The only specimens of theropods recovered from Upper Cretaceous (upper Campanian - lower Maastrichtian) deposits of western Canada with pedes large and robust enough to produce tracks of Bellatoripes fredlundi are those of tyrannosaurids, (the albertosaurines Albertosaurus or Gorgosaurus, and the tyrannosaurine Daspletosaurus [28]). Given the present osteological record, it is unlikely that these traces were made by an as yet unreported large Upper Cretaceous non-tyrannosaurid theropod, such as giant ornithomimosaurians or oviraptorosaurians. Giant ornithomimosaurians are reported from the Early Cretaceous of China but were likely functionally tetradactyl [43], and those reported from North America [44] are too small to have made these tracks. Many specimens of oviraptorosaurians possess a comparatively long digit I [45] and were likely functionally tetradactyl [46], [47]. Large-bodied oviraptorosaurians described to date from North America [48] are also too small (∼3.50 m body length) to be a potential track-maker of Bellatoripes fredlundi.

The pathology on digit II (left prints) of Trackway A does not appear to have significantly impaired the track-maker’s locomotion. Stride, pace and pace angulation values indicate a normal and efficient gait for a large theropod. The pes rotation of the second print (right) is the opposite of what is normally expected (outward rather than inward rotation from the midline of the trackway), and is consistent with compensation for this injury or deformity. This specimen is an interesting addition to the growing literature of dinosaur footprint pathology [49] and to the literature of tyrannosaurid-specific pathologies [50] , [49] .

There is an inferred pathology associated with digit II of the left footprint (seen in prints #1 and #3 of PRPRC 2011.11.001, Trackway A), reducing the length of digit II by at least 14 cm ( Table 1 ; Figs. 4 , 7 – 8 ). The pathology may have involved the loss of the distal and penultimate phalanges (II-2, II-3), or it may be a trace of a deformation or dislocation that prevented the distal portion of digit II from contacting the substrate. The rough, uneven margin of the distal ‘nub’ of the digit II impression is consistent with a wound that would have involved a loss of tissue and bone.

Locomotion and behavior

The individual footprints in PRPRC 2011.11.001 (Trackway A), the first print of PRPRC 2012.04.002 (Trackway B) and the second print of PRPRC 2012.04.003 (Trackway C) undercut the original surface of the track-bearing layer to a considerable degree. The skin impressions provide information on foot movement [51] and in addition are evidence of true tracks that are not compromised by poor preservation. Two areas of lengthy (7.2 cm and 12.0 cm lengths), parallel striations (4 striations per cm width perpendicular to the long-axis of the striations) are present on shallow drag marks leading up to the caudal edge of print #2, Trackway C (Fig. 10). Both sets of impressions are parallel to the direction of travel (7o toward digit II in relation to the central axis of digit III with a 10o plunge in the direction of travel). They are interpreted as being the result of the caudal portion of the foot making shallow contact with the substrate (pre-touch-down phase) as the foot moved forward towards the area where the foot begins to settle (touch-down phase) prior to the animal putting its full weight down (weight-bearing phase). The footprint cycle ends with the kick-off phase [52] leading towards the next touch-down phase. These striations are therefore identified as entry striations.

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larger image TIFF original image Download: Figure 10. Striations on Bellatoripes fredlundi paratype track. a) Photograph of silicone mold of print #2 Trackway C (PRPRC 2012.04.003), arrows pointing to areas with striations; b) photograph of striations on caudal drag marks leading up to print #2; c) photograph of striations on the outer margin of digit II print #2 Trackway C. https://doi.org/10.1371/journal.pone.0103613.g010

A third area of striations (4 striations/cm width) is present on the same footprint, but occurs along a 27 cm long portion of the outer edge of digit II. In relation to the rest of the footprint these striations extend from the surface of the substrate and run in an anterior (7.3 cm) and downward (6.2 cm) direction, representing a 50o plunge angle, 35o towards digit IV in relation to the central axis of digit III. The striations are deeply incised into the substrate on the caudal portion of the digit II impression, but become less distinct toward the cranial portion of this digit. These are interpreted as entry-striations recording the trajectory of the foot entering the substrate and quickly penetrating to the deepest point of the weight-bearing phase [52]. As the foot settled it slipped forward and away from the midline of the trackway. Alternatively, the digit II striation impressions could be interpreted as exit striations recording the trajectory of the foot as it is withdrawn backwards and slightly towards the trackway midline. The process of limb movement we propose below likely fits with this latter interpretation.

The foot movements deduced by study of the Bellatoripes fredlundi tracks contrasts with published observations of trackways of Triassic [53], Jurassic [54], and Cretaceous [55] theropods in which the footprints indicate that the track-makers’ feet were dragged cranially out of the substrate after registering during the kick-off phase [52]. This could be explained as a function of the depth of the substrate compared to the size of the animals involved. The difference may also be related to the consistency of the substrate: the substrate consistency for the reported Triassic prints [53] may have influenced the movement of the limbs such that caudal withdrawal of the pedes from the substrate was not possible, in contrast to the reported prints of Jurassic and Late Cretaceous theropod tracks [56], [57]. In the extant Struthio camelus, flexion and extension of the intertarsal and metatarsophalangeal joints are assisted by the elastic energy storage/release by ligaments, and tendons of the gastrocnemius and digital flexor muscles [58]: during a full-motion cycle, flexion of the intertarsal joint occurs automatically with tarsometatarsal abduction, while extension results in adduction [58] (the passive engage-disengage mechanism of Schaller et al. [59]). The track-makers of Bellatoripes fredlundi, while utilizing hip-driven rather than knee-driven locomotion [60], [61], may have consequently withdrawn their pedes during intertarsal flexion enough to retract the digits and remove them from the footprint caudally, instead of dragging the digits cranially through the substrate (Fig. 11). The claw impressions of several of the Bellatoripes fredlundi tracks from the British Columbia site undercut the substrate and were not disturbed by the withdrawal of the feet. This is consistent with the interpretation of the withdrawal of the foot caudally from the footprint during the take-off phase of the footprint cycle.

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larger image TIFF original image Download: Figure 11. Hypothesized pes movement of the track-maker for Bellatoripes fredlundi. The digits were not dragged cranially through the substrate as previously described in theropods footprints [53], [54], [55]. The pes and digits were retracted from the substrate along an opposite trajectory of their entry prior to the pes moving forward in the next step cycle. Arrows indicate trajectory of the foot of Trackway C, print #2 as deduced from entry striations at the point of pes entry (left frame) and exit (center frame) into the substrate. https://doi.org/10.1371/journal.pone.0103613.g011

In recent years, the evidence for gregarious behaviour in some species of theropod dinosaurs has substantially increased [14], [15], [62], [63]. This evidence takes the form of osteological signaling features and pathologies that show interactions between individuals, and analysis of monodominant bonebeds [15]. Although tyrannosaurid footprints are rare, it is significant that the first reported tyrannosaurid trackways represent three individuals moving in the same direction (roughly southeast: Trackway A –116°, Trackway B –120°, and Trackway C –128°, unadjusted) in close proximity (just over 5.5 meters between Trackways A and B, and just over 2.5 meters between Trackways B and C). Given that tyrannosaurids normally make up only five percent of the faunal composition [64], the probability of three unassociated tyrannosaurids walking in parallel (8.4 m between the two individuals that are farthest apart) is low. The preservation (depth of impression, lack of compression uplifts, evidence of skin impressions and striations) of the footprints in all three trackways suggests that they were made at approximately the same time, and increases the likelihood that these track-makers were associated. Tracks and trackways of smaller theropods and large ornithopods at this tracksite do not follow the same bearing as the tyrannosaurid trackways. In fact, the non-tyrannosaurid trackways are random in regards to compass bearing, which rules out a geographic barrier that might have compelled the tyrannosaurids to walk in the same direction and in close association. The inference that these three animals were moving as a social group is the most parsimonious interpretation based on current data [15] and provides the first trackway evidence showing gregarious behaviour in tyrannosaurs.

In calculating the relative velocity for the track-maker of Bellatoripes fredlundi, for Trackway A the estimated h of the track-maker is 2.87 m (+/–1.30 cm). It is worth pointing out that h calculated using the general large theropod equation [17] is 2.80 m. While the h for tyrannosaurids may not be significantly different from results obtained from the original equation [17], [18], the opportunity exists to determine the hip height to footprint length relationship for other taxa of both small and large theropods, which may be of use in studies that combine both computer simulations and known trackways.

One issue with using h to calculate relative velocity as per Thulborn and Wade [17] is that it only takes into account a completely straight hind limb, which is not anatomically accurate. The straight-leg hip height provides a lower limit to the velocity of the track-maker of Bellatoripes fredlundi. Taking into account a flexion of the knee of 110° and a flexion at the ankle of 140° [65], [66], an estimated hip height of 2.30 m is obtained. Using both values for h results in a range of relative velocities from 6.40 km/hr to 8.50 km/hr (+/–0.40 km/hr) for the maker of Trackway A, with a stride length (λ) to h ratio of 1.69 at the lower end of the range. This correlates with the hypothesized energetically optimal walking gait as determined for large bipedal dinosaurs [23], although the concept of such an optimum has been disputed [61]. Trackway A likely represents the optimal gait that the tyrannosaurid track-makers habitually used for general locomotion. While there is the need for caution in using footprint length in calculating track-maker velocities [67], the Bellatoripes fredlundi trackways comprise true tracks which are the least susceptible to erroneous velocity estimates.

The locomotory capabilities of tyrannosaurids have been studied and discussed at length in numerous articles [10], [60], [61], [68], [69], [70], [71], [72], [73], [74], [75], [76], [77], mostly addressing their speed and agility (specifically that of Tyrannosaurus rex). The calculated relative velocity of the tyrannosaurid track-maker of Trackway A of Bellatoripes fredlundi shows an animal that was moving at a typical walking gait, and does not provide insight into the top speed of the carnivorous track-maker. However, the trackways of Bellatoripes fredlundi provide the first record of the walking gait of tyrannosaurids. If tyrannosaurids were capable of higher-velocity gaits these would likely be at higher velocities than 8.50 km/h. Future models testing the potential velocity and gait of a tyrannosaurid will have the opportunity to incorporate the preserved track record of this group as an analytical control.