1DIRECT EVIDENCE OF TROPHIC INTERACTIONS AMONG APEX PREDATORS IN
2 THE LATE TRIASSIC OF WESTERN NORTH AMERICA
3
4 Stephanie K. Drumheller1*, Michelle R. Stocker2, 3, and Sterling J. Nesbitt2, 3
5
61Department of Earth and Planetary Sciences, The University of Tennessee, 306 EPS Building,
7Knoxville, TN, 37996, USA; 2Field Museum of Natural History, 1400 S Lake Shore Drive,
8Chicago, IL, 60605, USA; 3Department of Geosciences, 4044 Derring Hall, Virginia Polytechnic
9Institute and State University, Blacksburg, Virginia, 24061, USA; [email protected];
11* Corresponding author: [email protected]; phone: (865) 974-2366; fax: (865) 974-2368
12
13Keywords: Loricata, Phytosauria, tooth, computed tomography, apex predator
14
15 ABSTRACT
16 Hypotheses of feeding behaviors and community structure are testable with rare direct
17evidence of trophic interactions in the fossil record (e.g., bite marks). We present evidence of
18four predation, scavenging, and/or interspecific fighting events involving two large
19paracrocodylomorphs (= ‘rauisuchians’) from the Upper Triassic Chinle Formation (~220-210
20Ma). The larger femur preserves a rare history of interactions with multiple actors prior to and
21after death of this ~8-9 m individual. A large embedded tooth crown and punctures, all of which
22display reaction tissue formed through healing, record evidence of a failed attack on this
23individual. The second paracrocodylomorph femur exhibits four unhealed bite marks indicating
1 24the animal either did not survive the attack or was scavenged soon after death. The combination
25of character states observed (e.g. morphology of the embedded tooth, ‘D’-shaped punctures,
26evidence of bicarination of the marking teeth, spacing of potentially serial marks) indicates that
27large phytosaurs were actors in both cases. Our analysis of these specimens demonstrates
28phytosaurs targeted large paracrocodylomorphs in these Late Triassic ecosystems. Previous
29distinctions between ‘aquatic’ and ‘terrestrial’ Late Triassic trophic structures were overly
30simplistic and built upon mistaken paleoecological assumptions; we show they were intimately
31connected at the highest trophic levels. Our data also support that size cannot be the sole factor in
32determining trophic status. Furthermore, these marks provide an opportunity to start exploring
33the seemingly unbalanced terrestrial ecosystems from the Late Triassic of North America, in
34which large carnivores far out-number herbivores in terms of both abundance and diversity.
35
36 INTRODUCTION
37 Trophic structure (e.g. interactions among primary producers, primary consumers, and
38multiple levels of secondary consumers including apex predators) is rarely preserved in the fossil
39record, and direct evidence of trophic interactions within a community is particularly rare
40(Behrensmeyer 1981; Boucot 1990; Behrensmeyer et al. 1992; Jacobsen 2001; Kowalewski
412002). Reconstructing community relationships in the fossil record is complicated by a number
42of potentially compounding factors including taphonomic biases, specimen collection protocols,
43and unfamiliar or non-analogue paleoecologies (Olson 1952, 1966; Tedford 1970; Murry 1989;
44Brown et al. 2013; Läng et al. 2013 and references therein). Time-averaging of fossil
45assemblages adds an additional layer of complication in that fossils from temporally, and even
46geographically, separate communities can be deposited and preserved together, creating a
2 47potentially false sense of association within these mixed assemblages (Olson 1952, 1966, 1980;
48Behrensmeyer 1982; Kidwell and Flessa 1996). Despite the challenges, understanding vertebrate
49community interactions and ecology in deep time is a tantalizing avenue of study (e.g. Olsen
501952, 1966, 1980; Behrensmeyer et al. 1992; Benton et al. 2004; Roopnarine 2009).
51 The pinnacle of a community’s trophic structure, explicitly defined in terms of dietary
52selections and feeding interactions (Ritchie and Johnson 2009), is an apex predator. That
53behavioral definition allows for more than one apex predator within a given system, as well as
54within-species differences in classification, because variation in community composition may
55lead to members of a single species filling the role of apex predator in one ecological system and
56mesopredator in another (Ritchie and Johnson 2009). Therefore, the identification of apex
57predators in extinct communities can be of special interest to paleoecologists reconstructing the
58structure and evolution of trophic changes in those paleocommunities. Paleontologists, however,
59often resort to identifying apex predators in terms of their morphology; i.e., the physically largest
60or most robust organism (e.g. Smith et al. 2011; Stubbs et al. 2013; Zanno and Makovicky 2013;
61Cobos 2014) or the most ‘advanced’ (i.e. using erect posture; Charig 1972; Parrish 1986, 1989)
62taxon that possesses traits associated with carnivory and is recovered from a given assemblage.
63Whereas those interpretations could be reasonable assumptions to draw from a functional point
64of view based on living analogues (i.e. Ritchie and Johnson 2009), hypotheses of relationships
65continuously evolve, and the loss of the shifting aspects of both behavior and trophic structures
66often simplifies what was likely a much more dynamic system.
67 This is typified by the hypothesized trophic structures of the Chinle Formation terrestrial
68ecosystems outlined by Colbert (1972), Jacobs and Murry (1980), Murry (1989), and Parrish
69(1989). Though he did not discuss ‘rauisuchians’, Colbert (1972:8) proposed that phytosaurs
3 70were likely at the “very apex of the Chinle food pyramid” seemingly because of their large size
71and ecological and morphological similarity to extant crocodylians. Jacobs and Murry (1980:65)
72presented what they termed an “oversimplified” interpretation of the Late Triassic vertebrate
73community as inferred from the known vertebrate assemblages of the Placerias and Downs
74quarries in east-central Arizona. In that study, phytosaurs (identified as Phytosaurus) and
75‘rauisuchids’ were the dominant carnivores in the inferred aquatic and terrestrial schemes,
76respectively, with exchange of organic debris and predation resulting in a close linkage between
77those two ecosystems. Parrish (1989) maintained the largest ‘rauisuchians’ (poposaurids in his
78study) at the top of his terrestrial trophic structure because of his interpretation of the group as
79“erect, highly active predators” (Parrish 1989:235) and phytosaurs at the top of his aquatic
80trophic structure because of their “fusiform, crocodile-like bodies” (Parrish 1989:238). However,
81he implied firmer distinctions between his inferred terrestrial and aquatic ecosystems as
82preserved within the Chinle Formation than did Jacobs and Murry (1980) or Murry (1989), with
83the dicynodont Placerias (interpreted as herbivorous) as the only crossover taxon between the
84terrestrial and the aquatic.
85 Here we present rare direct evidence of trophic interactions between a purported
86terrestrial apex predator and a purported aquatic apex predator (paracrocodylomorphs [=
87‘rauisuchians’] and phytosaurs, respectively) from the Upper Triassic Chinle Formation (~225-
88202 Ma; Irmis et al. 2011; Ramezani et al. 2011, 2014; Atchley et al. 2013). Furthermore, we use
89an apomorphy-based approach to identify both the skeletal material and the feeding traces. Our
90direct evidence of trophic behavior tests previously hypothesized community interactions
91between these terrestrial and aquatic organisms (Jacobs and Murry 1980; Parrish 1989) with
92implications for the paleobiology and biomechanics of those Late Triassic apex predators.
4 93
94Institutional Abbreviations – FMNH UC, Field Museum of Natural History University of
95Chicago collections, Chicago, Illinois, U.S.A.; FMNH PR, Field Museum of Natural History
96Fossil Reptile collections, Chicago, Illinois, U.S.A.; GR, Ruth Hall Museum at Ghost Ranch,
97New Mexico, U.S.A.; PVL, Instituto Miguel Lillo, Tucuman, Argentina; PVSJ, Division of
98Paleontology of the Museo de Ciencias Naturales, Universidad Nacional de San Juan, Argentina;
99TTU P, Texas Tech University Museum of Paleontology, Lubbock, Texas, U.S.A.; UCMP,
100University of California Museum of Paleontology, Berkeley, California, U.S.A.; UTCT, The
101High-Resolution X-ray Computed Tomography Facility at The University of Texas at Austin,
102Austin, Texas, U.S.A; YPM, Yale Peabody Museum, New Haven, Connecticut, U.S.A.
103
104 MATERIALS AND METHODS
105 We examined the external surfaces of both GR 264 and FMNH PR 1694 for potential
106evidence of tooth marks. Bone surface modifications were discovered prior to the complete
107preparation of both FMNH PR 1694 and GR 264. One of us (SJN) carefully removed the
108mudstone matrix from known marks on both specimens with a Micro-Jack 1 from Paleotools
109(www.paleotools.com) under a dissection microscope (Leica MZ9.5) using at least 2X
110magnification. Smaller marks were cleaned with gentle scrubbing with a toothbrush and water.
111Butvar B-76 dissolved in acetone was applied with a small brush to reinforce unstable areas of
112each specimen.
113 An embedded tooth was identified near the proximal end of GR 264 (Figures 1A, 2).
114Previous studies, when faced with similarly embedded teeth, addressed this issue either by
115physically removing the tooth by preparing away the surrounding bone (Xing et al. 2012), or
5 116using computed tomographic (CT) scanning to visualize the tooth without destructive sampling
117(Boyd et al. 2013; DePalma et al. 2013). We opted for the less destructive method; the area
118surrounding the tooth was CT scanned in order to determine whether internal modifications had
119occurred to the bone and to determine the morphology and dimensions of the tooth itself without
120destroying the encasing bone. Scanning was performed by Matthew Colbert at UTCT as Archive
1212913 on 14 January 2013. Scanning parameters were set to 450 kV and 1.3mA. Slice thicknesses
122were 0.25 mm, with an inter-slice spacing of 0.23 mm, and field of reconstruction at 110 mm.
123Streak- and ring-removal processing was conducted by Julia Holland based on correction of raw
124sinogram data using IDL routines “RK_SinoDeStreak” with default parameters and
125“RK_SinoRingProcSimul” with parameter “sectors=100.” The resolution of the final images was
1261024 pixels by 1024 pixels, 16-bit gray scale, and the total number of final slices is 197.
127 CT data for GR 264 was imported into Mimics Innovation Suite 16.0 x64 as a series of
128stacked Tiff images. The embedded tooth was digitally isolated through segmentation (Figure 3),
129and measurements of the tooth and its orientation were taken of the digital volume render. The
130areas of reaction tissue and compressed bone were also isolated through segmentation (Figure 3;
131for additional imagery see Online Resources 1, 2). Reaction tissue was identified as the tissue
132within the cortex of the femur that is less dense than the surrounding bone and is directly
133associated with either bite marks or healed bite marks on the external surface of the femur.
134However, the exact boundary between the reactionary tissue and the surrounding cortex is
135gradational (over ~0.5 mm). As a result, we digitally isolated all of the tissue that was clearly
136less dense than that of the average density of the cortex.
137
138 FOSSIL DESCRIPTION AND SYSTEMATIC PALEONTOLOGY
6 139 Archosauria Cope, 1869 sensu Gauthier and Padian, 1985
140 Pseudosuchia Zittel, 1887–1890 sensu Sereno et al., 2005
141 Paracrocodylomorpha Parrish, 1993 sensu Sereno et al., 2005
142 Figures 1, 2, 3
143
144Specimen GR 264, proximal three-fifths of a right femur.
145
146Locality The specimen was discovered in the vicinity of Ghost Ranch, New Mexico, but the
147exact locality is unknown. The Upper Triassic sequence at Ghost Ranch, in stratigraphic order,
148consists of the Chinle Formation divided into the Agua Zarca Sandstone, Salitral Shale, Poleo
149Sandstone, Petrified Forest Member, and “siltstone member” (Irmis et al. 2007). Among these
150subunits, the preservation (color and style) of GR 264 is most similar to those vertebrates from
151the highly fossiliferous Petrified Forest Member (Camp 1930; Irmis et al. 2007) that lies at the
152base of the cliffs surrounding Ghost Ranch, and no significant vertebrate fossils have been
153documented from the Agua Zarca Sandstone, Salitral Shale, or Poleo Sandstone. The Petrified
154Forest Member was deposited during the Norian Stage of the Late Triassic based on single-
155crystal U-Pb age dating of detrital zircons which resulted in a maximum depositional age of
156~212 Ma for the Hayden Quarry within the same stratigraphic unit (Irmis et al. 2011); this also is
157consistent with magnetostratigraphic data (Zeigler and Geissman 2011).
158
159Taxonomic justification The specimen consists of a well-preserved proximal three-fifths of a
160femur. The surface of the bone near midshaft is abraded. The proximal end bears distinct and
161equally-sized anterolateral, anteromedial, and posteromedial tubera (sensu Nesbitt 2011).
7 162Equally sized medial condyles of the proximal end of the femur are present in
163paracrocodylomorphs (ACCTRAN synapomorphy in the analysis by Nesbitt 2011). Although the
164fourth trochanter is abraded, the strap-like shape is consistent with that of paracrocodylomorphs.
165Additionally, the femur is thin-walled near the midshaft, as is typical with, though not exclusive
166to, paracrocodylomorphs (Nesbitt 2011). The proximal articular surface lacks any kind of groove
167typical of most paracrocodylomorphs; however, the gigantic paracrocodylomorph Fasolasuchus
168tenax also lacks a proximal groove, although the presence or absence of a groove may be
169influenced by ontogeny. A proximal condylar fold is present in GR 264, and this character state
170is present in crocodylomorphs, rauisuchids, and F. tenax (Nesbitt 2011). GR 264 is identified as
171a paracrocodylomorph because the combination of character states presented above currently is
172known only in paracrocodylomorph archosaurs.
173
174Body size estimation Estimations of body size for extinct archosauriforms are often hampered by
175the lack of complete skeletons (but see Irmis 2011; Sookias et al. 2012; Turner and Nesbitt
1762013). Because GR 264 is extremely large but only consists of a portion of the femur, we used
177linear measurements of the femora of other archosauriform taxa to estimate its total length and
178approximate the body size (as in Barrett et al. 2014). The width of the proximal head of GR 264
179is approximately 125 mm. Based on a regression using 19 data points (Online Resource 3; best
180fit line: y = 4.459x+9.32056, R2 = 0.93077), we estimate the total length of GR 264 at 566 mm,
181with 95% confidence intervals (CI) of 405.5 mm (lower) and 1051 mm (upper). When only the
182closely related paracrocodylomorph taxa are included in the regression (best fit line: y =
1834.6324x+20.472, R2 = 0.96006), the estimated total length of GR 264 is 600 mm (lower CI = 470
184mm; upper CI = 728.8 mm). Therefore, our estimated total length of this femur (566-600 mm) is
8 185larger than the maximum reported femoral length for all Triassic non-dinosaurian
186archosauriforms other than Saurosuchus galilei, Postosuchus alisonae, and Fasolasuchus tenax
187(see Turner and Nesbitt 2013 for specimen data).
188 Tight correlations between total body length and femoral length have been found among
189crocodylians (e.g. Farlow et al. 2005); however, estimations for other clades based on this dataset
190have revealed uncertainty caused by variations in tail length as compared to snout-vent length
191related to ontogeny, ecology, and even sexual dimorphism (Vandermark et al. 2007). The total
192body length of Fasolasuchus tenax (PVL 3850; femoral length = 750 mm) was estimated to be
1938-10 m (Nesbitt 2011). The total body length of the poposauroid Sillosuchus longicervex (PVL
1942267; femoral length = 470 mm) was estimated at 9-10 m because of more elongated cervical
195vertebrae and an elongated tail in poposauroids (Nesbitt 2011). The 566-600 mm femoral length
196estimate for GR 264 represents a paracrocodylomorph that may have been comparable in size to
197those taxa (i.e. between 8 and 9 m). Another metric for size comparison is to estimate body mass
198using the minimum circumferences of the femoral and humeral shafts (Campione and Evans
1992012; Campione et al. in press). The minimum circumference of GR 264 is approximately 165
200mm, but without an associated humerus, body mass cannot be estimated for this individual at this
201time.
202 In order to estimate the minimum total body length of the phytosaur that attacked GR 264
203and embedded the tooth, we related the largest diameter of a phytosaur tooth to skull length
204based on our preliminary measurements of a series of complete phytosaur skulls (Online
205Resource 3). Few phytosaur skulls with prepared anterior alveoli and a measurable skull length
206(from the anterior edge of the premaxilla to the posterior portion of the occipital condyle) could
207be measured for this analysis; most phytosaur specimens either have incomplete or unprepared
9 208premaxillary alveoli, the skull is anteroposteriorly distorted, portions of the rostrum include
209reconstructed sections, or these measurement data are not reported in the literature. We identify
210the embedded phytosaur tooth as a ‘premaxillary fang’ (see below); this type of tooth is located
211in either the first or second alveolus in the premaxilla of phytosaurs as part of the ‘tip-of-snout
212set’ (Hungerbühler 2000). We measured the maximum diameter of the first and second
213premaxillary alveoli as a proxy for tooth crown width, and used the larger of the two
214measurements in our analysis. Skull length was measured from the anterior edge of the
215premaxilla to the posterior edge of the basioccipital in order to conform to the dorsal cranial
216length measurements used by Hurlburt et al. (2003). We recovered a positive relationship
217between premaxillary fang alveolus size and skull length (i.e. longer skulls had larger alveoli;
218best fit line: y = 0.0385x-13.332, R2 = 0.91). Applying those results to the maximum measured
219diameter of the embedded tooth crown (14.6 mm) resulted in a skull length of 725 mm for the
220phytosaur. However, this is a minimum anteroposterior skull length because of the incomplete
221preservation of the embedded tooth crown. Additionally, the low number of data points here (n =
2226) resulted in high 95% confidence intervals (lower CI = 272 mm; upper CI = 1860 mm). We
223related our skull length to total body length using data from Hurlburt et al. (2003) and found the
224individual that attacked the paracrocodylomorph to be approximately 5 to 6 m in total body
225length, though there is potential variation in skull to total body length within Phytosauria that
226would affect this estimate.
227
228 Archosauria Cope, 1869 sensu Gauthier and Padian, 1985
229 Pseudosuchia Zittel, 1887–1890 sensu Sereno et al., 2005
230 Paracrocodylomorpha Parrish, 1993 sensu Sereno et al., 2005
10 231 Figure 4
232
233Specimen FMNH PR 1694, distal portion of a left femur.
234
235Locality This specimen was collected by P. C. Miller in 1913 near Fort Wingate, McKinley
236County, western New Mexico. The specimen likely came from the lower half of the Chinle
237Formation in this area (Mehl et al. 1916), and these beds now are assigned to either the
238Bluewater Creek Member or the overlying Blue Mesa Member (Heckert and Lucas 2002). The
239age of those units is likely Norian and older than ~218 Ma given that they are stratigraphically
240below a well-dated sandstone just above the Bluewater Creek Member (= Six Mile Canyon bed;
241Irmis et al. 2011; Ramezani et al. 2014). Other fossils collected and originally catalogued with
242this specimen include the distal end of a humerus of a phytosaur (FMNH PR 1694; incorrectly
243identified as a proximal end of a femur) and a complete ilium of a phytosaur (FMNH UC 1252;
244plate II in Mehl et al. 1916).
245
246Taxonomic justification The distal end of the femur has a prominent crista tibiofibularis
247separated from the lateral distal condyle of the femur by an obtuse angle, and the posterior tips of
248the medial condyle and the crista tibiofibularis point posteriorly as in poposauroids and early
249diverging paracrocodylomorphs (Nesbitt 2011). Like GR 264, this femur is thin-walled as in
250paracrocodylomorphs. The posterior surface of the medial condyle is deflected posteroventrally
251as in Poposaurus gracilis (YPM 57100). Even though there are no clear apomorphies placing
252FMNH PR 1694 within the clade Archosauria, the combination of character states listed above
253result in an assignment in Paracrocodylomorpha, and possibly even a poposauroid affinity.
11 254
255 RESULTS
256DESCRIPTION OF BITE MARKS
257GR 264
258 GR 264 exhibits multiple morphologically distinct groupings of bite marks. The
259embedded tooth is along the proximal portion of the posterolateral margin of the femur. The
260tooth fragment ranges from flush with to slightly inset into the surrounding bone, so essentially
261none of the tooth’s exterior surface was immediately visible. The tooth is ovoid to nearly circular
262in cross section with carinae present along the mesial and distal edges. The exposed area of the
263tooth is 14.6 mm in diameter at the carinae and 12.6 mm in diameter perpendicularly to that, with
264exposed enamel approximately 2 mm in thickness. A halo of reaction tissue surrounds the tooth,
265extending from less than 1 mm to roughly 3.5 mm in thickness. CT scans revealed that the tooth
266fragment is 32.8 mm long and penetrated the femur from near the posterolateral margin of the
267femur and moved anteriorly where it came within approximately 5 mm (through roughly 87% of
268the bone cross sectional thickness) of exiting the anterolateral side of the element (Figure 3). The
269embedded tooth crown appears complete, is conical in shape, and bears mesial and distal carinae.
270The halo of reaction tissue is also visible in the CT scans, extending into the bone’s subsurface
271and surrounding the entire tooth.
272 Situated roughly 15 mm (21.4 mm from tooth to mark centers) distal to the embedded
273tooth is a heavily remodeled puncture (sensu Binford 1981). This mark also is roughly ovoid in
274cross section (9.8 mm by 7.5 mm in diameter) with a raised lip and is infilled with irregular
275reaction tissue (Figure 1A). CT data reveal that this mark was formed by a roughly conical tooth
276that penetrated the femur to a depth of approximately 11 mm and created reaction tissue related
12 277to the bite (Figure 3). This remodeling makes it unclear how well the ellipsoid shape of the mark
278at the surface of the bone reflects the original morphology of the tooth. However, the similarities
279in position, shape, position relative to the orientation of the embedded tooth, and extent of
280healing as represented by the reaction tissue suggest that this mark was formed during the same
281event in which the embedded tooth was implanted, possibly suggesting that the two structures
282were serial in origin (i.e. formed together during a single biting event).
283 Four additional partially healed bite marks are present on the proximal portion of GR
284264: two near the midline on the posteromedial surface (Figures 1B, 2) and two on the
285anterolateral, near the medial edge (Figure 1D). All are slightly more fusiform in shape, with
286irregular reaction tissue forming their interiors and raised lips around their margins. As with the
287previously described, partially healed bite mark, CT data suggest conical teeth formed these
288marks, though bone remodeling has hindered more detailed discussion of their morphology and
289orientation. The exposed mark on the anterolateral surface of the femur (8.4 mm by 4.4 mm) and
290the more medially positioned of the posteromedial marks (7.3 mm by 6.0 mm; Figure 2) are
291more D-shaped, with one side of the structure significantly more convex than the other. The
292mark more laterally positioned on the posteromedial surface of the femur is more symmetrical
293and is slightly elongate (9.5 mm by 4.8 mm). CT data revealed the final mark (~7 mm by ~8 mm
294based on measurements of the CT data), concealed under matrix approximately 15 mm distal to
295the exposed bite mark on the anterolateral surface of the bone, as well as regions of reaction
296tissue that are more conically shaped and extend beyond all the surficial marks (Figure 3).
297 A separate set of pits (sensu Binford 1981) is located on the anterolateral and
298posteromedial surfaces of the proximal end of GR 264. Unlike the marks described above, these
299traces exhibit no obvious reaction tissue, indicating that they were formed at or near time of
13 300death. Four of these pits are clustered together near the midline of the proximal posteromedial
301surface (Figure 1B). They are similar in shape (symmetrically fusiform) and size (8.76 mm by
3024.29 mm; 7.03 mm by 3.72 mm; 8.88 mm by 4.59 mm; 6.90 mm by 4.11 mm) suggesting a
303single trace maker. There are two possible pits on the anterolateral surface opposing this set
304(Figure 1C); these marks are similar in size and shape to the posterolateral pits, but this
305identification is tenuous due to the poor preservation of this region of the femur.
306 A final set of six bite marks was present on the posteromedial surface of the femur, near
307the midshaft of the bone. These scores all were oriented roughly perpendicular to the long axis of
308the femur with most marks subparallel (Figure 1E). Simple scores ranged from 0.5 mm to 1.0
309mm in width and 12 mm to 14 mm in length. One mark was identifiable as a hook score (sensu
310Njau and Blumenschine 2006), a feeding trace type whose ‘L’- to ‘J’-shaped morphology has
311been associated with organisms that practice an inertial feeding strategy (D’Amore and
312Blumenschine 2009; Drumheller and Brochu 2014). Unfortunately, the region of the femur
313exhibiting these marks was damaged during post-CT scanning shipment of the specimen, leaving
314only two intact.
315
316FMNH PR 1694
317 At least four bite marks are observed on FMNH PR 1694. All are asymmetrically
318fusiform and roughly ‘D’-shaped. The two largest marks are oriented on opposing sides of the
319femur, positioned slightly medially from the midline (Figures 4A, 4D). Both are situated with the
320more convex side oriented distally on the femur. The puncture in the anterior surface extends all
321the way into the medullary cavity of the femur, whereas the posterior mark penetrates to a depth
322of 9 mm. Both are also associated with secondary impact damage in the form of radiating
14 323fractures (sensu Byers 2005). The puncture on the posterior surface is further modified with
324depressed fractures, in which the surrounding bone collapsed under the force of the bite. These
325lines of evidence, partnered with their similar size (anterior puncture = 15.22 mm by 9.26 mm;
326posterior puncture = 15.37 mm by 9.33 mm) and the similar orientation of their long axes,
327strongly support our hypothesis that these two marks are serial in origin.
328 Another bite mark is present on the posterior surface of the femur near the broken edge
329(Figure 4C). This mark is truncated by the break and further obscured by the radiating and
330depressed fractures associated with the nearby puncture, rendering accurate measurements
331impossible. However, the size and curvature of the remaining margin of the mark indicates that it
332would have been of a similar size as the other two punctures.
333 The last bite mark is present on the lateral surface of the shaft at the distalmost end
334(Figure 4B). This pit is significantly smaller (7.61 mm by 5.60 mm) than the previously
335described punctures, and is roughly ‘D’-shaped, with the more convex side oriented posteriorly
336on the femur. This mark is also associated with prominent radiating fractures indicating that
337while this tooth did not penetrate to the same depth as the described punctures, it still impacted
338the femur with great force.
339
340 DISCUSSION
341IDENTIFICATION OF BITE MARKS
342 Bite marks are comparatively rare in the fossil record (e.g. Behrensmeyer 1981; Boucot
3431990; Behrensmeyer et al. 1992; Jacobsen 2001; Kowalewski 2002), and direct association
344between those trace fossils and embedded teeth even more so. Among archosaurs, embedded
345teeth previously were identified among theropod dinosaurs (Currie and Jacobsen 1995; Xing et
15 346al. 2012; DePalma et al. 2013) and crocodyliforms (Franzen and Frey 1993; Boyd et al. 2013).
347Though bite marks attributed to possible intraspecific fighting among phytosaurs have been
348reported previously (Abel 1922; Camp 1930; Stocker 2010), this fossil represents the first
349identification of an embedded phytosaurian tooth.
350 The identification of the embedded tooth as that of a phytosaur is based on its size and
351general morphology in comparison to the dental morphology detailed for Nicrosaurus kapffi
352(Hungerbühler 2000). Tooth morphology has the potential to be utilized to determine both
353positional relationships within a set of dentition as well as possible taxonomic and systematic
354identifications, but it has not been utilized for phytosaurs much beyond the detailed study by
355Hungerbühler (2000). Those data were used to identify the first isolated phytosaur teeth from
356Lithuania (Brusatte et al. 2012). The lack of bilaterally compressed teeth (= mediolaterally
357compressed) was suggested to be apomorphic for Phytosauria (Hungerbühler 2000). The exposed
358cross section of the embedded tooth in GR 264 is nearly circular; however, computed
359tomographic data reveal that the carinae extend along both the distal and mesial edges of the
360tooth as slight flanges, creating a ‘D’ shape in cross sectional view (Figure 3). The more
361pronounced carinae on the distal (= posterior) portion of the tooth, is comparable to that observed
362for the large first and second premaxillary teeth and the anteriormost dentary teeth of a
363phytosaur, as part of the ‘tip-of-snout set’ (Hungerbühler 2000).
364 Examination of the size, shape, location, and amount of healing of the more distally
365positioned, partially healed puncture suggests that it was formed serially with the embedded
366tooth. Therefore, we attribute this mark to the same phytosaur individual. As for the remaining
367partially healed bite marks, it is unclear how well the shape of the raised lip of reaction tissue on
368the surface of the bone reflects the shape of the original tooth. The reaction tissue visible in the
16 369subsurface using CT data extends away from the mark center beyond the surficial margins of the
370raised reaction tissue and appears to reflect damage caused by a conical, rather than
371mediolaterally compressed, tooth. Again, the similar extent and texture of the reaction tissue
372surrounding these marks seems to indicate that they occurred very close in time with the bite that
373left the embedded tooth and healed serial puncture. The most parsimonious explanation is that
374these marks were created by the same actor and represent separate biting events during a single
375trophic interaction or incidence of interspecific fighting.
376 All remaining bite marks on GR 264 exhibit crushing, impact damage, and no obvious
377evidence of healing. We interpret these marks as having occurred at or near time of death. The
378unhealed pits (four on the posteromedial surface of the femur; Figure 1B) are nearly identical in
379size and shape, indicating that they likely were formed by the same actor. These marks are
380fusiform in shape, indicating formation by bicarinated, laterally compressed teeth. Potential
381Triassic carnivores that possessed such teeth include some phytosaurs, dinosauromorphs, and
382paracrocodylomorphs. Because these marks lack other potentially diagnostic characteristics, we
383cannot exclude any of these possible groups as the potential actor at this time.
384 The scores that were present on GR 264 prior to damage (Figure 1E) were generally ‘U’-
385shaped in cross section. They lacked striations, which are characteristic of serrated teeth
386(D’Amore and Blumenschine 2009), bisections, which are formed by strongly bicarinated teeth
387(Njau and Blumenschine 2006; Drumheller and Brochu 2014), or any other potentially
388diagnostic trait that might facilitate more specific identification. The marks were small (0.5-1
389mm in width), relatively subparallel, and closely spaced (0.5-1 cm apart), potentially suggestive
390of a physically smaller actor than the one responsible for the associated pits described above, and
391one with a relatively homodont dentition. This leaves a wide variety of potential actors, including
17 392any carnivorous archosauriform.
393 There are three obvious ‘D’-shaped punctures on the femoral shaft of FMNH PR 1694
394and one other puncture truncated by fractures. Their morphology is consistent with a tooth that is
395not bilaterally compressed, such as a maxillary or posterior dentary tooth of a phytosaur
396(Hungerbühler 2000). We interpret the bites to be serial in origin because of the asymmetric
397convexity of the puncture on the anterior surface of FMNH PR 1694 and the orientation of the
398carinae on both the anterior and posterior punctures, representing a single bite from upper and
399lower teeth on the left side of the dentition of a single individual.
400 The truncated mark was not formed serially with the other two punctures. It is oriented at
401an opposing angle to the previous two marks, closer to parallel with the long axis of the femur
402rather than strongly transverse. Also, this truncated mark seems to further compromise the region
403of the bone already inset by the extensive depressed fractures associated with the complete
404puncture. Because one side of the mark intersects and is interrupted by one of the fractures
405generated by the completely preserved puncture, we interpret this trace to have occurred after the
406serial marks. The similarities between these marks indicate that they were created by a single
407trace maker.
408 The single pit, present on the lateral surface of the shaft, is also asymmetrically fusiform,
409again indicating a phytosaurian trace maker. Pit size, even among marks made by a single actor,
410can vary widely with factors such as bite force and density of the region of modified bone
411(Delaney-Rivera et al. 2009). Therefore, it is likely, but by no means certain, that this mark can
412be associated with the previously described punctures.
413
414PALEOBIOLOGICAL INTERPRETATIONS
18 415 The substantial reaction tissue in GR 264 surrounding the embedded phytosaur tooth and
416infilling the four punctures associated with it indicates that the paracrocodylomorph survived an
417attack by a large phytosaur long enough for extensive healing to occur. None of the healed
418wounds present on GR 264 exhibit the proliferative, spongy lesions that are indicative of
419widespread infection (e.g. Mackness and Sutton 2000). Considering the depth of the injuries, and
420the introduction of a foreign body into the bone itself in the form of the embedded tooth, this
421lack of evidence for infection is somewhat surprising. However, extant crocodylians are
422unusually resistant to many forms of infection (Merchant et al. 2003, 2006). This trait might have
423been shared with more distantly-related archosaurs, but our ability to identify this feature in
424paracrocodylomorphs is hindered because bracketing this specific immune response requires
425comparative knowledge of this process in crocodylians, birds, lepidosauromorphs, and possibly
426turtles.
427 Whether this was a failed predation attempt or an incident of interspecific fighting is not
428clear. Positive association of bite marks with predation versus scavenging behavior is difficult to
429determine with complete certainty for the marks that do not exhibit evidence of healing. One way
430to address this issue is by discussing order of access to remains and element food utility. Indices
431of skeletal element food utility can be calculated in a number of ways (Lyman 1994), but most
432rank bones in terms of the amount of associated edible tissues. In the case of low utility bones,
433such as phalanges and metapodials, bite marks concentrated in these regions have been
434associated with late access to remains (i.e., scavenging; Longrich et al. 2010). Conversely,
435concentrations of marks on high utility bones, such as the femur, are indicative of early access to
436remains. Whereas a predator would certainly have early access to a carcass, so too would a
437scavenger encountering the fresh remains of an animal which died through some other means.
19 438Both GR 264 and FMNH PR 1694 are high-utility, partial femora. We identify bite marks from
439at least three actors on GR 264, two of which occurred at or near time of death. Based on the
440food utility of these femora, we interpret that both of these actors had early access to the remains,
441though a determination of predation or scavenging is impossible to make with the current data.
442The same can be said of the bite marks present on FMNH PR 1694.
443 Many paleontological studies of bite marks focus on marks left by single actors (e.g.
444Currie and Jacobsen 1995; Erickson and Olson 1996), whereas, in current ecosystems, multiple
445predators and scavengers have been observed regularly interacting with the same set of remains
446(Selvaggio and Wilder 2001). Actualistic studies, many of which focused specifically on
447interactions between early hominins and other carnivores, attempted to identify patterns of
448modification that signal early versus late access to a prey item (Shipman 1986; Marean and
449Spencer 1991; Dominguez-Rodrigo 2002; Lupo and O’Connell 2002), and the general patterns
450uncovered in those studies should be applicable in non-human systems. For example, early
451access to remains results in higher mark density on the bones that supported more soft tissue
452during life (Shipman 1986; Marean and Spencer 1991; Lupo and O’Connell 2002; Longrich et
453al. 2010). The bite marks present on GR 264 preserve evidence of at least three distinct
454interactions. The partially healed marks attributable to a phytosaur (Figures 1-3) represent an
455incident that clearly pre-dated the paracrocodylomorph’s death. The larger pits associated with a
456more ziphodont predator occur on a high economy bone (the femur) at a grasping point of the
457limb (near the hip socket), a pattern which is associated with disarticulation behavior in modern
458crocodylians (Njau and Blumenschine 2006). In contrast, the smaller, subparallel scores are more
459consistent with flesh stripping behavior (D’Amore and Blumenschine 2009). These marks do
460demonstrate a faunal succession of carnivores interacting with this single prey item, but a more
20 461specific sequence to these two peri- or post-mortem events is impossible to elucidate.
462 Phytosaurs and ‘rauisuchians’ have been identified as dominant predators from the Late
463Triassic (e.g. Jacobs and Murry 1980; Murry 1989; Parrish 1989; Long and Murry 1995;
464Weinbaum 2013), and in part this line of thought was influenced by the large body size of these
465fossils. Phytosaur body mass calculated based on skull and limb length as well as an
466approximated snout-vent length resulted in estimated masses of 200-350 kg on average and
467lengths of near 4.5 m for pseudopalatine phytosaurs from the Canjilon and Snyder quarries
468(Hurlburt et al. 2003); our total body length estimate of 5-6 m for the phytosaur that attacked GR
469264 (see above) implies a larger individual than the average for those pseudopalatines. Excluding
470phytosaurs and saurischian dinosaurs, paracrocodylomorphs have the longest femora of any
471archosaur and thus are hypothesized to have had among the largest body sizes of Late Triassic
472Archosauriformes (Turner and Nesbitt 2013). The estimated 8 to 9 m total body length of GR
473264 based on comparisons with closely related forms, places it among the largest members of
474that group. Both paracrocodylomorph femora we described in this study came from some of the
475physically largest carnivorous taxa present at both localities, and yet they were targeted by other
476members of the fauna, specifically phytosaurs.
477 Phytosaurs are interpreted as having had piscivorous, generalist, or predatory ecologies
478depending on their skull morphologies as compared to those of extant crocodylians (e.g. Hunt
4791989; Murry 1989), but direct evidence to test those potential ecologies is rare and may not
480support previous hypotheses (e.g. Chatterjee 1978; Stocker and Butler 2013). For example,
481longirostrine crocodylians often are cited as piscivorous (e.g. Iordansky 1973; Langston 1973;
482Busby 1995), but ecological studies of extant groups do not always support this interpretation.
483Surveys of stomach contents of Mecistops cataphractus do demonstrate a diet dominated by fish
21 484(Pauwels et al. 2003), but diet is often more diverse in other longirostrine forms. Though extant
485gharials are considered strictly fish specialists, even they have been known to eat frogs,
486mammals, birds, and lepidosaurs (Whitaker and Basu 1983). Tomistoma schlegeii has been
487mistakenly considered almost entirely piscivorous for over 40 years because of a citation of a
488popular publication (Neill 1971). However, recent actualistic research (e.g. Selvaraj 2012)
489demonstrated that the diet of T. schlegeii is much more variable and includes teleost fish, turtles,
490monitor lizards, birds, and mammals (including primates). Ecological observations and surveys
491of stomach contents of Crocodylus johnstoni demonstrate that these crocodiles have a diverse
492diet that includes arthropods, anurans, fish, turtles, and snakes (Webb and Manolis 1988; Tucker
493et al. 1996). Therefore, a direct correlation between long, slender rostra and strict piscivory is not
494supported in living examples. Thus, the use of modern analogues for reconstructing the diet of
495phytosaurs and their placement in a trophic structure is only tentative until other evidence (direct
496or indirect) is supplied by the fossil record, as we demonstrate here. It is clear that phytosaurs
497and paracrocodylomorphs were part of a more complex network of community relationships in
498the Late Triassic than previously appreciated, and newer trophic models incorporating
499hypothesis-tested characteristics of extinct taxa and neural network-based methods (e.g.
500Roopnarine et al. 2007; Roopnarine 2009; Sidor et al. 2013) are required to provide testable and
501more accurately modeled community structure.
502 The complex trophic structure illustrated by large apex predators preying on each other
503hints at a broader question rarely mentioned: why are there so many large carnivorous tetrapods
504in the Upper Triassic assemblages of western North America? Seemingly carnivorous taxa are
505overrepresented in Late Triassic tetrapod assemblages (Heckert 2004; Heckert et al. 2005;
506Nesbitt and Stocker 2008) compared to extant mammalian or large squamate ratios (e.g. Bakker
22 5071972; Stock and Harris 1992). Part of this pattern may be explained by taphonomic size bias
508(Brown et al. 2013) or collection practices, because excavation of the Canjilon Quarry was
509focused on phytosaurs and complete specimens, and small and/or fragmentary specimens were
510not prioritized (Hunt and Downs 2002). However, this does not necessarily explain why
511unbalanced ratios still are recorded in other more comprehensively sampled localities from the
512Late Triassic, which include substantial small-bodied components in their faunas (i.e. Hayden
513Quarry; Irmis et al. 2007). Previously reported imbalances in Mesozoic ecosystems have been
514explained by greater than expected interactions between aquatic and terrestrial taxa (Läng et al.
5152013). A similar situation may be at play here, as demonstrated by the fossilized interactions
516presented in this study, but further research is required to fully explain this tangible unbalance.
517
518 ACKNOWLEDGEMENTS
519 Financial support for CT scanning was provided to MRS by the Jackson School of
520Geosciences and the William J. Powers, Jr. Presidential Graduate Fellowship, The University of
521Texas at Austin. W. Simpson provided details related to FMNH PR 1694. A. Downs confirmed
522information related to GR 264. P. Holroyd provided SKD initial access to and data on GR 264 at
523UCMP. B. Muller and J. Desojo provided measurement data for some taxa in Table 1 of the
524Electronic Supplemental Data. C. Sumrall, S. Sheffield, R. Roney, and J. Horton provided
525helpful discussion. C. Brown, an anonymous reviewer, and S. Thatje provided helpful comments
526that improved the quality of this manuscript.
527
528The research presented in this study complies with all relevant state and federal laws. The
529authors declare that they have no conflicts of interest.
23 530
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855
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865
866 FIGURE CAPTIONS
38 867
39 868Fig. 1 Paracrocodylomorpha (GR 264), partial left femur in posteromedial (left image) and
869anterolateral (right image) views. A) Embedded tooth and partially healed puncture; B) two
870partially healed punctures and group of four unhealed fusiform pits below; C) two possible pits
871(unprepared); D) partially healed puncture; E) group of scores prior to specimen damage. Scale
872bar next to complete fossil = 10 cm. Scale bars in magnified photographs = 1 cm.
873
40 874 41 875Fig. 2 Paracrocodylomorpha (GR 264), proximal end of partial left femur in posteromedial view
876(upper image) with interpretive line drawing (lower image), indicating positions of tubera, the
877embedded tooth, and healed and unhealed bite marks. ? = possible marks in regions of poor
878preservation, hindering more definite identification. Scale bar = 5 cm.
879
880
881Fig. 3 CT rendering of paracrocodylomorph (GR 264), partial right femur showing positions of
882embedded tooth and other bite marks in A) dorsal; B) ventral; C) anterolateral; D) posteromedial
883views; and E) ventral view without other marks highlighted. CT rendering of embedded tooth in
42 884F) labial and G) mesial/distal views. In F and G the distal end of the tooth is oriented towards the
885top of the page. Dorsal view slice images of the embedded tooth in the GR 264 from H) near the
886tip of the tooth; I) near midlength of the tooth; and J) near the base of the tooth. In each view
887(online-only), the embedded tooth is rendered in green, the reaction tissue surrounding the tooth
888is purple, and the other bite marks are orange.
889
890
891Fig. 4 Paracrocodylomorpha (FMNH PR 1694) partial left femur in anterior (top image) and
892posterior (bottom image) views. A) large puncture with associated fracturing; B) small pit with
43 893associated fracturing; C) truncated puncture with associated fracturing; D) large puncture with
894associated fracturing. Scale bar next to complete fossil = 5 cm. Scale bars in magnified
895photographs = 1 cm.
896
897 ELECTRONIC SUPPLEMENTAL DATA
898Online Resource 1: Spin movie of GR 264.
899https://www.youtube.com/watch?v=u61WTqmmyZs
900
901Online Resource 2: Roll movie of GR 264.
902https://www.youtube.com/watch?v=tbpy-dIE37E
903
904Online Resource 3: Body size estimation data.
905Institutional Abbreviations – AMNH, American Museum of Natural History, New York, New
906York, U.S.A.; BSPG, Bayerische Staatssammlung für Paläontologie und Geologie, Munich,
907Germany; NCSM, North Carolina Museum of Natural Sciences, Raleigh, North Carolina,
908U.S.A.; NMT, National Museum of Tanzania, Dar es Salaam, Tanzania; PEFO, Petrified Forest
909National Park, Petrified Forest, Arizona, U.S.A.; PIZ, Paläontologisches Institut und Museum
910der Universität, Zurich, Switzerland; UNC, University of North Carolina, Chapel Hill, North
911Carolina, U.S.A.
912
913
914
915
44 916
917
918 TABLE 1
Taxon and Voucher Specimen Width of Proximodistal Circumference of proximal head of length of femur minimal femoral femur shaft Fasolasuchus tenax (PVL 3851), 140 mm 700 mm Unavailable based on Bonaparte 1981 Ticinosuchus ferox (PIZ T2817), 50 mm 250 mm Unavailable based on Krebs 1965 Postosuchus kirkpatricki (TTU-P 94 mm 521 mm 154 mm 9000), partially based on Weinbaum 2013 Sillosuchus longicervex (PVSJ 85), 95 mm 470 mm Unavailable based on Nesbitt 2011 Alligator mississippiensis 15 mm 78 mm 24 mm (VT research collection unnumbered) Alligator mississippiensis 28.5 mm 138 mm 43 mm (VT research collection unnumbered) Alligator mississippiensis 39 mm 174 mm 61 mm (NCSM 19959) Alligator mississippiensis 12 mm 61 mm 20 mm (NCSM unnumbered) Hesperosuchus agilis (AMNH FR 20 mm 136.5 mm 35 mm 6758), Colbert 1952 Dromicosuchus grallator (UNC 20 mm 143 mm 34 mm 15574), Sues et al. 2003 Shuvosaurus inexpectatus (TTU-P 43.5 mm 234 mm 61 mm 9001) Prestosuchus chiniquensis (BSPG AS 110 mm 430 mm Unavailable XXV 10) Phytosauria (UCSM 25908) 92 mm 355 mm 124 mm Phytosauria (NCSM 27600) 85.5 mm 365 mm 131 mm Aetosauria (NCSM 27600) 73 mm 295 mm 108 mm Parringtonia gracilis (NMT RB426) 24 mm 90 mm 47 mm Revueltosaurus callenderi (PEFO 19 mm 80 mm 39 mm 34561) Unnamed archosauriform (NMT 69 mm 238 mm 98 mm RB48), Nesbitt et al. in press Paracrocodylomorph (GR 264) 125 mm 566-600 mm 165 mm 919
920
45 921
922Table 1 Data used for estimation of paracrocodylomorph body size. Width of the femoral head
923was taken either with digital calipers or with a flexible measuring tape. Femoral lengths are
924reported from the literature or from direct measurements when possible (from the proximal
925portion of the femoral head to the distal edge of the lateral condyle). Minimum femoral
926circumferences were measured with a flexible measuring tape and are reported for future
927estimations of body mass.
928 TABLE 2
Phytosaur specimens Largest premaxillary alveolus/tooth Anteroposterior skull length diameter (either 1st or 2nd position) TMM 31173-120 18.4 mm 805 mm
TMM 31100-418 9.8 mm 635 mm
TMM 31100-239 8.5 mm 600 mm
TMM 31213-16 21.6 mm 875 mm
TMM 31173-121 22.6 mm 980 mm
TMM 31100-1332 16.4 mm 705 mm
Embedded tooth in GR 264 14.6 mm Estimated 725 mm 929
930Table 2 Data used for estimation of phytosaur total body length. Alveolar measurements were
931taken of the diameters of both the first and second premaxillary alveoli with digital calipers to
932the nearest 0.1 mm. If a tooth was still present in either of the alveoli, the width of the tooth was
933measured as well. The largest diameter is reported here for each specimen. Skull lengths were
934measured using a flexible measuring tape and taken from the anterior edge of the premaxilla to
935the posterior edge of the occipital condyle while the skulls were in ventral view.
936
937 REFERENCES
46 938Bonaparte JF (1981) Descripcion de Fasolasuchus tenax y su significado en la sistematica y
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944
945Krebs B (1965) Die Triasfauna der Tessiner Kalkalpen. XIX. Ticinosuchus ferox, nov. gen. nov.
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47