Fifty modern shark jaws with associated teeth belonging to Carcharodon carcharias, Carcharhinus leucas and Galeocerdo cuvier were examined in the collection of the Department of Ichthyology of the American Museum of Natural History (AMNH). These species were selected based on serrated tooth shape that is generally similar to Squalicorax kaupi and Squalicorax pristodontus. Additionally, both these modern and fossil species of sharks are known to prey upon animals with robust skeletal anatomy. Similar prey should ideally result in equivalent damage to tooth cusps in functional teeth during feeding.

Four varieties of functional tooth cusp damage were identified among these fifty modern jaws: (A) labial damage on the tooth cusp apex; (B) labial damage on the mesial edge; (C) lingual damage on the tooth cusp apex; and, (D) lingual damage on the mesial edge (Figure 2). In some cases, observed functional tooth damage includes combinations of these four different varieties as seen on both the labial and lingual cusp faces. It is important to note that no developing (pre-functional teeth within individual tooth files) in these modern jaws had tooth cusp damage of the four varieties listed above. The majority of developing teeth along with their roots are protected within the epithelial jaw tissue from direct impact with prey during feeding.

Teeth in the functional position have fully-developed, bilobate roots, convex lingual cusp faces and concave labial cusp faces. The root and cusp are also well-mineralized, thick, and the serrations well-defined along the mesial and distal edges. Developing teeth lack all these features, particularly the well-developed, bilobate roots and convex lingual cusp faces. We also note that the roots in developing teeth are only partially permineralized and appear lighter in color than fully developed teeth. Developing teeth are lost upon the death of the animal or in extreme cases of feeding related injury. Table 1 lists the number of teeth in these categories and upon which this study is based.

Squalicorax kaupi and Squalicorax pristodontus teeth utilized in this study are housed in the William Paterson University (WPU) paleontological collections. These teeth were recovered from a lag deposit that drapes a disconformity and comprises the lowermost Navesink Formation [57] along Ramanessin, Big and Willow Brooks, Monmouth County, New Jersey. This lag consists of silty, micaceous marl with uncommon quartz pebbles up to 2.0 centimeters in diameter and ranges from 10–30 centimeters thick. Such lag deposits are common in the Late Cretaceous of North America and represent complex taphonomic histories that include multiple episodes of exhumation and reburial associated with sea level cyclicity [45,49,58,59].

An industrial grade rock tumbler was used to simulate taphonomic effects and distinguish them from feeding-related damage among functional teeth of Squalicorax kaupi and Squalicorax pristodontus. Although pre-functional teeth were also exposed to similar taphonomic effects, these teeth are not exposed directly to feeding-related impact along their cusp apices and were excluded from further consideration in our taphonomic simulation experiments. Five pristine, functional teeth of Squalicorax kaupi and Squalicorax pristodontus respectively were placed in 5.0 kg of sediment from the lowermost Navesink Formation and water was added to cover the top of the sediment. Teeth were tumbled for one month and removed at six day intervals for inspection and photography. The same procedure was utilized for five pristine, functional teeth from each of the three modern test species: Carcharodon carcharias, Carcharhinus leucas and Galeocerdo cuvier. All specimens were taken from WPU paleontological collections.

Details of Squalicorax kaupi and Squalicorax pristodontus tooth sample population are compiled in Table 1. Of the 1926 Squalicorax kaupi teeth analyzed, 239 teeth were determined to occupy the functional position and 1448 teeth were determined to be pre-functional based on the degree of cusp and root development. Of the 477 Squalicorax pristodontus teeth analyzed, 63 teeth were determined to occupy the functional position and 326 teeth were determined to be pre-functional based on the degree of cusp and root development using the criteria described above.

Teeth broken during field excavation and sieving along with those where not enough of the cusp and root were preserved to determine the exact location in the file constituted 12% of our total Squalicorax kaupi sample population or 237 teeth, and 18% of our total Squalicorax pristodontus sample population or 87 teeth. Figure 3 and Figure 4 show nine Squalicorax kaupi and nine Squalicorax pristodontus functional teeth respectively that display damage analogous to that seen in the modern AMNH jaws and determined to be feeding-related. This sample population also contained four pathological Squalicorax kaupi teeth and one pathological Squalicorax pristodontus tooth with highly deformed cusps and roots similar to pathological teeth from the Navesink Formation that we described earlier [53].

The results of tumbling experiments conducted on Squalicorax kaupi and Squalicorax pristodontus functional teeth are shown in Figure 5. After six days of tumbling, serrated edges of the teeth of both Squalicorax kaupi and Squalicorax pristodontus were completely removed.

This was followed by thinning and polishing of the enameloid and root on both the lingual and labial cusp faces. Near the cusp base after one month of tumbling, the enameloid was completely removed exposing the osteodentine and orthodentine, particularly on the labial cusp face. Squalicorax kaupi and Squalicorax pristodontus lost 14.4 and 14.2% of their original mass after one month of tumbling, respectively (Table 2). No splintering, cracking and flaking along the tooth cusp similar to that seen in the modern shark jaws illustrated in Figure 2, or in Squalicorax kaupi and Squalicorax pristodontus teeth (Figure 3 and Figure 4) were observed.

A similar pattern of material loss due to tumbling was observed in teeth of modern Carcharodon carcharias, Carcharhinus leucas, and Galeocerdo cuvier (Figure 6 and Figure 7). The teeth of these three sharks tested in the tumbler are clearly polished as indicated in Figure 7 and Figure 8, and show no indication of significant cracking, chipping, or other forms of breakage. One can also observe in Figure 6 and Figure 7 that the test specimens, particularly the roots, become darker in color as tumbling time increases. The roots of the modern teeth, and to a lesser extent the enameloid, incorporate iron staining from the host sediment in the tumbler almost immediately. At the end of one month, tooth roots and cusp edges were heavily iron-stained. Carcharodon, Carcharhinus and Galeocerdo teeth lost 42.6, 49.4 and 48.3 % of their original mass after one month of tumbling (Table 2). We attribute the smaller reduction in mass seen in the fossil teeth to increased durability associated with permineralization undergone by these teeth during fossilization and diagenesis.

All Squalicorax kaupi and Squalicorax pristodontus teeth utilized in this study were recovered from a lag deposit and therefore must have experienced some taphonomic transport and reworking. The central focus of this paper is to determine whether such reworking is the cause of the tooth damage we observe, or if, in contrast, damage can be attributed primarily to feeding injury. During feeding, maximum force is concentrated in teeth along the point of impact, often the cusp apex. In loading tests this force rapidly dissipates across the mesial and distal cutting edges toward the root [23,24]. This concentrated force on cutting surfaces results in the type of repeated tooth breaks of cusp and cutting surfaces, seen in modern sharks with serrated tooth shape (see Figure 2) and is the product of the cusp apices impacting bony anatomy in prey [60,61,62,63]. Comparing the broken Squalicorax kaupi and Squalicorax pristodontus teeth in Figure 3 and Figure 4 to the feeding damaged teeth of our modern analogues illustrated in Figure 2, indicates that the characteristics of the breaks in the fossil teeth, and in particular their association with cusp apex and cutting edges, are essentially the same as those of feeding damaged teeth in the modern examples. Moreover, the results of the tumbler experiment illustrated in Figure 5, Figure 6 and Figure 7, show that both modern and fossil teeth are polished by abrasion in the tumbler; they do not suffer major breaks. Because the test teeth were tumbled with lowermost Navesink sediment, we infer that post-mortem transport and reworking were not a factor in producing the major breaks in the fossil teeth seen in Figure 4 and Figure 5. Based on these observations, we suggest that the broken, chipped, and cracked teeth discussed here are the result of damage induced during feeding.

When a tooth damaged in feeding falls out of the jaw it becomes a sedimentary clast. It can then undergo transport, reworking, and the associated abrasion that acts on all such materials. As a result, fossil chondrichthyan teeth can be expected to show both types of damage, i.e., major breaks associated with feeding, and rounding and smoothing of edges and surfaces associated with taphonomic abrasion. The interplay of these two modes of tooth damage should be visible in many, if not most, damaged teeth. This viewpoint is reinforced by examination of the cusp apex of a Squalicorax kaupi tooth using an EVEX-3000 Scanning Electron Microscope. The distinct break of this tooth (Figure 8.1) is similar to feeding damage seen in Squalicorax kaupi and Squalicorax pristodontus (Figure 3 and Figure 4) as well as in modern teeth (Figure 2). However, at 70× magnification (Figure 8.2) the broken enameloid tooth edges and ridges in the surface of the exposed osteodentine are observed to be strongly rounded. They are not sharp or angular as would be expected in a tooth freshly damaged during feeding. This suggests that the cusp apex was broken prior to taphonomic reworking and more than likely occurred during a feeding-related impact. Rounding of the exposed edges and surfaces occurred after the tooth was shed or its owner died and the tooth was released onto the substrate as a sedimentary particle.

The types of cusp breaks seen in Squalicorax kaupi and Squalicorax pristodontus and the modern jaws with serrated teeth from the AMNH can also be observed in Cenozoic sharks. Three Miocene-Recent serrated fossil teeth from the Peace River in Hardee County, Florida are shown in Figure 9. These teeth were eroded out of the river banks and incorporated with stream gravels along the base of the river. These Cenozoic teeth have cusp breaks along both the lingual and labial faces analogous to those seen in the feeding damaged teeth of Squalicorax kaupi and Squalicorax pristodontus (Figure 3 and Figure 4) and the modern AMNH teeth (Figure 2).

Examination of the jaws of modern Carcharodon carcharias, Carcharhinus leucas and Galeocerdo cuvier demonstrates that it would not be uncommon to find as many as 300 teeth in the lower and upper jaws of an individual animal of these species with approximately 50 teeth, or seventeen percent, in the functional position [5,60,61]. This percentage compares very favorably to the fossil teeth in our sample population, where 14% of Squalicorax kaupi teeth and 16% of Squalicorax pristodontus teeth, were determined to have been in the functional position when the animals from which they derive were alive. Teeth broken during field collection or those where location in the tooth file could not be determined, 12% and 18% for Squalicorax kaupi and Squalicorax pristodontus respectively, may slightly alter the percentage of functional teeth involved in this study. However, the addition of a few functional or pre-functional teeth to this sample population does not drastically compromise our sorting techniques and ability to recognize functional and pre-functional teeth when compared to modern analogues.

Damaged functional teeth in the modern AMNH jaws determined to be the product of feeding-related behavior range from a few percent to as much as 10%. Our fossil population was determined to have 15% of Squalicorax kaupi, and 32% of Squalicorax pristodontus, functional teeth broken due to feeding-related behavior. While the exact cause of this larger percentage of broken teeth relative to the modern AMNH jaws remains unknown at this time, one of the more interesting possibilities is that Squalicorax kaupi and Squalicorax pristodontus may have had slightly slower rates of tooth production and replacement. This slightly slower rate of tooth replacement would have resulted in a greater residence time for any broken functional tooth and a higher percentage of broken teeth in the jaws at any one time. Similar results for slower tooth replacement have been previously identified in some Late Paleozoic and Mesozoic sharks [64,65,66,67,68,69]. Evidence from these studies includes large wear facets related to feeding on the tooth cusps and suggested slower rates of tooth replacement occurred in these ancestral sharks [69].

By analogy to modern sharks, teeth in the functional position in the jaws of fossil sharks were fully formed, fully biomineralized and fully ready for use. These teeth would thus have been extremely hard and highly resistant to taphonomically induced abrasion occurring within the depositional environmental prior to final burial and fossilization. Pre-functional teeth further back in the tooth files of fossil forms, like such teeth in modern sharks, would have been less mineralized and comprised of smaller amounts of enameloid, osteodentine and orthodentine. Such teeth released by death into the sediment before they are fully formed and shed by a live animal would be far more susceptible to taphonomically induced abrasion. As a consequence of such differential resistance, pre-functional teeth would be preferentially destroyed as recognizable fossils faster and by less abrasion then functional teeth. In a general way, therefore, the fossil record of shark teeth should primarily be a record of functional and late pre-functional teeth. Early pre-functional teeth should be relatively rare.

The bite force of modern sharks (e.g., taxa with serrated teeth) were analyzed in several studies and indicate forces of several thousands of Newton [21,22,23,24,70,71]. Serrated teeth form an effective cutting dentition that together with the tearing and sawing action produced as the shark shakes its head from side to side can remove large pieces from its prey [20,53,72]. Modeling based on tooth and jaw shape has also been utilized in the fossil sharks Carcharocles megalodon [1], Squalicorax kaupi and Squalicorax pristodontus to infer bite force [21,35,73,74]. By applying isometric scaling, Wroe et al. [21] estimated the bite force for Carcharocles megalodon at an incredible 93,127 N to 182,201 N. Shimada and Cicimurri [35] compared Meckel’s cartilage in the modern tiger shark, Galeocerdo cuvier, to Squalicorax kaupi and Squalicorax pristodontus. Their results indicate that Squalicorax had a larger surface area for the attachment of the quadratomandibularis muscle. This larger attachment surface implied a larger muscle, which led them to conclude that the biting force of Squalicorax was significantly greater than that of an equivalent sized Galeocerdo cuvier [35].

Large and mature sharks with serrated tooth shape such as Carcharodon carcharias, Carcharhinus leucas and Galeocerdo cuvier are opportunistic feeders which actively hunt and scavenge the world’s oceans. They also migrate seasonally to specific locations to take advantage of abundant food sources, such as pinnipeds and albatross [11,15]. Carcharodon carcharias, Carcharhinus leucas and Galeocerdo cuvier have also been documented scavenging marine mammals including whales and dolphins as well as turtles and large fish [10,14,17,75]. Bones recovered from the sea floor in regions where such sharks congregate often bear teeth marks created by the sawing and cutting behavior of serrated teeth [76,77].

Direct and indirect fossil evidence suggests similar feeding behavior among fossil sharks with serrated tooth shape, particularly in Carcharocles megalodon, Squalicorax pristodontus and Squalicorax kaupi. In locations where Carcharocles megalodon teeth are abundant, vertebral centra and ribs from marine mammals including whales, dolphin and dugongs bear serrated teeth marks from predation orscavenging [63,78,79,80,81]. In fact, the evolution of tooth shape and size in Carcharocles megalodon is thought to have occurred contemporaneously with the appearance in the Cenozoic of large mammals such as seals and whales [61,82]. Squalicorax kaupi and Squalicorax pristodontus teeth have been found embedded in mosasaur vertebral centra. This association provides direct evidence of predation or scavenging by these sharks on contemporary large marine reptiles [83]. Serrated teeth from Squalicorax kaupi and Squalicorax pristodontus leave a distinct and unmistakable striated tooth pattern on prey [39,40,84,85] which is similar to bite marks made by modern sharks with serrated tooth shape.

Turtle bones with striated tooth marks occur in the same stratigraphic horizon as the Squalicorax kaupi and Squalicorax pristodontus teeth utilized in the present study [86]. Additionally, this horizon contains pathologically deformed Squalicorax kaupi and Squalicorax pristodontus teeth caused by feeding damage to developing teeth [56] and spiral coprolites contains containing bone fragments [87]. Such associations provide additional evidence that the above described feeding behaviors also occurred at the Monmouth County collection sites.

The ability to rapidly replace teeth is one of the most significant evolutionary advantages achieved by neoselachians throughout the Mesozoic [34,70,88,89,90,91]. Rapid tooth replacement would have ensured maximum functionality of the dentition, particularly after feeding-related tooth damage occurred. Serrated teeth such as those seen in Squalicorax kaupi and Squalicorax pristodontus also provided an evolutionary blueprint for similar teeth seen in some of the larger carcharhiniforms and lamniforms throughout the Cenozoic. This type of tooth shape helped make possible successful scavenging and predation on marine mammals, turtles, birds, large osteichthyans and other chondrichthyans.