First report in the fossil record of a shark tooth embedded in a pinniped bone

There are now many examples in the fossil record of shark bite marks preserved on biogenic materials including coprolites, ammonoids, sea star ossicles, an echinoid, and bone and calcified cartilage. These exceptional fossils document evidence of exploratory behavior, active predation, and/or scavenging.

Godfrey S. J. et al.
However, only a small subset report on the presence of shark teeth embedded in fossilized bone or cartilage.Although a few shark tooth-marked seal bones are known from the fossil record, no direct evidence of predation or scavenging in the form of a shark tooth embedded in a fossil seal bone has yet been documented.Herein, we describe the first shark tooth embedded in a seal (Phocidae Gray, 1821) bone, a calcaneum (CMM-V-6964), that was surface collected in Mosaic's South Fort Meade Mine, Hardee County, Fort Meade, Florida, United States.The isolated bone originated from within the Bone Valley Member of the Peace River Formation (Hawthorn Group).The partial tooth is identified as having come from an Early Pliocene great white shark, Carcharodon carcharias (Linnaeus, 1758).This discovery also represents the first C. carcharias tooth ever found embedded in a fossil bone.The embedded tooth may have come about as a result of active predation or scavenging.The extant macropredatory sharks, Carcharodon carcharias (great white shark), Notorynchus cepedianus (Péron, 1807) (sevengill shark), Somniosus microcephalus (Bloch & Schneider, 1801) (the Greenland shark), and Somniosus antarcticus Whitley, 1939 (sleeper shark), are known to actively prey upon seals (Pinnipedia Illiger, 1811).If this peculiar fossil association resulted from active predation, the seal did not survive the encounter because there is no evidence of healing in the area around the embedded shark tooth.
Extant great white sharks (Carcharodon carcharias (Linnaeus, 1758)), sevengill sharks (Notorynchus cepedianus (Péron, 1807)), and Greenland and sleeper sharks (Somniosus microcephalus (Bloch &Schneider, 1801) andS. antarcticus Whitley, 1939) are known to actively prey upon seals, although there is strategic diversity in the ways in which they go about it (Ebert 1991: fig. 3;Klimley et al. 1996;Martin et al. 2005;Hammerschlag et al. 2006;Hoff & Morrice 2008;Laroche et al. 2008;Lucas & Natanson 2010;Martin & Hammerschlag 2012;Watanabea et al. 2012;Fallows et al. 2013).Sluggishly-slow swimming Greenland and sleeper sharks simply latch onto sleeping seals (Hoff & Morrice 2008;Watanabea et al. 2012), whereas great white sharks stalk and strike their phocid prey Shark tooth embedded in a pinniped bone from below or behind at speed (Martin & Hammerschlag 2012).Sevengill sharks employ a range of predatory strategies including burst speed, ambush, stealth, and social facilitation (Ebert 1991).While a few shark-bitten pinniped bones are known from the fossil record (Bigelow 1994;Govender & Chinsamy 2013;Boessenecker et al. 2014;Collareta et al. 2017;Govender 2021), no direct evidence of predation or scavenging in the form of a shark tooth embedded in a fossil seal bone has yet been reported.Herein, we describe the first shark tooth embedded in a seal (Phocidae Gray, 1821) bone, a calcaneum.Furthermore, the partial tooth is identified as that of a great white shark, Carcharodon carcharias, the first report in the fossil record of a tooth from this species of shark embedded in bone.Ames & Morejohn (1980) reported on the presence of an extant white shark tooth embedded in the skull of the sea otter, Enhydra lutris (Linnaeus, 1758), and Ehret et al. (2009Ehret et al. ( , 2012) )

MATERIAL AND METHODS
Herein, we describe a single seal calcaneum (CMM-V-6964), bearing the partial crown of an embedded shark tooth and possible shark bite marks.The specimen is housed in the Calvert Marine Museum (CMM).
The specimen was photographed on black velvet under flourescent light with a Nikon Coolpix P510 camera.The individual images were edited in Adobe Photoshop® and Figures 1-3 were assembled in Adobe Illustrator®.

GeoloGic settinG
The shark-bitten seal calcaneum, CMM-V-6964 (Fig. 1), was collected in April 2008 by author P. M. in Hardee County, Fort Meade, Florida, United States, at Mosaic's South Fort Meade Mine, presumably from the Bone Valley Member of the Peace River Formation (Hawthorn Group).CMM-V-6964 was not collected in situ, but rather from a spoil pile within the mine at approximately 27°29'58.52"N,82°06'05.93"W.Consequently, the precise stratigraphic provenance within the mine is not known.The Bone Valley Member was formerly the Bone Valley Formation of Matson & Clapp (1909), but was redefined as a member of the Peace River Formation by Scott (1988) due to the limited areal extent of the unit.The Peace River Formation comprises two subunits (both within the Bone Valley Member), an Upper Miocene unit (c.11-8.5 Ma) and a Lower Pliocene unit (c.5.2-4.3Ma) based on biostratigraphy, magnetostratigraphy, and strontium isotopes (Guertin 1998;Guertin et al. 1999Guertin et al. , 2000)).The vertebrate assemblage within the younger Pliocene unit has been described as the Bone Valley Fauna or the Palmetto Fauna and is assigned to the Hemphillian North American Land Mammal Age (Sellards 1916;Simpson 1930;MacFadden & Webb 1982;Webb & Crissinger 1983;Hulbert 2001;Webb et al. 2008).There are two specimens of Carcharodon carcharias known from the Pliocene Palmetto Fauna that are cataloged in the Florida Museum vertebrate paleontology collection (UF-VP-17916 and UF-VP-93661).There are no known definitive occurrences of C. carcharias from Florida prior to the Hemphillian (Perez 2022a, b); therefore, the seal calcaneum and embedded tooth most likely originated from the Lower Pliocene unit (Hemphillian NALMA/Zanclean Stage) of the Bone Valley Member within the Peace River Formation.
Description CMM-V-6964 is an almost complete, isolated right calcaneum with a maximum length of 78 mm (Fig. 1).Major anatomical features including the calcaneal tubercle, the cuboid articular facet, the sulcus for m. peroneus longus and the troclear sulcus confirm its identity as a calcaneum.The taxonomic identity of the calcaneum is discussed below.
Only a small portion of the tip of the shark tooth remains embedded in the calcaneum.The crown is embedded in the lateral surface of the bone immediately distal to the sulcus for m. peroneus longus (Fig. 1B).The broken enameloid edge of the tooth is fractured and ragged (Fig. 2), measuring 6.12 mm wide.The crown is infilled with osteodentine (Fig. 2B), with no evidence of a pulp cavity.Six serrations are visible along the cutting edge above the point where the tip of the tooth is embedded in the bone.The apex of each serration is very nearly evenly rounded and differing only slightly in size (Fig. 2B).The identification of this tooth as belonging to a great white shark is discussed below.
In addition to the anatomical features, and the embedded shark tooth shown in Figure 1, the outer surface of the calcaneum also preserves at least seven small roughly circular breaks/shallow depressions in the compact (i.e., cortical) bone (some of which are indicated by the black arrows in Figure 1).DISCUSSION iDentity of the prey A distinguishing characteristic of the calcaneum of Phocidae is the proportionally short medial and lateral tubercles (Fig. 1).Among Carnivora, this characteristic is shared only with Allodesmus Kellogg, 1922 and Odobenidae Allen, 1880  The height/length ratio of the calcaneum is approximately 48 mm/78 mm = 0.615.This groups with ratios observed among extant Lobodontini Gray, 1869 (0.583-0.633; notice that this ratio refers to extant Lobodontini), but exceeds the ratios observed in other extant and extinct Monachinae Gray, 1869 (0.509-0.541; the latter referring to Mirounga Gray, 1827 and Monachini Trouessart, 1897) and certainly Phocinae (0.444-0.500), in which the calcaneum is comparatively longer and less high (Muizon 1981: table 8).Furthermore, the sulcus for m. peroneus longus and the trochlear sulcus are well outlined in CMM-V-6469, a feature shared among Monachinae.Consequently, CMM-V-6469 is tentatively identified as a calcaneum from a monachine phocid.
Moreover, with a total length of 78 mm, the calcaneum is large for a monachine.Comparing it to the measurements presented by de Muizon (1981), this calcaneum is notably smaller than the exceptionally large elephant seals of the genus Mirounga, but slightly larger than the length of the calcaneum of the leopard seal Hydrurga leptonyx (de Blainville, 1820) as presented by de Muizon (1981): 76 mm.With a body length between 2.9 and 3.6 m, H. leptonyx is considered the largest extant phocid after the elephant seals Mirounga angustirostris (Gill, 1866) and Mirounga leonina (Linnaeus, 1758).Thus, with a length exceeding that of the calcaneum of the extant leopard seal Hydrurga leptonyx, CMM-V-6469 likely originated from a large seal, apparently exceeding 3 m in total body length.Koretsky & Ray (2008)  unequivocally be assigned to any of these, pending the discovery of more complete specimens including associated and articulated bones.Based on the size of the type specimens alone, S. magnus is the most likely candidate, estimated by Rule et al. (2020) to have had a body length of 2.83 m.Unfortunately, the incompleteness of the fossil record for these species makes identifying the most likely candidate uncertain.
CMM-V-6964 compares favorably to two calcanea (USNM PAL 205850 and 529247) from the Pliocene, Yorktown Formation, both found in the Aurora Phosphate Mine, Aurora, North Carolina, United States (Fig. 3).USNM PAL 205850 (Fig. 3A, D) is a right calcaneum from a partial but associated pes that Koretsky & Ray (2008: fig. 38) attributed to Callophoca obscura.USNM PAL 529247 (Fig. 3C, F) is a taxonomically unassigned and isolated left calcaneum (reflected in Figure 3) that is larger, more complete and better preserved than CMM-V-6964.Other than differing in size (one smaller and the other larger), both of the Yorktown Formation phocid calcanea are virtually identical to that of CMM-V-6964 (Fig. 3B, E).Despite their overall morphological similarity, an isolated calcaneum hardly seems to be sufficient to confirm the identity of a phocid to the specific level.Furthermore, given the historical and taxonomic uncertainties surrounding Callophoca obscura (see Rule et al. 2020), we do not think it prudent to assign CMM-V-6964 to that binomen, even though they may be conspecific (whatever USNM PAL 205850 turns out to be, Callophoca obscura or otherwise).Therefore, we will content ourselves with identifying the great white shark partial toothembedded seal calcaneum as monachine phocid in origin.iDentity of the preDAtor A total of 29 chondrichthyan genera, belonging to eight different orders, have been recognized from the Bone Valley Member of the Peace River Formation (Perez 2022a, b).Among these genera, only nine include taxa with serrated teeth.Assuming the tooth is broken close to the crown tip, the symmetry and size of the tooth fragment (6.12 mm wide) embedded in CMM-V-6964 further reduces the potential contenders to three possible taxa: Carcharodon carcharias, Hemipristis serra Agassiz, 1843 and Otodus megalodon (Agassiz, 1835).While all three taxa have large, serrated teeth, the size, shape and spacing of the serrations varies widely between them.Both Otodus megalodon and Hemipristis serra have serrations that are relatively uniformly spaced, whereas Carcharodon carcharias has more irregularly spaced serrations similar to the tooth fragment embedded in CMM-V-6964.
In addition to the tooth size and shape, we can also consider the tooth histology.Shark teeth can be categorized into three histotypes: orthodont, pseudoosteodont, and osteodont (Jambura et al. 2020).These histotypes correspond with the dentine patterns that underlie the enameloid crown and are reflective of the evolutionary history of different taxonomic groups.The tooth fragment in CMM-V-6964 lacks evidence of a pulp cavity and would consequently be assigned to the osteodont histotype (Kent 1994).The osteodont histotype is exclusively exhibited by lamniform sharks, which provides further evidence that the tooth could not have come from a carcharhiniform shark (e.g.Hemipristis serra) and supports the assignment to a lamniform shark (e.g.Carcharodon carcharias or Otodus megalodon).The serration morphology and spacing indicate that this tooth belonged to the great white shark, Carcharodon carcharias, given that teeth of Otodus megalodon are characterized by finer serrae (Nyberg et al. 2006: fig. 8).
Variation in the size and shape of the serrations in extant Carcharodon carcharias encompasses the size and shape of the serrations preserved in CMM-V-6964.The tips of proximal serrations on the teeth of C. carcharias are generally more pointed than those preserved on the embedded partially tooth in CMM-V-6964.However, the serrations on the tips of the teeth of C. carcharias are not as pointed as are more proximal ones; they are instead more comparable to those preserved in CMM-V-6964 (Fig. 2), indicating not unreasonably, that the embedded section of the tooth represents its tip.Unfortunately, from the limited preservation of the embedded crown, it is not possible to estimate the original size of the tooth, nor the size of the great white shark.
pAleoecoloGicAl AnD biomechAnicAl insiGhts Teeth attributed to Carcharodon carcharias are known from the Bone Valley Member of the Peace River Formation (Perez 2022a, b).Although uncommon, C. carcharias was obviously in the same place at the same time as was the shark-bitten phocid.Great white sharks are known to prey upon seals at seal rookeries worldwide (Hammerschlag et al. 2006;Johnson et al. 2009;Diedrich 2013;Fallows et al. 2013;de Vos et al. 2015).Therefore, the presence of the tip of a broken tooth embedded in a calcaneum is unsurprising.What is surprising is that no comparable seal bone or any vertebrate bone (or shark cartilage) preserving an embedded C. carcharias tooth has yet been described from the fossil record.Thus, despite   (Linnaeus, 1758).This illustration depicts an active predatory encounter between the seal and the great white, although it may have come about as a result of scavenging.Notes: the exact size of the predator and prey represented by CMM-V-6964 are not known.The life-restoration of the pinniped is based mostly on the extant Leopard seal.Credits: Clarence Schumaker.
the likely prevalence of predation on seals by C. carcharias throughout their c.6-million-year coexistence, the likelihood of a comparable find is evidently exceedingly low, perhaps because bitten bones are, more often than not, consumed, leaving no possibility for the preservation of a bone with an embedded tooth.Or bitten bones are taphonomically destroyed (or almost so) so that they are no longer recognizable.The bone shows no obvious signs of having been ingested; there are no signs of bone dissolution (like gastric pitting) from digestive acids, therefore, the calcaneum was probably not swallowed by the shark.However, Boessenecker et al. (2014: fig.29K-M) figured a distal femur from a fur seal (Pinnipedia Illiger, 1811: Otariidae Gray, 1825: Thalassoleon sp., cf.T. macnallyae) with gastric acid pitting and linear scrape marks.There are two seemingly, equally likely scenarios to account for the presence of the partial shark tooth crown embedded in the calcaneum: successful active predation or scavenging.There is no osteological evidence of healing (i.e., no evidence of new bone growth around the embedded partial crown, there is no evidence of periosteal reaction [as in Kallal et al. 2012]), so if the encounter came about as a result of active predation, the seal did not survive for long.
Although great white sharks actively prey upon small marine mammals, they have only infrequently been reported to scavenge seals or diminutive odontocetes, thus seemingly preferring large, fat-rich whale carcasses (Fallows et al. 2013;Collareta et al. 2017).Although, these purported scavenging preferences may have resulted from observer lack of opportunity: it would be easier to observe a great white shark scavenging a large baleen whale carcass than to observe the same behavior on small marine mammal carcasses.However, if in fact great white sharks only rarely scavenge the carcasses of seals, then this find would tilt the balance towards active predation.Furthermore, one could argue that there is not much flesh on the foot of a seal.In terms of return on effort, a powerful bite to the foot might more strongly Shark tooth embedded in a pinniped bone suggest active pursuit for the purpose of immobilizing the seal, versus scavenging.Furthermore, Long et al. (1996) pointed out that seals use hind flipper propulsion and are not as able (as sea lions) to escape from a posterior attack by a great white shark.At this point, although we favor active predation, there does not appear to be any definitive evidence pointing conclusively to one or the other.
Although the surface of the bone is marked by at least seven small areas of broken/perforated bone, it is not known if these represent postmortem taphonomic damage to the exterior surface of the bone or if they are shark bite marks, collateral damage from the same attack during which the tooth became embedded, or a subsequent scavenging encounter.If they are shark bite marks in origin, they most closely conform to the trace fossil Nihilichnus nihilicus Mikuláš, Kadlecová, Fejfar & DvoŘák, 2006(Mikuláš et al. 2006).However, the aforementioned identification is not compelling and the surface markings on the calcaneum could also be interpreted as evidence for the activity of the osteophagous worms Osedax Rouse, Goffredi & Vrijenhoek, 2004(Annelida Lamarck, 1809: Siboglinidae Caullery, 1914); their galleries that collapsed under burial compaction (Boessenecker & Fordyce 2015).To complicate matters, it is within the realm of possibility that they represent biogenic markings made by ectoparasites (i.Only a few publications implicate C. carcharias in preying or scavenging on Neogene marine mammals (Bianucci et al. 2002;Govender 2015;Cortés et al. 2019;Govender 2021).No publications to date have described an embedded C. carcharias tooth in a prey item from the fossil record.Therefore, CMM-V-6964 is a unique morderolite in the fossil record.However, Ames & Morejohn (1980) did describe an embedded C. carcharias tooth in a modern sea otter skull.Interestingly, there are publications that document evidence of great white sharks off the California coast attacking, but not consuming, sea otters (e.g.Moxley et al. 2019;and references therein).These shark attacks are due to mistaken identity (mistargeted prey) with their preferred prey, juvenile elephant seals (Mirounga angustirostris (Gill, 1866)) at coastal rookeries (Moxley et al. 2019).
Although we cannot say with certainty, we think that the embedded tooth broke at the time when it became embedded in the calcaneum (Fig. 4).The fact that this bite was concentrated on an area of the body with minimal fat may have led to tooth failure, as it punctured the hard bone.Broadly triangular, serrated teeth, like those of Carcharodon carcharias, are regarded as representative of the cutting functional type and are thought to be adapted for feeding on large, fleshy prey (Frazzetta 1988;Kent 1994;Perez 2022a).Having a dentition equipped with cutting-type teeth allows predators to dismember their prey more effectively than other tooth morphologies.However, even with these cutting-type teeth, CMM-V-6964 demonstrates that tooth failure is possible when the bite force is concentrated on bone and even cartilage.This is also evident by more recent examples, including partial teeth of great white sharks found embedded in the skull of a sea otter (Ames & Morejohn 1980) and within another great white (Fallows et al. 2013).entirety of her amazingly productive career as an exceedingly gifted fossil preparator and artist.Obviously, this publication would not have been possible without access to Mosaic's South Fort Meade Mine (Mosaic Fertilizer, LLC).Consequently, we thank the management of the mine for granting access to the spoil piles so that scientifically important fossils, like the one described herein, could be collected.We gratefully and specifically acknowledge the following mine employees who worked at the mine when the seal calcaneum was collected: Howie Stoughton (Mine Manager), Diana Youmans (Mine Sr. Public Relations), and Bonnie Dodson (Mine Geologist).
We would like to express our thanks to CMM Paleontology Collections Manager, John R. Nance for encouraging access to specimens in his care.We are also grateful to the constructive reviews given by Dr Robert W. Boessenecker (Mace Brown Museum of Natural History, College of Charleston), Dr Alberto Collareta (Museo di Storia Naturale, Università di Pisa), and Dr Olivier Lambert (Institut royal des Sciences naturelles de Belgique, Belgium), which improved upon our initial effort, and Dr Michel Laurin who kept the manuscript moving through the publication process.We are grateful that Dr Robert R. Reisz invited us to contribute to this issue.This research was funded in part by the citizens of Calvert County Maryland, the County Board of Calvert County Commissioners, and the Clarissa and Lincoln Dryden Endowment for Paleontology at the Calvert Marine Museum.
fig. 1. -CMM-V-6964, phocid right calcaneum found in the Bone Valley Member of the Peace River Formation (Hawthorn Group), Mosaic South Fort Meade Mine (Hardee County, Fort Meade, Florida, United States): A, ventral view; B, lateral view; C, dorsal view; D, medial view.The embedded Carcharodon carcharias (Linnaeus, 1758) partial tooth is visible in A and B. The black arrows point out some of the possible biogenic traces.Scale bar: 50 mm.
fig. 2. -CMM-V-6964: A, phocid right calcaneum looking proximally along the lateral surface of the bone showing the sulcus for m. peroneus longus in the left half of the image with, in the foreground, a view of the embedded Carcharodon carcharias (Linnaeus, 1758) partial tooth showing both its broken and serrated edges; B, an enlarged view of the shark tooth in A looking distally, i.e., 180° from the side shown in A. Notice that the interior of the tooth comprises osteodentine.Scale bars: A, 10 mm; B, 1 mm.
fig. 3. -A, D, USNM PAL 205850, right calcaneum of Callophoca obscura (Van Beneden, 1876) (sensu Koretsky & Ray 2008) in medial and lateral views respectively from an associated partial right pes; B, E, CMM-V-6964, right calcaneum in medial and lateral views respectively with embedded shark tooth visible in E; C, F, USNM PAL 529247, left calcaneum (reflected vertically 180º in both) of an unnamed phocid in medial and lateral views respectively.Scale bar: 50 mm.
fig.4.-Rendering of one of the ways in which the seal calcaneum may have been bitten by the great white shark, Carcharodon carcharias(Linnaeus, 1758).This illustration depicts an active predatory encounter between the seal and the great white, although it may have come about as a result of scavenging.Notes: the exact size of the predator and prey represented by CMM-V-6964 are not known.The life-restoration of the pinniped is based mostly on the extant Leopard seal.Credits: Clarence Schumaker.