Identification of trace maker

Taking the age and provenance of the fossils into account, there are three broad groupings of animals which could have created the larger of the two sets of bite marks seen on these bones: theropod dinosaurs, mammals or non-mammalian mammaliaforms, or crocodyliforms. There is an extensive literature documenting theropod feeding traces on a variety of dinosaur bones (e.g., [28]–[36]). The feeding traces on the ‘Kaiparowtis hypsilophodontid’ material lack striations, which are often caused by the serrations on ziphodont teeth, such as those possessed by theropods. This does not fully exclude theropods, because serrated teeth have been demonstrated to create un-striated bite marks [41]; however, the partial tooth crown embedded in the femur is ovoid in cross section. This tooth morphology is markedly different from the mediolaterally compressed teeth of most theropods [42]. Therefore, it is unlikely that theropod dinosaurs are the trace maker.

Some Cretaceous mammals were capable of preying on small dinosaurs (e.g., [43]). Again, the shape of the broken tooth embedded in UMNH VP 21107 does not resemble typical heterodont mammalian dentition, though it is possibly congruent with a broken tip of a caniniform tooth. However, the presence of the broken tooth itself would be highly unusual if the bite mark was made by a mammal. While crocodyliforms and theropods continually shed teeth throughout their lives, mammalian feeding behavior and tooth morphologies are at least partially driven by their inability to repeatedly replace old or damaged teeth. Even though it is possible that a mammalian caniniform tooth could be broken and embedded in prey bone owing to an injudiciously placed bite, this scenario does not reflect normal mammalian feeding behavior and tooth use [37]. The presence of a bisected pit goes further to rule out a mammalian trace-maker, as this type of bite mark is inconsistent with all published descriptions of mammalian bite marks [3].

Previous studies of crocodyliform bite marks on dinosaurian prey have often focused on large-bodied taxa, particularly Deinosuchus [17], [21], [44]–[45]. While bite marks from other crocodyliforms on dinosaurians are known [19], [46], the majority of examples come from other prey clades [8], [14]–[15], [47] such as turtles and mammals. The recent actualistic study involving Crocodylus niloticus [3] identified bite mark types and damage patterns created by modern crocodylians, including: 1) bisected pits and scores (diagnostic of crocodylians) and hook scores (diagnostic of taxa that utilize inertial feeding strategies [41]; 2) concentrations of feeding traces (> 10 marks) on major grasping areas (such as the neck of the scapula) resulting from attempts to disarticulate the skeleton into sections small enough to be swallowed; 3) a lower proportion of bones left by crocodyliforms bear feeding traces than those fed on by mammals (< 21% compared to > 50% [3]); 4) evidence of gnawing behavior is absent, which particularly differentiates crocodyliforms with their more restricted jaw mechanics from mammalians; and, 5) crocodyliforms typically leave whole bones or articulated skeletal units whereas mammalian carnivores tend to leave fragmented bones. These patterns have been found to be largely applicable to other extant and extinct crocodyliforms [3], [5], [17]–[19], [20].

The feeding traces on UMNH VP 21104 and 21107 and the condition of other associated material were evaluated using these six criteria to determine if they corresponded with either a mammalian or crocodyliform trace-maker. The presence of a bisected pit on the proximal scapula, the low frequency of bones recovered from UMNH locality 303 displaying feeding traces (< 10%), and the absence of gnawing on any broken margins or ends of long bones are consistent with a crocodyliform trace-maker. Evaluation of the fifth criterion is more difficult because this material was surface collected and not excavated in-situ. Most, if not all, observed bone fractures propagate perpendicularly to the long axis of long bones, which is characteristic of post-depositional, ‘dry’ fractures. This lack of green stick or spiral fracturing means that there is no evidence of breakage while the bone was still fresh, or ‘wet.’ Also, one set of metatarsals (II through IV) was articulated when collected and further articulation was possible at the time of initial deposition, as demonstrated by the roughly equivalent MNE (minimum number of elements) for long bones from the same skeletal regions. While tenuous, it is at least possible to state that the condition of the remains from UMNH locality 303 associated with specimens UMNH VP 21104 and 21107 is not inconsistent with criterion five.

The tooth fragment embedded in UMNH VP 21107 would have been roughly conical in shape prior to the loss of the tip and is ovoid in cross section, consistent with typical crocodyliform teeth. Despite the fact that modern crocodylians shed teeth throughout their lives, particularly during feeding [3], embedded teeth are quite rare. This specimen represents only the second report of a fossilized crocodyliform tooth found lodged directly in prey bone [48]. This tooth, partnered with the identification of a diagnostic crocodyliform feeding trace (the bisected pit) and other corroborating evidence (the placement and frequency of the bite marks) makes associating the larger bite marks (i.e., the puncture in the femur and the bisected pit on the scapula) with a crocodyliform trace maker possible.

As for the group of smaller bite marks on UMNH VP 21104, identification of the trace maker is more problematic. Rodents [49] and earlier mammalian taxa interpreted to have filled somewhat similar ecological niches [50] tend to create groups of subparallel or fan-shaped bite marks by gnawing on bone margins with their paired incisors. These marks are arranged together since they are created by repetitive, often overlapping bites from a small number of teeth. Such behavior is unlikely to have created the similar length, strongly parallel orientation, and nearly uniform spacing seen in all but two of the smaller bite marks present on UMNH VP 21104, implying instead that these were created by a series of teeth during a single biting event. If this is the case, then the similar cross-sectional profiles and spacing of these scores implies that the trace-maker had homodont rather than heterodont dentition. This excludes mammalians as the potential trace maker.

The smaller set of bite marks present on UMNH VP 21104 are not bisected, hooked (sensu [3]), or striated (sensu [41]). However, none of these types of bite marks were present in all, or even a majority, of sampled feeding traces created by crocodyliform teeth with prominent carinae or taxa with ziphodont dentition, such as theropods and some lizards. The concentration of at least fifteen scores on the base of the neck of the scapula (a major grasping point during disarticulation of the forelimb from the carcass) is consistent with criterion three from the Njau and Blumenschine study [3]. In the absence of other corroborating evidence, we cannot positively exclude crocodyliforms, theropods, or other small-bodied vertebrate groups with relatively homodont dentition as the trace maker for these small scores.

The Kaiparowits Formation preserves a particularly diverse crocodyliform faunal assemblage [51]–[53]. Two particularly large taxa have been identified, the gigantic alligatoroid Deinosuchus riograndensis ([52], [53]; Deinosuchus hatcheri sensu Irmis et al. [54]) and a possible goniopholidid or pholidosaurid [23], [54]. Adult individuals of these taxa can safely be excluded from consideration due to the size of the bite marks and embedded tooth fragment; yet, juvenile individuals cannot be summarily dismissed.

Other crocodyliforms that have been identified in the Kaiparowits Formation include Brachychampsa n. sp., either Leidyosuchus or Borealosuchus [53], [55], as many as four separate species of alligatoroid, including durophagous forms similar to Allognathosuchus or Ceratosuchus [51], [53], and a caimanine [51]. Many of these taxonomic assignments were based on highly fragmentary and/or undescribed material. A recent, apomorphy-based reanalysis of the Kaiparowits crocodyliforms limits this possible number of taxa considerably [54]. Many specimens previously identified as belonging to a particular genus or species were found to lack diagnostic features identifying them beyond broad taxonomic classifications (e.g., Crocodyliformes, Mesueucrocodylia, Neosuchia). The presence of a possible new species of Brachychampsa was verified, with a formal description of the material forthcoming [54]. At least one additional alligatoroid, distinct from Brachychampsa, was also identified, but multiple taxa may also be present. Irmis et al. [54] identified no conclusively durophagus forms. Even though the recent revision greatly clarifies Kaiparowits crocodyliform diversity at around four to five taxa, without the discovery of more complete specimens and further descriptions of existing specimens, eliminating any of these taxa as the potential trace maker remains difficult.

When attempting to further characterize the crocodyliform trace maker from a gross morphological instead of a systematic standpoint, the isolated, fragmented nature of the embedded tooth makes estimating vital statistics such as exact size of the entire animal difficult. However, the small minimum size of the tooth (2.5 mm in diameter) in rough comparison to modern crocodylian dentition (Alligator mississippiensis; CAB, pers. obs.) suggests a small individual, perhaps one meter in length. The lack of extensive secondary alterations, in the form of widespread crushing and fracturing related to the biting event [56], also points towards a smaller individual, since crocodyliform bite force has been shown to scale with body size [57]–[58]. Extant crocodylians between 1 and 1.8 m in length are known to prey on animals between five and twenty-five kg in mass [3], consistent with the estimated size of the ‘Kaiparowits hypsilophodontid’ individuals preserved at UMNH locality 303 (13–21 kg based on femur circumference [39]).