupy the tops of many of the pedicels (Parris et al. 2001). Tooth crowns and pedicels are also preserved on a specimen from the Bluffport Marl Member of the Demopolis Chalk in Marengo County, Alabama, ASM-PV 994.2.111 (Parris et al. 2001). Both tooth-bearing specimens are Late Cretaceous in age. Other Cretaceous specimens, including Leidy’s type material from New Jersey (ANSP 5186-5188) and the Cretaceous specimen that was sectioned for this study (Figure 1C) preserve tooth pedicels but do not preserve any teeth. Some Eocene specimens from North Carolina (Figure 1B, D) and Alabama (Parris et al. 2001) preserve tooth pedicels; these specimens also lack associated teeth. No tooth crowns were preserved with any of the Eocene specimens we have examined to date. Tooth pedicels in Eocene specimens are smaller than those in Cretaceous specimens (Parris et al. 2001). Tooth pedicels on the New Jersey Cretaceous specimen are about 1mm across. Tooth pedicels on the North Carolina Eocene specimens are about 0.4mm across. Absence of tooth crowns in most of the specimens that preserve tooth pedicels suggests the teeth are easily lost post mortem. Both of the Cylindracanthus specimens that preserve teeth (SDSM 30638 and ASM-PV 994.2.111) were recovered from sediments which record low energy depositional environments (shale and chalk respectively). Tooth pedicels are not preserved in all Eocene specimens. Their absence might be taphonomic given that some Cylindracanthus specimens show significant loss of surface detail due to transport abrasion. The pedicels in Cylindracanthus occupy a relatively protected position at the bottoms of the surface grooves, however, and some relatively unworn Eocene specimens (such as ASM-PV 989.4.200) lack tooth pedicels. Fierstine (2001) reported that tooth pedicels are found on only some Cylindracanthus specimens. Teeth and tooth pedicels may have been entirely lacking in some Eocene members of this genus. 132 Proceedings of the South Dakota Academy of Science, Vol. 96 (2017)

Distribution of Cylindracanthus. Cylindracanthus fossils have been found in North America, Europe, and Africa. Specimens of Cylindracanthus range from Cenomanian (Vullo et al. 2009) to Eocene (Leriche 1905; Fierstine 2001) in age, and Cylindracanthus has been reported from rocks as young as Miocene (Adnet et al. 2010). The South Dakota specimen (SDSM 30638) comes from the Verendrye Formation of the Pierre Shale Group (Campanian). Other specimens included in this study were recovered from the Cretaceous and Eocene of Alabama, the Eocene of North Carolina, and the Cretaceous of New Jersey.

Figure 1. Cretaceous (A, C) and Eocene (B, D) specimens. Arrows indicate locations of tooth-bearing grooves. A. South Dakota Cretaceous specimen SDSM 30638 showing one of two grooves in which tooth pedicels and teeth are located. B. Eocene from North Carolina. The two wider grooves with tooth pedicels are visible running down the center Proceedings of the South Dakota Academy of Science, Vol. 96 (2017) 133 of the specimen. A and B are at the same scale. C. New Jersey Cretaceous specimen donated by Mr. Tony Fabian prior to sectioning. A line of tooth pedicels is visible running along the length of the specimen. Scale is in millimeters. The specimen as figured here was sacrificed; it is now preserved as histologic slides NJSM PH1 through NJSM PH7. D. Eocene specimen from North Carolina showing a closer view of the tooth pedicels in wider grooves near the middle and bottom of the image. C and D are at the same scale to facilitate comparison of tooth pedicel sizes in Cretaceous and Eocene specimens; scale is in millimeters. The specimen figured in B and D is in the private collection of Mr. Eric Sadorf.

METHODS

Transverse and longitudinal histologic thin sections were made through tooth pedicels on a Cretaceous Cylindracanthus specimen from New Jersey (now NJSM PH1 through PH7) and an Eocene Cylindracanthus specimen from North Carolina (NJSM 24275). Lesions on a second Eocene specimen from North Carolina (NJSM 24276) were sectioned. No Cylindracanthus teeth were sectioned due to the extreme rarity of tooth-bearing specimens. Transverse and longitudinal histologic sections were made on segments removed from the middle of the bill and predentary of an Atlantic blue marlin taxidermy mount (Makaira cf. nigricans, NJSM TC1061). One marlin bill longitudinal section was oriented horizontally to sample histology along the length of the tooth-bearing band that covers the lateral aspect of the bill. Polyodon (paddlefish) sections were cut from a dermal scale removed near the edge of the rostrum about a quarter of the way behind the tip of the rostrum and from the rostral portion of one of the nasal bones of a desiccated head collected from the Missouri River banks south of Yankton, South Dakota (NJSM B477). The Polyodon dermal scale was sectioned horizontally, parallel to its surface. Both a transverse section and a vertical (para- sagittal) longitudinal section were made of the paddlefish nasal bone. Histologic sections were prepared at the New Jersey State Museum by one of us (R.A.P). Fossil specimens were impregnated with Epo-tek 301 epoxy resin before thin sectioning; impregnation was done under vacuum to minimize bubbles. The modern Polyodon specimens were not impregnated prior to sectioning. Both transverse (mediolateral) and longitudinal (anteroposterior) histologic sections were made of Cylindracanthus, Makaira, and Polyodon. All thin sections were cut using a low-deformation wafer saw, ground flat on lap tables, then hand- finished and mounted on glass slides. Slide-mounted samples were processed on a Hillquist thin-section machine and hand polished to appropriate thickness for histologic study (approximately 0.1mm). Final polishing was done using cerium oxide from Covington Engineering. Photomicrographs were made using a Canon Rebel XSi EOS 450D camera and Clearshot 600 Digital Camera Adapter System for Canon SLR cameras from Alexis Scientific fitted to an Amscope Trinocular Polarizing Microscope. Photographs were made under both plane-polarized and cross-polarized light. The same Canon Rebel camera was used to make macro- photographs of intact specimens. Measurements on gross specimens were made with a bar caliper. 134 Proceedings of the South Dakota Academy of Science, Vol. 96 (2017)

Institutional Abbreviations. Specimens mentioned in this study are reposited at the Academy of Natural Sciences of Drexel University (ANSP), the Alabama Museum of Natural History (ASM), the New Jersey State Museum (NJSM), and the South Dakota School of Mines and Technology (SDSM). All histologic slides are reposited at the New Jersey State Museum’s paleohistology collection (NJSM PH). The South DakotaCylindracanthus , SDSM 30638, was collected from SDSM locality V9544. One specimen figured herein (Figure 1B, D) is in the private collection of Mr. Eric Sadorf of North Carolina.

RESULTS

The structure of Cylindracanthus is unusual in that the rostrum is made up of numerous wedge-shaped elements surrounding a central canal (paired at the base) that extends the length of the rostrum. Each wedge forms a ridge on the surface of the rostrum. Except for the presence of tooth pedicels and associated tissues, the transverse and longitudinal histologic sections of the Cretaceous (Figure 2A, B) and Eocene (Figure 2C, D) Cylindracanthus specimens in this study show the same fan-shaped array of small tubules within each wedge-shaped plate and the same porous zone between plates reported by Williamson (1849) and Carter (1927). The tooth pedicels are located in two wider inter-wedge grooves on the ventral side of the rostrum. Tooth pedicels are supported by a zone of irregular dense tissue that lacks the tubules seen within the wedges. Vascular channels lead into the tooth pedicels from deep within the rostrum. Histologic sections of the tooth pedicels of NJSM 24275 (Figure 2D) resemble the acro-protothecodontal attachment described by Gaengler (2000). Tooth Figure 2. Transverse histologic sections under plane-polarized light. A. NJSM PH1. Plates pedicels in all of the specimens we have examined conform to Gaengler’s group 4 flanking the tooth row in the rostrum of a Cretaceous specimen from New Jersey. Tissue acro-protothecodont attachment type, in which teeth are attached to the pedicel associated with the tooth pedicels is visible in the center of the image. The growth lines by a ring of connective tissue fibers and the pedicel is fused to the underlying jaw. described by Williamson (1849), which are essentially parallel to the ridge surface, are Tooth pedicels are hollow, and had a pulp cavity. The teeth sit with their bases labeled. B. NJSM PH1. Tissue lying within the tooth-bearing groove in the New Jersey directly against the top surface of the hollow pedicels (Figure 2D, 3A). Tooth Cretaceous specimen (arrow) at higher magnification. Williamson’s growth lines do surfaces are covered by enamel, which forms a translucent cap at the tips of the not penetrate into the tissue wedge associated with the tooth pedicels. The tubules teeth (Figure 3B). The teeth are recurved, with the tip of each tooth extending (labeled) that were described by both Williamson (1849) and Carter (1927) can be seen caudal to its base. fanning out from the ridge core. These tubules also do not penetrate the tooth groove Pitting was observed in two places on one North Carolina specimen (NJSM tissue. C. NJSM PH9. Tips of several plates making up the rostrum in NJSM 24275, an 24276, Figure 3C). This pitting could represent pathologic lesions or in vivo Eocene specimen from North Carolina. Each plate forms a ridge on the surface of the traumatic damage to the rostrum. The pits do not appear to have been produced rostrum. Two of the ridges can be seen coalescing in the middle of this image. A fan of by taphonomic abrasion to the specimen, since the pit edges and ridged surface radiating tubules is visible in the upper portion of each plate (ridge). D. NJSM PH8. texture of the specimen are not very worn. The bottoms of the pits have an irregu- Tooth pedicel (arrow) in NJSM 24275 (Eocene, North Carolina). Tubules are visible in lar surface, with variable depth. The pits have irregular edges that are undercut by the ridges flanking the tooth-bearing groove but do not extend into the tissue under- zones of tissue loss. Their overall appearance is unlike pits produced by boring lying the pedicel. This tooth pedicel is nearly centered in its groove, but pedicels can organisms or by tooth punctures. The pits are much wider and deeper than the also be confluent with one of the two ridges which border the tooth-bearing groove. shallow “feeding trace” grooves observed on another North Carolina specimen, NJSM 24278. Histologic sections were made across both lesions on NJSM 24276. While the lesions have irregular surfaces and extend almost to the central cavity of the rostrum, they lack any clear indication of activity by either Proceedings of the South Dakota Academy of Science, Vol. 96 (2017) 135

RESULTS

The structure of Cylindracanthus is unusual in that the rostrum is made up of numerous wedge-shaped elements surrounding a central canal (paired at the base) that extends the length of the rostrum. Each wedge forms a ridge on the surface of the rostrum. Except for the presence of tooth pedicels and associated tissues, the transverse and longitudinal histologic sections of the Cretaceous (Figure 2A, B) and Eocene (Figure 2C, D) Cylindracanthus specimens in this study show the same fan-shaped array of small tubules within each wedge-shaped plate and the same porous zone between plates reported by Williamson (1849) and Carter (1927). The tooth pedicels are located in two wider inter-wedge grooves on the ventral side of the rostrum. Tooth pedicels are supported by a zone of irregular dense tissue that lacks the tubules seen within the wedges. Vascular channels lead into the tooth pedicels from deep within the rostrum. Histologic sections of the tooth pedicels of NJSM 24275 (Figure 2D) resemble the acro-protothecodontal attachment described by Gaengler (2000). Tooth Figure 2. Transverse histologic sections under plane-polarized light. A. NJSM PH1. Plates pedicels in all of the specimens we have examined conform to Gaengler’s group 4 flanking the tooth row in the rostrum of a Cretaceous specimen from New Jersey. Tissue acro-protothecodont attachment type, in which teeth are attached to the pedicel associated with the tooth pedicels is visible in the center of the image. The growth lines by a ring of connective tissue fibers and the pedicel is fused to the underlying jaw. described by Williamson (1849), which are essentially parallel to the ridge surface, are Tooth pedicels are hollow, and had a pulp cavity. The teeth sit with their bases labeled. B. NJSM PH1. Tissue lying within the tooth-bearing groove in the New Jersey directly against the top surface of the hollow pedicels (Figure 2D, 3A). Tooth Cretaceous specimen (arrow) at higher magnification. Williamson’s growth lines do surfaces are covered by enamel, which forms a translucent cap at the tips of the not penetrate into the tissue wedge associated with the tooth pedicels. The tubules teeth (Figure 3B). The teeth are recurved, with the tip of each tooth extending (labeled) that were described by both Williamson (1849) and Carter (1927) can be seen caudal to its base. fanning out from the ridge core. These tubules also do not penetrate the tooth groove Pitting was observed in two places on one North Carolina specimen (NJSM tissue. C. NJSM PH9. Tips of several plates making up the rostrum in NJSM 24275, an 24276, Figure 3C). This pitting could represent pathologic lesions or in vivo Eocene specimen from North Carolina. Each plate forms a ridge on the surface of the traumatic damage to the rostrum. The pits do not appear to have been produced rostrum. Two of the ridges can be seen coalescing in the middle of this image. A fan of by taphonomic abrasion to the specimen, since the pit edges and ridged surface radiating tubules is visible in the upper portion of each plate (ridge). D. NJSM PH8. texture of the specimen are not very worn. The bottoms of the pits have an irregu- Tooth pedicel (arrow) in NJSM 24275 (Eocene, North Carolina). Tubules are visible in lar surface, with variable depth. The pits have irregular edges that are undercut by the ridges flanking the tooth-bearing groove but do not extend into the tissue under- zones of tissue loss. Their overall appearance is unlike pits produced by boring lying the pedicel. This tooth pedicel is nearly centered in its groove, but pedicels can organisms or by tooth punctures. The pits are much wider and deeper than the also be confluent with one of the two ridges which border the tooth-bearing groove. shallow “feeding trace” grooves observed on another North Carolina specimen, NJSM 24278. Histologic sections were made across both lesions on NJSM 24276. While the lesions have irregular surfaces and extend almost to the central cavity of the rostrum, they lack any clear indication of activity by either 136 Proceedings of the South Dakota Academy of Science, Vol. 96 (2017)

osteoclasts or osteoblasts (Figure 3D). No osteocyte lacunae are visible in associa- tion with either lesion. A second North Carolina specimen, collected by one of us (D. C.), also has surface pits. This specimen (NJSM 24279) is quite worn and the pit edges are rounded, suggesting they could result from taphonomic modi- fication. This specimen comes from near the distal end of the rostrum, in the area where the central canal is small. It has not yet been sectioned. Wall thickness (the distance between the outer surface of the canal and the surface of the specimen) and central canal diameter vary along the length of the Cylindracanthus rostrum. The wall is comparatively thin and the central canal is wide at the base of the rostrum. It is thicker, relative to the central canal in the distal part of the rostrum. The central canal at the base of NJSM 24277, an Eocene specimen from the Castle Hayne Formation in North Carolina, is about 8 mm wide and 6 mm high; basal wall thickness of this specimen is about 3 mm. Diameter of the canal is only about 3 mm closer to the tip of the rostrum, with a wall thickness of about 4 mm. In the Cretaceous South Dakota specimen (SDSM 30638), the central cavity is about 4 mm wide at the caudal end of the specimen, with a wall thickness of about 5 mm. Closer to the tip of the South Dakota specimen the central cavity is about 3 mm across, and the wall thickness is about 3 mm. The thin proximal walls of the rostrum could have represented a zone of weakness during lateral strikes. Any inherent weakness in the basal part of Cylindracanthus rostra might explain why the rostra are always found in isolation, with no associated skeletal elements. The distal end of the rostrum is preserved in the Cretaceous Alabama specimen, ASM-PV994.2.111 (Figure 3E). In this specimen, the top of the rostrum is quite worn, yet its base is relatively unworn and retains sharply defined ridges. The tip wear does not appear to be taphonomic. This wear may have occurred during the life of the animal, and supports use of the rostrum as a stabbing weapon. The presence of two rows of backwardly-pointing teeth would have provided a fric- tion surface that might have helped the animal procure food, possibly by extract- ing ammonites from their shells. The Castle Hayne Formation of North Carolina preserves a second fish taxon Figure 3. A. Tooth pedicels (white arrows) on the South Dakota Cretaceous specimen that has an elongated, billfish-like rostrum. This taxon has wide bands of small (SDSM 30638). Tooth pedicels tilt toward the caudal end of the rostrum; each is approx- tooth pedicels on its ventral surface. Some “Cylindracanthus group” taxa have imately 1 mm in diameter. B. Teeth on SDSM 30638. Tooth crowns slope toward the similar tooth-bearing bands (Fierstine 1974 2001; Fierstine and Applegate 1974). caudal end of the rostrum, with the tip of each tooth overlapping the base of the tooth Leriche (1908) reported tooth pedicels in specimens of Glyptorhynchus, a genus caudal to it. Tooth tips are covered in translucent enamel (white arrows). Photographs in he had erected (Leriche 1905) to replace Coelorhynchus Agassiz. He later (1910) both A and B are 5 mm long, with caudal to the left. C. NJSM 24276 prior to sectioning, restricted Glyptorhynchus to G. denticulatus, a species with broad bands of tooth showing pits (possibly pathologic lesions) on a rostrum from North Carolina (dashed pedicels extending along the length of the rostrum. Glyptorhynchus was originally circles). D. NJSM PH12. Transverse histologic section of the larger lesion at the right end proposed as a replacement for Coelorhynchus sensu Agassiz, and restricting the of NJSM 24276 (as shown in C) in plane-polarized light. The surface of the rostrum is to genus to G. denticulatus is invalid (Purdy et al. 2001). Casier (1946) therefore cre- the upper right in this image. Arrowheads point toward a dense layer that covers parts ated a new genus, Hemirhabdorhynchus, for G. denticulatus. Fierstine (1974) and of the tissue around the lesion. S = sediment grains partially filling the lesion. E. Worn Fierstine and Applegate (1974) included Hemirhabdorhynchus in their informal tip of Alabama Cretaceous rostrum (ASM-PV 994.2.111). Scale is in millimeters. F. Detail “Cylindracanthus group”. Hemirhabdorhynchus (Leriche 1910; Purdy et al. 2001) of tip wear on the Alabama Cretaceous rostrum (ASM-PV 994.2.111). and Aglyptorhynchus (Weems 1999; Fierstine 2001, 2005; Monsch 2005) rostra have broad bands of tooth attachments on the ventral surface; both resemble the non-Cylindracanthus rostra found in North Carolina. Hemirhabdorhynchus has 138 Proceedings of the South Dakota Academy of Science, Vol. 96 (2017) been recovered from Miocene sediments in North Carolina (Purdy et al. 2001). Both Hemirhabdorhynchus and Aglyptorhynchus are known from more complete remains than is Cylindracanthus. Additional cranial and postcranial remains are known for Aglyptorhynchus (Fierstine 2001, 2005), and vertebral material has been found with rostra of Hemirhabdorhynchus (Purdy et al. 2001). Histology of Cylindracanthus was compared to that of a modern billfish, an Atlantic marlin, and to a modern paddlefish because Cylindracanthus has pre- viously been classified as Xiphiidae incertae sedis or hypothesized as a possible chondrostean. Histology of the bill and predentary (Figure 4A-C) of the marlin (NJSM TC1061: Makaira cf. nigricans) is quite different from histology of the Cylindracanthus rostrum. The radial structure of the Cylindracanthus rostrum is seen both in its gross morphology and histologically (Figure 2). Histologic sections of the marlin are dominated by longitudinal canals (Figure 4B). Teeth are located in wide bands that extend along the lateral edges of the rostrum (Figure 4A) and form a shagreen covering the oral surface of the predentary (Figure 4C). The teeth are not confined in a groove, as they are in Cylindracanthus, but rather are located on the bone surface. Marlin teeth are smaller than those of Cretaceous Cylindracanthus. They are short and blunt, rather than long, sharply pointed, and recurved. Marlin tooth attachment rings are barely visible to the unaided eye, whereas tooth pedicels in both Cretaceous and Eocene Cylindracanthus are easily visible. Polyodon spathula (paddlefish, NJSM B477) histology was examined for both a cranial osteoderm (Figure 4C, D) and in a skull bone, the nasal (Figure 4F). Osteocytes are present in both. Bone histology of Polyodon is very different from that of both Cylindracanthus and the living blue marlin, neither of which shows clear evidence of osteocyte lacunae. Internal structure of the Polyodon nasal is dominated by circumferential organization of growth lines and osteocyte lacunae. Weisel (1975) reported that osteocytes are present in dermal denticles located on the back and sides of Polyodon. While he described the gross appearance of Polyodon rostral squamation, Weisel did not describe the histology of rostral scutes. Sturgeons (Acipenser) also have cellular bone in both their axial skeleton Figure 4. Histologic thin sections of blue marlin (NJSM TC1061) and paddlefish (NJSM and their dermal scutes (Leprévost et al. 2017). B477) bones. Both animals are adults. A. NJSM PH18. Transverse section of the lateral edge of the marlin bill showing the lateral tooth band. B. NJSM PH19. Horizontal longitudinal section taken at mid-length of the marlin bill showing teeth (upper edge) and DISCUSSION underlying longitudinal canals in the bone. C. NJSM PH17. Transverse section taken at mid-length of the marlin predentary showing the surface shagreen of small teeth, Several conclusions can be drawn from this comparison of Cylindracanthus covered by a thin epidermis. The dentine basal portions of four of the teeth are marked bone histology to the histology of extant holosteans (paddlefish, sturgeon) and (*). The rounded, enamel-covered crowns of two of these teeth are visible just below the billfish (the marlin). These are: epidermis. A-C were taken in cross-polarized light. D. NJSM PH21. Paddlefish rostral 1. Cylindracanthus bone histology differs from that of both billfish (Atkins et scute in horizontal longitudinal section. This section was taken parallel to the surface al. 2014) and paddlefish (Weisel 1975). Our histologic sections confirm of a scute from approximately the mid-length of the rostrum. Numerous osteocytes are these differences. visible even at this magnification. E. NJSM PH21. Higher magnification view of osteo- 2. Gross similarity of the Cylindracanthus rostrum to the billfish rostrum is cytes and canaliculi in the paddlefish rostral scute. F. NJSM PH14. Paddlefish nasal bone hypothesized to be functional convergence – as is the similarity between in transverse section. This section comes from midway along the anterior-to-posterior the rostra of billfish and sawfish. The complex function (or functions) of length of the nasal bone. Osteocytes are arranged along the surfaces of layers that the billfish rostrum are still not completely understood. The rostrum can parallel the surface of the nasal bone. Three of the osteocytes are indicated by arrows. affect hydrodynamic drag during swimming (Sagong et al. 2013). It can D-F were taken in plane-polarized light. Proceedings of the South Dakota Academy of Science, Vol. 96 (2017) 139 been recovered from Miocene sediments in North Carolina (Purdy et al. 2001). Both Hemirhabdorhynchus and Aglyptorhynchus are known from more complete remains than is Cylindracanthus. Additional cranial and postcranial remains are known for Aglyptorhynchus (Fierstine 2001, 2005), and vertebral material has been found with rostra of Hemirhabdorhynchus (Purdy et al. 2001). Histology of Cylindracanthus was compared to that of a modern billfish, an Atlantic marlin, and to a modern paddlefish because Cylindracanthus has pre- viously been classified as Xiphiidae incertae sedis or hypothesized as a possible chondrostean. Histology of the bill and predentary (Figure 4A-C) of the marlin (NJSM TC1061: Makaira cf. nigricans) is quite different from histology of the Cylindracanthus rostrum. The radial structure of the Cylindracanthus rostrum is seen both in its gross morphology and histologically (Figure 2). Histologic sections of the marlin are dominated by longitudinal canals (Figure 4B). Teeth are located in wide bands that extend along the lateral edges of the rostrum (Figure 4A) and form a shagreen covering the oral surface of the predentary (Figure 4C). The teeth are not confined in a groove, as they are in Cylindracanthus, but rather are located on the bone surface. Marlin teeth are smaller than those of Cretaceous Cylindracanthus. They are short and blunt, rather than long, sharply pointed, and recurved. Marlin tooth attachment rings are barely visible to the unaided eye, whereas tooth pedicels in both Cretaceous and Eocene Cylindracanthus are easily visible. Polyodon spathula (paddlefish, NJSM B477) histology was examined for both a cranial osteoderm (Figure 4C, D) and in a skull bone, the nasal (Figure 4F). Osteocytes are present in both. Bone histology of Polyodon is very different from that of both Cylindracanthus and the living blue marlin, neither of which shows clear evidence of osteocyte lacunae. Internal structure of the Polyodon nasal is dominated by circumferential organization of growth lines and osteocyte lacunae. Weisel (1975) reported that osteocytes are present in dermal denticles located on the back and sides of Polyodon. While he described the gross appearance of Polyodon rostral squamation, Weisel did not describe the histology of rostral scutes. Sturgeons (Acipenser) also have cellular bone in both their axial skeleton Figure 4. Histologic thin sections of blue marlin (NJSM TC1061) and paddlefish (NJSM and their dermal scutes (Leprévost et al. 2017). B477) bones. Both animals are adults. A. NJSM PH18. Transverse section of the lateral edge of the marlin bill showing the lateral tooth band. B. NJSM PH19. Horizontal longitudinal section taken at mid-length of the marlin bill showing teeth (upper edge) and DISCUSSION underlying longitudinal canals in the bone. C. NJSM PH17. Transverse section taken at mid-length of the marlin predentary showing the surface shagreen of small teeth, Several conclusions can be drawn from this comparison of Cylindracanthus covered by a thin epidermis. The dentine basal portions of four of the teeth are marked bone histology to the histology of extant holosteans (paddlefish, sturgeon) and (*). The rounded, enamel-covered crowns of two of these teeth are visible just below the billfish (the marlin). These are: epidermis. A-C were taken in cross-polarized light. D. NJSM PH21. Paddlefish rostral 1. Cylindracanthus bone histology differs from that of both billfish (Atkins et scute in horizontal longitudinal section. This section was taken parallel to the surface al. 2014) and paddlefish (Weisel 1975). Our histologic sections confirm of a scute from approximately the mid-length of the rostrum. Numerous osteocytes are these differences. visible even at this magnification. E. NJSM PH21. Higher magnification view of osteo- 2. Gross similarity of the Cylindracanthus rostrum to the billfish rostrum is cytes and canaliculi in the paddlefish rostral scute. F. NJSM PH14. Paddlefish nasal bone hypothesized to be functional convergence – as is the similarity between in transverse section. This section comes from midway along the anterior-to-posterior the rostra of billfish and sawfish. The complex function (or functions) of length of the nasal bone. Osteocytes are arranged along the surfaces of layers that the billfish rostrum are still not completely understood. The rostrum can parallel the surface of the nasal bone. Three of the osteocytes are indicated by arrows. affect hydrodynamic drag during swimming (Sagong et al. 2013). It can D-F were taken in plane-polarized light. 140 Proceedings of the South Dakota Academy of Science, Vol. 96 (2017)

be used as a defensive or offensive weapon (Shimose et al. 2007; Habegger et al. 2015). Rostra of some taxa, including paddlefish, have electrosen- sory organs that can assist in locating prey (Wueringer et al. 2012). The Cylindracanthus rostrum is morphologically more similar to the bill of a marlin than the rostrum of a swordfish. The marlin bill can be used for strikes from a variety of directions (Habegger et al. 2015), but the thin wall bounding the central cavity in the proximal part of the Cylindracanthus rostrum could have been a zone of weakness that might fracture during lateral strikes. A marlin bill may not be the best mechanical analog for the Cylindracanthus rostrum. 3. The tissue of Cylindracanthus is acellular. The cells that produced the calcified rostral tissue were probably located in a periosteum, as sug- gested by Meunier (2011) for other fishes with acellular bone. Osteoblasts might also have resided in the central canal. No soft tissue is preserved in Cylindracanthus, and osteoblast location in this genus cannot be known for certain. The surface of NJSM 24278, a specimen from the Eocene Castle Hayne Formation in North Carolina, has clusters of short, narrow, steep- sided scrapes that were probably produced by postmortem scavengers. These marks suggest there was at least a thin tissue layer on the surface of the rostrum during life. 4. Phylogenetic relationships of Cylindracanthus remain unclear. Meunier and Huysseune (1992) considered the distribution of cellular bone in Osteichthyes to be plesiomorphic, and that of acellular bone to be apo- morphic in higher teleosts, but Meunier later (2011) described loss of bone cells as a heterochronic process. While the presence of acellular bone in the rostrum can support placement of Cylindracanthus within derived teleosts (Meunier and Huysseune 1992; contra Parris et al. 2001, 2007) it does little to clarify where this genus might lie within teleosts. Kranenbarg et al. (2005) demonstrated that acellular bone is found in multiple actinopterygian clades. More recent phylogenetic interpretations (Near et al. 2012) do not alter the paraphyletic nature of acellular bone distribution within ray-finned fishes. 5. The greatest similarity of the Cylindracanthus rostrum, the only skeletal element known in this genus, is to rostra of other extinct fishes. Except for the presence of tooth pedicels (and the associated wedge of tissue support- ing the pedicels) transverse histologic sections of Cylindracanthus are very similar to a transverse histologic section of Glyptorhynchus that Fierstine published (at three magnifications) in 1974 (see his figure 14). Carter (1927) noted histologic similarities between Cylindracanthus and Blochius, and Fierstine (1974, 2001) has placed the “Cylindracanthus group” within the Blochiidae. 6. Fierstine (1974, 2001) and Fierstine and Applegate (1974) considered the relationship of “Cylindracanthus-group” genera to Xiphoidei to be questionable; the presence of acellular bone in Cylindracanthus does not change that interpretation. Unraveling the phylogenetic relationships of Cylindracanthus still awaits the discovery of more complete specimens. Proceedings of the South Dakota Academy of Science, Vol. 96 (2017) 141

ACKNOWLEDGMENTS

The authors thank Gudni A. “Tony” Fabian for his generous donation of a Cretaceous specimen from New Jersey. We thank Eric Sadorf and Joy Harrington for allowing us to study specimens in their private collections. We are grateful for the financial support provided by the Richards Fund of the New Jersey State Museum Foundation. The wafer saw and lap table used to produce the histologic slides used in this study were donated by Derek Yoost. The Amscope petrographic microscope used to study and photograph the slides was donated by the Bergen County Mineralogical Society. This manuscript was greatly improved by suggestions from Drs. Robert Carlton and Lincoln Hollister, and by the suggestions of an anonymous reviewer.

LITERATURE CITED

Adnet, S., H. Cappetta, and R.A.Tabuce. 2010. Middle-Late Eocene vertebrate fauna (marine fish and mammals) from southwestern Morocco; preliminary report: age and palaeobiogeographical implications. Geological Magazine 147(6):860-870. Agassiz, L. 1833-1843. Recherches sur les Poissons Fossiles. vol.5, p.92. Atkins, A., M.N. Dean, M.L. Habegger, P.J. Motta, L. Ofer, F. Repp, A. Shipov, S. Weiner, J.D. Currey, and R. Shahar. 2014. Remodeling in bone without osteocytes: Billfish challenge bone structure–function paradigms. PNAS 111(45):16047-16052. Available at www.pnas.org/cgi/doi/10.1073/ pnas.1412372111 Carter, J. T. 1927. The rostrum of the fossil swordfish Cylindracanthus, Leidy (Coelorhynchus, Agassiz), from the Eocene of Nigeria. Geological Survey of Nigeria Occasional Paper 5. 15 pages, 11 plates. Casier, E. 1946. La faune ichthyologique de l’Yprèsien de la Belgique. Mèmoires du Musée Royal d’Histoire Naturelle de Belgique 104:1-267, 6 plates. Dixon, F. 1850. The Geology and Fossils of the Tertiary and Cretaceous Formations of Sussex. Longman, Brown, Green, and Longmans, London. 558pages. Fierstine, H.L. 1974. The paleontology of billfish – the state of the art. In: Shomura, R.S. and Williams, F. (eds): Proceedings of the International Billfish Symposium Kailua-Kona, Hawaii, 9-12 August 1972. Part 2. Review and Contributed Papers. NOAA Technical Report NJFS SSRF-675. U.S. Department of Commerce. Pages 34-44. Fierstine, H.L. 2001. A new †Aglyptorhynchus (Perciformes: Scrombroidei: †?Blochiidae) from the Late Oligocene of Oregon. Journal of Vertebrate Paleontology 21(1):24-33. Fierstine, H.L. 2005. A new Aglyptorhynchus (Perciformes: Scombroidei) from the Lincoln Creek Formation (Late Oligocene, Washington, U.S.A.). Journal of Vertebrate Paleontology 25(2):288-299. Fierstine, H.L. and Applegate, S.P. 1974. Xiphiorhynchus kimblalocki, a new billfish from the Eocene of Mississippi with remarks on the systematics of 142 Proceedings of the South Dakota Academy of Science, Vol. 96 (2017)

xiphioid fishes. Bulletin of the Southern California Academy of Sciences 73(1):14-22. Friedman, M., 2012. Ray-finned fishes (Osteichthyes, Actinopterygii) from the type Maastrichtian, the Netherlands and Belgium Scripta Geologica 8: 113-142. Gaengler, P. 2000. Evolution of tooth attachment in lower vertebrates to tetrapods. In: Teaford, M.F., Smith, M.M., and Ferguson, M.W.J. (eds) Development, Function and Evolution of Teeth. Pages 173-185. Cambridge University Press, 314pp. Paperback reissue printed in the U.K. by Lightning Source UK Ltd, Milton Keynes. Habegger, M.L, M.N. Dean, J.W.C. Dunlop, G. Mullins, M.Stokes, D.R. Huber, D. Winters, and P.J. Motta. 2015. Feeding in billfishes: inferring the role of the rostrum from a biomechanical standpoint. Journal of Experimental Biology 218:824-836. Kranenbarg, S., T. van Cleynenbreugel, H. Schipper, and J. van Leeuwen. 2005. Adaptive bone formation in acellular vertebrae of sea bass (Dicentrarchus labrax L.). Journal of Experimental Biology 208:3493-3502. Leidy, J. 1857a. Description of two ichthyodorulites. Proceedings of the Academy of Natural Sciences of Philadelphia 8:11-12. Leidy, J. 1857b. Remarks on certain extinct species of fishes. Proceedings of the Academy of Natural Sciences of Philadelphia 8:301-302. Leprévost, A., T. Azaïs, M. Trichet, and J.-Y. Sire. 2017. Vertebral development and ossification in the Siberian sturgeon (Acipenser baerii), with new insights on bone histology and ultrastructure of vertebral elements and scutes. The Anatomical Record 300:437-449. Leriche, M. 1905. Les Poissons Éocènes de la Belgique. Mémoires du Musée Royal d’Histoire Naturelle de Belgique T.III:57-228. Leriche, M. 1908. Note préliminaire sur de Poissons nouveaux de l’Oligocène belge. Bulletin de la Société Belge de Géologie de Paléontologie et d’Hydrologie 22:378-384. Leriche, M. 1910. Les Poissons Oligocènes de la Belgique. Memoires du Musée Royal d’Histoire Naturelle de Belgique V:229-363, plus 15 plates. Meunier, F.J. 2011.The osteichthyes, from the Paleozoic to the extant time, through histology and palaeohistology of bony tissues. Comptes Rendus Palevol 10:347-355. Meunier, F.J., and A. Huysseune. 1992.The concept of bone tissue in Osteichthyes. Netherlands Journal of Zoology 42(2-3):445-458. Monsch, K.A. 2005. Revision of the scrombroid fishes from the Cenozoic of England. Transactions of the Royal Society of Edinburgh: Earth Sciences 95:445-489. Near, T.J., R.I. Eytan, A. Dornburg, K.L. Kuhn, J.A. Moore, M.P. Davis, P.C. Wainwright, M. Friedman, and W.L. Smith. 2012. Resolution of ray-finned fish phylogeny and timing of diversification. PNAS 109:13698-13703. Parris, D.C., B.S. Grandstaff, and G.L. Bell. 2001. Reassessment of the Affinities of the Extinct Genus Cylindracanthus (Osteichthyes). Proceedings of the South Dakota Academy of Science 80:161-172. Proceedings of the South Dakota Academy of Science, Vol. 96 (2017) 143

Parris. D.C., B.S. Grandstaff, and W.B. Gallagher. 2007. Fossil fishes from Pierre Shale Group – clarifying the fossil record. Geological Society of America Special Paper 427:99-109. Purdy, R.W., V.P. Schneider, S.P. Applegate, J.H. McLellan, R.L. Meyer, and R.H. Slaughter. 2001. The Neogene sharks, rays, and bony fishes from Lee Creek Mine, Aurora, North Carolina. in Ray, C.E. and D.J. Bohaska, (editors) Geology and Paleontology of the Lee Creek Mine, North Carolina, III. Smithsonian Contributions to Paleontology 90:71-202. Sagong, W., W.-P Jeon, and H. Choi. 2013. Hydrodynamic characteristics of the sailfish (Istiophorus platypterus) and swordfish (Xiphias gladius) in glid- ing postures at their cruise speeds. PLOS One 8(12), p.e81323. Available at http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0081323 [5/12/2017] Shimose, T., K. Yokawa, H. Saito, and K. Tachihara. 2007.Evidence for use of the bill by blue marlin, Makaira nigricans, during feeding. Ichthyological Research 54(4):420-422. Smith Woodward, A. 1888. On the fossil fish-spines named Coelorhynchus Agassiz. Annals and Magazine of Natural History vol 2 – 6th series:223-226. Smith Woodward, A. 1891. Catalogue of the Fossil Fishes in the British Museum (Natural History) Part II. Printed for the Trustees of the British Museum by Longmans and Company, London. 700 pages. Vullo, R., E. Bernárdez, and A.D. Buscalioni,. 2009. Vertebrates from the middle?-late Cenomanian La Cabaña Formation (Asturias, northern Spain): Palaeoenvironmental and palaeobiogeographic implications. Palaeogeography, Palaeoclimatology, Palaeoecology 276:120-129. Weems, R.E. 1999. Part 4. Actinopterygian fishes from the Fisher/Sullivan Site. in Weems, R.E. and G.J. Grimsley (editors). Early Eocene Vertebrates and Plants from the Fisher/Sullivan Site (Nanjemoy Formation) Stafford County, Virginia. Virginia Division of Mineral Resource Publication 152, pages 53-100. Weisel, G.F., 1975. The integument of the paddlefish, Polyodon spathula. Journal of Morphology 145(2), pp.143-150 Williamson, W.C. 1849. On the microscopic structure of the scales and dermal teeth of some ganoid and placoid fish. Philosophical Transactions of the Royal Society of London 139:435-475. Wueringer, B.E., L. Squire, S.M. Kajiura, N.S. Hart, and S.P. Collin. 2012. The function of the sawfish’s saw. Current Biology 22(5), R150-R151