Naturwissenschaften DOI 10.1007/s00114-014-1238-3

ORIGINAL PAPER

Direct evidence of trophic interactions among apex predators in the Late Triassic of western North America Stephanie K. Drumheller & Michelle R. Stocker & Sterling J. Nesbitt

Received: 21 April 2014 / Revised: 31 August 2014 / Accepted: 2 September 2014 # Springer-Verlag Berlin Heidelberg 2014

Abstract Hypotheses of feeding behaviors and community structure are testable with rare direct evidence of trophic interactions in the fossil record (e.g., bite marks). We present evidence of four predation, scavenging, and/or interspecific fighting events involving two large paracrocodylomorphs (=‘rauisuchians’) from the Upper Triassic Chinle Formation (∼220–210 Ma). The larger femur preserves a rare history of interactions with multiple actors prior to and after death of this ∼8–9-m individual. A large embedded tooth crown and punctures, all of which display reaction tissue formed through healing, record evidence of a failed attack on this individual. The second paracrocodylomorph femur exhibits four unhealed bite marks, indicating the animal either did not survive the attack or was scavenged soon after death. The combination of character states observed (e.g., morphology of the embedded tooth, ‘D’-shaped punctures, evidence of bicarination of the marking teeth, spacing of potentially serial marks) indicates that large phytosaurs were actors in both cases. Our analysis of these specimens demonstrates phytosaurs targeted large paracrocodylomorphs in these Late Triassic ecosystems. Previous distinctions between ‘aquatic’ and ‘terrestrial’ Late Communicated by: Sven Thatje Electronic supplementary material The online version of this article (doi:10.1007/s00114-014-1238-3) contains supplementary material, which is available to authorized users. S. K. Drumheller (*) Department of Earth and Planetary Sciences, The University of Tennessee, 306 EPS Building, Knoxville, TN 37996, USA e-mail: [email protected] M. R. Stocker : S. J. Nesbitt Field Museum of Natural History, 1400 S Lake Shore Drive, Chicago, IL 60605, USA M. R. Stocker : S. J. Nesbitt Department of Geosciences, 4044 Derring Hall, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA

Triassic trophic structures were overly simplistic and built upon mistaken paleoecological assumptions; we show they were intimately connected at the highest trophic levels. Our data also support that size cannot be the sole factor in determining trophic status. Furthermore, these marks provide an opportunity to start exploring the seemingly unbalanced terrestrial ecosystems from the Late Triassic of North America, in which large carnivores far outnumber herbivores in terms of both abundance and diversity.

Keywords Loricata . Phytosauria . Tooth . Computed tomography . Apex predator

Abbreviations FMNH Field Museum of Natural History University of UC Chicago collections, Chicago, Illinois, U.S.A. FMNH Field Museum of Natural History Fossil Reptile PR collections, Chicago, Illinois, U.S.A. GR Ruth Hall Museum at Ghost Ranch, New Mexico, U.S.A. PVL Instituto Miguel Lillo, Tucuman, Argentina PVSJ Division of Paleontology of the Museo de Ciencias Naturales, Universidad Nacional de San Juan, Argentina TTU P Texas Tech University Museum of Paleontology, Lubbock, Texas, USA UCMP University of California Museum of Paleontology, Berkeley, California, USA UTCT The High-Resolution X-ray Computed Tomography Facility at The University of Texas at Austin, Austin, Texas, U.S.A YPM Yale Peabody Museum, New Haven, Connecticut, USA

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Introduction Trophic structure (e.g., interactions among primary producers, primary consumers, and multiple levels of secondary consumers including apex predators) is rarely preserved in the fossil record, and direct evidence of trophic interactions within a community is particularly rare (Behrensmeyer 1981; Boucot 1990; Behrensmeyer et al. 1992; Jacobsen 2001; Kowalewski 2002). Reconstructing community relationships in the fossil record is complicated by a number of potentially compounding factors including taphonomic biases, specimen collection protocols, and unfamiliar or non-analogue paleoecologies (Olson 1952, 1966; Tedford 1970; Murry 1989; Brown et al. 2013; Läng et al. 2013 and references therein). Time-averaging of fossil assemblages adds an additional layer of complication in that fossils from temporally, and even geographically, separate communities can be deposited and preserved together, creating a potentially false sense of association within these mixed assemblages (Olson 1952, 1966, 1980; Behrensmeyer et al. 1992; Kidwell and Flessa 1996). Despite the challenges, understanding vertebrate community interactions and ecology in deep time is a tantalizing avenue of study (e.g., Olson 1952; 1966; 1980; Behrensmeyer et al. 1992; Benton et al. 2004; Roopnarine 2009). The pinnacle of a community’s trophic structure, explicitly defined in terms of dietary selections and feeding interactions (Ritchie and Johnson 2009), is an apex predator. That behavioral definition allows for more than one apex predator within a given system, as well as within-species differences in classification, because variation in community composition may lead to members of a single species filling the role of apex predator in one ecological system and mesopredator in another (Ritchie and Johnson 2009). Therefore, the identification of apex predators in extinct communities can be of special interest to paleoecologists reconstructing the structure and evolution of trophic changes in those paleocommunities. Paleontologists, however, often resort to identifying apex predators in terms of their morphology, i.e., the physically largest or most robust organism (e.g., Smith et al. 2011; Stubbs et al. 2013; Zanno and Makovicky 2013; Cobos et al. 2014) or the most ‘advanced’ (i.e., using erect posture; Charig 1972; Parrish 1986, 1989) taxon that possesses traits associated with carnivory and is recovered from a given assemblage. Whereas those interpretations could be reasonable assumptions to draw from a functional point of view based on living analogues (i.e., Ritchie and Johnson 2009), hypotheses of relationships continuously evolve, and the loss of the shifting aspects of both behavior and trophic structures often simplifies what was likely a much more dynamic system. This is typified by the hypothesized trophic structures of the Chinle Formation terrestrial ecosystems outlined by Colbert (1972), Jacobs and Murry (1980), Murry (1989), and Parrish (1989). Though he did not discuss ‘rauisuchians’,

Colbert (1972:8) proposed that phytosaurs were likely at the “very apex of the Chinle food pyramid” seemingly because of their large size and ecological and morphological similarity to extant crocodylians. Jacobs and Murry (1980:65) presented what they termed an “oversimplified” interpretation of the Late Triassic vertebrate community as inferred from the known vertebrate assemblages of the Placerias and Downs quarries in east-central Arizona. In that study, phytosaurs (identified as Phytosaurus) and ‘rauisuchids’ were the dominant carnivores in the inferred aquatic and terrestrial schemes, respectively, with exchange of organic debris and predation, resulting in a close linkage between those two ecosystems. Parrish (1989) maintained the largest ‘rauisuchians’ (poposaurids in his study) at the top of his terrestrial trophic structure because of his interpretation of the group as “erect, highly active predators” (Parrish 1989: 235) and phytosaurs at the top of his aquatic trophic structure because of their “fusiform, crocodile-like bodies” (Parrish 1989: 238). However, he implied firmer distinctions between his inferred terrestrial and aquatic ecosystems as preserved within the Chinle Formation than did Jacobs and Murry (1980) or Murry (1989), with the dicynodont Placerias (interpreted as herbivorous) as the only crossover taxon between the terrestrial and the aquatic. Here, we present rare direct evidence of trophic interactions between a purported terrestrial apex predator and a purported aquatic apex predator (paracrocodylomorphs [=‘rauisuchians’] and phytosaurs, respectively) from the Upper Triassic Chinle Formation (∼225–202 Ma; Irmis et al. 2011; Ramezani et al. 2011, 2014; Atchley et al. 2013). Furthermore, we use an apomorphy-based approach to identify both the skeletal material and the feeding traces. Our direct evidence of trophic behavior tests previously hypothesized community interactions between these terrestrial and aquatic organisms (Jacobs and Murry 1980; Parrish 1989) with implications for the paleobiology and biomechanics of those Late Triassic apex predators.

Materials and methods We examined the external surfaces of both GR 264 and FMNH PR 1694 for potential evidence of tooth marks. Bone surface modifications were discovered prior to the complete preparation of both FMNH PR 1694 and GR 264. One of us (SJN) carefully removed the mudstone matrix from known marks on both specimens with a Micro-Jack 1 from Paleotools (www.paleotools.com) under a dissection microscope (Leica MZ9.5) using at least ×2 magnification. Smaller marks were cleaned with gentle scrubbing with a toothbrush and water. Butvar B-76 dissolved in acetone was applied with a small brush to reinforce unstable areas of each specimen. An embedded tooth was identified near the proximal end of GR 264 (Figs. 1a and 2). Previous studies, when faced with

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similarly embedded teeth, addressed this issue either by physically removing the tooth by preparing away the surrounding bone (Xing et al. 2012), or using computed tomographic (CT) scanning to visualize the tooth without destructive sampling (Boyd et al. 2013; DePalma et al. 2013). We opted for the less destructive method; the area surrounding the tooth was CTscanned in order to determine whether internal modifications had occurred to the bone and to determine the morphology and dimensions of the tooth itself without destroying the encasing bone. Scanning was performed by Matthew Colbert at UTCT as Archive 2913 on 14 January 2013. Scanning parameters were set to 450 kV and 1.3 mA. Slice thicknesses were 0.25 mm, with an inter-slice spacing of 0.23 mm, and field of reconstruction at 110 mm. Streak- and ring-removal processing was conducted by Julia Holland based on correction of raw sinogram data using IDL routines “RK_SinoDeStreak” with default parameters and “RK_SinoRingProcSimul” with parameter “sectors=100.” The resolution of the final images was 1,024 pixels by 1,024 pixels, 16-bit gray scale, and the total number of final slices is 197. CT data for GR 264 was imported into Mimics Innovation Suite 16.0 ×64 as a series of stacked Tiff images. The embedded tooth was digitally isolated through segmentation (Fig. 3), and measurements of the tooth and its orientation were taken of the digital volume render. The areas of reaction tissue and compressed bone were also isolated through segmentation (Fig. 3; for additional imagery see Online Resources 1, 2). Reaction tissue was identified as the tissue within the cortex of the femur that is less dense than the surrounding bone and is directly associated with either bite marks or healed bite marks on the external surface of the femur. However, the exact boundary between the reactionary tissue and the surrounding cortex is gradational (over ∼0.5 mm). As a result, we digitally isolated all of the tissue that was clearly less dense than that of the average density of the cortex.

Fossil description and systematic paleontology Archosauria Cope 1869 sensu Gauthier and Padian 1985 Pseudosuchia Zittel 1887–1890 sensu Sereno et al. 2005 Paracrocodylomorpha Parrish 1993 sensu Sereno et al. 2005 Specimen GR 264, proximal three-fifths of a right femur. Locality The specimen was discovered in the vicinity of Ghost Ranch, New Mexico, but the exact locality is unknown. The Upper Triassic sequence at Ghost Ranch, in stratigraphic order, consists of the Chinle Formation divided into the Agua Zarca Sandstone, Salitral Shale, Poleo Sandstone, Petrified Forest Member, and “siltstone member” (Irmis et al. 2007).

Among these subunits, the preservation (color and style) of GR 264 is most similar to those vertebrates from the highly fossiliferous Petrified Forest Member (Camp 1930; Irmis et al. 2007) that lies at the base of the cliffs surrounding Ghost Ranch, and no significant vertebrate fossils have been documented from the Agua Zarca Sandstone, Salitral Shale, or Poleo Sandstone. The Petrified Forest Member was deposited during the Norian Stage of the Late Triassic based on singlecrystal U-Pb age dating of detrital zircons which resulted in a maximum depositional age of ∼212 Ma for the Hayden Quarry within the same stratigraphic unit (Irmis et al. 2011); this also is consistent with magnetostratigraphic data (Zeigler and Geissman 2011). Taxonomic justification The specimen consists of a wellpreserved proximal three-fifths of a femur. The surface of the bone near midshaft is abraded. The proximal end bears distinct and equally sized anterolateral, anteromedial, and posteromedial tubera (sensu Nesbitt 2011). Equally sized medial condyles of the proximal end of the femur are present in paracrocodylomorphs (ACCTRAN synapomorphy in the analysis by Nesbitt 2011). Although the fourth trochanter is abraded, the strap-like shape is consistent with that of paracrocodylomorphs. Additionally, the femur is thin-walled near the midshaft, as is typical with, though not exclusive to, paracrocodylomorphs (Nesbitt 2011). The proximal articular surface lacks any kind of groove typical of most paracrocodylomorphs; however, the gigantic paracrocodylomorph Fasolasuchus tenax also lacks a proximal groove, although the presence or absence of a groove may be influenced by ontogeny. A proximal condylar fold is present in GR 264, and this character state is present in crocodylomorphs, rauisuchids, and F. tenax (Nesbitt 2011). GR 264 is identified as a paracrocodylomorph because the combination of character states presented above currently is known only in paracrocodylomorph archosaurs. Body size estimation Estimations of body size for extinct archosauriforms are often hampered by the lack of complete skeletons (but see Irmis 2011; Sookias et al. 2012; Turner and Nesbitt 2013). Because GR 264 is extremely large but only consists of a portion of the femur, we used linear measurements of the femora of other archosauriform taxa to estimate its total length and approximate the body size (as in Barrett et al. 2014). The width of the proximal head of GR 264 is approximately 125 mm. Based on a regression using 19 data points (Online Resource 3; best fit line, y=4.459x+9.32056, R2 =0.93077), we estimate the total length of GR 264 at 566 mm, with 95 % confidence intervals (CI) of 405.5 mm (lower) and 1,051 mm (upper). When only the closely related paracrocodylomorph taxa are included in the regression (best fit line, y=4.6324x+20.472, R2 =0.96006), the estimated total length of GR 264 is 600 mm (lower CI=470 mm; upper CI=

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728.8 mm). Therefore, our estimated total length of this femur (566–600 mm) is larger than the maximum reported femoral length for all Triassic non-dinosaurian archosauriforms other than Saurosuchus galilei, Postosuchus alisonae, and F. tenax (see Turner and Nesbitt 2013 for specimen data). Tight correlations between total body length and femoral length have been found among crocodylians (e.g., Farlow et al. 2005); however, estimations for other clades based on this dataset have revealed uncertainty caused by variations in tail length as compared with snout-vent length related to ontogeny, ecology, and even sexual dimorphism (Vandermark et al. 2007). The total body length of F. tenax (PVL 3850; femoral length=750 mm) was estimated to be 8–10 m (Nesbitt 2011). The total body length of the poposauroid Sillosuchus longicervex (PVL 2267; femoral length = 470 mm) was Fig. 1 Paracrocodylomorpha (GR 264), partial left femur in posteromedial (left image) and anterolateral (right image) views. a Embedded tooth and partially healed puncture; b two partially healed punctures and group of four unhealed fusiform pits below; c two possible pits (unprepared); d partially healed puncture; e group of scores prior to specimen damage. Scale bar next to complete fossil=10 cm. Scale bars in magnified photographs=1 cm

estimated at 9–10 m because of more elongated cervical vertebrae and an elongated tail in poposauroids (Nesbitt 2011). The 566–600 mm femoral length estimate for GR 264 represents a paracrocodylomorph that may have been comparable in size to those taxa (i.e., between 8 and 9 m). Another metric for size comparison is to estimate body mass using the minimum circumferences of the femoral and humeral shafts (Campione and Evans 2012; Campione et al. 2014). The minimum circumference of GR 264 is approximately 165 mm, but, without an associated humerus, body mass cannot be estimated for this individual at this time. In order to estimate the minimum total body length of the phytosaur that attacked GR 264 and embedded the tooth, we related the largest diameter of a phytosaur tooth to skull length based on our preliminary measurements of a series of complete phytosaur skulls (Online Resource 3). Few phytosaur

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skulls with prepared anterior alveoli and a measurable skull length (from the anterior edge of the premaxilla to the posterior portion of the occipital condyle) could be measured for this analysis; most phytosaur specimens either have incomplete or unprepared premaxillary alveoli; the skull is anteroposteriorly distorted; portions of the rostrum include reconstructed sections; or these measurement data are not reported in the literature. We identify the embedded phytosaur tooth as a ‘premaxillary fang’ (see below); this type of tooth is located in either the first or second alveolus in the premaxilla of phytosaurs as part of the ‘tip-of-snout set’ (Hungerbühler 2000). We measured the maximum diameter of the first and second premaxillary alveoli as a proxy for tooth crown width and used the larger of the two measurements in our analysis. Skull length was measured from the anterior edge of the premaxilla to the posterior edge of the basioccipital in order to conform to the dorsal cranial length measurements used by Hurlburt et al. (2003). We recovered a positive relationship between premaxillary fang alveolus size and skull length (i.e., longer skulls had larger alveoli; best fit line, y= 0.0385x−13.332, R2 = 0.91). Applying those results to the maximum measured diameter of the embedded tooth crown (14.6 mm) resulted in a skull length of 725 mm for the phytosaur. However, this is a minimum anteroposterior skull length because of the incomplete preservation of the embedded tooth crown. Additionally, the low number of data points here (n=6) resulted in high 95 % confidence intervals (lower CI= 272 mm; upper CI=1,860 mm). We related our skull length to total body length using data from Hurlburt et al. (2003) and found the individual that attacked the paracrocodylomorph to be approximately 5 to 6 m in total body length, though there is potential variation in skull to total body length within Phytosauria that would affect this estimate. Archosauria Cope 1869 sensu Gauthier and Padian 1985 Pseudosuchia Zittel 1887–1890 sensu Sereno et al. 2005 Paracrocodylomorpha Parrish 1993 sensu Sereno et al. 2005

2014). Other fossils collected and originally catalogued with this specimen include the distal end of a humerus of a phytosaur (FMNH PR 1694; incorrectly identified as a proximal end of a femur) and a complete ilium of a phytosaur (FMNH UC 1252; plate II in Mehl et al. 1916). Taxonomic justification The distal end of the femur has a prominent crista tibiofibularis separated from the lateral distal condyle of the femur by an obtuse angle, and the posterior tips of the medial condyle and the crista tibiofibularis point posteriorly as in poposauroids and early diverging paracrocodylomorphs (Nesbitt 2011). Like GR 264, this femur is thin-walled as in paracrocodylomorphs. The posterior surface of the medial condyle is deflected posteroventrally as in Poposaurus gracilis (YPM 57100). Even though there are no clear apomorphies placing FMNH PR 1694 within the clade Archosauria, the combination of character states listed above result in an assignment in Paracrocodylomorpha, and possibly even a poposauroid affinity.

Specimen FMNH PR 1694, distal portion of a left femur. Locality This specimen was collected by P. C. Miller in 1913 near Fort Wingate, McKinley County, western New Mexico. The specimen likely came from the lower half of the Chinle Formation in this area (Mehl et al. 1916), and these beds now are assigned to either the Bluewater Creek Member or the overlying Blue Mesa Member (Heckert and Lucas 2002). The age of those units is likely Norian and older than ∼218 Ma, given that they are stratigraphically below a well-dated sandstone just above the Bluewater Creek Member (=Six Mile Canyon bed; Irmis et al. 2011; Ramezani et al.

Fig. 2 Paracrocodylomorpha (GR 264), proximal end of partial left femur in posteromedial view (upper image) with interpretive line drawing (lower image), indicating positions of tubera, the embedded tooth, and healed and unhealed bite marks. Question mark=possible marks in regions of poor preservation, hindering more definite identification. Scale bar=5 cm

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Results Description of bite marks GR 264 GR 264 exhibits multiple morphologically distinct groupings of bite marks. The embedded tooth is along the proximal portion of the posterolateral margin of the femur. The tooth fragment ranges from flush with to slightly inset into the surrounding bone, so essentially none of the tooth’s exterior surface was immediately visible. The tooth is ovoid to nearly circular in cross section with carinae present along the mesial and distal edges. The exposed area of the tooth is 14.6 mm in diameter at the carinae and 12.6 mm in diameter perpendicularly to that, with exposed enamel approximately 2 mm in thickness. A halo of reaction tissue surrounds the tooth, extending from less than 1 mm to roughly 3.5 mm in thickness. CT scans revealed that the tooth fragment is 32.8 mm long and penetrated the femur from near the posterolateral margin of the femur and moved anteriorly where it came within approximately 5 mm (through roughly 87 % of the bone crosssectional thickness) of exiting the anterolateral side of the element (Fig. 3). The embedded tooth crown appears complete, is conical in shape, and bears mesial and distal carinae. Fig. 3 CT rendering of paracrocodylomorph (GR 264), partial right femur showing positions of embedded tooth and other bite marks in a dorsal; b ventral; c anterolateral; d posteromedial views; and e ventral view without other marks highlighted. CT rendering of embedded tooth in f labial and g mesial/distal views. In f and g, the distal end of the tooth is oriented towards the top of the page. Dorsal view slice images of the embedded tooth in the GR 264 from h near the tip of the tooth; i near midlength of the tooth; and j near the base of the tooth. In each view (online-only), the embedded tooth is rendered in green; the reaction tissue surrounding the tooth is purple, and the other bite marks are orange

The halo of reaction tissue is also visible in the CT scans, extending into the bone’s subsurface and surrounding the entire tooth. Situated roughly 15 mm (21.4 mm from tooth to mark centers) distal to the embedded tooth is a heavily remodeled puncture (sensu Binford 1981). This mark also is roughly ovoid in cross-section (9.8 by 7.5 mm in diameter) with a raised lip and is infilled with irregular reaction tissue (Fig. 1a). CT data revealed that this mark was formed by a roughly conical tooth that penetrated the femur to a depth of approximately 11 mm and created reaction tissue related to the bite (Fig. 3). This remodeling makes it unclear how well the ellipsoid shape of the mark at the surface of the bone reflects the original morphology of the tooth. However, the similarities in position, shape, position relative to the orientation of the embedded tooth, and extent of healing as represented by the reaction tissue suggest that this mark was formed during the same event in which the embedded tooth was implanted, possibly suggesting that the two structures were serial in origin (i.e., formed together during a single biting event). Four additional partially healed bite marks are present on the proximal portion of GR 264: two near the midline on the posteromedial surface (Figs. 1b and 2) and two on the

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anterolateral, near the medial edge (Fig. 1d). All are slightly more fusiform in shape, with irregular reaction tissue forming their interiors and raised lips around their margins. As with the previously described, partially healed bite mark, CT data suggest conical teeth formed these marks, though bone remodeling has hindered more detailed discussion of their morphology and orientation. The exposed mark on the anterolateral surface of the femur (8.4 by 4.4 mm), and the more medially positioned of the posteromedial marks (7.3 by 6.0 mm; Fig. 2) are more D-shaped, with one side of the structure significantly more convex than the other. The mark more laterally positioned on the posteromedial surface of the femur is more symmetrical and is slightly elongate (9.5 by 4.8 mm). CT data revealed the final mark (∼7 by ∼8 mm based on measurements of the CT data), concealed under matrix approximately 15 mm distal to the exposed bite mark on the anterolateral surface of the bone, as well as regions of reaction tissue that are more conically shaped and extend beyond all the surficial marks (Fig. 3). A separate set of pits (sensu Binford 1981) is located on the anterolateral and posteromedial surfaces of the proximal end of GR 264. Unlike the marks described above, these traces exhibit no obvious reaction tissue, indicating that they were formed at or near time of death. Four of these pits are clustered together near the midline of the proximal posteromedial surface (Fig. 1b). They are similar in shape (symmetrically fusiform) and size (8.76 by 4.29 mm; 7.03 by 3.72 mm; 8.88 by 4.59 mm; 6.90 by 4.11 mm), suggesting a single trace maker. There are two possible pits on the anterolateral surface opposing this set (Fig. 1c); these marks are similar in size and shape to the posterolateral pits, but this identification is tenuous due to the poor preservation of this region of the femur. A final set of six bite marks was present on the posteromedial surface of the femur, near the midshaft of the bone. These scores all were oriented roughly perpendicular to the long axis of the femur with most marks subparallel (Fig. 1e). Simple scores ranged from 0.5 to 1.0 mm in width and 12 to 14 mm in length. One mark was identifiable as a hook score (sensu Njau and Blumenschine 2006), a feeding trace type whose ‘L’- to ‘J’-shaped morphology has been associated with organisms that practice an inertial feeding strategy (D’Amore and Blumenschine 2009; Drumheller and Brochu 2014). Unfortunately, the region of the femur exhibiting these marks was damaged during post-CT scanning shipment of the specimen, leaving only two intact. FMNH PR 1694 At least four bite marks are observed on FMNH PR 1694. All are asymmetrically fusiform and roughly ‘D’-shaped. The two largest marks are oriented on opposing sides of the femur,

positioned slightly medially from the midline (Fig. 4a, d). Both are situated with the more convex side oriented distally on the femur. The puncture in the anterior surface extends all the way into the medullary cavity of the femur, whereas the posterior mark penetrates to a depth of 9 mm. Both are also associated with secondary impact damage in the form of radiating fractures (sensu Byers 2005). The puncture on the posterior surface is further modified with depressed fractures, in which the surrounding bone collapsed under the force of the bite. These lines of evidence, partnered with their similar size (anterior puncture=15.22 mm by 9.26 mm; posterior puncture=15.37 mm by 9.33 mm) and the similar orientation of their long axes, strongly support our hypothesis that these two marks are serial in origin. Another bite mark is present on the posterior surface of the femur near the broken edge (Fig. 4c). This mark is truncated by the break and further obscured by the radiating and depressed fractures associated with the nearby puncture, rendering accurate measurements impossible. However, the size and curvature of the remaining margin of the mark indicates that it would have been of a similar size as the other two punctures. The last bite mark is present on the lateral surface of the shaft at the distalmost end (Fig. 4b). This pit is significantly smaller (7.61 mm by 5.60 mm) than the previously described punctures and is roughly ‘D’-shaped, with the more convex side oriented posteriorly on the femur. This mark is also associated with prominent radiating fractures, indicating that, while this tooth did not penetrate to the same depth as the described punctures, it still impacted the femur with great force.

Discussion Identification of bite marks Bite marks are comparatively rare in the fossil record (e.g., Behrensmeyer 1981; Boucot 1990; Behrensmeyer et al. 1992; Jacobsen 2001; Kowalewski 2002), and direct association between those trace fossils and embedded teeth even more so. Among archosaurs, embedded teeth previously were identified among theropod dinosaurs (Currie and Jacobsen 1995; Xing et al. 2012; DePalma et al. 2013) and crocodyliforms (Franzen and Frey 1993; Boyd et al. 2013). Though bite marks attributed to possible intraspecific fighting among phytosaurs have been reported previously (Abel 1922; Camp 1930; Stocker 2010), this fossil represents the first identification of an embedded phytosaurian tooth. The identification of the embedded tooth as that of a phytosaur is based on its size and general morphology in

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Fig. 4 Paracrocodylomorpha (FMNH PR 1694) partial left femur in anterior (top image) and posterior (bottom image) views. a Large puncture with associated fracturing; b small pit with associated fracturing; c truncated puncture with associated fracturing; d large puncture with associated fracturing. Scale bar next to complete fossil=5 cm. Scale bars in magnified photographs=1 cm

comparison to the dental morphology detailed for Nicrosaurus kapffi (Hungerbühler 2000). Tooth morphology has the potential to be utilized to determine both positional relationships within a set of dentition as well as possible taxonomic and systematic identifications, but it has not been utilized for phytosaurs much beyond the detailed study by Hungerbühler (2000). Those data were used to identify the first isolated phytosaur teeth from Lithuania (Brusatte et al. 2012). The lack of bilaterally compressed teeth (=mediolaterally compressed) was suggested to be apomorphic for Phytosauria (Hungerbühler 2000). The exposed cross section of the embedded tooth in GR 264 is nearly circular; however, computed

tomographic data reveal that the carinae extend along both the distal and mesial edges of the tooth as slight flanges, creating a ‘D’ shape in cross-sectional view (Fig. 3). The more pronounced carinae on the distal (=posterior) portion of the tooth is comparable to that observed for the large first and second premaxillary teeth and the anteriormost dentary teeth of a phytosaur, as part of the ‘tip-of-snout set’ (Hungerbühler 2000). Examination of the size, shape, location, and amount of healing of the more distally positioned, partially healed puncture suggests that it was formed serially with the embedded tooth. Therefore, we attribute this mark to the same phytosaur individual. As for the remaining partially healed bite marks, it is unclear how well the shape of the raised lip of reaction tissue on the surface of the bone reflects the shape of the original tooth. The reaction tissue visible in the subsurface using CT data extends away from the mark center beyond the surficial margins of the raised reaction tissue and appears to reflect damage caused by a conical, rather than mediolaterally compressed, tooth. Again, the similar extent and texture of the reaction tissue surrounding these marks seems to indicate that they occurred very close in time with the bite that left the embedded tooth and healed serial puncture. The most parsimonious explanation is that these marks were created by the same actor and represent separate biting events during a single trophic interaction or incidence of interspecific fighting. All remaining bite marks on GR 264 exhibit crushing, impact damage, and no obvious evidence of healing. We interpret these marks as having occurred at or near time of death. The unhealed pits (four on the posteromedial surface of the femur; Fig. 1b) are nearly identical in size and shape, indicating that they likely were formed by the same actor. These marks are fusiform in shape, indicating formation by bicarinated, laterally compressed teeth. Potential Triassic carnivores that possessed such teeth include some phytosaurs, dinosauromorphs, and paracrocodylomorphs. Because these marks lack other potentially diagnostic characteristics, we cannot exclude any of these possible groups as the potential actor at this time. The scores that were present on GR 264 prior to damage (Fig. 1e) were generally ‘U’-shaped in cross-section. They lacked striations, which are characteristic of serrated teeth (D’Amore and Blumenschine 2009), bisections, which are formed by strongly bicarinated teeth (Njau and Blumenschine 2006; Drumheller and Brochu 2014), or any other potentially diagnostic trait that might facilitate more specific identification. The marks were small (0.5– 1 mm in width), relatively subparallel, and closely spaced (0.5–1 cm apart), potentially suggestive of a physically smaller actor than the one responsible for the associated pits described above, and one with a relatively homodont dentition. This leaves a wide variety of potential actors, including any carnivorous archosauriform.

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There are three obvious ‘D’-shaped punctures on the femoral shaft of FMNH PR 1694 and one other puncture truncated by fractures. Their morphology is consistent with a tooth that is not bilaterally compressed, such as a maxillary or posterior dentary tooth of a phytosaur (Hungerbühler 2000). We interpret the bites to be serial in origin because of the asymmetric convexity of the puncture on the anterior surface of FMNH PR 1694 and the orientation of the carinae on both the anterior and posterior punctures, representing a single bite from upper and lower teeth on the left side of the dentition of a single individual. The truncated mark was not formed serially with the other two punctures. It is oriented at an opposing angle to the previous two marks, closer to parallel with the long axis of the femur rather than strongly transverse. Also, this truncated mark seems to further compromise the region of the bone already inset by the extensive depressed fractures associated with the complete puncture. Because one side of the mark intersects and is interrupted by one of the fractures generated by the completely preserved puncture, we interpret this trace to have occurred after the serial marks. The similarities between these marks indicate that they were created by a single trace maker. The single pit, present on the lateral surface of the shaft, is also asymmetrically fusiform, again indicating a phytosaurian trace maker. Pit size, even among marks made by a single actor, can vary widely with factors such as bite force and density of the region of modified bone (Delaney-Rivera et al. 2009). Therefore, it is likely, but by no means certain, that this mark can be associated with the previously described punctures.

Paleobiological interpretations The substantial reaction tissue in GR 264 surrounding the embedded phytosaur tooth and infilling the four punctures associated with it indicates that the paracrocodylomorph survived an attack by a large phytosaur long enough for extensive healing to occur. None of the healed wounds present on GR 264 exhibit the proliferative, spongy lesions that are indicative of widespread infection (e.g., Mackness and Sutton 2000). Considering the depth of the injuries, and the introduction of a foreign body into the bone itself in the form of the embedded tooth, this lack of evidence for infection is somewhat surprising. However, extant crocodylians are unusually resistant to many forms of infection (Merchant et al. 2003, 2006). This trait might have been shared with more distantly related archosaurs, but our ability to identify this feature in paracrocodylomorphs is hindered because bracketing this specific immune response requires comparative knowledge of this process in crocodylians, birds, lepidosauromorphs, and possibly turtles.

Whether this was a failed predation attempt or an incident of interspecific fighting is not clear. Positive association of bite marks with predation versus scavenging behavior is difficult to determine with complete certainty for the marks that do not exhibit evidence of healing. One way to address this issue is by discussing order of access to remains and element food utility. Indices of skeletal element food utility can be calculated in a number of ways (Lyman 1994), but most rank bones in terms of the amount of associated edible tissues. In the case of low utility bones, such as phalanges and metapodials, bite marks concentrated in these regions have been associated with late access to remains (i.e., scavenging; Longrich et al. 2010). Conversely, concentrations of marks on high utility bones, such as the femur, are indicative of early access to remains. Whereas a predator would certainly have early access to a carcass, so too would a scavenger encountering the fresh remains of an animal which died through some other means. Both GR 264 and FMNH PR 1694 are highutility, partial femora. We identify bite marks from at least three actors on GR 264, two of which occurred at or near time of death. Based on the food utility of these femora, we interpret that both of these actors had early access to the remains, though a determination of predation or scavenging is impossible to make with the current data. The same can be said of the bite marks present on FMNH PR 1694. Many paleontological studies of bite marks focus on marks left by single actors (e.g., Currie and Jacobsen 1995; Erickson and Olson 1996), whereas, in current ecosystems, multiple predators and scavengers have been observed regularly interacting with the same set of remains (Selvaggio and Wilder 2001). Actualistic studies, many of which focused specifically on interactions between early hominins and other carnivores, attempted to identify patterns of modification that signal early versus late access to a prey item (Shipman 1986; Marean and Spencer 1991; Domínguez-Rodrigo 2002; Lupo and O’Connell 2002), and the general patterns uncovered in those studies should be applicable in non-human systems. For example, early access to remains results in higher mark density on the bones that supported more soft tissue during life (Shipman 1986; Marean and Spencer 1991; Lupo and O’Connell 2002; Longrich et al. 2010). The bite marks present on GR 264 preserve evidence of at least three distinct interactions. The partially healed marks attributable to a phytosaur (Figs. 1, 2, and 3) represent an incident that clearly pre-dated the paracrocodylomorph’s death. The larger pits associated with a more ziphodont predator occur on a high economy bone (the femur) at a grasping point of the limb (near the hip socket), a pattern which is associated with disarticulation behavior in modern crocodylians (Njau and Blumenschine 2006). In contrast, the smaller, subparallel scores are more consistent with flesh stripping behavior (D’Amore and Blumenschine 2009). These marks do demonstrate a faunal succession of carnivores interacting with this single prey item,

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but a more specific sequence to these two peri- or post-mortem events is impossible to elucidate. Phytosaurs and ‘rauisuchians’ have been identified as dominant predators from the Late Triassic (e.g., Jacobs and Murry 1980; Murry 1989; Parrish 1989; Long and Murry 1995; Weinbaum 2013), and in part, this line of thought was influenced by the large body size of these fossils. Phytosaur body mass calculated based on skull and limb length as well as an approximated snout-vent length resulted in estimated masses of 200–350 kg on average and lengths of near 4.5 m for pseudopalatine phytosaurs from the Canjilon and Snyder quarries (Hurlburt et al. 2003); our total body length estimate of 5–6 m for the phytosaur that attacked GR 264 (see above) implies a larger individual than the average for those pseudopalatines. Excluding phytosaurs and saurischian dinosaurs, paracrocodylomorphs have the longest femora of any archosaur and thus are hypothesized to have had among the largest body sizes of Late Triassic Archosauriformes (Turner and Nesbitt 2013). The estimated 8 to 9 m total body length of GR 264, based on comparisons with closely related forms, places it among the largest members of that group. Both paracrocodylomorph femora we described in this study came from some of the physically largest carnivorous taxa present at both localities, and yet, they were targeted by other members of the fauna, specifically phytosaurs. Phytosaurs are interpreted as having had piscivorous, generalist, or predatory ecologies, depending on their skull morphologies as compared to those of extant crocodylians (e.g., Hunt 1989; Murry 1989), but direct evidence to test those potential ecologies is rare and may not support previous hypotheses (e.g., Chatterjee 1978; Stocker and Butler 2013). For example, longirostrine crocodylians often are cited as piscivorous (e.g., Iordansky 1973; Langston 1973; Busby 1995), but ecological studies of extant groups do not always support this interpretation. Surveys of stomach contents of Mecistops cataphractus do demonstrate a diet dominated by fish (Pauwels et al. 2003), but diet is often more diverse in other longirostrine forms. Though extant gharials are considered strictly fish specialists, even they have been known to eat frogs, mammals, birds, and lepidosaurs (Whitaker and Basu 1983). Tomistoma schlegeii has been mistakenly considered almost entirely piscivorous for over 40 years because of a citation of a popular publication (Neill 1971). However, recent actualistic research (e.g., Selvaraj 2012) demonstrated that the diet of T. schlegeii is much more variable and includes teleost fish, turtles, monitor lizards, birds, and mammals (including primates). Ecological observations and surveys of stomach contents of Crocodylus johnstoni demonstrate that these crocodiles have a diverse diet that includes arthropods, anurans, fish, turtles, and snakes (Webb and Manolis 1988; Tucker et al. 1996). Therefore, a direct correlation between long,

slender rostra and strict piscivory is not supported in living examples. Thus, the use of modern analogues for reconstructing the diet of phytosaurs and their placement in a trophic structure is only tentative until other evidence (direct or indirect) is supplied by the fossil record, as we demonstrate here. It is clear that phytosaurs and paracrocodylomorphs were part of a more complex network of community relationships in the Late Triassic than previously appreciated and newer trophic models incorporating hypothesis-tested characteristics of extinct taxa and neural network-based methods (e.g., Roopnarine et al. 2007; Roopnarine 2009; Sidor et al. 2013) are required to provide testable and more accurately modeled community structure. The complex trophic structure illustrated by large apex predators preying on each other hints at a broader question rarely mentioned: Why are there so many large carnivorous tetrapods in the Upper Triassic assemblages of western North America? Seemingly carnivorous taxa are overrepresented in Late Triassic tetrapod assemblages (Heckert 2004; Heckert et al. 2005; Nesbitt and Stocker 2008) compared with extant mammalian or large squamate ratios (e.g., Bakker 1972; Stock and Harris 1992). Part of this pattern may be explained by taphonomic size bias (Brown et al. 2013) or collection practices, because excavation of the Canjilon Quarry was focused on phytosaurs and complete specimens, and small and/or fragmentary specimens were not prioritized (Hunt and Downs 2002). However, this does not necessarily explain why unbalanced ratios still are recorded in other more comprehensively sampled localities from the Late Triassic, which include substantial small-bodied components in their faunas (i.e., Hayden Quarry; Irmis et al. 2007). Previously reported imbalances in Mesozoic ecosystems have been explained by greater than expected interactions between aquatic and terrestrial taxa (Läng et al. 2013). A similar situation may be at play here, as demonstrated by the fossilized interactions presented in this study, but further research is required to fully explain this tangible unbalance.

Acknowledgments Financial support for CT scanning was provided to MRS by the Jackson School of Geosciences and the William J. Powers, Jr. Presidential Graduate Fellowship, The University of Texas at Austin. Details related to FMNH PR 1694 were provided by W. Simpson. Information related to GR 264 was confirmed by A. Downs. Initial access to and data on GR 264 at UCMP was provided to SKD by P. Holroyd. Measurement data for some taxa in Table 1 of the Electronic Supplemental Data was provided by J. Desojo and B. Muller. Helpful discussion with C. Sumrall, S. Sheffield, R. Roney, and J. Horton, as well as informative comments from reviewer C. Brown, an anonymous reviewer, and editor S. Thatje, improved the quality of this manuscript. The research presented in this study complies with all relevant state and federal laws. The authors declare that they have no conflicts of interest.

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